Ecology, Epidemiology, and Control of Plant Viruses

Chapter 14

Ecology, Epidemiology, and Control of Plant Viruses SUMMARY In this chapter, I will consider the more important of the interactions involved in the ecology and epidemiology of plant viruses, with illustrations of the ways they affect their survival and distribution. An understanding of the ecology and epidemiology of a virus in a particular crop and locality is essential for the development of appropriate methods for the control of the disease it causes. I then discuss the various approaches to controlling plant virus diseases.

In order to survive, a plant virus must have (i) one or more host plant species in which it can multiply, (ii) an effective means of spreading to and infecting fresh individual host plants, and (iii) a supply of suitable healthy host plants to which it can spread. The actual situation that exists for any given virus in a particular locality, or on the global scale, will be the result of complex interactions between many physical and biological factors the major ones of which are shown in Figure 14.1.

As with most other obligate parasites, a dominant ecological and epidemiological factor to be considered is usually the way viruses spread from plant to plant and the ways that other factors influence such spread. As can be seen from Figure 14.1, the interactions between three entities—the virus, the host, and the vector—are involved in the spread of most viruses. Superimposed on these are the impacts of environmental factors that can affect each of the three entities and the overall interactions between all three. Ecology has yet a further superimposition of how the infected plant interacts with the ecosystem in which it grows (Section II, H).

A.  Virus–Host Interactions 1.  Properties of Viruses and Their Host Plants Various biological properties of a virus and its host(s) affect this interaction.

I.  ECOLOGY AND EPIDEMIOLOGY

Acronyms of virus names are shown in Appendix D

Plant Virology, Fifth Edition. © 2014 2012 Elsevier Inc. All rights reserved.

V Tra H irule os nc n Re Sym spor t ran e sis pto t an ge tan m d ce exp spr an res ead d p si rot on ec tio n

Virus

Plant

Ecology and climate Genotype and phenotype Feeding behavior Other interactions Vector specificity

n itio gn tion tor co i c y Re quis n fa ienc Ac issio effic ty i m ns sion cific Tra mis spe ns or Tra Vect

We should distinguish between the terms epidemiology and ecology, which in many papers have been used interchangeably. Ecology describes the factors influencing the behavior of a virus in a given physical situation and the impact that infection of a plant has on the surrounding flora and fauna. These factors include host range, tissue tropism, pathogenesis, and host responses. It is a fundamental concept based on the relational properties of the virus to the host. Epidemiology is the study of the determinants, dynamics, and distribution of viral diseases in host populations. It includes a dimensional aspect of the factors determining the spread of a virus into a given situation. The two terms often interlink, but even though each has a specific meaning, I will consider them both together in this section.

Vector

FIGURE 14.1  Some of the interactions involved in the natural infection of a plant by a virus. From Hull (1991) with permission of the publishers.

809

810

a.  Physical Stability of Viruses and Concentrations Reached For viruses that depend on mechanical transmission, a virus that is stable, both inside and outside the plant, and that reaches a high concentration in the tissues is more likely to survive and spread than one that is highly unstable. The survival and spread of certain viruses appear to depend largely on a high degree of stability and the large amounts produced in infected tissues. For example, TMV may survive for long periods in dead plant material in the soil, which is then a source of infection for subsequent crops (Johnson and Ogden, 1929). TMV was recovered from 42 brands of cigarettes in Germany by Wetter and Bernard (1977), the virus yield being 0.1–0.3 mg/g tobacco. TMV from cigarette tobacco has about one-half the specific infectivity of that isolated from fresh leaf. High concentrations of virus at a particular season may be important. Stellaria media is an overwintering weed host for CMV. Walkey and Cooper (1976) found that CMV reached its highest concentration in this host at low temperatures. Thus, the plant would provide a very good source for acquisition of virus by aphids in the early spring. b.  Rate of Movement and Distribution Within Host Plants Viruses or virus strains that move slowly through the host plant from the point of infection are less likely to survive and spread efficiently than ones that move rapidly. However, speed of movement should be measured relative to the lifetime of individual host plants. Viruses that infect long-lived shrubs or trees can afford to move much more slowly through their hosts than those affecting annual plants. Another factor for aerial-borne viruses is the speed of movement within the host relative to the life cycle or seasonal cycle of the vector. Viruses that move into the seed and survive there have an important advantage in spread and survival. TNV is confined to the roots in most hosts, and in nature, it depends on transmission through the soil and infection of new hosts with the aid of fungal vectors. c.  Severity of the Disease A virus that kills its host plant with a rapidly developing systemic disease is much less likely to survive than one that causes only a mild or moderate disease that allows the host plant to survive, compete with surrounding plants, and reproduce effectively. There is probably a natural selection in the field against strains that cause rapid death of the host plant. As discussed in Chapter  8, Section VII, it is likely that viruses have coevolved with their natural hosts and that many crop diseases are severe because there has not been sufficient time for a stable relationship to have evolved. Leafhoppers living on desert plants of the western United States are infective primarily with strains of BCTV that cause mild symptoms in beet. Virulent strains of BCTV kill

Plant Virology

certain desert plant species before they can allow a generation of leafhoppers to mature. Thus, virulent strains in the desert tend to be self-eliminating (Bennett, 1963). Synergistic interactions between viruses can lead to more severe disease (see Chapter  4, Section IX, B, 1). Zhang et  al. (2001) analyze the epidemiological implications of such interactions. d.  Mutability and Strain Selection As described in Chapter  8, Section III, viral mutation and recombination provides molecular diversity. This variation within viral populations can impact on the epidemiology of the virus (reviewed by Moury et al., 2006). Thus, the extent to which a virus is able to mutate to produce strains that can cope effectively with changes in the environment may well affect survival and dispersal of the virus (Section II, J). General rates of mutation are discussed in Chapter  7, Section IX, A, but can vary between viruses and virus strains. For example, PLRV seems relatively stable (although this may merely reflect lack of experimentation or appropriate techniques for this virus), while many other viruses such as CMV and TSWV exist in nature as numerous strains. There is fairly good evidence that different strains of the same virus may vary in the rate at which they produce a certain type of mutant. Mild strains of PVX isolated from potato frequently give rise to ringspot strains in tobacco, but the TBR strain originally isolated from tomato was never observed to do so (Matthews, 1949). The common TMV can give rise to a wide range of mutant types (Bawden, 1964). Invertebrate vectors have sometimes been shown to transmit some strains of a virus more efficiently than others. These experiments illustrate ways in which strains might become selected under natural conditions. In districts where an annual crop such as tobacco has been farmed for many years, characteristic strains may come to dominate. Thus, Johnson and Valleau (1946) described how different dominant strains of TMV tend to be characteristic of different tobacco farms in old tobaccogrowing areas. On a wider scale, geographical isolation may lead to divergence of strains, particularly where climatic conditions are different. Such geographical variation in the dominant strain type is not uncommon. One strain of a virus may remain dominant for many seasons in a particular crop and region if there exists a stable natural reservoir host for the strain in that region. In regions with high year-round temperatures, strains of viruses may be adapted to grow at such temperatures. However, where summer temperatures are very high, viruses may actually be inactivated in vivo. For example, SCV was eliminated from strawberry plants grown in the Imperial Valley of California (Frazier et al., 1965). Season appeared to be a factor in the dominance of two strains of CMV in tomato and pepper crops in southeastern France. A thermosensitive strain dominates in spring, while a thermoresistant strain is prevalent

Chapter | 14  Ecology, Epidemiology, and Control of Plant Viruses

in summer (Quiot et  al., 1979). BYDV-related viruses (then considered to be strains) can be distinguished by severity of disease and by the species of aphid that transmits them. The dominant strains in New York State changed gradually over 20 years from isolates of the vector-specific MAV type to those similar to PAV strains (Rochow, 1979). By contrast, in a given crop and season there may be no detectable variation in the pathogenicity of the virus over wide areas, for example, BPMV in soybean (Ross and Butler, 1985). Where there is a source of virus for an annual agricultural crop in perennial weeds and wild hosts, successive crops may become infected with strains that never have the opportunity to become well adapted to the crop plant. When agricultural operations or other factors do not bring about sudden changes, we can envisage, for any particular host species and environment, that selection of strains of a virus will occur until those best adapted for survival will dominate. Factors important for survival of a strain will include: (i) efficient transmission by insects or other means; (ii) more rapid multiplication and movement in the plant than any competing strains, and (iii) the production of mild or only moderately severe disease. These factors have been studied experimentally for BSMV in barley by Timian (1974). e.  Virus Hosts Various aspects of virus hosts impact upon epidemiology of a virus in a crop. These include the virus host range, the wild (noncrop species that the virus infects) and the genetic vulnerability of the crop species. i. Host Range  Viruses vary greatly in the range of species they are able to infect (see Chapter  4, Section VI). Some viruses affecting strawberries appear to be confined to the genus Fragaria. Other viruses may be able to infect a wide range of plants. For example, the host range of CMV includes over 1200 host species in more than 100 families. Other viruses having very narrow host ranges presumably survive because either their host is perennial, or it is vegetatively propagated, or the virus is transmitted efficiently through the seed. A diversity of hosts gives a virus much greater opportunities to maintain itself and spread widely but places the virus under different selection pressures. Viruses that have perennial ornamental plants and other agricultural and horticultural species as hosts have become widespread around the world. Important examples among ornamental flowering species are: (i) BYMV and CMV carried in gladioli; (ii) TSWV carried in dahlia, which is frequently infected and is a major reservoir of this virus in many countries (dahlia may also carry CMV, often without symptoms); and (iii) CMV carried in lilies, often without symptoms.

811

ii. Wild Species (reviewed by Cooper and Jones, 1996)  Weeds, wild plants, hedgerows, and ornamental trees and shrubs may also act as virus reservoirs. The actual importance of these various sorts of host for neighboring crops will depend on circumstances, particularly on the presence of active invertebrate vectors. For example, the presence of OkMV in three malvaceous weed species in Nigeria appears to be an important source of the virus for crop plants (Atiri et  al., 1984). Solanum sarrachoides is an alternate host for PVY and a preferred host for Myzus persicae and Macrosiphum euphorbiae, both vectors of PVY (Cervantes and Alvarez, 2011); it is thought to be an important reservoir for the spread of PVY into potato crops in the Pacific Northwest of the United States of America. Similarly, the perennial legume, Hardenbergia comptoniana, is endemic in the Southwest Australian Floristic Region and is a source of the potyvirus HarMV which spreads to the recently introduced crop Lupinus angustifolius (Luo et al., 2011). On the other hand, although ACLSV was found in a significant proportion of hedgerow hawthorn plants in England, these hosts appear to be of little significance for spread of the virus to fruit trees (Sweet, 1980). As noted in Chapter  8, Section VII, coevolution of a virus with its host often leads to reduced symptoms or symptomless plants. Thus, since it is likely that many viruses that have been infecting “wild” host species for a long time will show few, if any, symptoms. A possible example of this is of the eight viruses isolated from 92 Plantago lanceolata plants growing wild in the United Kingdom only two showed distinct symptoms; one showed slight symptoms and five no symptoms (Hammond, 1982). However, there have not been many studies on this as it is hard to justify funding for research on viruses in symptomless wild species. For a wild host to be significant in the epidemiology of a virus it has to be a host for the vector and to be reasonably near the crop. The natural hosts of EHBV and RHBV occupy different ecological niches and thus, although EHBV can infect rice, it does not often under field conditions (Madriz et al., 1998). However, it must be remembered that virus can be transmitted in two directions and that a virus introduced into a crop from another source could spread to a nearby wild host which could then be a reservoir for infection of subsequent crops. Many nematodes and the viruses transmitted by them have wide host ranges, including woody perennial plants. Such viruses and their vectors can often survive in woody plants in hedges and forests in the absence of suitable agricultural crop plants. GFLV and its nematode vector Xiphinema index are unusual in that they are both largely confined to the grape plant in the field. Since the grape vine is long-lived, alternative hosts may not be necessary for survival. Furthermore, vector and virus can survive for several years in viable roots that may remain in the soil after the grape vine tops have been removed.

812

iii. Genetic Vulnerability of the Host (reviewed by Thresh, 2006a)  The growing of large areas of vulnerable cultivars of crops can disrupt the natural equilibria between the viral pathogen and its hosts. A new crop or new cultivars introduced to an area can become severely affected by viruses or virus strains not previously encountered. An example of this is the severe outbreaks of CSSV in cacao in West Africa. Cacao was introduced from the Amazonian jungle to West Africa in the late nineteenth century, and since then major commercial production has developed there. The swollen shoot disease, first reported in cacao in 1936 (caused by CSSV), was very probably transmitted from natural West African tree hosts of the virus by the mealybug vectors that are indigenous to the region. Another example is epidemics of MSV in maize introduced into Africa from Central America. In both these cases, the susceptible introduced crop became infected with a virus present in the indigenous vegetation. Changes in cultivation techniques can lead to serious outbreaks of virus diseases, for example, in the “Green Revolution” (Section II, D, 1, a).

B.  Virus–Vector Interactions The three basic interactions between viruses and their arthropod vectors, nonpersistent, semipersistent, and persistent, are described in Chapter 12, Section III.

C.  Vector–Host Interaction 1.  Vector Movement a.  Host Seeking The host-seeking behavior of arthropods is described in Chapter 12, Section II. A virus with a non- or semipersistent interaction with aerial vector is most likely to be transmitted during short visit host-seeking flights of the vector and one with a persistent interaction is most likely transmitted by vectors that colonize that host. Other factors can affect the field transmission of viruses by arthropods. For example, antipredator behavior of aphids and their reaction to parasitoids can increase the dispersal of nonpersistently transmitted viruses (Belliure et  al., 2011; Hodge et  al., 2011); the effects of parasitoid disturbance on virus transmission have been modeled (Jeger et al., 2011a). b. Migration (reviewed by Reynolds et al., 2006) In most cases, arthropod flight is over short distances, but plant virus vectors (particularly some species of Homoptera) can also migrate tens or hundreds of kilometers and cause disease outbreaks far from the source of infection. As most vectors are relatively small insects, movements over any substantial distance will necessarily

Plant Virology

entail the power of the wind to transport individuals much further and faster than would be possible by self-propelled flight alone. It is thought that these long-range movements are seldom “accidental” but are actively initiated and maintained through specialized behavior patterns occurring during a distinct migratory phase in the life cycle. Migration will usually be initiated by sustained climbing flight taking the individual out of its “flight boundary layer” (a layer of air, extending a variable distance up from the ground, where the wind speed is lower than the insect’s flight speed), thus facilitating long-distance, windborne transport. As noted in Chapter 12, Section II, A, 2, c, several types of alate insects are attracted by UV light early in flight and then by yellow/blue regions of the spectrum later in flight. Migratory locomotion thus tends to be more continuous than other types of movement and the migrant’s track over the ground becomes straightened out, causing an individual to be transported away from a localized area (home range). Long-distance migratory transport has been reported for members of the Aleyrodidae, Aphididae, Cicadellidae, Delphacidae, and Piesmidae families (listed in Reynolds et al., 2006). There are various techniques for monitoring insect migration (reviewed by Reynolds et al., 1997 and Osborne et  al., 2002). These include aerial sampling using nets attached to aircraft or tethered balloons; networks of ground-based traps (e.g., see http://www.rothamsted.ac.uk/ insect-survey/); radar (Figure 14.2); artificial markers such as labels, dyes, and radioactive isotopes; natural markers such as gut contents and molecular markers (e.g., DNA, allozymes); flight mills and flight chambers which can assess the flight potential for an insect species; and meteorological data to predict source and sink areas and trajectories (Figure 14.3). The advantages and disadvantages of these methods are discussed by Reynolds et al. (2006). The severity of BCTV has a very different effect in beet plantings to that described above for the natural desert situation. Sugar beet is a good host for the leafhopper if the plants are small and exposed to full sunlight. They are poor hosts when large, providing much shade. For this reason, severe strains of BCTV facilitate their own spread in beet by producing small, stunted plants, which favor vector multiplication (Bennett, 1963). The spread of severe strains is further assisted by the fact that mild strains do not protect against infection. Leafhoppers overwintering near beet fields carry strains of higher virulence than hoppers found in the desert.

D.  Virus–Vector–Host Plant Interactions (reviewed by Colvin et al., 2006) As discussed in Chapter 12, Section II, A, 2, d, virus infection of a plant can have significant effects on a potential vector, both in the attractiveness (or repulsion) to host-seeking insects and as a potential host plant for colonizing.

(A)

(B)

900

19.00 h

800

Height (m)

22.00 h

18.00 h

17.30 h

700

21.00 h

23.30 h

600 500 400 300 200 100 0

1

10

100

1000 1

10

100

1000

Numbers per 104 cu. m 35° Yellow Sea Jiangsu 17 Yang ts

Anhui

Nanjing

Hubei

Ya n

gt

se

20

e R.

Shanghai

23

30°

26

R.

24

25

Nanchang

100 km

Jiangxi

East China Sea 25° 110°

115°

120°

125°

FIGURE 14.2  Panel (A) Photograph of the display of the 8-mm wavelength scanning radar at 22.04 h on September 28, 1988 at Jiangpu (near Nanjing) China, showing a dense layer comprising mainly brown planthoppers (Niloparvata lugens) overflying the radar site between 380 and 825 m above ground level. N. lugens comprised 90% of the radar-detectable insects in an aerial netting sample taken from the bottom of this layer. [Radar beam elevation = 44°; distance to outer range ring = 0.75 nautical miles (1390 m)]. (Note: As the radar antenna rotates around the vertical with a selected elevation angle, the beam sweeps through a cone-shaped section of the sky. A horizontal layer is thus detected at the same slant ranges all around the radar and therefore appears as an annulus on the radar display). Panel (B) Radar-derived vertical profiles of insect density during the evening of September 28, 1988 at Jiangpu. The profiles at 17.30 and 18.00 h reflect the mass take-off and ascent of small insects, particularly N. lugens, from around, and a few km upwind of, the radar site. From 19.00 h onwards, the insects were mainly concentrated in a high-altitude layer with a well-defined upper boundary. Densities in the layer were particularly great at c. 21.00–22.00 h, due to the mass overflight of N. lugens from outbreaks extending c. 200 km to the northeast of the radar. (C) Examples of 12-h forward trajectories of N. lugens observed emigrating from around a radar site at Jiangpu on nights in the second half of September 1988. The trajectories are for 18.00 h departures on 17, 20, 23, 24, and 25 September 1988 (at 900 m altitude) and 26 September (at 600 m). The names of provinces are underlined. It can be seen that all-night flights in late September can take migrant planthoppers from southern Jiangsu as far as southern Hubei or northern Jiangxi provinces. Panel (A) from Riley et al. (1991), panel (B) from Riley et al. (1991), and panel (C) from Riley et al. (1994) with permission of the publishers.

814

Plant Virology

II.  ASPECTS OF EPIDEMIOLOGY

A.  Sources of Viral Inoculum

As noted above, the spread of viruses in the field brings together the three entities shown in Figure 14.1. The epidemiology of a virus infection of a field is a result of several biological aspects including sources of the virus, initial spread into the crop, and spread through the crop. Impacting upon these are various physical aspects, such as cultural practices, and meteorological factors.

Sources of virus inoculum can vary according to the climatic zone in which the crop is being grown. In regions where successive plantings of a crop are made throughout the year (e.g., rice under irrigation), a virus can spread from an old crop to a new one. This may also happen where seed crops of the species are grown through the winter and overlap with production crops, or with wheat, where spring and winter crops are grown in the same area. The cultivation cycle of crops in some regions of Europe and North America allows a continuous food source for polyphagous aphids (Figure 14.4). Another example is the substantial increases in the planting of winter oilseed rape in England posing a threat to vegetable crops because of a range of viruses have been identified in these winter crops (Walsh and Tomlinson, 1985). However, in temperate regions, and even in many tropical regions, there is a seasonal cycle of cropping dictated by cold winters, dry hot conditions, and rainfall patterns. Viruses can survive such cold winter periods or a dry summer seasons in various ways. Some have more than one means of survival: (i) many viruses readily survive from season to season in the same host plant or propagation material from it. These include viruses in perennial hosts, in tubers, runners, and so on, and viruses that are transmitted through the seed. Similarly, crops stored overwinter in the field, such as mangolds, may act as a source of both viruses and vectors; (ii) viruses with a wide host range are well adapted to survive, provided their hosts include perennial species, a group of annual species with overlapping growing seasons, or species in which seed transmission occurs; (iii) biennial or perennial wild plants, ornamental trees and shrubs, or weed hosts such as Plantago spp. may be important sources for overwintering or oversummering of many viruses (Hammond, 1982); (iv) leafhopper-transmitted viruses that pass through the egg of the vector may overwinter in the egg, or in young nymphs (Figure 14.5); (v) TMV and a few other viruses can survive through the

FIGURE 14.3  Typical synoptic weather situation transporting aphids, leafhoppers, and other migrant insects northwards in North America in spring and early summer, showing the anticlockwise wind flow around a mid-latitude depression. The shaded area shows the region where lowlevel jets occur. From Johnson (1995) with permission of the publishers.

FIGURE 14.4  Temporal relations between aphid flights and periods of cultivation of various crops. From Robert (1999) with permission of the publishers.

Chapter | 14  Ecology, Epidemiology, and Control of Plant Viruses

815

In many infections of annual crops, and in some cases with perennial crops, by arthropod vectors, there are two phases in the epidemiology or spread of a virus. Primary infections are brought in by winged vectors, or are due to a few plants infected by, say seed transmission, followed by secondary spread from the primary foci which often leads to patches of infected plants within a crop with gradients of infection from the primary foci (Figure 14.6A).

1.  Airborne Vectors

FIGURE 14.5  Survival of maize rough dwarf Fijivirus through the seasonal cycle in northern Italy. Laodelphax stratellus overwinters as a young nymph in diapause. This vector carries the virus through the winter when no known plant hosts are available. The black line and arrows indicate movement of the virus to and from its various hosts. From Conti (1972) with permission of the publishers.

winter under appropriate conditions in plant refuse, and perhaps free in the soil. TMV can also survive in plant litter left in places such as curing sheds. In the past, attention has been focused on virus surviving as free virus particles. However, it is known that many viruses infecting vertebrates may adsorb to inanimate surfaces and survive there (Gerpa, 1984). More attention should be paid to the possible survival of plant viruses adsorbed to minerals. Piazzolla et  al. (1989) have shown that CMV adsorbs readily to montmorillonite (an expandable layer silicate). In this state, it was resistant to inactivation by a strong salt solution; (vi) viruses carried within the resting spores of fungal vectors and in nematodes may survive for long periods in soil.

B.  Initial Spread into the Crop Dispersal of viruses by airborne or soil-inhabiting vectors, by seed and pollen, and over long distances by human activities plays a key role in the ecology and epidemiology of viruses.

Taking plant viruses as a whole, the flying, sap-sucking groups of insect vectors, particularly the aphids, are by far the most important agents of spread and survival. The pattern of spread in the crop and the rate and extent of spread will depend on many factors, including: (i) the source of the inoculum—whether it comes from outside the crop, from diseased individuals within the crop arising from seed transmission or through vegetative propagation, from weeds or other plants within the crop, or from crop debris; (ii) the amount of potential inoculum available; (iii) the nature and habits of the vector, for example, with aphids, whether they are winged transients or colonizers; (iv) whether virus is transmitted in a nonpersistent, semipersistent, or persistent manner by the vector; (v) the time at which vectors become active in relation to the lifetime of the crop; and (vi) weather conditions. Migrant alate aphids that move through the crop early in the year can make a significant contribution to the introduction of primary infections (Doncaster and Gregory, 1948).

2.  Soilborne Viruses a.  Viruses with No Known Vector TMV is one of the few viruses transmitted through the soil to any significant extent without the aid of any known vector. The stability of this virus allows it to survive from season to season in plant remains, provided conditions are suitable. A susceptible crop planted in contaminated soil will become infected, presumably through small wounds made in the roots during transplanting cultivation, or root growth. As shown in Appendix B, members of several virus genera are soil transmitted without any recognized vector. Viruses with no known vectors, such as members of the Potexvirus and Tobamovirus genera, are widespread in soils of forest ecosystems in Germany (Büttner and Nienhaus, 1989). An increasing number of viruses are being found in water (rivers, lakes, etc.) (Section II, E, 6, d) and presumably these could spread to soil. b.  Viruses with Fungal Vectors The initial infection by fungal vectors depends on the way in which the fungus carries the virus (Chapter 12, Section V).

816

Plant Virology

FIGURE 14.6  Panel (A) Aerial view of a sugar beet field with patches of plants infected with virus yellows (BYV and/or BMYV) and gradients of infection spreading from the patches. Panel (B) Aerial view of beet field with patches of plants infected with a nematode-transmitted virus. Panel (C) Relationship between density of nematode infestation and an outbreak of virus disease. Left: Population contours of Xiphinema diversicaudatum. Right: Outbreak of SLRSV in a 10-year-old raspberry plantation. The virus causes a reduction in cane height. Plants were spaced 1.8 m between rows and 9.6 m within rows. Panels (A) and (B) courtesy of Broom’s Barn Research Centre and panel (C) from Taylor and Thomas (1968) with permission of the publishers.

Chapter | 14  Ecology, Epidemiology, and Control of Plant Viruses

Viruses such as SBWMV and PMTV are carried in the resting spores of their plasmodiophoromycete vectors. In these spores, the viruses may survive in air-dried soil or in soil that has been stored for many years. Buildup of infection may take several seasons but once established in a field, viruses with this type of vector may persist for many years even in the absence of suitable plant hosts (Jones and Harrison, 1972). Localized spread of these viruses is by zoospores and resting spores, soil water being a major factor influencing local movement. Viruses with this type of transmission tend to have rather narrow host ranges. Viruses transmitted by Olpidium brassicae, such as TNV, STNV, and CuNV, are carried on the surface of the spores. Zoospores carrying virus probably survive only a few hours. However, virus that is free in the soil may be picked up and transmitted by newly released zoospores. If the soil is moist, Olpidium zoospores can recover TNV from soil for at least 11 weeks (Matthews, 1991). Viruses transmitted by Olpidium do not survive in airdried soil. In general, viruses of this type have wide host ranges and probably survive in the soil by frequent transmission to successive hosts. Drainage water and movement of soil and root fragments are probably important in the spread of these viruses from one site to another. In model experiments in which viruses were added to a soilless recirculating water supply, several viruses, including some such as TMV with no known vectors, were transmitted (Paludan, 1985). Polymyxa betae, the fungal vector of BNYVV, forms very persistent cystosores. These were transmitted to infected soil, and both cystosores and BNYVV could pass through the digestive system of the sheep (Heijbroek, 1988). c.  Viruses with Nematode Vectors The initial infection by viruses with nematode vectors (tobraviruses and nepoviruses) differs considerably from that of viruses with airborne vectors. Nematodes are longlived, may have wide host ranges, and are capable of surviving in adverse conditions and in the absence of host plants for considerable periods. Vector nematodes do not have a resistant resting stage, but can survive adverse soil conditions by movement through the soil profile. As soils become dry in summer or cold in winter, nematodes move to the subsoil and return when conditions are favorable. Some of the viruses (e.g., ArMV) may persist through the winter in the nematode vector. Nematode-transmitted viruses usually have two other characteristics in common—a wide host range, especially among annual weed species, and seed transmission in many of their hosts. Thus, nematode vectors that lose infectivity during the winter may regain it in the spring from germinating infected weeds (Murant and Taylor, 1965). The spread of nematodes in undisturbed soil may be rather slow. Harrison and Winslow (1961) calculated that a population of X. diversicaudatum invaded uncultivated

817

woodland at the rate of about 30 cm per year. Agricultural practices will increase distribution of the vectors during cultivation and probably in drainage or floodwater. Farm workers’ footwear and machinery contaminated with infested soil may transmit nematodes and their associated viruses over both short and long distances (Boag, 1985). However, the pattern of infection observed in a crop may often depend largely on the vector and virus situation in the soil before the crop was planted. In a field already infected with nematodes and planted with a biennial or perennial crop, it may take 1 or 2 years before the initial pattern of infection becomes apparent, since leaf symptoms may not show until about a year after infection. Subsequent spread may give rise to slowly expanding patches of infected plants within the field (Figure 14.6B and C). Individual woody trees or hedges of long-lived woody species have been implicated as a reservoir of vector nematodes (Figure 14.6C). Sometimes such species may harbor a virus as well.

3.  Seed and Pollen Transmission The occurrence of and mechanisms for seed and pollen transmission were discussed in Chapter 12, Sections VII, B and C. These two methods of transmission may be of crucial importance in the ecology and epidemiology of certain viruses. Survival in the seed can be particularly important for viruses that have only annual plants as hosts, and for those that have invertebrate vectors, such as nematodes that normally move only slowly. CMV persists in seeds of Stellaria media buried in soil for at least 12 months (Tomlinson and Walker, 1973). If 107 seeds are present per hectare, with 1% infected with CMV, then a 10% emergence of seedlings would give rise to about one infected seedling per square meter. Under such conditions, a rapid buildup of CMV infection in a crop might result. LMV in lettuce is an outstanding example of the importance of seed transmission in a commercial crop, as is infection of tomato crops with several viruses in Spain (Soler et al., 2010). Seeds are dispersed by birds, wind, water, or by humans. Seed output per plant may be very large for windborne seeds, but wastage is also high. Transmission by pollen may be the major, and perhaps only, method of introduction of certain viruses, for example, PNRSV into a crop.

C.  Spread Through the Crop 1.  Airborne Vectors (reviewed by Fereres and Moreno, 2009; Mazzi and Dorn, 2012) Secondary spread of an arthropod-borne virus may be by winged vectors flying locally between plants or by wingless vectors walking from plant to plant when leaves are in contact. Frequently, secondary spread of viruses with

818

Plant Virology

CABYV

WMV-2

Days after planting: 0

Days after planting: 7

Days after planting: 14

Days after planting: 21

Days after planting: 28

FIGURE 14.7  Comparative spatial spread of two viruses transmitted by aphids either persistently (CABYV) or nonpersistently (WMV-2) in a melon field (Avignon, 1992). Every plant was tested at weekly intervals for infection by CABYV or WMV-2 by ELISA tests. Individual melon plants are represented by white squares, which are shaded when found infected by one of these two viruses. After 4 weeks, most plants were doubly infected. From Lecoq (1999) with permission of the publisher.

non- or semipersistent relationships is by winged vectors on their host-seeking flights, whereas spread of persistent viruses is by insects that colonize that plant species. The size of the largely static populations of aphids that build up on individual plants depends to a great extent on the local weather and other conditions within the crop. Populations can increase at a very rapid rate (about 10-fold in 7 days) and population density may vary widely even in a small region within a crop. When plants within a crop touch each other, apterous aphids can walk from heavily infested to uninfested plants potentially transmitting persistent viruses. To study the importance of aphid migrations early in the season, Heathcote and Broadbent (1961) placed potatoes growing in pots and infected with PLRV or PVY in plots or in the field for successive periods through the season noting aphid numbers and subsequent virus incidence. The viruses spread from the infected plants early in the season

when there were few aphids colonizing plants, but not later in midseason when wingless aphids were numerous. With different viruses, even those transmitted by members of the same group of vectors, rates and patterns of spread in a crop can vary widely. Two different patterns of spread are illustrated in Figure 14.7. A virus brought into a crop from outside by vectors does not necessarily spread from the first infected plant in a crop to other plants. Little spread within the crop may occur if the invasion occurs late in the growing season, or if the presence of the vectors in the crop is very transient. This sort of situation is illustrated by WMV-2 spread in Figure 14.7. This represents part of a melon field that was initially free of WMV2, and was then infected from a source several hundred meters away. The rapid accumulation of CABYV-infected plants (Figure 14.7) shows that plant-to-plant spread within the crop had taken place with this virus.

Chapter | 14  Ecology, Epidemiology, and Control of Plant Viruses

van der Plank (1946) developed a method for testing whether virus was spreading from diseased plants within a crop. It is based on the assumption that virus coming from outside the crop will infect plants at random. On this basis, there will be a certain expectation of the frequency with which infected plants will occur side by side as pairs: p = X [( X !1) / n], where p is the expected number of infected pairs, n is the number of consecutive plants examined, and X is the number of infected plants observed. For high values of n, the standard error of p is √p. If the observed number of pairs (counting three plants together as two pairs) is significantly greater than expected, then spread from infected plants within the field can be assumed. Spread within a crop need not necessarily favor neighboring plants, so that an apparently random distribution cannot exclude the possibility of such spread. The pattern of infection brought about in a field by one vector species may be confused if two forms of the vector are active at the same time, one causing spread to neighbors and the other “jump” transmission to plants at a distance. More sophisticated procedures are now available for analyzing the extent of randomness or clumping (patchiness) in the distribution of infected plants during an epidemic (Madden and Campbell, 1986; Madden et al., 1987a,b). Various kinds of traps have been developed for assessing the number of flying aphids, including yellow pan traps, vertical sticky traps, conical nets, or suction traps. Suction traps are used to provide data for warnings to growers. The horizontal mosaic green pan trap designed by Irwin is proving useful (Irwin and Ruesink, 1986). Different types of traps may give somewhat different answers with different aphid species, and the height at which the traps are set will affect the data obtained. In general, the frequency of flying aphids decreases with increasing height, and relative numbers of vector species caught in traps may not correspond to relative numbers found on the crop (Tatchell et  al., 1988). Furthermore, trapping alone merely gives an estimate of numbers of aphids of various species and the morphs involved and not the numbers actually infective for particular viruses. As noted above, transient winged forms of aphids that do not colonize the crop at all, but move from plant to plant, may be especially important with nonpersistent viruses. Though they may form a small proportion of the total population, they may introduce virus from outside or acquire it from infected plants within the crop and spread it rapidly as they move about seeking suitable food plants. Colonizers will also be important if they move about within the crop. Ideally, from the point of view of virus transmission, we want to know the numbers of infective aphids that are flying and that will land on the crop of interest. Sensitive

819

techniques, such as PCR, can detect virus in individual aphids (Stevens et al., 1997), but even these do not tell us if the aphid is able to transmit the virus. To determine this may be a very tedious and labor-intensive task, especially when nonpersistent viruses are involved. Trapped aphids then have to be placed on healthy test plants as soon as possible after capture. Nevertheless, as they land in a crop, winged aphids can be collected, identified, and tested on appropriate plants to determine whether they are carrying particular viruses. For example, Ashby et  al. (1979) used wind sock traps to assess numbers of viruliferous vectors of subterranean clover red-leaf virus (now known as SbDV). On average over the season 1972–1977, 40–50% of alate Aulacorthum solani (Kltb.) carried this virus. Using similar traps in a potato field, Piron (1986) collected 101 aphid species. Twenty-three species transmitted PVYN, and 22 of these were recorded as new vectors of the virus. This experiment illustrates the fact that a lot more information than presently available may be needed about vectors active in the field in relation to the epidemiology of particular viruses in particular locations. The “infection pressure” to which a crop is subjected can also be assessed by placing sets of bait plants in pots within the field for successive periods of a few days. The sets of plants are then maintained in the greenhouse and observed for infection. Figure 14.8 illustrates such a trial in relation to the prevalence of potential vector species. The frequency with which aphids were trapped clearly implicates the early flights of Cavariella aegopodii as being of prime importance in the spread of PVY in this particular field and season. Measurement of vector activity has been discussed by Irwin and Ruesink (1986). If particular virus strains are of interest it is important to know whether the bait plant being used is preferentially infected by one out of two or more stains that are present or is particularly attractive to the vector (Marrou et al., 1979). Most of the preceding discussion has been concerned with variation in the number of plants infected with a virus. In addition to this aspect, the severity of the disease in individual plants may be substantially increased by an increased dose of virus provided by numerous aphids (Smith, 1967). Disease is also generally more severe when younger plants are infected. The number of aphid species known to transmit different viruses varies widely. For example, SCV has two vector species, while more than 60 vector species have been recorded for CMV. The fact that the majority of epidemiological studies have been carried out on aphid-borne viruses reflects the importance of this group of vectors. Other groups of airborne vectors such as hoppers and beetles are, of course, also of crucial importance in both the epidemiology and ecology of the viruses they transmit. Beetles may differ from aphids and hoppers in the pattern of virus incidence they bring about. For example, flea beetles differ significantly

820

Plant Virology

100

1000

50

500

May

June

July

Number of aphids

Percent infected tobaccos

1500

August

FIGURE 14.8  Infection pressure of PVY in a field of potatoes. Batches of 100 tobacco plants in pots were set out in the field for 7 days. The left-hand axis and the solid line show the percentage of these plants that subsequently developed infection with PVY in the greenhouse. The number of aphids of three species trapped each week is given by the axis on the right. o-o, PVYN in tobacco in percentage; —, Myzus persicae; ---, Rhopalosiphum padi; and ⚬, Cavariella aegopodii. From van Hoof (1977) with permission of the publisher.

growing adjacent to a block of plants infected mechanically with the virus. The initially healthy field was divided into strips parallel to the block of infected plants. A strong gradient of infection developed in the field (Markham and Smith, 1949). Similar gradients of infection have been observed for spread by aphids under some conditions.

11 10 9

Percentage infection

8 7

2.  Contact-Transmitted Viruses

6 5 4 3 2 1 0

1 2 3 4 5 6 7 8 9 10 11 12 13 14

Strip no. FIGURE 14.9  Gradient of infection due to spread by flea beetles. Percentage infection in each strip of plants is plotted against distance from the source of infection, which was next to strip no. 1. Natural spread of TYMV in turnips. Each strip was 2 m wide. From Markham and Smith (1949) with permission of the publisher.

from the aphids in their patterns of movement within a crop. They are generally much more active than aphids and tend to move from plant to plant over short distances much more frequently than wingless aphids, but they do not usually travel as far as winged forms. Figure 14.9 shows the pattern of spread of TYMV by flea beetles in a field of turnips

Compared to transmission by invertebrate vectors or vegetative propagation, field spread by contact transmission is usually of minor importance. However, with some viruses it is of considerable practical significance. TMV can readily contaminate hands, clothing, and implements and be spread by workers and, for instance, birds, in tobacco and tomato crops (Broadbent, 1963, 1965; Broadbent and Fletcher, 1963). This is particularly important during the early growth of the crop, for example, during the setting out of plants. Plants infected early act as sources of infection for further spread either during cultural operations as disbudding or by rubbing together of healthy and infected leaves by wind. TMV may be spread mechanically by tobacco smokers, because the virus is commonly present in processed tobacco leaf. For example, all 37 brands of cigarette sold in Germany contained TMV (Wetter, 1975) and in 60 out of 64 pipe-smoking tobaccos (Broadbent, 1962). PVX can also be readily transmitted by contaminated implements or machines and by workers or animals that have been in contact with diseased plants (Todd, 1958). On some materials, the virus persists for several weeks. PVX can also spread either by direct leaf contact between neighboring plants (Clinch et  al., 1938) or between neighbors

Chapter | 14  Ecology, Epidemiology, and Control of Plant Viruses

when leaves are not in contact. This has been assumed to be due to mechanical inoculation by contact between roots, but a soil-inhabiting vector has not been excluded. Some viruses of fruit trees have been shown to be spread in orchards by cutting tools (Wutscher and Shull, 1975). Some other viruses that reach high concentrations are transmitted during cultivation. For example, RCMV can be readily transmitted by mowing machines (Rydén and Gerhardson, 1978) and SCMoV by heavy tramping by livestock and by crushing infected plants under vehicle wheels (Jones, 2004). RYMV is transmitted through the dung of cattle and donkeys fed on infected rice stubble which is then put on seedbeds and through leaf contact when transplanting from seedbeds (reviewed by Traoré et  al., 2009). On the other hand, Heard and Chapman (1986) concluded that in mown ryegrass swards most of the local spread of RGMV was due to transmission by mites rather than the mowing operation though the mowing may disturb the mites.

3.  Viruses with Fungal and Nematode Vectors As noted above, fungal and nematode vectors move very slowly in the soil. Most of the transmission in a crop is by other means such as crop roots growing toward the vector and soil cultivation moving the vector around which gives characteristic “kite marks” of infection pattern (Figure 14.6B).

4.  Seed and Pollen Transmission The movement of seed is usually not a factor in the secondary spread of viruses. Transmission by pollen may be involved in secondary spread, and is perhaps a major method of natural spread in the field for certain viruses, e.g., PNRSV. On the other hand, pollen dispersal is probably of little or no ecological significance when the host plant is mainly or entirely self-pollinated, e.g., barley. However, Shepherd (1972) pointed out that some barley varieties produce large amounts of pollen which, if infected with BSMV, could lead to mechanical transmission by abrasion between leaves. SoMV can be mechanically transmitted by pollen from infected plants (Francki and Miles, 1985); infestation with thrips can cause the mechanical damage that effects this pollen transmission (Hardy and Teakle, 1992).

D.  Cultural Practices The way a particular crop is grown and cultivated in a particular locality and the ways land is used through the year in the area may have a marked effect on the incidence of a virus disease in the crop. This may, of course, offer the opportunity to prevent infection by appropriate cultural practices. Many diverse situations arise. The impact of various cultural practices on the epidemiology (and ecology)

821

of the virus infection of a plant species can be on the host, the vector, and on the virus–vector interactions. These can be varied and complex and some examples that illustrate the kinds of factors involved are given below.

1.  Cropping System a. Monocropping Cultivation of a single crop, or at least a very dominant crop, over a wide area continuously for many years may lead to major epidemics of virus disease, especially if an airborne vector is involved. The development of such an epidemic is shown in Figure 14.10. Soilborne vectors may also be important from this point of view, for example, with GFLV in vineyards, where the vines are cropped for many years. Monocropping may also lead to a buildup of crop debris and the proliferation of weeds that become associated with the particular crop. As pointed out by Diener (1987), most viroid diseases in crops have appeared only in recent decades. He suggested that viroids themselves have existed for a very long period in wild host species, causing little disease there and escaping from time to time into agricultural crops that were grown on a small scale with varying genetic composition of the crop plants. Under these conditions, they would cause no widespread disease. However, with the advent of modern large-scale monocultures of genetically uniform plants, the opportunities for serious outbreaks of viroid diseases have greatly increased. This is particularly so with crops such as chrysanthemums, where propagation of vegetative stocks may be highly centralized. An outstanding example of the effects of monocropping is the rise in importance of certain virus diseases of rice and of their hopper vectors as a consequence of the “Green Revolution” that began in the middle of the twentieth century. New rice varieties introduced as part of the green revolution in tropical and subtropical areas are a major factor in the greatly improved yields that have been achieved. However, the gains have been seriously impaired by the increased prevalence of several serious virus diseases of rice, and also of their hopper vectors (Thresh, 1988, 2008). Important examples are RGSV and RRSV and their rice brown planthopper vector (BPH) (Nilaparvata lugens) (Thresh, 1989). As well as transmitting these viruses, the BPH can itself cause serious crop damage. The first new rice cultivars released during 1966–1971 were all susceptible to both vector and RGSV. Effective sources of resistance to both were found and incorporated into new varieties that were released in 1974–1975. These were at first grown widely and successfully in the Philippines, Indonesia, and elsewhere. However, severe infestations with the BPH were reported within 2–3 years, and in 1982–1983, a resistance-breaking strain of RGSV was reported. No new source of virus

822

Plant Virology

Coral Sea 79 78 77 76 75 74 80 Bundaberg 10 km

Limit of cane growing

FIGURE 14.10  Development of an epidemic of planthopper-transmitted virus disease in sugarcane over 7 years. The incidence of Fiji disease Fijivirus in the Bundaberg district of Queensland, Australia, 1974–1980. Disease contours indicate the boundary of the area with an average of at least 1% affected cane. The solid line is the outer limit of the main cane-growing area. Modified from Egan and Hall (1983) and used with permission of the publisher.

resistance has been found. Some further forms of resistance to the four known biotypes of the BPH have potential for breeding programs (Wang et al., 2012). Even within one country, the viruses infecting a particular host plant may well be influenced by a new development in agricultural practice. For example, Solanum laciniatum, an indigenous plant in New Zealand, had no virus infections recorded from natural habitats. Shortly after commercial plantings were begun, field infections with PVX, PVY, TMV, and CMV were recorded (Thomson, 1976). b.  Crop Rotation The kind of crop rotation practiced may have a marked effect on the incidence of viruses that can survive the winter in weeds or volunteer plants. With certain crops, volunteer plants that can carry viruses may survive in high numbers for considerable periods. Doncaster and Gregory (1948) showed that it may take 5 or 6 years to eliminate volunteer potatoes from a field in which potatoes had been grown. For a crop such as carrots, fields for seed production (carrot is a biennial) and for root production together with volunteer plants may form a continuous yearly cycle

enabling viruses to be perpetuated (Howell and Mink, 1977). The importance of volunteer plants in the spread of beet viruses is illustrated in Figure 14.11. With perennial crops, virus incidence will tend to increase as the crop ages. c.  Field Size The influence of the size of field on the spread of a virus will depend to a great extent on the source of initial infection. If virus is coming from outside the crop, then, as pointed out by van der Plank (1948), concentration of the crop into large fields of compact shape will reduce infection from outside the crop to a minimum. For example, this situation has been shown to occur with AMV in Lucerne (alfalfa) (Gibbs, 1962).

2.  Planting System a.  Planting Date The date of planting controls the stage of growth of the crop at the time that aerial vectors arrive thus influencing the attractiveness of the plants to the vector on host searching flights and also the susceptibility of the plants with younger plants tending to be more susceptible. Also, if

823

Chapter | 14  Ecology, Epidemiology, and Control of Plant Viruses

80

1968 yellows

1968 mosaic

Disease incidence (%)

60 40 20

80

1969

1969

60 40 20

M

J

J

A

S

M

J

J

A

S

Month FIGURE 14.11  The relationship between volunteer sugar beets and the occurrence of beet mosaic Potyvirus and beet western yellows Luteovirus in beet fields in Washington State during 1968 and 1969. ○, fields containing volunteer plants; ●, fields adjacent to volunteer plants; □, fields at least 1 mile from known volunteer plants. From Howell and Mink (1971) with permission of the publishers.

the newly sown crop overlaps the maturing crop, virus can spread from the latter. A clear-cut example of the way time of sowing seed affects virus incidence occurs with the winter wheat crop in southern Alberta. In a normal season, the percentage infection with WSMV is markedly dependent on the time at which the seed is sown (Slykhuis et  al., 1957). For sowing dates earlier than September, the springsown crop, carrying disease, overlaps with the autumn-sown crop. High air temperatures may cause a dramatic reduction in some aphid vector populations. Changes in planting practice that provide an overwintering crop may cause an increased virus incidence. Thus, the increased incidence of BaYMV in the United Kingdom has been attributed, in part, to the growing of winter malting barley as a profitable spring crop, leading to increased perpetuation of the virus through its fungal vector (Coutts, 1986). The increase in BaYMV has also been associated with a switch from spring-sown to autumn-sown barley in various parts of the United Kingdom. In Washington State, the highest incidence of BYDV in winter wheat crops occurred in irrigated areas that supported aphid vectors during the summer, and with early planting dates (Wyatt et al., 1988). Planting date is also important in tropical situations. For example, from studies on planting dates of rice in Maros and Lanrang (Indonesia) for 7 years, Manwan et al., (1987) identified the best time to plant to avoid tungro virus disease. These were based on the times that the leafhopper vector populations were low and climatic conditions were suitable for planting rice.

In tropical African countries, groundnuts are traditionally sown at the start of the main rainy season which is controlled by the Intertropical Convergence Zone (ITCZ). The ITCZ is a band of upwelling moist air near the equator which moves with the seasons to the north and south. Thus there is band of sowing of groundnuts moving from northern countries (e.g., Uganda) to southern countries (e.g., South Africa) and back again through the year. It is most likely that virus diseases such as groundnut rosette and its aphid vector move from country to country in parallel with the crop development (Hull, personal observation). b.  Population Density and Plant Size Airborne vectors bringing a virus into a crop from outside will infect a greater proportion of the plants in a given area when they are widely spaced than when they are close together. For example, the incidence of beet yellows was reduced where the distances between plants or between rows were reduced (Blencowe and Tinsley, 1951). Crop spacing may affect the landing response of flying aphids. Closely spaced groundnuts are not visited by alate Aphis craccivora as frequently as widely spaced plants (Hull, 1964). The frequency of alates being found in the crop decreases significantly after the plants had met within and between rows. Some species are trapped more frequently over widely spaced crops of cocksfoot and kale (A’Brook, 1973). Large plants in a crop might be expected to become infected more readily with insect-borne viruses than small ones, since they are more likely to be visited by a vector.

824

Plant Virology

Broadbent (1957) found that this held in cauliflower seedbeds. In 1 year, 30% of large seedlings 15% of mediumsized seedlings, and 5% of small seedlings were infected with CaMV.

cherry orchard is caused by the practice of moving commercial beehives directly from earlier blooming orchards.

3. Cultivation

Plant nurseries, especially where they have been used for some years, may act for themselves as important sources of virus infection. For example, Hampton (1988) found in several US states no evidence of infection in wild Humulus lupulus plants tested for two ilarviruses and three carlaviruses common in cultivated hops, and in particular AHLV. Several hundred hop plants, primarily from breeding nurseries in Oregon, had substantial infection rates with these viruses. Fifty-three non-Humulus species growing around infected hop yards and nurseries were found to be free of AHLV. Thus, the commercial yards and nurseries appeared to be the only source of infection for this virus. Nursery beds for transplanted rice can be important in the epidemiology of rice tungro disease. The young plants are very susceptible to virus infection and furthermore, the process of uprooting the plants and transplanting them disturbs the leafhopper vectors, which will move to other plants (Mukhopadhyay and Chowdhury, 1973; Chancellor et al., 2006).

a.  Soil Cultivation Soil cultivation practices may affect the spread and survival of viruses in the soil or in plant remains. Nematode and fungal vectors may be spread by movement of soil during cultivation. The extent to which soil is aerated and kept moist may affect the survival of TMV in plant remains. Cultivation during frosty weather of fields previously cropped in potatoes may greatly reduce the survival of volunteer potato plants (Doncaster and Gregory, 1948). It has been thought that BNYVV was spread at a significant level by irrigation. However, a comparison of the spread of the virus by irrigation with spread by the physical movement of soil tillage and harvesting operations showed that the latter is the major means of spread of the virus from a point source (Harveson et al., 1996). b.  General Cultivation As noted in Section II, C, 2, some viruses can be transmitted mechanically say by handling plants, by farm animals, and on farm machinery.

4.  Effects of Greenhouses It might be expected that the use of greenhouses and polythene tunnels would favor the survival of a stable virus such as TMV, since the structures remain at one site and are in use for intensive cultivation. On the other hand, they might provide some protection against aphid-borne viruses. Thus, Conti and Masenga (1977) reported that in the Piedmont, in pepper crops under plastic tunnels, 84% of virus-infected plants contained TMV; the remaining 16% were infected with aphid-borne viruses. By contrast, 88% of virus-infected pepper plants grown outdoors were infected by viruses transmitted by aphids in a nonpersistent manner. Greenhouses are normally used in regions with cool winters and will therefore favor the introduction of viruses more adapted to tropical and subtropical climates, such as with TSWV.

6.  Nurseries and Production Fields as Sources of Infection

7.  Movement of Crop Plants into New Areas As well as distributing viruses around the world (Section II, E, 6, a), humans have moved crop species to new countries, often with disastrous consequences as far as virus infection is concerned. Plant species that were relatively virus-free in their native land may become infected with viruses that have long been present in the countries to which they were moved for commercial purposes. It is often difficult to prove a sequence of events of this sort, especially if the movement took place before virologists could investigate and record events. Thresh (1980) documents several instances such as CSSV mentioned above (Section I, A, 1, e, iii). Movement of plant species between countries and continents has been carried out with increasing frequency during the last two centuries. Agriculture in India, North America, and Australia is almost totally dependent on introduced crop plants (Thresh, 1980). Thus, there has been ample opportunity for events such as that outlined for cacao to occur. Many cases of the rapid increase of begomoviruses in crops introduced into tropical countries probably arise from indigenous viruses.

5.  Pollination Practices The horticultural practice of planting mixtures of varieties or pollinators in orchards may favor the spread of pollenborne viruses. Howell and Mink (1988) present circumstantial evidence suggesting that the annual appearance of new sites of infection with pollen-borne PNRSV in a sweet

E.  Physical Aspects 1. Rainfall Rainfall may influence both airborne and soilborne virus vectors. The timing and extent of rainfall may alter the

825

Chapter | 14  Ecology, Epidemiology, and Control of Plant Viruses

Windward

Percentage catch per aphid species

100

Leeward

80

60

40

20

0

R. maidis

R. padi

A. spiraecola

FIGURE 14.12  Variation in flying direction by different aphid species under low wind velocities. The percentage catch of selected aphid species on the windward and leeward sides of a sticky cylinder set vertically just above a soybean canopy, Urbana, IL, USA, 1978. Modified from Irwin and Ruesink (1986) with permission of the publishers.

influence it has on vector populations. For example, some rainfall or high humidity is necessary for the buildup of whitefly populations, while continuous heavy rainfall may be a factor in reducing the size of such populations (Vetten and Allen, 1983). Similarly, heavy rainfall just after airborne aphids have arrived in a crop may kill many potential vectors, thus reducing subsequent virus incidence (Wallin and Loonan, 1971). PMTV has its highest incidence in Scotland in areas with the highest rainfall (Cooper and Harrison, 1973), which is correlated with increased incidence of the fungal vector (Spongospora subterranea) in wetter soils. Similarly, in Peru this virus is widely distributed in Solanum spp. in the highlands of the Andes, where rainfall and temperature favor the fungal vector (Salazar and Jones, 1975). Symptoms of the virus were not seen in plantings in the dry coastal region. The effect of seasonality of rainfall on cropping is discussed in Section II, D, 2, a.

2. Wind Wind may be an important factor not only in assisting or inhibiting spread of viruses by airborne vectors and pollen, but also in determining the predominant direction of spread both over long distance (Figure 14.2C) and locally. Windbreaks may affect the local incidence of vectors and viruses in complex ways (Lewis and Dibley, 1970). Winged aphids tend not to fly when wind speed is too great, although their direction of flight can be influenced by the prevailing wind. At low wind speeds, some species may fly with the wind and others against it (Figure 14.12). Freak wind conditions may cause annual epidemics. In 1977, there was a massive and unexpected epidemic

of MDMV in the corn crop of the northern US state of Minnesota. This virus had been usually confined to southern states. From studies of the continental weather patterns in 1977 and from the fact that aphid vectors could retain the virus for more than 19 h, Zeyen et al. (1987) proposed that low-level jet winds (Figure 14.3) rapidly transported infective aphid vectors from drought-stricken southern areas north to Minnesota. The direction of movement of leafhoppers may also be markedly influenced by wind speed and direction. The beet hopper C. tenellus cannot make progress against a headwind stronger than about 3 km/h. Movement of whiteflies is also substantially influenced by wind (Figure 14.13). Mealybugs, which transmit swollen shoot disease of cacao, are relatively inactive and move only short distances on the plant, although they are carried about by ants. The young stages may, however, be carried some distance by wind. The spread of BRV by its gall mite vector (Phytoptus ribis) is influenced to a substantial extent by the prevailing wind over distances of about 15 m from infected plants. However, other factors, such as air turbulence caused by nearby buildings and trees, may influence the passive movement of this vector and spread of the virus (Thresh, 1966). With certain climates and soil types, nematodes of many genera may also be passively carried in wind-borne dust (Orr and Newton, 1971). However, virus vector species have not yet been identified in such dust. Wind can also cause abrasive contact between leaves of plants and has been suggested as being involved in the spread of RYMV (Sarra et al., 2004). On a smaller scale, wind might move plant signals of herbivore and pathogen attack (see Chapter  12, Section II, A, 2, c, i) from an affected plant to adjacent ones thus influencing local spread of a virus.

826

Plant Virology

100 80 100

60

80

40

60

20

40 20 0

0

S

E N

W

FIGURE 14.13  The effect of wind direction on the incidence of ACMV infection in a 0.8-ha field of cassava surrounded by a sugarcane windbreak at a coastal site in the Côte d’Ivoire. 0–100 = percentage infection in each block of plants. Wind frequency and direction are indicated by the length of the lines to the right of the block graph. The pattern of catch of whitefly vectors (Bemisia) was very similar to that shown for virus incidence. From Fargette et al. (1985) with permission of the publisher.

3.  Air Temperature Air temperature may have marked effects on the rate of multiplication and movement of airborne virus vectors. For example, winged aphids tend to fly only when conditions are reasonably warm. However, very high temperatures may be particularly effective in reducing certain aphid populations. Exposure of the planthopper vector of MRDV to 36°C prevents virus replication in the vector and suppresses transmission (Klein and Harpaz, 1970).

4. Soil Conditions in the soil can influence the incidence of virus disease in various ways. Highly fertile soils tend to increase the incidence of virus disease. For example, animal manure and several inorganic fertilizers increase the incidence of leaf roll and rugose mosaic diseases in potato crops (Broadbent et al., 1952). Some species of aphid vectors also multiply faster on such plants. Plant nutrition may also influence the apparent amount of virus infection by accentuating or suppressing symptom expression. Soil conditions can have a marked effect on the survival of TMV in plant debris. Moist well-aerated soils favor inactivation of the virus compared with dry, compacted, or waterlogged soils (Johnson and Ogden, 1929). Soil temperature may have a marked effect on the transmission of viruses by nematodes. The optimum temperature and temperature range may vary with different viruses, hosts, and nematode species (Cooper and Harrison, 1973; Douthit and McGuire, 1975). However, in spite of seasonal fluctuations in temperature, populations of nematodes in the field may remain quite stable

for years. WSSMV in Canada is transmitted by its fungal vector with an optimal soil temperature of 10°C (Slykhuis, 1974). This may be a geographical adaptation since SBWMV from Illinois develops optimally at about 16°C. The physical soil type may also affect vector distribution, and thus the incidence of viral disease. Nepoviruses predominate in cruciferous species on light soils in Germany (Shukla and Schmelzer, 1975). In Scotland, TRV in potatoes is found in freely draining podsols but not in heavy, badly drained soils (Cooper, 1971). Soil type may influence virus incidence in yet another way—by the extent to which moisture is retained. For example, in Tasmania, BYDV infection is consistently higher in pastures on heavier soils, probably because plant growth is better on such soils under drought conditions (Guy, 1988).

5.  Seasonal Variation in Weather and the Development of Epidemics The wide annual variation that can occur in the incidence of virus disease in an annual crop is shown in Figure 14.14 for beet yellowing viruses in sugar beet. Factors that might be involved are early migration of M. persicae for subsequent disease spread, extent of infection in nearby seed crops and continuing effects of weather conditions on the aphid vector population through most of the season, affecting timing and size of early migrations into the crop, buildup of population within the crop, and the mobility of this population. A sequence of unusual weather conditions can lead to a severe outbreak of a disease that is normally present at fairly low levels in a crop in a particular region each year. The history of a severe epidemic of WSMV that developed

827

Chapter | 14  Ecology, Epidemiology, and Control of Plant Viruses

West 40

East

North

1972

1972

1972

1974

1974

1974

1976

1976

20 0

Infection (percent)

100 80 60 40 20 0

60

1976

40 20 0

June July

Aug Sept

June July

Aug Sept

June July

Aug Sept

FIGURE 14.14  Variation in virus incidence with year and location. Mean monthly incidence of sugar beet yellows disease in different regions of England in years with greatly differing amounts of spread. Data supplied by G.D. Heathcote (Broom’s Barn Experimental Station) for representative crops sown annually in March or April in eastern England (Suffolk, Essex, and Cambridgeshire), in wetter areas to the west (Shropshire and Worcestershire), and in cooler areas to the north (Yorkshire). The dashed lines indicate the mean incidence of yellows at the end of September as calculated for the entire English crop. From Thresh (1983) with permission of the publisher.

in southern Alberta in the autumn of 1963 will serve to illustrate the kinds of interactions involved. Winter wheat is normally sown in the first 2 weeks of September; this sowing date normally allows the crop to escape infection from maturing spring-sown wheat. In 1963, an unusual sequence of weather conditions prevailed (Atkinson and Slykhuis, 1963). Spring rainfall was much below normal, crops of spring-sown grain were sparse, and not much seed germinated. This situation was suddenly changed in late June by very heavy rains. In the area that had previously suffered from drought, seed of spring wheat and barley that had lain dormant germinated, now about a month late, and previously stunted plants tillered profusely. Above normal rainfall in June and July assured further vigorous development of the crop and, by reducing the effectiveness of summer fallow operations, allowed extensive and profuse development of volunteer wheat. In this zone, where spring rainfall had been low, extensive acreages of wheat and barley did not mature until late September. The late-developing wheat and barley crops became massive reservoirs of inoculum for the virus and for its mite vector. Winter wheat sown at the normally recommended

time in the first 2 weeks of September then became heavily infected. The autumn weather was also abnormal and facilitated massive spread of virus by the mite. The mean September temperature was 62°F (10° above the 30-year average). These unusually high temperatures continued well into October. The 1964 season was not conducive to spread of the virus, but because of the very extensive spread that had occurred in the winter wheat before the freeze in 1963, very large acreages of grain were lost. The distribution of this epidemic outbreak in 1964 showed a clear relationship with the lack of spring rainfall in 1963 (Atkinson and Grant, 1967).

6.  Dispersal over Long Distances a.  Human Dispersal Even in countries that have had a highly developed agricultural technology for some time, it may be very difficult or impossible to document the arrival and spread of particular viruses. However, it is widely accepted that over the past few centuries, humans have been mainly responsible for the wide distribution around the world of many

828

70 19

viruses that were previously localized in one or a few geographical areas. Viruses have been transported in plants or plant parts and perhaps occasionally in invertebrate vectors. There is little doubt that many of the virus diseases of potato and some of their vectors were brought to Europe with the potato from America and have since been spread to many other countries in tubers (Jones and Harrison, 1972). For example, based on a phylogenetic analysis, it is suggested that PVX isolates spread to China from different sources, one from Europe and another from Asia (Yu et al., 2010). LMV, because it is seed transmitted, has probably been distributed wherever this crop is grown. The fact that TMV can survive in infectious form in prepared smoking tobacco is probably sufficient to account for its presence wherever tobacco is grown commercially. The spread of some viruses may be a more complex problem, involving the necessity for spread of a suitable invertebrate or fungal vector as well as the virus and appropriate host plants. For example, Raski and Hewitt (1963) consider that humans have been largely responsible for the dispersal of GFLV (and its nematode vector) around the world as grape vines (together with soil) were taken from place to place. In relation to worldwide dispersal of viruses, New Zealand is an interesting example, since it is geographically perhaps the most isolated of the countries that have a diverse and modern agriculture and horticulture. Polynesian immigrants introduced a few food plants, for example, taro (Colocasia esculenta) and kumara (Ipomea batatas). Over the past 170 years or so, European immigrants have introduced a wide range of agricultural and horticultural crop plants, together with a large selection of weed species. By 1990, 139 viruses had been recorded in the country, all present in introduced species. These have almost all been identified as viruses occurring elsewhere, mainly Europe or North America, with a few from Australia. It is easy to see how most of these could have arrived in tubers, corms, runners, rootstocks, seed, and so on. For example, 38 of the 139 viruses infect vegetatively propagated fruit trees and vines. Most of the vectors for these viruses are introduced species of aphids. New Zealand is very deficient in endemic aphids, their place in the fauna being taken by Psyllidae. It is a curious fact that no viruses with leafhopper vectors are yet known in New Zealand, although representatives of some potential vector genera occur. There are other examples where the effects of human activities can be more precisely dated. PPV infects Prunus spp. and is transmitted in a nonpersistent manner by aphids. The disease was reported first in Bulgaria in 1915. It has since spread through Europe as indicated in Figure 14.15. Aphids spread the virus to nearby orchards. Long-distance spreading is most probably by means of vegetative plant material distributed by humans (Walkey, 1985).

Plant Virology

1964

1967 1965 1956 1970 1984

1961

1966

52 67 61 1948 1964 1941 1935 1915 67

1968

FIGURE 14.15  First reports of plum pox Potyvirus in Europe and western Asia. Dates signify the year the virus was first recorded. Courtesy of J.M. Thresh.

The more recent movements of BNYVV, which causes the important rhizomania disease in sugar beet, and of tomato yellow leaf curl viruses are summarized in Box 14.1. A virus arriving in a new environment may sometimes find conditions suitable for very rapid spread. Stubbs (1956) pointed out that carrot motley dwarf virus disease spread very rapidly in Australia, where the aphid vector Cavariella aegopodii was already plentiful as an introduced species which lacked natural enemies. By contrast, spread was slow in California, where the aphid vector was heavily parasitized. Human activities may spread both virus and vector within a country. For example, soils of nurseries in southern England frequently contain nepoviruses and their vectors, which can be transported with the host plants, especially if the infection is latent (Sweet, 1975). b.  Airborne Vectors The long-distance movement of arthropod vectors is discussed in Section I, C. The movement of pollen by wind is usually to much shorter distances, but that by insects can potentially be over several or many kilometers. Seedtransmitted viruses might be transported over considerable distances by birds, but there is no documented example. Proctor (1968) has shown that viable seeds may persist in the alimentary tract of migratory seabirds for as long as 340 h, long enough to be transported several thousand kilometers. c.  Vectors of Soilborne Viruses The movement of nematodes and soil fungi is described in Section II, B, 2, b and c.

Chapter | 14  Ecology, Epidemiology, and Control of Plant Viruses

BOX 14.1  Spread of Viruses by Humans This box gives two examples of the recent spread of viruses by humans—that of tomato yellow leaf curl disease which is resulting in the evolution of new viruses and that of BNYVV, causing an important disease of sugar beet. The Andean region of South America is the center of domestication of tomato (Lycopersicon esculentum) and the crop was introduced to the Mediterranean region in the post-Colombian era. TYLCV-I is indigenous to the eastern Mediterranean region and it first encountered tomato after this crop was introduced there. From there the disease has spread initially through the Mediterranean basin (Figure 14.16A) and then worldwide (Figure 14.16B) together with the B biotype of its whitefly vector, Bemisia tabaci (reviewed by Jones, 2009).

In the course of its movement it has recombined and evolved into new viruses. Three viruses are currently known to cause the disease, Tomato yellow leaf curl virus (TYLCV), Tomato yellow leaf curl Sardinia virus (TYLCSV), and Tomato yellow leaf curl Sudan virus (TYLCSDV); these viruses are all begomoviruses but differ in sequence. Various recombinants have now been detected between these viruses. For example, TYLCV has recombined with TYLCSV to give a new virus, Tomato yellow leaf curl Malaga virus, which has subsequently recombined with TYLCSDV and also formed further recombinants with its parents. Both TYLCV and TYLCSV have also recombined with TYLCSDV. Thus, there is rapid variation in this group of viruses.

(A)

(B)

FIGURE 14.16  Spread of tomato yellow leaf curl viruses. Panel (A) Origin in the East Mediterranean and spread through the Mediterranean basin. Dates are of the first records in individual countries. Panel (B) Spread from the Mediterranean basin (indicated by red box) to other countries worldwide.

829

830

Plant Virology

BNYVV is another example of the rapid spread of a virus through human activities, especially trade. Figure 14.17 illustrates the spread of the virus from early reports in Italy in the 1950s.

In this case much of the spread was through soil containing the virus and its vector, Polymyxa betae, which contaminated transported commodities such as potatoes.

FIGURE 14.17  Spread of beet rhizomania caused by Beet necrotic yellow vein virus through Europe and worldwide. Data courtesy Dr. M. Stevens (Broom’s Barn Experimental Station).

d.  Water Dispersal Over many years, methods have been developed for screening water for the presence of human and animal viruses. These have also been applied to a search for waterborne plant viruses, especially in Europe, with some surprising results. The work has been reviewed by Koenig (1986). Most sampling has been done in rivers and lakes. Infectious viruses isolated from such waters include TMV, CGMV, and other tobamoviruses; a potexvirus; TNV and STNV; TBSV, CIRV, and other tombusviruses; CarMV; CMV; and CRSV. In addition, CarMV was isolated from Baltic Sea water (Kontzog et  al., 1988). New tombusviruses were isolated from surface waters in Germany and New Zealand (Koenig et al., 2004; Mukherjee et al., 2012).

Many of these viruses share several properties. Most of them are very stable and lack airborne vectors that would allow spread over long distances. They occur in high concentrations in infected plants and are released from infected roots and can infect roots without vectors. Many have a wide host range. Most of the infectious virus probably moves in water while adsorbed onto organic and inorganic colloidal particles, especially clays (Koenig, 1986). In this state, they would be substantially more resistant to inactivation than as free virus. The viruses found in water originate by release of virus from living roots, or from decaying plant material, or from sewage. Tomlinson and Faithfull (1984) isolated TBSV from waters of the River Thames in England. This virus and

Chapter | 14  Ecology, Epidemiology, and Control of Plant Viruses

others were isolated from a large number of tomato plants growing in semisolid or dried sludge in the primary settlement beds of various sewage works. They concluded that these tomato plants and at least some of the viruses were derived from infected tomatoes eaten raw by humans. It is known that TBSV can pass in an infectious state through the human alimentary tract (Tomlinson et al., 1982). CRSV was isolated from water of a canal near a sewage works in northern Germany, again implicating sewage in possible long-distance dissemination (Koenig et  al., 1988). These waterborne viruses may be a factor in the forest decline occurring in Europe, but further research is needed on this question (Koenig, 1986; Büttner et al., 1987). Viruses (TMV and PepMV) have been found in closed recycling hydroponic systems (Park et al., 1999; Schwartz et al., 2010). As Olpidium is also found in hydroponic systems (Schnitzler, 2004), it is likely that viruses transmitted by this fungus can be transmitted in such systems.

F.  Disease Forecasting An understanding of the epidemiology and ecology of some major crop virus diseases has led to procedures for forecasting potential epidemics. This is very useful in implementing control measures (Section III). There are three main approaches to forecasting—predicting the onset of a disease, monitoring the progress of a disease, and developing mathematical models.

1.  Data Acquisition To be able to predict and monitor virus diseases, it is important to have reliable sources of information. Much information comes from field observations by extension services and from monitoring vector movement (Sections II, B, 1 and II, C, 1). Many large-scale farmers routinely monitor their crops and apply control measures at an appropriate time. However, as virus diseases take several days or even weeks to show symptoms after infection, the application of control measures based on symptom appearance can be too late. It also depends on the correct diagnosis of the disease and knowledge of how it is spread. Remote sensing is being increasingly used to detect early stages of epidemics. Remotely sensed multispectral reflectance, based on the reflectivity and propagation of light radiation inside plant tissues can indicate early stages of infection or latent infection by some viruses (Steddom et al., 2003; Chavez et al., 2009; Grisham et al., 2010). Foci of infection can be detected by aerial photography and from satellites using direct colors (Figure 14.6B) or changes in reflectance in certain parts of the spectrum (Gaborjanyi et al., 2003; Mirik et al., 2011). Molecular studies of viruses, and especially those using new sequencing techniques (e.g., pyrosequencing) are throwing light on both the ecology and epidemiology

831

of plant viruses (Fargette et al., 2006; Garrett et al., 2006; Traoré et  al., 2009; Roossinck et  al., 2010). However, as pointed out by Duffy and Seah (2010) care must be taken in using sequence data in plant virus epidemiology. Meta-analysis is the analysis of results of multiple studies and can be used for evidence synthesis in plant pathology. Madden and Paul (2011) review meta-analysis noting the advantages and potential problems of this approach.

2.  Mathematical Modeling (reviewed by Jones et al., 2010) There are an increasing number of mathematical models directed at forecasting the outcome of the spread of a disease in an agronomic situation. Basically, there are two types of models: prediction models to predict a possible epidemic and simulation models to understand the factors that give rise to and control a given situation. A model is developed to answer specific questions and there is no general model to predict the potential and outcome of all potential viral epidemics. In developing a model, as many factors as can be predicted are taken into account. These include knowledge on the virus, its vector, the virus–vector interaction, type of crop, the cropping system, and various environmental factors that can impact on these biological factors. A good model enables one to make strategic management decisions on whether the problem is going to be significant and, if so, when and how to deal with it (Jeger and Chan, 1995; Irwin, 1999). As pointed out by Jones et al. (2010), predicting epidemics is a challenging undertaking because of the three-cornered pathosystem (virus, vector, and host) and the complicated nomenclature used in developing epidemiological models. Chan and Jeger (1994) and Jeger et al. (1998) describe a model based on transmission characteristics of arthropod virus vectors to analyze the effects of roguing of diseased plants (Section III, A, 1, c) and/or reduction of the vector population size by insecticide treatment. From this model, they suggest that roguing would only be effective for nonpersistently transmitted viruses at low population densities and for propagative viruses at high population densities. There would be a clear advantage for reducing vector population densities for propagative viruses but not for nonpersistent viruses. Similarly, models have been developed for assessing the potential effects of factors such as the virus–vector interaction on the development of plant virus epidemics (Madden et  al., 2000), the basic reproduction number of plant pathogens (van den Bosch et  al., 2008), and linking virus transmission at the host population level with virus multiplication in the plant (Jeger et al., 2011b). There are numerous models for specific disease situations. Some examples to show the range are: i. Predicting the effects of using healthy and infected cassava cuttings on the spread of ACMV (Holt et al., 1997). If virus-free cuttings are used then either high

832

Plant Virology

Percent plants infected (angle)

(A) 80 1965-1985 1986-1996 60

40

20

0

Percent plants infected (angle)

(B)

10 20 30 50 Ground frosts in Jan. and Feb. at Broom’s Barn

80 60 1965-1985

40

1986-1996

20

0

80

100 120 140 160 180 200 220 Date of first flight of Myzus persicae (after 1 January)

FIGURE 14.18  Factors for predicting occurrence of virus yellows of sugar beet in England. Panel (A) Effect of winter weather on virus yellows incidence in sugar beet in the eastern region of the United Kingdom: 1965–1996. Ground frosts were measured at Broom’s Barn Experimental Station in Eastern England. Panel (B) Relationship between aphid migrations and virus yellows incidence in sugar beet in the eastern region of the United Kingdom: 1965–1996. From Dewar and Smith (1999) with permission of the publishers.

rates of virus transmission by the whitefly vector of large populations of vectors could lead to persistent cycles of disease incidence. If some of the cuttings are infected, the model predicts three possible outcomes: disease elimination, persistence of both healthy and infected plants, or total infection, depending on various parameters. ii. A model for predicting virus yellows disease of sugar beet (BMYV and BYV) in the United Kingdom is based on the preceding winter weather (Watson et  al., 1975) (especially the number of frost days) (Figure 14.18A), the dates when the aphid vectors begin their spring migration (Harrington et  al., 1989) (Figure 14.18B) and region in which the beet is being grown (eastern, western, and northern regions). This model has been refined to allow for the numbers of migrating M. persicae, the major vector (Werker et  al., 1998). For a different environment and crop, the epidemiology of BWYV in Brassica napus has been modeled for a Mediterraneantype environment (Maling et al., 2010).

iii. A model based on vector preference for healthy plants or those infected by BYDV shows that the effect of vector preference for infected plants depends on the frequency of the infected plants in the population (McElhany et al., 1995). The effect of vector preference depends on the persistence of the virus in the vector. The results of the analysis contrast with the assumption that preference for diseased plants automatically leads to increase in disease spread. A model has been developed to predict aphid arrival, epidemics of BYDV and yield losses in wheat in Australia (Thackray et al., 2009). Another model shows that the spatial structure of host population influence patterns of infection incidence of yellow dwarf viruses of cereals (Moore et al., 2011). iv. To investigate the effects of competition between viruses, Power (1996) analyzed the interactions between BYDVMAV and BYDV-PAV. Transmission rate plays an important role in determining the outcome of competition between the viruses as does the interaction between transmission rate and vector behavior. A mathematical model analyzes the competition in a complex plant–pathogen system comprising these two viruses and their respective aphid vectors (Amaku et al., 2010). v. Many annual crops in tropical regions are grown in continuous, contiguous cultivation without a seasonal break. Holt and Chancellor (1997) developed a model for this situation. The model predicts that, in a given region, disease incidence depends on infection efficiency, the dispersal gradient, and the variance in planting date. This model is discussed in relation to the spread of rice tungro virus disease. The above examples show some of the complexities that have to be taken into account in developing meaningful models. Thus, one has to analyze the temporal dynamics (Nutter, 1997) and the spatial patterns both of the plant host and of the vector(s) and its hosts (Real and McElhany, 1996; Perry, 1998; Raybould et al., 1999). The spatial patterns have to be large scale and take account of the landscape ecology (Barnes et al., 1999).

3.  Information Flow and Warnings It is important for disease control to have a transparent information flow from those collecting the data to those implementing control measures.

G.  Conclusions on Epidemiology We can see from this brief account that the factors and interactions involved in the ecology and epidemiology of viruses in crops are extremely complex. This can be illustrated by the processes involved in the spread of luteoviruses within and between crops (Figure 14.19). The luteoviruses are among the most studied of virus groups

833

Chapter | 14  Ecology, Epidemiology, and Control of Plant Viruses

Aphid nonhost

Migration

Virus nonhost

Virus nonhost “Healthy” aphid reservoir and source

Virus-free host

Aphid host reservoir and source “relay plant”

Virus host reservoir and source “relay plant”

Virus Introduction “Infector” plant

Secondary

Spread

Potato

Cereals, sugar beet,...

FIGURE 14.19  The epidemiological process of luteovirus spread showing the various routes of infection and the relevant differences between potato and other crops. From Robert (1999) with permission of the publisher.

as far as epidemiology is concerned, but the complexities shown in Figure 14.19 are just as applicable to other crop situations. There are virtually no data on the epidemiology (ecology) of viruses in non-crop natural systems. It is important to note that not all viruses possess all characteristics that are generally favorable to survival and spread, which is perhaps just as well. Each virus has some combination of properties that allows it to persist more or less effectively. TMV has no significant invertebrate vector, but survives because of its high resistance to inactivation, the high concentration it generally reaches in its host, the ease with which it can be mechanically transmitted, and its wide host range. By contrast, viruses that multiply in the insect vector and are transmitted through the egg have a complete alternative to the plant host for survival. TSWV is an example of a very unstable virus that is extremely successful in the field. It can retain infectivity only for periods of hours under normal conditions outside the plant. It has a specialized type of vector (species of thrips that can acquire virus only as nymphs), and yet it is widespread around the world and common within individual countries. Its success probably depends on several factors (Best, 1968): (i) its very wide host range, including many perennial symptomless carriers that provide

year-round reservoirs of the virus; (ii) the widespread distribution of species of thrips capable of transmitting the virus; (iii) the existence of a wide range of strains in strain mixtures, and the probable occurrence of recombination or gene reassortment allowing rapid adaptation of the virus to new hosts to give relatively mild disease; and (iv) humans providing suitable conditions through their agricultural practices. Many nematode-transmitted viruses are also transmitted through the seed in a range of weed and crop plant hosts. Infected seedlings often appear to be healthy. The combination of nematode and seed transmission may be important for the survival and dispersal of many of these viruses (Murant and Lister, 1967). Germination of infected weed seeds may allow reinfection of the nematode population in a field, and infected seeds may be transferred over longer distances than nematodes to set up new centers of infection. Murant and Lister (1967) noted that viruses such as TBRV, which are commonly found in soils in infected weed seeds, do not persist more than about 9 weeks in their vector Longidorus elongatus. In contrast, two nepoviruses (ArMV and GFLV), which can persist for 8 months or more in the vectors Xiphinema spp., were rarely or never found in seed in infected soil.

834

H.  Plant Virus Ecology (reviewed by Malmstrom et al., 2011; Roossinck, 2013) Agricultural practices, even in fairly early primitive stages, must have changed the environment in which viruses existed in several important ways. Viruses impact on the ecology in three situations: the controlled agricultural situation described above, the peri-agricultural situation at the interface of agriculture, and the “natural” vegetation and the “natural” situation; obviously, there is usually a gradient between these situations. Viruses existing in completely natural or peri-agricultural habitats and their ecology have been very little studied. Most of our knowledge is a by-product of the investigation of commercially important diseases. Malstrom et  al. (2011) emphasize that expanding the knowledge on plant viral ecology requires study of: The ecological roles of plant-associated viruses and their vectors in managed and unmanaged ecosystems. ● The reciprocal influences of ecosystem properties on the distribution and evolution of plant viruses. ●

In the peri-agricultural situation, the study of the ecology of viruses should not be undertaken on just viruses of the non-agricultural species but must include the “crosstalk” between the “natural” and agricultural environments. Obviously, there will be two-way traffic of viruses between the two environments and the agricultural practices will impact on the natural environment in many ways. Amongst various factors that agriculture introduces into the periagricultural situation are: (i) cultivation brings together new communities of plants, both the useful species and the weeds associated with cultivation; (ii) these agricultural communities of plants have been transported about the world and have become neighbors of the indigenous floras. Viruses present in these have moved into the agricultural crops; (iii) along with the plants, insect vectors, and potential vectors have been transported into the new areas, and insects already present in the new areas may have been able to spread into the agricultural crops; (iv) culture of a single species as the major plant over wide areas may allow the development of enormous populations of insect vectors and the consequent large-scale outbreaks of disease. This possibility may be made more likely by the maintenance of a particular species throughout the year in the same locality (e.g., the growing of seed crops of biennial plants such as sugar beet) or by the introduction of weeds that harbor the virus; (v) agricultural practices such as cultivation and drainage may change soil conditions so as to markedly affect the population of soil-inhabiting virus vectors. A few agricultural practices may have played a part in unconscious selection of mild strains of a virus, but, generally, the foregoing factors combine in various ways continually to produce new and unstable ecological situations

Plant Virology

in which outbreaks of disease can occur in agricultural and horticultural crops. On the other hand, in regions where a crop has been grown continually for long periods under conditions favoring infection with a virus, resistant cultivars may have developed without a conscious selection procedure. For example, many cultivars of barley from the Ethiopian plateau have been found to have a high degree of resistance to BYDV and BSMV (Harlan, 1976). It is probable that barley has been grown in this region for millennia. This probably applies also to susceptible species in the peri-agriculture situation. Very little is known about any impact that viruses have on the ecology in the truly “wild” situation (reviewed by Cooper and Jones, 2006). It seems probable that under conditions where natural selection had operated on the virus and the host plant genotype over long periods undisturbed by the activities of humans, viruses would be closely adapted to their plant hosts and invertebrate or other vectors. As discussed in Chapter  8, Section VII, coevolution could result in the effects of virus infection on plant growth being minimal. Severe disease in individual plants might occur occasionally, but epidemics would be rare. Several investigations suggest that in wild plants, symptomless infection is the most common situation. Thus, many weed hosts of CMV in both England (Tomlinson et  al., 1970) and Germany (Shukla and Schmelzer, 1973) are infected without symptoms. There may be regional adaptation between virus and host genotype to give mild disease. Tomlinson and Walker (1973) found that Stellaria media plants grown from seed from Britain, North America, and Australia are least severely affected by the CMV strain obtained from their country of origin. Thus, natural selection of tolerant races of the species and mild strains of the virus had probably taken place. As noted in Section II, F, 1, advanced sequencing techniques are being used to provide further data on viral ecology.

I.  Emergence of New Viruses (reviewed by Fargette et al., 2006; Jones, 2009) Epidemics by apparently “new” viruses occur regularly and attract much attention. There are at least three basic scenarios by which such epidemics can arise. In the first scenario, the virus(es) may be present at a low level for a considerable time and changes in agronomic practice lead to more favorable conditions for its rapid spread. Examples of this are the great increase in rice virus epidemics possibly associated with the Green Revolution (discussed in Section II, D, 1, a). Secondly, as well as distributing viruses around the world, humans have moved crop species to new countries; often with disastrous consequences as far as virus infection is concerned. Plant species that were relatively virus-free in their native land may become infected with viruses that

Chapter | 14  Ecology, Epidemiology, and Control of Plant Viruses

have long been present in the countries to which they were moved for commercial purposes. Examples of CSSV in cacao and MSV in maize are mentioned earlier (Section I, A, 1, e, iii). Another example of international trade leading to the spread of an important disease is exemplified by the spread of BNYVV, which causes the important rhizomania disease in sugar beet (Box 14.1). In this case, it is likely that one major way that the virus was introduced to a new location was in contaminated soil on even a non-host crop such as potatoes. In the third scenario, new viruses can arise by mutation or more often by recombination. The spread of tomato yellow leaf curl disease from the Eastern Mediterranean (Box 14.1) is associated with new viruses arising from recombination as well as human influences. New diseases can also be caused by two viruses or a virus and satellite coming together and causing a synergistic reaction (see Chapter 4, Section IX, B, 1, a). In many cases, the emergence of a new virus disease is driven by a mixture of the three scenarios (e.g., TYLC disease, Box 14.1) and can be affected by factors such as changes in biodiversity (Keesing et al., 2010) and climate (see Anderson et al., 2004 and Section II, J).

J.  Possible Effects of Climate Change on Plant Virus Epidemiology and Ecology We are currently in a period of global warming which is largely attributed to increases of man-made CO2 and which is projected to increase in the future (IPCC, 2007). Increases in mean temperature are predicted to lead to an increased risk of high temperature extremes, such as intense, longer-lasting, and more frequent heat waves, increases in mean precipitation in the tropics, widespread decreases in mean precipitation bringing mid-latitudes an increased risk of drought and changes in seasonality (Meehl et al., 2007). Such changes in climate will obviously affect the complex interactions between viruses, their hosts, and vectors, as well as impacting on the agricultural and nonagricultural environments. Potential effects are as follows: Changes in the geographical distribution, densities, migration potential, and phenology of host plant and insect vector populations affecting the epidemiology of viruses (reviewed by Shaw and Osborne, 2011). ● Changes in the interactions between managed agricultural and natural environments may lead to the emergence of new crop virus diseases and changes in epidemiology (reviewed by Jones, 2009). ● Alterations in host plant physiological processes affecting virus–host interactions (e.g., changes in metabolism, leaf temperature, and host defense against virus ●

835

infection. For example, environmental conditions can affect RNA recombination (Jaag and Nagy, 2010); RNA silencing defense is temperature sensitive (see Chapter 9, Section V, F, 4); virus infection can improve drought tolerance (Xu et al., 2008). ● Changes affecting host–vector interactions (Canto et al., 2009). ● Changes in agricultural practices such as crops grown, and cropping seasons, affecting coincidence of susceptible crop and prevalence of vector (Reynaud et al., 2009; Roos et al., 2011). There are an increasing number of studies predicting the effects of climate change on plant diseases in general (reviewed by Chakraborty and Newton, 2011; Garrett et al., 2011) and on specific virus–vector–host systems and for specific countries and regions (Canto et al., 2009; Roos et  al., 2011). Example case studies show an increase in number of aphid species present in Europe and their earlier flight over the last 30 years (Hullé et  al., 2010), and prediction of effects of climate change on the pest status, vectoring potential, and crop–vector–virus pathosystem of Rhopalosiphum padi (Finlay and Luck, 2011) (Box 14.2). The predicted effects of climate change on plant diseases are that they will not all be detrimental, and there will be cases where the disease risk will be mitigated (Chakroborty and Newton, 2011).

III.  CONTROL OF PLANT VIRUSES BY AVOIDANCE AND VECTOR CONTROL (reviewed by Jones, 2006; Thresh, 2006b) As outlined in Chapter 4, Section I, viruses cause considerable losses; there is a range of control measures aimed at trying to mitigate these losses which I will describe in this section. The use of fungicidal chemicals that, when applied to crop plants protect them from infection or minimize invasion, is an important method for the control of many fungal diseases. No such direct method for the control of virus diseases is yet available for widespread use. Most of the procedures that can be used effectively involve measures designed to reduce sources of infection inside and outside the crop, to limit spread by vectors, and to minimize the effect of infection on yield. Generally, such measures offer no permanent solution to a virus disease problem in a particular area. Control of virus disease is usually a running battle in which organization of control procedures, care by individual growers, and cooperation among them is necessary year by year. The few exceptions are where a source of resistance to a particular virus has been found in, or successfully incorporated into, an agriculturally useful cultivar. This is becoming of increasing importance with the development of transgenic protection of plants against

836

Plant Virology

BOX 14.2  Case Study on Effects of Climate Change on the Rhopalosiphum Padi Crop–Vector–Virus Pathosystem (Finlay and Luck, 2011) The bird cherry-oat aphid, Rhopalosiphum padi is a major vector of the yellow dwarf viruses (YDVs) that infect cereals. R. padi has a complex life history. Many populations in temperate regions that have cold winters reproduce combining sexual and asexual phases (holocycly), alternating

(A)

between primary winter tree hosts (e.g., Prunus padus in Europe and Prunus virginiana and Prunus pennsylvanica in North America) and secondary summer Poaceae hosts (Figure 14.20A). In contrast, the reproduction of populations in regions where the winters are mild, and in some temperate

Sexual reproduction Primary host– Prunus padus (Bird Cherry) Eggs Spring Winter

Summer Autumn

Asexual reproduction Secondary hosts (Poaceae)

(B)

Population builds

Hosts– grasses (Poaceae)

Spring Summer

Winter

Population declines

Autumn Hosts– cereals (Poaceae)

Population builds

FIGURE 14.20  Life cycles of Rhopalosiphum padi. Panel (A) Holocyclic life cycle of R. padi found typically in Europe. The species alternates between the primary winter host, bird cherry (Prunus padus) where sexual reproduction occurs and secondary summer Poaceae hosts. Panel (B) Anholocyclic life cycle of R. padi found typically in Australia. The majority of individuals are females, and males are rarely seen and do not contribute to the life cycle. Continuous asexual reproduction occurs with the winged forms moving from cereals in the autumn and winter to grasses during the spring and summer. From Finlay and Luck (2011) with permission of the publishers.

837

Chapter | 14  Ecology, Epidemiology, and Control of Plant Viruses

countries where the primary host is scarce, is completely parthenogenic (anholocyclic) (Figure 14.20B). YDVs comprise two species in the family Luteoviridae, the luteovirus BYDV and the polerovirus CYDV both of which are transmitted in the nonpropagative circulative manner (see Chapter  12, Section III, D, 1). Each virus has several strains distinguished by distinct genome properties and their primary aphid vectors but the vectors of all include R. padi. All the strains have worldwide distribution but some tend to be more widespread and abundant in many areas. These viruses infect many species of grasses (Poaceae). Three results of climate change, increasing temperatures, elevated CO2, and altered rainfall patterns coupled with severe weather events are considered to impact on the R. padi–YDV–cereal pathosystem. It is suggested that these

Increasing temperatures

interact directly on R. padi and indirectly on the aphid–virus and aphid–plant interactions (Figure 14.21). This case study identifies many gaps in the knowledge that is needed to be able to predict the effects of climate change on plant viral pathosystems with more certainty. These gaps include: ● The effects of the three direct impact effects of climate change on the vector and on the host. ● The effects of temperature on the virus and the virus–host interaction. ● The development of models to integrate the effects of climate change on the members of the pathosystem and to identify which specific parameters are most crucial in determining the overall consequence of climate change.

Direct impact of climate change on R. padi Elevated CO2 • ∆ population size and

• increased development rate from 4 to 25°C • increase in mean TBR from 10 to 25°C • increase in rm from 10 to 25°C • Shorter life cycles • longer development times for alatae compared with

apterae, particularly at lower temperatures (10 to 25°C) • acclimation to high temperatures (> 30°C) • higher apterae production • alate production suppressed

fecundity but direction unclear • ∆ feeding behavior (more phloem feeding and sap ingestion) • greater alate production

• compensatory feeding

• higher thermal thresholds for development and flight • increase in number of seasonal generations • ∆ predator and parasitoid associations

Impact through climate induced aphid-virus interactions Increasing temperatures

• mean vector transmission efficiencies increased from 5 to 25°C higher for apterae • more efficient transmission when virus acquisition period occurs at higher temperatures • reduced latent periods for virus transmission at higher temperatures

Altered rainfall patterns and severe weather events

• smaller infestations in winter crops due to previous poor summer and autumn rainfall • ∆ dispersal activity under drought conditions but direction unclear • heavy precipitation → poor colonization and dispersal • movement of aptetae induced by wind disturbance • high winds → greater aphid densities, and long distance dispersal / migration • greater infestations on drought/food stressed plants • ∆ predator and parasitoid associations

R. padi

Impact through climate induced aphid-host plant interactions Increasing temperatures/ altered rainfall patterns

Whole system interactions

• ∆ to aphid fecundity due to different host plant associations • ∆ host plant distribution and

• nonviruligerous aphid

availability

migration preference for virusinfected plant → greater apterae immigration, longer migration flights for alates

• new aphid–host plant interactions

due to asynchrony between aphid and host plant phenology → ∆ to aphid developmental rates • aphid encounters with new (not previously recorded) host plants → ∆ to aphid developmental rates

• aphid feeding on virus infected host→ increased alate production, changes in development parameters and feeding behavior Yellow dwarf virus

Host plant, wheat

Elevated CO2 • Increase in host plant biomass and yield → compensatory feeding

FIGURE 14.21  Observed (blue text) and expected (red text) impacts of climate change either directly in the aphid vector (R. padi) or indirectly through the aphid–wheat–virus pathosystem interactions. (For interpretation of the references to color in this figure legend, the reader is referred to Finlay and Luck, 2011). From Finlay and Luck (2011) with permission of the publishers.

viruses (discussed in Chapter  15, Section I). Even with conventional and transgenic resistance, protection may not be permanent when new strains of the virus arise that can cause disease in a previously resistant cultivar.

It should be borne in mind that virus infection can sometimes increase the incidence of some other kind of disease. In such situations, different sorts of control may be needed. For example, yellowing viruses in sugar beet

838

increase susceptibility to Alternaria infection. Spraying with appropriate fungicides reduces this secondary effect of virus infection in some seasons (Russell, 1966). Correct identification of the virus or viruses infecting a particular crop is essential for effective control measures to be applied. Disease symptoms alone may be very misleading. For example, virus disease in lettuce can be caused by some 14 viruses with an aphid, leafhopper, thrip, nematode, or a fungus vector (Cock, 1968). Many of these viruses produce brown necrotic spots or bronzing on leaves, and later chlorotic stunting. Another example is that of the yellowing diseases of beets in the United Kingdom (Russell, 1958) and the western United States. Of major importance in designing a strategy for control of a virus in a specific crop is an understanding of the epidemiology of that virus. This enables disease outbreaks to be forecasted and these aspects were discussed in Sections I and II. As pointed out above, most of the serious virus disease problems around the world are the direct or indirect result of human activities. Important activities leading to epidemics include: (i) introduction of viruses into new areas through transport of infected seed or vegetative material; (ii) introduction of virus vectors into new areas; (iii) introduction of a new crop or variety into an area when that crop or variety is especially susceptible to a virus already present there; (iv) use of monocultures replacing traditional polycultures; (v) use of irrigation to prolong the cropping season with overlapping crops; (vi) repeated use of the same fields for the same crop; and (vii) increased use of fertilizer and herbicides or other forms of weed control. In recent years, the most active areas of research into the control of virus diseases have been: (i) the breeding of resistant or immune cultivars by classic genetic procedures; (ii) the production of transgenic plants containing viral or other genes that confer resistance to the virus; (iii) the control of vectors by various strategies; and (iv) the production of virus-free stocks of seed and vegetative propagules. General approaches to control are discussed in Jones (2006) and Thresh (2006b), and control of specific viruses is reviewed in several places, e.g., control of luteoviruses (Smith and Barker, 1999), of ACMV (Thresh and Otim-Nape, 1994), of PRSV (Gonsalves, 1998), and in several chapters in Hadidi et al. (1998). Data for many of the control measures discussed in this chapter are derived from laboratory and field trials. Because of the many variables, and the large number of countries involved, it is often difficult to assess the extent to which any particular procedure or set of procedures has actually been adopted on a regular basis into commercial practice. More and more attention is being given to the possibilities of integrated control involving several strategies. Again, it is often difficult to assess whether these are actually being effectively used in the field, or whether they remain optimistic dreams. When adequate facilities and expertise are available, a multidisciplinary approach may be useful as exemplified by the attempts to control diseases caused by

Plant Virology

TSWV in Hawaii (Cho et al., 1989). Control of plant pathogens integrated with control of pests in integrated pest management (IPM) systems is discussed in Jacobsen (1997).

A.  Removal or Avoidance of Sources of Infection 1.  Removal of Sources of Infection in or near the Crop It is obvious that there is unlikely to be a virus problem if the crop is free of virus when planted and when there is no source of infection in the field, or none near enough to allow it to spread into the crop. The extent to which it will be worthwhile to attempt to eliminate sources of infection in the field can only be decided on the basis of a detailed knowledge of such sources of virus and of the ways in which the virus is spreading from them into a crop. Eradication as a control measure has been reviewed by Thresh (2006b) focusing primarily on the schemes to eradicate CSSV. a.  Living Hosts for the Virus Living hosts as sources of infection may include: (i) perennial weed hosts, annual weed hosts in which the virus is seed transmitted, or annual weed hosts that have several overlapping generations throughout the year; (ii) perennial ornamental plants that often harbor infection in a mild form. For instance, gladioli are often infected with BYMV that can spread to adjacent annual legume crops (Hull, 1965); (iii) unrelated crops; (iv) plants of the same species remaining from a previous crop; these may be groundkeepers, as with potatoes, or seedling volunteers; and (v) seed crops of biennial plants that may be approaching maturity about the time the annual crop is emerging. In theory, it should be possible to eliminate most of such sources of infection. In practice, it is usually difficult and often impossible, particularly in cropping areas that also contain private gardens. Private household gardens and adjacent farms in temperate and subtropical regions often contain a diverse collection of plants, many of which can carry economically important viruses. It is usually difficult or impossible to control such gardens effectively. In tropical countries, the diversity of cropping makes control of living sources of infection very difficult. The extent to which attempts to remove other hosts of a virus from an area may succeed will depend largely on the host range of the virus. It may be practicable to control alternative hosts where the virus has a narrow host range, but with others, which have large host ranges, such as CMV and TSWV, the task is usually impossible. b.  Plant Remains Plant remains in the soil, or attached to structures such as greenhouses, may harbor a mechanically transmitted virus

839

Chapter | 14  Ecology, Epidemiology, and Control of Plant Viruses

c.  Roguing and Eradication Schemes Sometimes, it may be worthwhile to remove infected plants from a crop. If the spread is occurring rapidly from sources outside the crop, roguing the crop will have no beneficial effect. If virus spread is relatively slow and mainly from within the crop, then roguing may be worthwhile, especially early in the season. Even with a perennial crop, if a disease spreads slowly, roguing and replanting with healthy plants may maintain a relatively productive stand. A study of the distribution of infected plants within the field using the formula developed by van der Plank (Section II, C, 1) may give an indication as to whether spread within the crop is taking place. In certain situations, roguing may exacerbate disease spread by disturbing vectors on infected plants (Rose, 1974). In many crops, newly infected plants may be acting as sources of virus for further vector infection before they show visible signs of disease (Beemster, 1979). Most of the successful eradication schemes have been on tree crops. Among the factors that dictate success are: (i) relatively small numbers of infected trees and infection foci; (ii) low rate of natural spread; (iii) good data on extent and distribution of infection; (iv) rapid, reliable, and inexpensive diagnostic procedure for the virus; (v) resources for rapid and extensive surveys and tree removal; and (vi) legislation and system for recompensing affected farmers for losses. One of the most successful examples of disease control by roguing of infected crop plants has been the reduction in incidence of the BBTV in bananas in eastern Australia. Legislation to enforce destruction of diseased plants and abandoned plantations was enacted in the late 1920s. Within about 10 years, the campaign was effective to the point where bunchy top disease was no longer a limiting factor in production. Dale (1987) and Dale and Harding (1998) attribute the success of the scheme to the following main factors: (i) absence of virus reservoirs other than bananas, together with a small number of wild bananas; (ii) knowledge that the primary source of virus was planting material, and that spread was by aphids; (iii) cultivation of the crop in small, discrete plantations, rather than as a scattered subsistence crop; (iv) strict enforcement of strong government legislation; and (iv) cooperation of most farmers; however, Smith et al. (1998) identified some problems with this approach. A model has shown that extensive eradication should control CTV (Figure 14.22). An analytical model of the virus disease dynamics with roguing and replanting has

600 Suppression programs

CTV positive trees (x 1000)

and act as a source of infection for the next crop. With a very stable virus, like TMV, general hygiene is very important for control, particularly where susceptible crops are grown in the same area every year. ToMV may be very difficult to eliminate completely from greenhouse soil using commercially practicable methods of partial soil sterilization (Broadbent et al., 1965; Broadbent, 1976; Lanter et al., 1982). A major development has been the replacement of soil by sand/peat substrates that are renewed every year.

500

No removal 6, 000/year 15, 000/year 25, 000/year 35, 000/year 50, 000/year

400 300 200 100 0 1995

1996

1997 1998 Year

1999

2000

FIGURE 14.22  Effects of various tree removal rates on suppression of CTV infection. Figure is from a model developed for a tree removal project in California. Surveys indicated c. 75,000 CTV-infected trees in an area of c. 80,000 ha. An infection increase of 50% per year of existing trees is assumed. If 25,000 of the existing trees are removed, then a 50% increase in the remaining 50,000 creates essentially a static situation. Increasing the initial tree removal to 50,000 rapidly reduces the population of infected trees and lowers the overall tree removals compared to less aggressive initial approaches. From Garnsey et al. (1998) with permission of the publishers.

been put forward by Chan and Jeger (1994). They showed that roguing only in the postinfectious category confers no advantage. At low contact rates, roguing only when plants became infectious is sufficient to eradicate the disease but at high contact rates, roguing latently infected as well as infectious plants is advisable. The model indicates that eradication is achievable with realistic roguing intensities. d. Hygiene For some mechanically transmitted viruses, and particularly for TMV or ToMV, human activities during cultivation and tending of a crop are a major means by which the virus is spread. Once TMV or ToMV enters a crop like tobacco or tomato, it is very difficult to prevent its spread during cultivation and particularly during such processes as removing lateral shoots and tying of plants. Control measures consist of treatment of implements and washing of the hands. For this, Broadbent (1963) recommends a 3% solution of trisodium orthophosphate. Workers’ clothing may become heavily contaminated with TMV and thus spread the virus by contact. TMV persists for over 3 years on clothing stored in a dark enclosed space (Broadbent and Fletcher, 1963), but is inactivated in a few weeks in daylight. Clothing is largely decontaminated by dry cleaning or washing in detergents with hot water. While TMV is the most stable of the mechanically transmitted viruses, others can be transmitted more or less readily on cutting knives and other tools. These include TBV, CymMV, PVX, PSTVd, and citrus viroids (Barbosa et  al., 2005). These mechanically transmitted agents may be a particular problem in greenhouse crops, where lush

840

growth, close contact between plants, high temperatures, and frequent handling are important factors in facilitating virus transmission. Six carnation viruses (CarMV, CVMV, CRSV, CIRV, and CLV with RNA genomes and CERV with a DNA genome) are inactivated by treatment with 7% (v/v) commercial bleach or 0.5% (w/v) NaOH for 60 s (SanchezNavarro et al., 2007). Since mechanical transmission is an important means whereby viroids are spread in the field, decontamination of tools and hands is an important control measure. However, this presents difficulties because of the stability of viroids to heat and many decontaminating agents as normally used. Brief exposure to 0.25% sodium or calcium hypochlorite is probably the best procedure (Garnsey and Randles, 1987). One of the earliest and most effective methods for the control of viroids has been the avoidance of sources of infection. This method has been particularly successful for vegetatively propagated crops susceptible to viroids, such as potatoes and chrysanthemums. This success is probably due to the absence of vectors in the field apart from humans.

2.  Virus-Free Seed (reviewed in Maury et al., 1998) Where a virus is transmitted through the seed, such transmission may be an important source of infection, since it introduces the virus into the crop at a very early stage, allowing infection to be spread to other plants while they are still young. In addition, seed transmission produces scattered foci of infection throughout the crop. Where seed infection is the main or only source of virus, and where the crop can be grown in reasonable isolation from outside sources of infection, virus-free seed may provide a very effective means for control of a disease. Factors that affect seed transmissibility of viruses are discussed in Chapter 12, Section VII, B, 1. LMV is perhaps a good example of controlling a virus problem through clean seed (Dinant and Lot, 1992). Grogan et  al. (1952) found that crops grown from virusfree seed in California had a much lower percentage of mosaic at harvest than adjacent plots grown from standard commercial seed. For a time, control was unsatisfactory, until it was realized that even a small percentage of seed infection could give much infection within the crop if the aphid vector was active (Zink et al., 1956). To obtain effective control by the use of virus-free or low-virus seed, a certification scheme may be necessary, with seed plants being grown in appropriate isolation. Although 0.1% seed transmission did not give effective control of lettuce mosaic (Kimble et  al., 1975), the use of seed stocks that tested < 0.003% infection in the Salinas Valley area of California has given consistent control in practice. ELISA tests are used to test for the presence of a virus in batches of seed. If there is a significant amount of virus in the seed coats that is not involved in seed transmission it may be necessary to remove the seed coats before

Plant Virology

testing the embryos (Maury et al., 1987). Seed certification schemes against BSMV have been credited with avoiding millions of dollars in losses due to this disease in barley crops in some US states (Carroll, 1983). To improve the quality control of analyzing large quantities of seed being tested for PSbMV, statistical and serological approaches were taken to identify thresholds for identification (Masmoudi et al., 1994). Large groups (200–500 seeds per group) were tested by ELISA and account was taken of detecting one infected embryo in such a group size. Seed from ToMV-infected tomatoes carries the virus on the surface of the seed coat. As the seed germinates, virus contaminates the cotyledons and is inoculated into the plant by handling during pricking out. Seed can be cleaned by extraction in HCl, heating dried seed in 0.1N HCl, or treatment with trisodium orthophosphate or sodium hypochlorite (Gooding, 1975). Immersing tomato seeds on 10% trisodium phosphate for 3 h prevents seed transmission of PepMV (Cordoba-Selle et al., 2007). It may be particularly important to attempt to eliminate seed-transmitted viruses from national or international germplasm collections. Among 207 Phaseolus vulgaris accessions in the USDA germplasm collection, about 60% contained some seed infected with BCMV (Klein et  al., 1988). In at least one instance, that of PSbMV in peas, elimination of infected individuals led to a loss of genetic diversity, as judged by seed coat color and isoenzyme genotypes (Alconero et  al., 1985). In this circumstance, methods that do not involve selective loss of particular plant types might be used to eliminate the virus (see the following section).

3.  Virus-Free Vegetative Stocks For many vegetatively propagated plants, the main source of virus is chronic infection in the plant itself. With such crops, one of the most successful forms of control has involved the development of virus-free plant clones, that is, clones free of the particular virus under consideration. Two problems are involved. First, a virus-free line of the desired variety with good horticultural characteristics must be found. When the variety is 100% infected, attempts must be made to free a plant or part of a plant from the virus. Second, having obtained a virus-free clone, a foundation stock or “mother” line must be maintained virus free, while other material is grown up on a sufficiently large scale under conditions where reinfection with the virus is minimal or does not take place. These stocks are then used for commercial planting. a.  Methods for Identification of Virus-Free Material Visual inspection for symptoms of virus disease is usually quite inadequate when selecting virus-free plants. Appropriate indexing methods are essential. A variety of methods are available, and the most suitable will depend on the host plant and virus (see Chapter 13, Section V). For many viruses, especially those of woody plants, the rather

841

Chapter | 14  Ecology, Epidemiology, and Control of Plant Viruses

b.  Methods for Obtaining Virus-Free Plants i. Naturally Occurring Virus-Free Material  Occasionally, individual plants of a variety, or plants in a particular location, may be found to be free of the virus. If all plants are infected, advantage may sometimes be taken of uneven distribution of the virus in the plant. This is not uncommon with some viruses in fruit trees. Budwood can be taken from uninfected parts of the tree. The shoot tips of rapidly growing stems may sometimes be free of a virus that is systemic through the rest of the plant. Thus, Holmes (1955) was able to obtain dahlia cuttings free of TSWV. This sort of procedure has been used successfully for several viruses in certain hosts. However, many vegetatively reproduced varieties appear to be virtually 100% infected with a virus, and with these, one or more of the special treatments and methods described next have to be used to obtain a nucleus of virusfree material. Some examples have been reported where natural elimination of a virus occurred. When TRV-infected tulip bulbs were grown for several seasons in soil free of the nematode vector, a proportion of the bulbs were found to be free of the virus (van Hoof and Silver, 1976). ii. Heat Therapy (Thermotherapy) (reviewed in Mink et al., 1998)  Heat treatment has been a most useful method for freeing plant material from viruses. Many viruses have been eliminated from at least one host plant by heat treatment (Walkey, 1991). Two kinds of plant material have been used. Dormant plant parts such as tubers or budwood can generally stand higher temperatures than growing tissues, and the method probably depends on direct heat inactivation of the virus. Temperatures and times of treatment vary widely (35–54°C for minutes or hours). Hot water treatments are often used,

as hot air tends to give uneven heating during short treatments. Unless tissues are thoroughly hydrated, dry heat is much less effective than wet heat. Growing plants are much more generally used, and hot air rather than hot water is applied. Temperatures in the range of 35–40°C for periods of weeks are commonly employed. This form of treatment gives a better survival rate for growing plant material. Details of the treatment vary widely and have to be worked out empirically for each host–virus combination. Very frequently, small cuttings are taken from the shoot tips immediately after the heat treatment, as these may be free of virus when the rest of the plant is not. For example, culture of shoot tips from heat-treated sprouting potatoes gives a useful proportion of plantlets free of PVX (Faccioli and Rubies-Autonell, 1982). The percentage of garlic plants free of three viruses that are regenerated from meristem tip culture increases from 25–50% to 85% when infected plants are treated at 38°C prior to tip culture (Walkey et al., 1987). Alternatively, apical explants established in culture may be given the heat treatment. Thus, SMYEV potexvirus was eliminated from 4-mm-long strawberry stolon explants held at 38°C (Converse and Tanne, 1984). These authors suggest that heat therapy and stolon apex culture contribute independently to the process. A regime of alternating high (~40°C) and normal (~20°C) temperatures may help to reduce the damaging effects of high temperatures on the plant tissues while still allowing some shoot tips to be freed of virus. Detailed regimes have to be developed for each host and virus. Reduction and elimination of virus may depend on the total hours held at the high temperature, as illustrated for CMV in Figure 14.23. The actual temperature within plant tissues may be several degrees below the measured ambient temperature. At present, there is no basis for predicting that tissue from a certain plant species can, or cannot, be freed of a particular virus. The mechanisms underlying the

100 Infectivity (% of control)

laborious process of graft-indexing to one or more indicator hosts is essential. Distribution of a virus within the tree may be uneven, especially in the early stages after infection, so that tests repeated in successive seasons may be necessary to ensure freedom from virus. For example, Hampton (1966) found, using four buds for indexing per tree, that first-year infection with PDV is not detected in a high proportion of cherry trees (29–63%, depending on the variety). The probability of detection improves substantially in trees that had been infected for 3 years. Distribution may also be uneven in herbaceous plants (Chapter  10, Section V, E). Thus, Beemster (1967) found that in potatoes inoculated with PVY, not all tubers are infected and not all parts of a single tuber might be infected. The heel end of tubers is less frequently infected than the rose end which is, therefore, a more reliable source material for testing. Mechanical inoculation to indicator hosts can be used with some viruses, but other methods of diagnosis now rival infectivity tests in their sensitivity for the detection of viruses (Table 13.3).

10

1.0

0.1 500

1000

1500

2000

2500

Total hour-degrees above 25° FIGURE 14.23  Relationship between inactivation of CMV in infected tissue cultures of Nicotiana rustica and the total hour-degrees above 25°C resulting from various alternating diurnal temperature regimes. From Walkey and Freeman (1977) with permission of the publishers.

842

Plant Virology

(A) Infected in virto stock cultures

Excision of shoot tips

Manipulation of shoot tips to increase their tolerance to dehydration and cryo-treatment

Regenerated shoots indexed for freedom from pathogens and verified for the true type

Postculture for survival and plant regeneration

(B) P V N Nu M LP 1

AD

LP 2

Dehydration of cells to increase their tolerance of ultralow temperatures

Brief treatment in liquid nitrogen

Cells are smaller, more isodiametric in shape, and possess a larger nucleo cytoplasmic volume ratio. Vacuoles are small and scattered through the protoplast.

Cells at top layers of AD and basal part of LP

HC

KC

Cryotherapy

PIC

SC

N Nu V P

Shoot tip before freezing (Pathogen infected)

KC

M

Cells at basal layers of AD and upper part of LP

Shoot tip after freezing (Pathogen free) Cells are larger, contain larger vacuoles, and have a smaller nucleo cytoplasmic ratio.

FIGURE 14.24  Elimination of infected cells by cryotherapy of shoot tips. Panel (A) Overview of the main steps of the procedure. Panel (B) Schematic illustration of the anatomical differences between the cells in the meristematic zone in the apical dome (AD) and other, more differentiated cells in the shoot apex. The least differentiated cells, close to the AD of the meristem are packed closely together without intercellular cavities, are small and isodiametric in shape and possess a large nucleocytoplasmic volume ratio. Vacuoles are small and scattered in the cell. The protoplasm contains a large number of cell organelles such as proplastids, mitochondria, Golgi apparatus, and ribosomes associated with the endoplasmic reticulum (Fahn, 1985). The sizes of cells and vacuoles increase, the nucleocytoplasmic ratio decreases, and the propensity for injuries at ultra-low temperatures grows with increasing distance from the AD (Helliot et  al., 2003a; Wang et  al., 2008). For successful cryotherapy, lethal intracellular injury of the pathogen-infected cells should be promoted to remove them. It can be enhanced by combinatorial use of thermo- and cryotherapy (Wang et al., 2008). Abbreviations: AD, apical dome (top layer of cells of apical meristem); HC, healthy cells; KC, killed cells; LP 1; leaf primordium 1 (the youngest leaf primordium); LP 2, leaf primordium 2; M, mitochondria; N, nucleus; P, proplastid; PIC, pathogen-infected cells; SC, surviving cells; V, vacuole. From Wang and Valkonen (2009) with permission of the publishers.

preferential elimination of virus are not yet understood, but they presumably involve inactivation both of intact virus already synthesized and of the means for making more. A protocol suitable for demonstrating heat treatment curing of a plant virus is given by Dijkstra and de Jager (1998). iii. Low Temperatures and Cryotherapy The effect of holding plants at lower than normal temperatures on virus survival has not been widely investigated. Low temperatures might be expected to have little effect on viruses that are stable in vitro. In a few instances, growth at low temperatures has given virus-free plant material. Selsky and Black (1962) grew cuttings from sweet clover plants infected with WTV at 14°C, and no tumors developed even after several vegetative generations. After three

generations, cuttings were taken from the plants and grown under normal greenhouse conditions. Ninety-five percent of these gave rise to a second generation of greenhousegrown cuttings that were 90% free of virus as indicated by absence of tumors. However, maintenance of three peach cultivars at 4°C for long periods did not free them of PNRSV (Heuss et al., 1999). Potato and chrysanthemum plants freed from four different viruses were regenerated from meristem tip cultures that had been held for 6 months in the dark at 6–7°C (Paduch-Cichal and Krycyznski, 1987). Cryotherapy (reviewed by Wang and Valkonen, 2009) uses the techniques of cryopreservation to produce virusfree regenerants. The basic features of the procedure are shown in Figure 14.24.

Chapter | 14  Ecology, Epidemiology, and Control of Plant Viruses

843

Basically, cryotherapy kills the infected, more differentiated, cells but not the virus-free least differentiated meristematic cells which then regenerate giving a high proportion of shoots that are virus free. This technique has been shown to eradicate not only viruses but also phytoplasma and other bacteria-like pathogens from species of at least six plant families including important crops such as potato, sweet potato, banana, and citrus. As with meristem culture, cryotherapy is only of use in eliminating viruses that do not invade the plant meristem (Gallard et al., 2011). However, when it is combined with thermotherapy a higher proportion of virus-free plants can be obtained (Wang et al., 2008). iv. Meristem Tip Culture (reviewed in Faccioli and Marani, 1998; Grout, 1999)  The distribution of virus in apical meristems was considered in Chapter  10, Section V, E, 8. Culture of meristem tips has proved an effective way of obtaining vegetatively propagated plants free from certain viruses. Hollings (1965) defined meristem tip culture as aseptic culture of the apical meristem dome plus the first pair of leaf primordia. This piece of tissue is about 0.1–0.5 mm long in different plants. The minimum size of tip that will survive varies with different species. For example, it is necessary to use tips at least 0.3 mm long to obtain survival of rhubarb (Walkey, 1968). The kind of meristem tip usually taken is illustrated in Figure 14.25. The smaller the excised tips are at the time of removal, the better the chance that they will give rise to virus-free plants, although the more difficult they are to regenerate. For many plants, at least with the culture methods currently used, one leaf primordium needs to be included to get regeneration of a complete plant. A wide range of nutrient media have been used by different workers. The basic ingredients are an appropriate selection of mineral salts (macro- and micronutrients), sucrose, and one or more growth-stimulating factors such as indole acetic acid or gibberellic acid, sometimes in agar. Only a proportion of meristem tip cultures yield virusfree plants. It is not always clear to what extent the success of the method depends on: (i) the regular absence of virus from meristem tissue, some tips being accidentally contaminated; (ii) some meristematic regions in the plant containing virus and others containing none; or (iii) virus present in the meristem being inactivated during culture on the synthetic medium. Some viruses, for example, those present in members of the Araceae (Hartman, 1974), appear to be readily eliminated by culture in a suitable medium at 20–25°C. For others, such as TRSV and PVX, most or all such cultures remain infected. In this situation, it is now common practice to combine meristem tip culture with heat therapy as discussed in the Section III, A, 3, b, ii.

FIGURE 14.25  Apical meristem tip culture. Panel (A) Stem of potato a week after it emerged from a dormant meristem. Panel (B) Plantlet of potato at a stage ready to be transferred to soil. Panel (C) A histological section along the axis of the apical meristem of a potato sprout showing a two-leaf primordium. The piece including one leaf primordium that is excised for tip culture is shown above the black line. From Kassanis and Varma (1967) with permission of the publisher.

As an alternative to direct culture on a synthetic medium, shoot tips up to ≈1.0 mm long may be grafted aseptically onto virus-free seedling plants growing in vitro. Several viruses have been eliminated from peaches by this procedure (Navarro et al., 1983). The additional treatment of “electrotherapy” before meristem culture has been used to free potatoes from PVX (Lozoya-Saldaña et  al., 1996). In this treatment, potato stems were exposed to 5, 10, or 15 mA for 5–10 min before the axillary bud was taken. Organogenesis and virus elimination were both stimulated by the electrical treatment. Where the virus occurs in the apical meristem it may be difficult to obtain virus-free plants by tip culture (Toussaint et al., 1984). Virus-free plants of several important tropical food crops have been obtained using meristem tip culture.

844

These include cassava (Adejare and Coutts, 1981), sweet potato (Frison and Ng, 1981), and various aroids (Zettler and Hartman, 1987). A protocol suitable for demonstrating curing of a plant virus by meristem culturing is given by Dijkstra and de Jager (1998). v. Tissue Culture  Culture of single cells or small clumps of cells from virus-infected plants may sometimes give rise to virus-free plants. For example, two viruses were eliminated from Euphorbia pulcherrima by cell suspension culture followed by regeneration of plants in vitro (Preil et al., 1982). Plants regenerated from shake subculture of small pieces of tobacco tissue originally from TMV-infected plants were free of TMV (Toyoda et al., 1985). A significant proportion of calli obtained from yellow-green areas of TMV-infected Nicotiana tomentosa gave rise to regenerated plants that were free of virus (White, 1982). This may mean that some cells in TMV-infected zones of the leaf are in fact free of virus, as appears to be the situation for some cells in TYMV local lesions. In coupling tissue culture with heat treatment, BBTVinfected plantlets of Cavendish banana were exposed to 40°C for 16 h per day for 12 weeks but this failed to eliminate the virus (Wu and Su, 1991). Culturing for 3 months at 35°C gives some healthy buds (Wu and Su, 1991) as does culturing at 28°C for 9 months (Thomas et al, 1995). As noted in Chapter 7, Section IX, B, 3, a, tissue culture is a stress that can activate some EPRV, such as BSV. vi. Chemotherapy Chemotherapy is discussed below in Section IV, C. c.  The Importance of Using Selected Clones The selection of horticulturally phenotypically desirable clonal material free of virus infection is an important aspect of any program. Selection may need to be carried out both before and after the material has been rendered virus free by any of the preceding procedures. For example, in New Zealand the planting of apple trees freed from virus infection by heat therapy has resulted in higher yields and better trees, but problems have occurred with poor skin color in colored varieties. This may have been due to poor clone selection prior to treatment (Wood, 1983). The problems caused by variation are even greater if clones are regenerated from single cells. Similarly, there may be horticultural variability in the material after it has been freed of virus. For example, van Oosten et al. (1983) noted variation in fruit skin properties in Golden Delicious apples that had been rendered virus free. d.  The Importance of Adequate Virus Testing Plants found to be apparently free of the virus at an early stage of growth may develop infection after quite a long

Plant Virology

incubation, so that, in practice, it is very important that apparently virus-free plants obtained by meristem tip culture be tested over a period before release. For example, Mullin et  al. (1974) monitored the progeny of meristemcultured strawberry plants and found them to be still free of graft-transmissible disease after 7 years. The finding that sequences of certain reverse transcribing plant viruses can be activated by stresses such as tissue culture and crossing (see Chapter 7, Section IX, B, 3) throws an even greater emphasis on the need for robust diagnostic procedures and frequent monitoring.

4.  Propagation and Maintenance of VirusFree Stocks (reviewed by Hadidi et al., 1998) Once suitable virus-free material of a variety is obtained, it has to be multiplied under conditions that preclude reinfection of the nuclear stock and that allow the horticultural value of the material to be assessed with respect to trueness to type. Nuclear stock is then further multiplied for commercial use. This multiplication and distribution phase requires a continuing organization for checking on all aspects of the growth and sale of the material. A classic example is the potato certification scheme in Great Britain, which, over many decades, led to a two- to threefold increase in yield, much of which was due to decreased incidence of virus infection. Tested foundation stocks, which are virtually free of virus, are grown in isolation in parts of Scotland that are unfavorable to early aphid migration and colonization (Todd, 1961). High-grade stocks are grown from this seed elsewhere in Britain, in areas selected because of the low incidence of aphid vectors. Health of the stocks is regularly checked. The use of systemic insecticides has extended the areas in which seed potato crops can be grown (for reviews, see Ebbels, 1979; Slack and Singh, 1998). Many such schemes are now in operation around the world for a variety of agricultural and horticultural plants, including stone and pome fruits, grape vines, and berry fruits, as well as potatoes (Hadidi et al., 1998). For example, the Australian Fruit Variety Foundation supplies virusfree trees to Australian growers (Smith, 1983). On the other hand, for some groups of plants, particularly those grown for cut flowers and bulbs, lack of cooperation by individual growers may limit the effective application of virus eradication programs. It may be possible to obtain rapid initial multiplication of virus-free material. For example, Logan and Zettler (1985) describe a procedure involving repeated rapid shoot proliferation on an appropriate medium that has the potential to produce more than 50,000 virus-free gladioli within 30 weeks from a single shoot tip. As virus-free material is introduced into commercial planting, grower cooperation is essential for the implementation of measures to minimize reinfection. Avoidance of soil containing nematode

845

Chapter | 14  Ecology, Epidemiology, and Control of Plant Viruses

vectors may be important in the propagation of virus-free crops such as hops (Cotten, 1979). One problem that often arises as a certification scheme develops is that many plants need to be checked for infection before release. Markham et  al. (1948) suggested a group testing procedure to save labor. Using appropriate sampling conditions, the number of plants infected in a field can be estimated from the proportion of groups found to be infected. The reliability of the test of course increases as the number of plants tested increases. Any sampling and testing scheme should be considered from two points of view: first, the probability required that a crop of a certain “high” level of infection will be rejected, and second, the probability required that a crop of a certain “low” level of infection will be accepted. It is possible to construct schemes having various probability levels of acceptance or rejection. This sort of procedure has been developed by Marrou et  al. (1967) for testing lettuce seeds for freedom from LMV. In their test, several hundred seeds are extracted together and inoculated to a sensitive indicator host; results are interpreted in relation to graphs or tables based on the binomial distribution. When large numbers of virus-free plants or seeds are being produced, it is necessary to have an “audit trail” so

5.  Modified Planting and Harvesting Procedures a.  Breaks in Infection Cycle Where one major susceptible annual crop or group of related crops is grown in an area and where these are the main hosts for a virus in that area, it may be possible to reduce infection significantly by ensuring that there is a period when none of the crop is grown. A good example of this is the control of planting date of the winter wheat crops in Alberta to avoid overlap with the previous spring- or winter-sown crop (Figure 14.26). This procedure, together with elimination of volunteer wheat and barley plants and grass hosts of WSMV before the new winter crop emerges, can give good control in most seasons.

Aug

y

Jul y

Sept

W Growth

Vo l

at

un

te

e

Oct he

whe

r

W

S pr i n g

in r

June

te

at

or

ba

rle

that any problems that may arise can be traced back to source. One way of doing this is to use bar coding coupled to computer records that would enable individuals or batches to be followed through all the stages of propagation and release. This is especially important for hosts of endogenous pararetroviruses such as banana (see Box 7.5) where multiplication from mother plants (e.g., by tissue culture) can lead to activation of an integrated virus.

May

Nov

Apr

Dec

Mar

Jan Feb

FIGURE 14.26  Wheat streak mosaic disease cycle. Preventing the infection of winter wheat in the autumn is the key to controlling this disease in southern Alberta. Dark area, period during which effective control can normally be achieved; broken hatched bands, problems presented by volunteer seedlings, early-seeded winter wheat, and/or late-maturing spring wheat or barley; arrows, transfer of virus by windblown mites. Diagram courtesy of T.G. Atkinson; From Matthews (1991).

846

b.  Changed Planting Dates The effect of infection on yield is usually much greater when young plants are infected. Furthermore, older plants may be more resistant to infection and virus moves more slowly through them. Thus, with viruses that have an airborne vector, the choice of sowing or planting date may influence the time and amount of infection. The best time to sow will depend on the time of migration of the vector. If it migrates early in the growing season, late sowing may be advisable. If it is a late migration, early sowing may allow the plants to become quite large and probably less susceptible before they are infected. To reduce the incidence of rice tungro disease, which is transmitted by the rice green leafhopper, in irrigated rice grown under highly intensive conditions, farmers are encouraged to plant synchronously, to allow a break between crops and to avoid very late planting. In Indonesia they are advised to adopt recommended planting dates so that the plants are not exposed to infection when they are most vulnerable to incoming vectors (Manwan et al., 1985; Sama et al., 1991) For any particular crop, the effectiveness of changed planting or harvesting dates in minimizing virus infection has to be considered in relation to other economic factors. Thus, Broadbent et  al. (1957) found that potatoes planted early and lifted early had reduced virus infection, but a quite uneconomic reduction in yield also resulted. Thus there has to be a balance between reducing the possibility of virus infection and the best growing season for maximum yield. c.  Plant Spacing The fact that a higher percentage of more closely spaced plants tend to escape infection than widely spaced ones is discussed in Section II, D, 2, b. The practical effects of planting density on incidence of a virus and its aphid vectors and on plant yield are well illustrated from the work of Hull (1964) and of A’Brook (1964, 1968) on groundnuts and rosette virus disease. A’Brook tested a wide range of planting densities over several seasons. Aphid densities were higher over well-spaced plants. Figure 14.27 shows the marked reduction in rosette infection with higher plant densities (number of infections was transformed to allow for multiple infections).

Percentage rosette, multiple infection transformation

A break during the year where no susceptible plants are grown has proved effective in the control of certain other viruses with limited host ranges, even though they have efficient airborne vectors. Control measures of this sort may be difficult to implement in developing countries where a major food plant is traditionally grown in an overlapping succession; rice is the major example. The increased use of irrigation in the tropics and protected cropping in cold temperate regions limits the options available to growers for breaking the infection cycle.

Plant Virology

400

300

200

100

0 5

10 15 Week after planting

20

FIGURE 14.27  Effect of planting density on the percentage of groundnut plants infected with rosette virus. Plants per acre: …, 9600; --, 19,050; −·−, 38,550; — —, 78,750; ———, 160,200. From A’Brook (1964) with permission of the publishers. For derivation of multiple-infection transformation, see Gregory (1948).

Although larger populations decreased rosette incidence, plant competition tends to decrease yield with the very high densities, and seed costs are greatly increased. The objective is to use a planting rate that will achieve complete ground cover as soon as possible without reducing yield significantly due to competition and to balance potential yield against possible loss. Grain yields are significantly higher for some rice varieties planted in a close spacing, which reduces the incidence of rice tungro disease (Shukla and Anjaneyulu, 1981). Incidence of yellows in sugar beet is also reduced by increasing plant density (Johnstone et al., 1982). Thus, the phenomenon may be a fairly general one. d.  Destruction of Aerial Parts of the Plant To limit virus spread late in the season, some certification schemes for virus-free vegetative stocks require the crop to be harvested before a certain date. This applies to seed potatoes in Holland, where lifting of the crop or killing of the haulms is required before a date determined each season from aphid trapping data (De Bokx, 1972). Fodder-beet and mangolds are stored overwinter in clamps to supply animal feed. The retention of these into the spring when the roots start resprouting can act as reservoirs leading to severe infections of BMYV and BYV (Smith, 1986). e.  Isolation of Plantings Where land availability and other factors permit, isolation of plantings from a large source of aphid-borne infection might give a useful reduction in disease incidence.

847

Chapter | 14  Ecology, Epidemiology, and Control of Plant Viruses

Thus, isolation of beet fields from a large source of beets infected with two viruses markedly reduces infection (Figure 14.28). Production of virus-free seed potatoes is frequently carried out in areas that are well separated from crops being grown for food. Distances may be controlled

Percent disease

30 Early yellows

20

10

Early mosaic 20 5 10 15 Distance from large source of disease (miles)

FIGURE 14.28  Effect of distance from a large source of infection with two aphid-borne viruses on percentage of sugar beet plants infected early in the season. The large source was about 30,000 acres of infected beets in the Sacramento Valley, California. From Shepherd and Hills (1970) with permission of the publishers.

Severe CTV strains in a latent condition, with no apparent spread for 20–50 years

by legislation, and the planting of home garden potatoes forbidden within a prescribed area. f.  Prevention of Long-Distance Spread Most agriculturally advanced countries have regulations controlling the entry of plant material in attempts to prevent the entry of diseases and pests not already present. Many countries also now have regulations aimed at excluding specific viruses and their vectors, sometimes from specific countries or areas. The setting up of quarantine regulations and providing effective means for administering them is a complex problem with economic and political factors frequently having to be considered. Quarantine measures may be well worthwhile with certain viruses, such as those transmitted through seed, or in dormant vegetative parts such as fruit trees and budwood. There is good evidence indicating that infected rootstocks were important in the worldwide distribution of grape vine viruses (Luhn and Goheen, 1970). Similarly, the spread of CTV worldwide is associated with infected budwood and exacerbated by efficient transmission by its aphid vector (Figure 14.29).

Natural spread of severe CTV strains by Aphis gossypii, inducing scattered CTV outbreaks

Campaigns of CTV detection/eradication of infected trees and replanting on either sour orange or CTV tolerant rootstocks

Endemic Condition California Florida Spain Israel

(A)

Introduction of “tristeza” into a citrus industry via CTV-infected budwood

Presence or arrival of Toxoptera citricida into a citrus industry with no apparent CTV spread during 1–5 years

Endemic Condition Spread of severe CTV strains by T. citricida, scattered first, then widespread

Emergence of CTV strains that cause severe stem pitting with a deteriorating effect on tree vigor and fruit size

Removal of dead trees and reestablishment of the citrus industry on CTV-tolerant rootstocks

Argentina Brazil Uruguay Peru Venezuela South Africa

Occurrence of citrus blight, exocortis, cachexia, and other virus and virus-like diseases in trees grafted on CTVtolerant rootstocks

(B)

(C)

FIGURE 14.29  Introduction of CTV and epidemics in several parts of the world. Panel (A) CTV epidemics in California, Florida, Spain, and Israel with the melon aphid Aphis gossypii as primary vector. Panel (B) CTV epidemics in Argentina, Brazil, Uraguay, etc., where CTV after arrival and co-localization of the brown citrus aphid, Toxoptera citricida. In both cases, CTV was present in a latent condition in CTV-infected propagative material brought from abroad. The simultaneous presence of CTV strains and T. citricida notably shortens the time of occurrence of CTV epidemics. Panel (C) After 10–20 years of CTV epidemics and establishment of T. citricida, the citrus industries contend with the occurrence of severe CTV stem-pitting strains, citrus blight, and other virus and virus-like diseases. From Rochon-Peña et al. (1995) with permission of the publishers.

848

Kahn (1976) suggested the use of aseptic plantlet culture for the transfer of vegetatively propagated material between countries. Cooperation between importing and exporting countries or areas may greatly improve the effectiveness of quarantine regulations. Quarantine in relation to plant health is reviewed in Hewitt and Chaiarappa (1977), Khan (1989), Foster and Hadidi (1998), and Waterworth (1998). FAO/IBPRG-IPGRI produce guidelines for the safe movement of germplasm of specific crops (Diekmann and Putter, 1996); FAO also organizes the World Information and Early Warning System (WIEWS) (http://apps3.fao.org/wiews/wiews.jsp). The value of quarantine regulations will depend to a significant degree on the previous history of plant movements in a region. For example, active exchanges of ornamental plants between European countries have been going on for a long period, leading to an already fairly uniform geographical distribution of viruses infecting this type of plant (Lovisolo, 1985). On the other hand, the European Plant Protection Organization found it worthwhile to set up quarantine regulations against fruit tree viruses not already recorded in Europe (Ronde Kristensen, 1983; Krczal, 1998). It is difficult to obtain any objective assessment as to how effective quarantine regulations have been in limiting long-distance spread of viruses. Because of its long-standing geographical isolation and the fact that almost all crop species have been imported, it is likely that most of the plant viruses recorded in New Zealand have arrived from other countries within the last 200 years. Viruses were first listed in New Zealand quarantine regulations in 1952 and by 1990 about 130 viruses had been found in that country (Matthews, 1991). One example is the introduction of RgMV, which is thought to have been introduced to New Zealand, together with its mite vector, on perennial ryegrass vegetative material (Guy et al., 1998). Studies on the CP of the virus suggest that there are two strains present, one in the south and one in the north indicating two separate introductions. There is also good evidence in particular instances that quarantine measures can limit further long-distance dispersal of viruses. For example, 37 out of 61 importations of cuttings of Datura species from South America grown under quarantine in the United States were found to be infected with a range of viruses (Kahn and Monroe, 1970). South American potato viruses have been found in potatoes in quarantine in Europe. An effective quarantine system requires an effective technological infrastructure that is capable of detecting viruses under a variety of circumstances. Furthermore, quarantine must be concerned not only with important crop species but also with species, unimportant in themselves, that may harbor viruses infecting major crops. However, natural spread of some viruses over very long distances by invertebrate vectors may negate some of the effects of quarantine measures.

Plant Virology

In spite of many countries having regulations designed to prevent the entry of damaging viruses they can spread internationally very rapidly. A good example is the rhizomania disease of sugar beet (Box 14.1). However, any quarantine system is only as effective as the state of knowledge at that time as exemplified by the introduction of RBDV into New Zealand in raspberry variety “Canby” in 1965 (Wood and Hall, 2001).

B.  Control or Avoidance of Vectors Before control of virus spread by vectors can be attempted, it is necessary to identify the vector(s). This information has sometimes been difficult to obtain. Not uncommonly, it is an occasional visitor rather than a regular colonizer that is the main or even the only vector of a virus. Furthermore, some aphid species are more efficient vectors than others. For instance, the brown citrus aphid (Toxoptera citricida) is a much more efficient vector of CTV than is the melon aphid (Aphis gossypii) (Figure 14.30). Control or avoidance of invertebrate or fungal vectors is of prime importance for the limitation of crop damage by viruses that have such vectors. For this reason more than one method for control may be used simultaneously for a particular crop, location, virus, and vector.

1.  Airborne Vectors a. Insecticides (reviewed by Perring et al., 1999; Dedryver et al., 2010) A wide range of insecticides is available for the control of insect pests on plants. To prevent an insect from causing direct damage to a crop, it is necessary only to reduce the population below a damaging level. Control of insect vectors to prevent infection by viruses is a much more difficult problem, as relatively few winged individuals may cause substantial spread of virus. Contact insecticides would be expected to be of little use unless they are applied very frequently. Persistent insecticides, especially those that move systemically through the plant, offer more hope for virus control. Viruses are often brought into crops by winged aphids, and these may infect a plant during their first feeding, before any insecticide can kill them. When the virus is nonpersistent, the incoming aphid when feeding rapidly loses infectivity anyway, so that killing it with insecticide will not make much difference to infection of the crop from outside. On the other hand, an aphid bringing in a persistent virus is normally able to infect many plants, so that killing it on the first plant will reduce spread. As far as subsequent spread within the crop is concerned, similar factors should operate. Spread of nonpersistent viruses should not be reduced as much by insecticide treatment as a persistent virus where the insect requires a fairly long feed on an infected plant. Thus,

849

Chapter | 14  Ecology, Epidemiology, and Control of Plant Viruses

% CTV infected trees

100 T. citricids induced epidemic

80 60

A. gossypii actual predicted

40 20 0 0

2

4

6

8

10 12 Time (years)

14

16

18

20

FIGURE 14.30  Comparative increase of CTV infection in field situations when vectored by the brown citrus aphid (Toxoptera citricida), an efficient vector, and by the melon aphid (Aphis gossypii), a less efficient vector. Data for the brown citrus aphid was taken from test plots in Costa Rica and the Dominican Republic. Data for the melon aphid was taken from surveys and experimental plots in Spain, Florida, and California. Initial infection levels were less than 1%. Note “stairstep” progression in infection with the melon aphid which is believed to correspond to periodic heavy aphid migrations. From Garnsey et al. (1998) with permission of the publishers.

spread of the persistent PLRV in potato crops is substantially reduced by appropriate application of insecticides but spread of the nonpersistent PVY is not (Burt et  al., 1964; Webley and Stone, 1972). Burt et al. (1964) used systemic insecticides, applied as sprays at different times during the season, to estimate the stage at which most spread of PLRV occurred in potatoes in England. Their results emphasize the importance of spread early in the season by winged aphids and the need for plants to be made lethal for aphids as early as possible. Like PVY, other nonpersistent viruses, such as LMV, have not been controlled in any useful way by insecticide treatments. A screen or “trap crop” of plants sprayed with a systemic insecticide may reduce virus infection in plants growing within the screened field (Gay et  al., 1973). Use of inappropriate insecticides may actually cause an increase in virus infection, either by disturbing the aphids present in the crop or by destruction of predators (Broadbent et al., 1963). Spraying as a farming operation has certain disadvantages. It is an extra operation to be performed, tractor damage to the crop occurs, and spraying may not be practicable at the time required. Drifting spray can also lead to damage in other crops. Persistent systemic insecticides applied in granular form at the time of planting overcome many of these difficulties. With leafhopper vectors, the speed at which they are killed after feeding on a treated plant may be an important factor for virus control. For example, several synthetic pyrethroids that killed the vector Nephotettix virescens within 7 min prevented spread of the rice tungro disease (Anjaneyulu and Bhaktavatsalam, 1987). Slower-acting chemicals were ineffective in reducing virus incidence. From the point of view of the economics of insecticide use it may be important to forecast whether applications are necessary and, if so, to define optimal times for treatment.

For example, in China two crops of rice followed by winter barley and wheat give the planthopper Laodelphax striatella a year-round succession of hosts. The best timing for the application of insecticides has been found to be at the winter seedling stage of barley and wheat and at the early paddy stage of the second crop of rice (Yi-Li et al., 1981). In India, where an overlapping cropping pattern is also common, application of systemic insecticides under rice nursery conditions appears to be the most effective for the control of tungro disease (Shukla and Anjaneyulu, 1982). Aphid infestation and disease forecasting data can be an important factor in the economic use of insecticides (Dedryver et  al., 2010). Sometimes a long-term program of insecticide use aimed primarily at one group of viruses will help in the control of another virus. Thus, the welltimed use of insecticides in beet crops in England, aimed mainly at reducing or delaying the incidence of yellows diseases (BYV and BMYV), has also been a major factor in the decline in the importance of BtMV in this crop (Heathcote, 1973). A warning scheme to spray against the vectors of beet yellows viruses was initiated in the United Kingdom in 1959 and is based on monitoring populations of aphids in crops from May until early July (reviewed in Dewar and Smith, 1999). As well as the problems described above, there may be other adverse biological and economic consequences related to the use of insecticides. These include (i) development of resistance by the target insect to the insecticide (Georghiou and Saito, 1983); (ii) resurgence of the pest once the insecticide activity has worn off; and (iii) possible effects on humans and other animals in the food chain. The use of unsprayed refuges can help to reduce the development of resistance to insecticides (Carriére et al., 2012). In spite of these problems, the use of insecticides for virus control is widespread. This is because, among other

850

reasons: it is the way that growers control pests and thus, they think it will control viruses; there are few alternative strategies; it is difficult to predict epidemics and thus, prophylactic applications are used; the cost of materials is low relative to the total production costs. b.  Oil Sprays (reviewed by Perring et al., 1999) Bradley (1956) and Bradley et  al. (1962) showed that when aphids carrying PVY probed a membrane containing oil their subsequent ability to transmit the virus was greatly reduced. These observations led to considerable interest in the possibility of using oil sprays in the field to control viruses spread by aphids. Compared to synthetic insecticides, oil sprays have considerable appeal because of their lack of toxicity for man and animals. However, various limitations have emerged, and their commercial use is not widespread. In some reports, oil sprays have given useful results with field trials against a range of nonpersistent viruses (Hein, 1971) and also BYV, which is semipersistent. However, oil does not prevent the spread of persistent viruses. Other limitations involve possible plant toxicity, volatility, or viscosity of the oil (de Wijs, 1980), adequate coverage of the leaves, removal of the oil cover by rain or irrigation water, and effects on the marketable quality of the food produced. Mineral oil sprays have proved useful in controlling viruses in bulb crops in the Netherlands (Asjes, 1978, 1980), in controlling PVY on potato seed crops in Brittany (Kerlan et al., 1987), and on limiting the spread of whiteflytransmitted geminiviruses on tomatoes in Sudan (Yassin, 1983). On the other hand, no control of several nonpersistent viruses was obtained with oil sprays in England (Walkey and Dance, 1979), or of MDMV in sweet corn in Ohio (Szatmari-Goodmann and Nault, 1983). The combined use of mineral oils and pyrethroids gives better control in trials with PVY and BtMV than either component alone (Gibson and Rice, 1986). The combination of oil sprays and a fallow or grass border significantly reduces the spread of PVY into potatoes (Boiteau et al., 2009). The mechanism by which the application of oil controls virus spread is unknown. There are two hypotheses: (i) that it affects the acquisition or inoculation of the virus by the vector and (ii) that it affects the infection process of the virus. Oil sprays do not appear to affect significantly the susceptibility of the plant, aphid behavior, or virus infectivity. When aphids probe leaves sprayed with oil, the oil spreads readily over the whole length of the stylets. This observation and various experiments summarized by Vanderveken (1977) and Wang and Pirone (1996) support the idea that oil alters the surface structure or charge on the stylets, thus limiting the ability to adsorb (or release) virus particles. In light of the wide range of non- and semipersistently transmitted viruses that oil interferes with, it is likely that the mechanism is non-specific and is not targeted to any specific virus–vector interaction.

Plant Virology

The normal feeding behavior of the leafhopper Nephotettix virescens is disrupted on rice leaves sprayed with oil. There is reduced phloem feeding and increased xylem feeding, with restless behavior, repeated probing, and profuse salivation. These effects may explain the reduced survival time of the insect and the decrease in virus transmission (Saxena and Khan, 1985). c.  Pheromone Derivatives (reviewed by Vandermoten et al., 2012) The process of virus transmission is influenced by a variety of insect behaviors, such as leaving and alighting on plants, probing and feeding, interactions with adjacent insects, and response to alarms. These behaviors are influenced by a wide range of chemicals and it is suggested that manipulating them may be a way of effecting virus control. Derivatives prepared from the pheromone (E)-βfarnesene (EBF) and related compounds interfere with the transmission of PVY by M. persicae in greenhouse experiments (Gibson et al., 1984); application of EBF also reduced the colonization of plants by Acyrthosiphon pisum (Wohlers, 1981). However, the transgenic expression of EBF does not repel the colonization, reproduction, or production of M. persicae alates (Kunert et al., 2010). On the other hand, such transgenic plants attract aphid predators (de Vos et al., 2010). d.  Non-chemical Barriers Against Infestation (reviewed by Hooks and Fereres, 2006) There are various forms of non-chemical barriers against virus vectors including plant and fallow barriers around the crop, cover crops within the crop, and artificial winged vector repellents. i. Plant Barriers  An ideal plant barrier should be a nonhost for the virus and vector but appealing to aphid landing and probing, and attractive to their natural enemies. As vectors lose nonpersistently transmitted viruses on short feeds (see Chapter 12, Section III, A), a plant barrier surrounding the crop should reduce such viruses entering the crop. Table 14.1 lists some examples of barrier crops that have been used to control the movement of nonpersistently transmitted viruses into a crop. There are several hypotheses on the mechanisms by which barrier crops control virus spread. These include operating as a virus-sink in which the vector “loses” the virus in a non-host, being a physical barrier or being a trap crop which is a plant species (preferably a non-host to the virus) that is more attractive to the targeted vector than the neighboring primary crop and in which the vector can be controlled, say by spraying; these are discussed in detail by Hooks and Fereres (2006). A tall cover crop will sometimes protect an undersown crop from insect-borne viruses. For example, cucurbits

851

Chapter | 14  Ecology, Epidemiology, and Control of Plant Viruses

TABLE 14.1  Effects of Barrier Plants on Aphids Transmitting Nonpersistent Plant Viruses Barrier Plant(s)

Crop Protected

Virus Targeted Response

Factors Involved

Buckwheat, weeds, and yellow mustard

Zucchini

PRSV-W

Increased marketable yields during 1 of 2 years

Delayed virus onset, no. of alates reduced

Maize, brinjal

Chilli

CVMV

Higher yields when interplanted with barrier plant; maize better protector

Less alate vectors and slower disease spread faster than in monocrop

Maize, sorghum, sunflower

Chilli

CMV

Reduced disease incidence and increased yield; maize most effective barrier; insecticidal sprays on barrier plants further suppressed disease spread

Prevents direct aphid colonization of chilli plants

Sorghum

Pepper

CMV, PVY

Significant reduction of CMV spread and Barrier acted as sink for both delay of PVY spread viruses

Pearl millet

Cowpea

CpMV

Reduction in infected plants; yield increase further by use of insecticide on barrier

Vector population greater near barrier and reduced significantly by insecticide

Sorghum, maize, okra, sunflower, amaranthus

French bean

BCMV

Maize most effective at reducing disease incidence and increasing yield followed by sorghum

Taller barrier broke aphid flight by intercepting them and then served as sink

Straw mulch

Lupin

BYMV

Reduced rate and amount of virus spread Decreased landing rate of incoming vector alates

Wheat straw mulch

Potato

PVY

Reduced PVY incidence; no significant impact on yield

Plant barrier

Mulch

Reduced optical contrast between plant and soil

Adapted from Hooks and Fereres (2006) with permission of the publishers.

are sometimes grown intermixed with maize. Broadbent (1957) found that surrounding cauliflower seedbeds with quite narrow strips of barley, which is not a host to crucifer viruses, reduces virus incidence in seedlings to about onefifth. Many incoming aphids are assumed to land on the barrier crops, feed briefly, and either stay there or fly off. If they then land on the Brassica crop they may have lost any nonpersistent virus they were carrying during probes on the barrier crop. ii. Photoselective Barriers Migratory flights and host selection by many plant vector species is controlled by the insect’s response to different regions of the light spectrum (see Chapter  12, Section II, A, 2, c). UV-blocking materials, such as polyethylene films and nets, can be very effective for controlling insect vectors in protected crops (greenhouses and tunnels) (reviewed by Diaz and Fereres, 2007). The exclusion of part of the UV radiation within the greenhouse environment has a marked effect on insect orientation, movement, and on the spread of insecttransmitted virus diseases. The level of protection of the different UV-blocking materials varies among different designs of greenhouses and the geographic location that

determines different internal climatic conditions and the amount of UV and visible light absorbed and transmitted within the covered structures. For example, UV nets that reflected the highest amount of UV radiation are best at protecting pepper crops against the main pests [thrips, whiteflies, and the broad mite (Polyphagotarsonemus latus)] (Legarrea et al., 2010). In unprotected field crops, the reflected UV light from aluminum strips laid on the ground is thought to repel aphids coming in to land. Reflective aluminum polythene mulches reduce the incidence of WMV and increase yields of cucurbits in Western Australia under conditions where both insecticide and oil sprays prove ineffective (McLean et al., 1982). However, these reflective mulches are expensive, and where they have come into regular use, difficulties in disposal at the end of the season may occur, at least when disposal by burning is forbidden (Nameth et al., 1986). A strip of sticky yellow polythene, 0.5 m wide and 0.7 m above the soil, surrounding trial plots reduces the incidence of aphid-transmitted viruses in peppers (Cohen and Marco, 1973). Yellow polythene mulch significantly delays the appearance of a yellow vein mosaic virus in okra in India (Khan and Mukhopadhyay, 1985). Nets

852

Plant Virology

spread above the crop may also reduce the winged aphid population and virus infection while allowing normal plant growth. Coarse white nets may be the most effective under some conditions (Cohen, 1981). However, most of the findings noted in this section have not moved beyond the experimental stage into commercial practice. e.  Vector Resistance Plant resistance to vectors is discussed in Sections III, E and F. f.  Control by Predators or Parasites Parasites and predators undoubtedly play a major role in limiting the population growth of aphids and other insects. As well as using integrated pest management strategies such as selection of variety, planting date, and the planned and controlled use of insecticides, a potential strategy for increasing the effectiveness of natural enemies is to incorporate natural enemy-enhancing traits into crop plants by breeding (reviewed by Bottrell and Barbosa, 1998). This approach has not been used much for virus control. However, it does have some promise under certain circumstances as exemplified by Figure 14.31, which shows the results of an experiment by Evans (1954) in Tanzania. He established small colonies of Aphis craccivora (one adult and five nymphs) on single plants in various parts of a field of groundnuts. He then followed the growth of the aphid colonies and the appearance of predators. Under some circumstances, predators might play a part in limiting spread of a virus, but generally they will have little effect if they arrive after the early migratory aphids, which are so important for virus spread. In West Africa, introduction of fungal and hymenopterous parasites of the mealybug vectors to control CSSV were unsuccessful, even though the vector is relatively immobile (Thresh, 1958).

2.  Soilborne Vectors Most work on the control of viruses transmitted by nematodes and fungi has centered on the use of soil sterilization with chemicals. However, several factors make general and long-term success unlikely: (i) huge volumes of soil may 8

Predators

30

6

20 10 0

4

s

hid

Ap

0

1

2

2 3

4

5 Days

6

7

8

Predators per plant

Aphids per plant

40

9

FIGURE 14.31  Growth of initially small aphid colonies on groundnuts and their subsequent destruction by predators. From Evans (1954) with permission of the publishers.

have to be treated; (ii) a mortality of 99.99% still leaves many viable vectors; and (iii) use of some of the chemicals involved has been banned in certain countries, and such bans are likely to be extended. In any event, chemical control will be justified economically only for high-return crops, or crops that can remain in the ground for many years. However, some recent advances in nematode control procedures may be applicable to the control of viruses that they transmit and may be adaptable to the control of fungus-transmitted viruses. a. Nematodes (reviewed by Zasada et al., 2010; Li et al., 2011; Molinari, 2011) There are four basic strategies for nematode control: (i) exclusion or avoidance; (ii) reduction of the initial population density; (iii) plant resistance to nematodes; and (iv) restriction of the current or future crop damage. Within each strategy, there are various tactics that reduce the nematode population or minimize the interaction that the nematode has with the plant. As with other vectors, it is important to have a method for identification of the potential virus vector species, and there have been considerable advances in the development of molecular diagnostics (Hyman, 1996). In this section, I will briefly describe these strategies and summarize the approaches already used to control nematode-borne viruses. Some future approaches avoiding the use of methyl bromide are discussed in Zasada et al. (2010), Li et al. (2011), and Molinari (2011). i. Exclusion or Avoidance of Nematodes Exclusion or avoidance is usually by quarantine. However, this can be difficult to implement as large quantities of root vegetables and rooted plants containing soil are traded worldwide. ii. Reduction of Population Density There are several tactics to reduce the initial population density. These include cultural approaches such as use of clean planting stock, crop rotation with a break crop of a species that is not a host for the target nematode, weed host control which is important as several nematode-transmitted viruses are also seed transmitted in weed species, and the use of plant species that are antagonistic to the target nematode species. The main approach to controlling nematode-transmitted viruses has been by the use of nematicides; nematicides fall into two groups, fumigant (e.g., methyl bromide) and nonfumigant (e.g., aldicarb). In principle, this control method should be effective. Movement and dispersal of nematodes are generally slow, so that one treatment might be expected to remain effective for longer periods than with airborne vectors. On the other hand, as pointed out by Sol (1963), infective nematodes may occur at considerable depths. Nematodes in soil samples taken up to 80–100 cm deep were able to infect plants with TRV. Thus, it is possible that fumigated soil could be reinfested by nematodes moving up from deep sites where they had escaped the effects

Chapter | 14  Ecology, Epidemiology, and Control of Plant Viruses

of fumigation. Furthermore, these chemicals are toxic, environmentally damaging, and expensive, and their use is being discontinued in many places. Biological agents antagonistic to nematodes such as nematophagous bacteria (reviewed by Tian et  al., 2007) can provide some control as can the use of soil organic amendments. iii. Nematode Vector Resistance Conventional resistance to nematodes is discussed in Section III, F. iv. Controlling Nematode Virus Vectors Overall, the best way to minimize the impact of nematodes is a combination of the above strategies and tactics in an integrated manner to discourage the nematode and to encourage organisms and soil conditions antagonistic to them (Stirling, 1999). The reduction of nematode populations should lead to a reduction of the chances of plant infection by the viruses that they may carry. b. Fungi (reviewed by Walsh, 1998) There are two agronomic situations in which fungustransmitted viruses are important—fields and nutrient or aquatic hydroponic systems. The major control measures are chemical and virus-resistant plants. There is little detailed information on resistance to the fungal vectors. However, wild sea beet (Beta vulgaris ssp. maritima) contains two interacting factors (QTLs on different chromosomes), Pb1 and Pb2, that confer partial resistance to Polymyxa betae (Asher et al., 2009). In general, attempts to control infection with viruses having fungal vectors by application of fungicides. For example, various fungicides failed to control transmission of BaYMV to winter barley by Polymyxa graminis (Proeseler and Kastirr, 1988). Several fungicides prevented infection of sugar beet by BNYVV in greenhouse trials, but were ineffective in the field, even at high rates of application (Hein, 1987). The zoospores of Olpidium brassicae are susceptible to several fungicides and surfactants in laboratory tests (Tomlinson and Faithfull, 1979). Chemical controls involving surfactants, heavy metals, or fungicides are used mainly in hydroponic systems. Thus the major approach to control fungus-transmitted viruses is the use of virus-resistant plants, for example, controlling SBCMV by developing resistant wheat cultivars (Bayles et al., 2007). Furthermore, there may be some potential sources of resistance to the fungal vector which could be combined with the virus resistance (Asher et al., 2009).

IV.  CONTROL BY PROTECTING THE PLANT FROM SYSTEMIC DISEASE Even if sources of infection are available, and the vectors are active, there is a third kind of control measure available—protecting inoculated plants from developing

853

systemic disease. There are essentially three approaches that have been used to protect plants, using a mild strain of the virus (termed cross-protection or mild strain protection), the use of chemicals, and genetic protection (conventional resistance and transgenic resistance).

A.  Mild Strain Protection (CrossProtection) (reviewed by Urban et al., 1990; Lecoq, 1998) Infection of a plant with a strain of virus causing only mild disease symptoms (the protecting strain; also known as the mild, attenuated, hypovirulent, or avirulent strain) may protect it from infection with severe strains (the challenging strain) (Chapter 9, Section IV, H, 1). Thus, plants might be purposely infected with a mild strain as a protective measure against severe disease. This was first reported by McKinney (1929), who observed that tobacco plants systemically infected by a “green” strain of TMV were protected from infection by another strain that induced yellow mosaic symptoms. While such a procedure could be worthwhile as an expedient in very difficult situations, in many cases it is not to be recommended, for the following reasons: (i) socalled mild strains often reduce yield by about 5–10%; (ii) the infected crop may act as a reservoir of virus from which other more sensitive species or varieties can become more severely infected; (iii) the dominant strain of protecting virus may change to a more severe type in some plants; (iv) serious disease may result from mixed infection when an unrelated virus is introduced into the crop; (v) the genome of the mild strain may recombine with that of another virus leading to the production of a new virus; and (vi) for annual crops, introduction of a mild strain is a labor-intensive procedure. In spite of these difficulties, the procedure has been used successfully, at least for a time, with some crops. A suitable mild isolate should have the following properties: (i) it should induce milder symptoms in all the cultivated hosts than isolates commonly encountered and should not alter the marketable properties of the crop products; (ii) it should give fully systemic infections and invade most, if not all, tissues; (iii) it should be genetically stable and not give rise to severe forms; (iv) it should not be easily disseminated by vectors to limit unintentional spread to other crops; (v) it should provide protection against the widest possible range of strains of the challenging virus; and (vi) the protective inoculum should be easy and inexpensive to produce, check for purity, provide to farmers, and to apply to the target crops. Mild protecting strains are produced from naturally occurring variants, from random mutagenesis or from directed mutagenesis of severe strains. Broadbent (1964) suggested that, because of late infection of greenhouse tomatoes, ToMV often causes

854

a severe reduction in quality of the fruit compared with early infection and that growers who regularly suffer those losses should inoculate their plants at an early stage with a mild strain of the virus. Rast (1975) obtained a nitrous acid mutant of ToMV that was symptomless in tomato. Seedling inoculation with this strain was widely practiced for a time in some Western European countries and in Canada, New Zealand, and Japan. However, cultivars with resistance genes or with multiple genes for tolerance to ToMV have largely replaced seedling inoculation with the attenuated strain in commercial practice. CTV provides the most successful example for the use of cross-protection. Worldwide, this is the most important virus in citrus orchards. In the 1920s, after its introduction to South America from South Africa, the virus virtually destroyed the citrus industry in many parts of Argentina, Brazil, and Uruguay. The successful application of crossprotection by inoculation with mild CTV isolates is reviewed by Moreno et al. (2008). Other viruses and crops for which attempts are being made to develop effective cross-protection include PRSV in papaya (Yeh et al., 1988; Gonsalvez et al., 1998), TMV in pepper (Tanzi et  al., 1986), and ZYMV in courgette (Walkey et  al., 1992). In principle, CSSV should be controllable to some degree by cross-protection with mild strains of the virus (Posnette and Todd, 1955; Hughes and Ollennu, 1994), but various difficulties have prevented its effective application (Fulton, 1986). In particular, the use of the technique was incompatible with the objective of treating all known outbreaks by removal of infected trees. This is no longer feasible, so that there is now scope for using mild strain protection in the worst affected areas of Ghana, where other control measures have been abandoned (Thresh, 2006b). In Chapter  9 I describe the recent developments in understanding host response to virus infection by post-transcriptional gene silencing. It is most likely that one likely mechanism for mild strain protection is by the mild strain “priming” this defense system so that it operates against the superinfecting severe strain. With this in mind, it is important that the sequence of the protecting mild strain is similar to that of the superinfecting severe strain. An analysis of sequence of CTV isolates from different sites and collected at different times showed that the mild strains used in Florida and Spain are very similar to a diverse range of isolates (AlbiachMartí et  al., 2000). This was unexpected as the first two CTV isolates to be sequenced had up to 60% sequence divergence. However, it is possible that, in some instances of mild strain protection, other mechanisms, such as competition for replication sites, operate.

Plant Virology

B.  Satellite-Mediated Protection (reviewed by Tien and Wu, 1991; Jacquemond and Tepfer, 1998) Satellite viruses and RNAs are described in Chapter  5, Section II and fall into three categories, those that enhance the helper virus symptoms, those that have no effect and those that reduce the helper virus symptoms. It is the latter that have potential as biocontrol agents. Most of the work has focused on the satellites of CMV. Tien et  al. (1987) obtained mild strains of CMV by adding selected satellite RNAs to a CMV isolate. This procedure has been tested, with increased yields, in many areas of China for the control of CMV in peppers. The extent of the protective effect depends on such factors as inoculation time, percentage of plants inoculated, the nature of virulent CMV strains already in the field, and variety of pepper. Wu et  al. (1989) compared the degree of protection obtained by preinoculating tobacco and pepper plants with a mild strain of CMV with or without satellite RNA. The presence of satellite RNA increases the protection obtained. Similar results were obtained in greenhouse experiments with CMV in tomato. In field trials, protection is maintained when the virus is introduced by aphids (Montasser et al., 1991). This work has been taken a stage further by Gallitelli et  al. (1991), who inoculated several hundred young tomato seedlings using several varieties, with CMV strain S carrying a non-necrogenic satellite called S-CARNA5. These were planted out at the seedling stage in spring on a farm in southern Italy, where a severe epidemic of the tomato necrosis disease was expected (see Box 5.3). The epidemic occurred, with 100% of plants being destroyed in some fields. In the field containing the inoculated plants, protection against necrosis was almost 100%, while 40% of uninoculated plants developed lethal necrosis. Fruit yields were about doubled in the protected plants. Satellite protection against CMV infection of tomato has also been used in Japan (Sayama et al., 1993) and in China (Tien and Wu, 1991) and against CMV in pepper and melon plants in the United States of America (Montasser et al., 1998). A model suggests that inoculation with CMV containing a mild satellite RNA prior to challenge with a severe satellite isolate with or without CMV interferes with the replication and symptom production of the severe strain (Smith et al., 1992). However, there has been concern over the durability of using satellites as biocontrol agents. There is a wide range of necrogenic and other virulent strains of satCMV (Jacquemond and Tepfer, 1998). Passage of a benign satellite of CMV through Nicotiana tabacum led to the satellite rapidly mutating to a pathogenic form (Palukaitis and

Chapter | 14  Ecology, Epidemiology, and Control of Plant Viruses

855

FIGURE 14.32  Alignment of the 55 3′-terminal residues of the satellite RNA variants mutated from a necrogenic form toward a non-necrogenic one or vice versa. From Jaquemond and Tepfer (1998) with permission of the publishers.

Roossinck, 1996), and mutations of a single or a few bases can change a non-necrogenic variant to a necrogenic one (Figure 14.32). Necrogenic variants of the CMV satellite have a greater virulence than non-necrogenic variants (Escrui et  al., 2000), but, as they depress the accumulation of the helper virus more than do non-necrogenic variants, the necrogenic variants are not so efficiently aphid transmitted.

C.  Antiviral Chemicals 1.  Chemical Control of Viruses (reviewed by Hansen, 1989) Considerable effort has gone into a search for inhibitors of virus infection and multiplication that could be used to give direct protection to a crop against virus infection in the way that fungicides protect against fungi. There has been no successful control on a commercial scale by the application of antiviral chemicals. The major difficulties are: (i) an effective compound must inhibit virus infection and multiplication without damaging the plant. This is a major problem as virus replication is so intimately bound up with cell processes that any compound blocking virus replication is likely to have damaging effects on the host; (ii) an effective antiviral compound would need to move systemically through the plant if it were to prevent virus infection by invertebrate vectors; (iii) a compound acting systemically would need to retain its activity for a reasonable period. Frequent protective treatments would be impracticable. Many compounds that

have some antiviral activity are inactivated in the plant after a time; (iv) for most crops and viruses, the compound would need to be able to be produced on a large scale at an economic price. This might not apply to certain relatively small-scale, high-value crops, such as greenhouse orchids; and (v) for use with many crops, the compound would have to pass food and drug regulations. Many of the compounds that have been used experimentally would not be approved under such regulations. Many substances isolated from plants and other organisms, as well as synthetic organic chemicals, have been tested for activity against plant viruses. Almost all the substances showing some inhibition of virus infectivity do so only if applied to the leaves before inoculation or very shortly afterward. An example is a glucan preparation obtained from Phytophthora megasperma f. sp. glycinea, which appears to inhibit infection by several viruses by a novel, but unknown mechanism (Kopp et  al., 1989). Work in this field has been reviewed by Matthews (1981), Tomlinson (1981), White and Antoniw (1983), and by Verma et al. (1998). Synthetic analogs of the purine and pyrimidine bases found in nucleic acids have been widely studied, and the search for inhibitory compounds of this type continues (Dawson and Boyd, 1987). The substituted triazole, 4(5)-amino-1H-1,2,3-triazole-5(4)-carboxyamide, can be regarded as an aza analog of the substituted imidazole compound that is known to be a precursor of the purine ring in some systems. This compound shows some plant virusinhibitory activity but is less effective than 8-azaguanine.

856

The riboside of this compound was suggested as a possible antiviral agent by Matthews (1953). It was later found to have a broad-spectrum activity in experimental animal virus systems and given the name Virazole (Sidwell et al., 1972). Virazole, also known as ribavirin, has been studied in a variety of plant–virus systems. For example, pretreatment of tobacco plants with the compound delays or prevents systemic infection with TSWV (de Fazio et  al., 1980). Virazole has been used to eliminate ACLSV from apple shoot cultures (Hansen and Lane, 1985), ORSV from Cymbidium cultures (Toussaint et  al., 1993) and PPV infected shoots of plum (Paunovic et  al., 2007). It also reduces the concentration of CMV and AMV in cultured plant tissues, but virus-free plants are obtained from meristem tip cultures whether or not Virazole had been in the medium (Simpkins et al., 1981). Other virus-inhibitory compounds have been included in culture media in attempts to improve the efficiency of meristem tip culture for obtaining virus-free plants. None has found widespread use. 2,4-dioxohexahydro-1,3,5-triazine was used to eliminate potato viruses in potato meristem cultures (Borissenko et al., 1985) and potato stem cuttings (Bittner et al., 1987). Treatment with acyclic nucleoside phosphonate analogs such as tenovir reduces the concentration of the pararetroviruses BSV (episomal form) in banana (Helliot et al., 2003b) and CaMV in Brassica pekinensis (Spak et  al., 2011) to undetectable levels. In comparing different antiviral agents, Spak et  al. (2010) showed that ribavirin has a significant effect against TYMV whereas acyclic nucleoside phosphonate analogs have no effect. On the other hand, ribovirin has no effect against SDV in Citrus sp. whereas foscarnet has a significant effect (Ohta et al., 2011).

2.  Suppression of Disease Symptoms by Chemicals For a time, there was considerable interest in the use of certain systemic fungicides to suppress the symptoms of virus infection without necessarily having any effect on the amount of virus produced in the leaves. The fungicides concerned (e.g., Benlate and Bavistin) break down in aqueous solution to give methylbenzimidazole-2-yl-carbamate (MBC or carbendazim). It has been reported that these systemic fungicides possess cytokinin-like activity, although at a low level compared to kinetin. Application of MBC as a soil drench causes a substantial reduction in leaf symptoms caused by TMV in tobacco (Tomlinson et al., 1976). However, this compound or others with similar effects have not found commercial application. The severity of infection of tomato plants by ToMoV is reduced by treatment with plant growth-promoting rhizobacteria (PGPR) (Murphy et al., 2000). It is suggested that the use of PGPR could become a component of an integrated program for management of this virus in tomato.

Plant Virology

It should be noted that, in some cases, high applications of nitrogen fertilizers can suppress virus disease symptoms. However, virus concentrations are not diminished.

D.  Conventional Resistance to the Virus 1.  The Kinds of Host Response The genetic makeup of the host plant has a profound influence on the outcome following inoculation with a particular virus. The kinds of host response are defined in Table 11.1 and molecular aspects are discussed in Chapter  11. Defining the response of a particular host species or cultivar to a particular virus must always be regarded as provisional. A new mutant of the virus may develop in the stock culture, or a new strain of the virus may be found in nature that causes a different response in the plant. This applies particularly to non-host immunity. For example, for many decades the potato seedling USDA 41956 was considered immune to PVX. However, in due course a strain of this virus was discovered that can infect this genotype (Moreira et al., 1978). Nevertheless, immunity with long-term durability must occur frequently in nature. It has been suggested with respect to cellular parasites that long-lived plants, such as trees, and species naturally dominant over large areas, such as prairie grasses and aggressive weeds, must have developed greater resistance to lethal parasites than other species. Similar considerations may apply as far as virus infection is concerned, but little relevant experimental evidence is available. It is probable that many of the plants described in the past as immune to a particular virus are in fact infectible, but resistant and showing extreme hypersensitivity as defined in Table 11.1. The viruses concerned may have cell-to-cell movement proteins that are defective in the particular plant, resulting in multiplication only in the initially infected cells. This phenomenon may be detectable only by special procedures. The following points concerning the effects of host genes on the plant’s response to infection emerge from many different studies: (i) both dominant and recessive Mendelian genes may have effects. However, while most genes known to affect host responses are inherited in a Mendelian manner, cytoplasmically transferred factors may sometimes be involved (Nagaich et  al., 1968); (ii) there may or may not be a gene dose effect; (iii) genes at different loci may have similar effects; (iv) the genetic background of the host may affect the activity of a resistance gene; (v) genes may have their effect with all strains of a virus, or with only some; (vi) some genes influence the response to more than one virus; (vii) plant age and environmental conditions may interact strongly with host genotype to produce the final response; (viii) route of infection may affect the host response. Systemic necrosis

Chapter | 14  Ecology, Epidemiology, and Control of Plant Viruses

857

may develop following introduction of a virus by grafting into a highly resistant host that does not allow systemic spread of the same virus following mechanical inoculation (e.g., ToMV in resistant tomato lines; Stobbs and McNeill, 1980); and (ix) resistance originally thought to be to the virus may be really to the vector (Dahal et al., 1990a,b). As pointed out by Fraser (1988, 1992), there are three main types of resistance and immunity to a particular virus, considered from the point of view of the complexity of the host population involved: (i) immunity involves every individual of the species; little is known about the basis for immunity, but it is related to the question of the host range of viruses discussed in Chapter  4, Section VI; (ii) cultivar resistance describes the situation where one or more cultivars or breeding lines within a species show resistance while others do not; and (iii) acquired or induced resistance is present where resistance is conferred on otherwise susceptible individual plants following inoculation with a virus. This last phenomenon is discussed in Chapter  11, Section III, I. Some authors have considered that immunity and cultivar resistance are based on quite different underlying mechanisms. However, studies with a bacterial pathogen in which only one pathogen gene was used show that for this class of pathogen at least the two phenomena have the same basis (Whalen et al., 1988).

i. Resistance of Cowpea to CPMV The cowpea cultivar Arlington shows a unique form of extreme resistance to CPMV which is described in detail in Chapter  11, Section III, H.

2.  Genetics of Resistance to Viruses

iii. Non-specific Virus Inhibitors Extracts of many plants contain substances that inhibit infection by viruses when mixed with the inoculum. Some may inhibit virus replication in experimental systems, and many are known to be proteins or glycoproteins. The relevance of any of these substances to plant resistance to viruses has not been established. One of the most studied is a 29-kDa protein isolated from pokeweed (Phytolacca Americana) (pokeweed antiviral protein—PAP) which is a ribosome inactivating protein (RIP); virus resistance mediated by RIPs is reviewed by Wang and Tumer (2000). PAP is an N-glycosidase that cleaves specific purine residues from the sarcin/ricin loop of the large rRNA (Hudak et al., 2000) binding to the cap structure and depurinating downstream of the cap (Hudak et al., 2002). As described in Box 6.3, the potyvirus virus genome-linked protein (VPg) acts as a cap analog. TuMV VPg binds PAP with high affinity and is a potent inhibitor of PAP depurination (Domashevskiy et  al., 2012). It is suggested that the VPg confers an evolutionary advantage by suppressing one of the plant defense systems.

(reviewed by Kang et al., 2005) About 50% of the characterized plant resistance factors are dominant and monogenic, and about 50% are recessive. Most of the dominant resistance factors give either a hypersensitive response (R genes) or limitation of the virus to the initially infected cell (extreme resistance). The molecular mechanisms of these forms of resistance in which factors from the virus and host interact to give a defense response cascade are described in Chapter  11, Section III. Recessive resistance (also termed passive resistance) is often due to the host not having a compatible factor essential for virus replication, and thus there is no functional activity required by the plant (see Chapter  11, Section IV). Some resistance traits are polygenic. For example, two independent quantitative trait loco are responsible for resistance to BCTV in bean (Larsen et  al., 2010) (see Chapter 11, Section IV, C). a.  Mechanisms of Host Immunity and Resistance Related to Control The dominant R gene and the recessive passive resistance are the most general mechanisms preventing or limiting the spread of a virus in its host and they effect control of viruses in obvious ways. Here I discuss some other aspects related to the control of plant viruses.

ii. Impaired Systemic Movement of the Virus  In some cultivars that have a genotype conferring resistance to a particular virus, movement through the vascular tissue is affected in a manner that appears not to involve a viruscoded cell-to-cell movement protein. For example, the spread of PLRV infection within the phloem of resistant potato cultivars appears to be impaired, leading to much less efficient acquisition of the virus by the aphid vector M. persicae (Barker and Harrison, 1986). Similarly, the pattern of virus spread in inoculated leaves in corn resistant to MDMV suggests that the plant inhibits the virus from moving through the vascular system (Lei and Agrios, 1986). The molecular mechanism for such host effects is unknown. The expression of the TMV 30-kDa movement protein is strongly and selectively enhanced in tobacco protoplasts by actinomycin (Blum et al., 1989). It was suggested that the drug may act by selectively inhibiting a host factor that normally suppresses the expression of the 30-kDa viral protein.

iv. Ineffective Viral Genes As discussed in Chapter  10, Section IV, B, many viruses code for a gene product that is necessary for cell-to-cell movement. If a movement protein is ineffective in a particular host plant then virus replication is confined to the initially infected cells. Consequently, the plant shows extreme hypersensitivity

858

(Table 11.1) (though not necessarily a necrotic response) and is effectively resistant to the virus. A virus that does not normally move systemically in a particular plant species may do so in the presence of an unrelated virus that does infect systemically and complements the movement of the defective virus (Chapter  10, Section IV, C). This indicates that a mismatch between viral movement protein and plant species may be a quite common mechanism for plant resistance, though an inadvertent one. b.  Clustering of Resistance Genes In several plant species, the virus resistance genes are clustered to specific loci on the chromosomes; in this, virus resistance resembles that for fungi (Boller and Meins, 1992; Pryor and Ellis, 1993). For instance, in Pisum sativum, the resistances to the lentil strain of PSbMV, BYMV, WMV-2, CYVV, and BCMV NL-8 strain are controlled by tightly linked recessive genes on chromosome 2 (Provvidenti and Alconero, 1988; Provvidenti, 1990). Other examples include the close linkages between resistance to WMV and ZYMV in melon (Cucumis melo) (Anagnostou et al., 2000), between resistance to PRSV-W, ZYMV, WMV, and MWMV in cucumber (C. sativa) (Grumet et al., 2000) and “hotspots” of R genes in potato (Gebhardt and Valkonen, 2001); the characterization of a cluster of R-like genes containing the tobamovirus L3 resistance gene in Capsicum chinense (Tomita et al., 2008) shows the range of techniques that can be used. As noted in Chapter 11, Section III, many of the dominant R genes giving virus resistance are clustered with each other and with R genes giving resistance against bacteria, fungi, nematodes, and arthropods.

3. Tolerance The classic example of genetically controlled tolerance is the Ambalema tobacco variety. TMV infects and multiplies through the plant, but in the field, infected plants remain almost normal in appearance. This tolerance is due to a pair of independently segregating recessive genes rm1 and rm2, and perhaps to others as well with minor effects. Other examples are known where either a single gene or many genes control tolerance. For example, tolerance of a set of barley genotypes to BYDV is controlled by a single major gene probably with different alleles giving differing degrees of tolerance (Catherall et  al., 1970). From a study of the relative abundance of DNA forms and viral RNAs in plants infected with CaMV, Covey et  al. (1990) concluded that the expression of the CaMV minichromosome is a key phase in the replication cycle that is regulated by the host. Kohlrabi is a host that is tolerant of infection compared with turnip. In this host, high levels of supercoiled DNA accumulate, with very little generation of RNA transcripts, viral products, and virus.

Plant Virology

4.  Use of Conventional Resistance for Control Reviews of the breeding strategies and program for resistance in an important crop (potatoes) and to an important virus that causes rhizomania of sugar beet are given in Solomon-Blackburn and Barker (2001) and Scholten and Lange (2000), respectively; Wang and Krishnaswamy (2012) review that utility of translation initiation factor 4E-mediated recessive resistance in crop improvement. Many of the aspects that they discuss are applicable to breeding programs for resistance in other crop and to other viruses. In this section, I discuss some examples of the application of conventional resistance to the control of viruses. a. Immunity True immunity against viruses and viroids, which can be incorporated into useful crop cultivars, is a rather uncommon phenomenon. As described in Chapter  11, some dominant NBS-LRR R genes and recessive viral VPgtranslational initiator factor interactions act early enough to prevent initial multiplication of viruses giving effectortriggered immunity. Also non-host resistance is effectively immunity, but the genetic basis of this is not known. b. Resistance Where suitable genes can be introduced into agriculturally satisfactory cultivars, breeding for resistance to a virus provides one of the best solutions to controlling virus disease. Attempts to achieve this objective have been made with many of the virus diseases of major importance. Genes for resistance or hypersensitivity have often been found, but it has frequently proved very difficult to incorporate such factors into useful cultivars. A hypersensitive reaction to a virus involving necrotic local lesions with no systemic spread as discussed in Chapter 11, Section III, can give effective resistance in the field. For example, the necrotic reaction of N. glutinosa to TMV was bred into some commercial lines of N. tabacum (Valleau, 1946) and has since been used very widely with Virginia-type tobacco cultivars but not with flue-cured types. Occasionally, very high resistance to a virus has been discovered even in a plant where most known cultivars were highly susceptible. However, the designation of a variety or genotype as very highly resistant to a particular virus must always be provisional, because it is always possible that a mutant of the virus will arise that can overcome the plant resistance.

E.  Plant Resistance to Insect Vectors There has been increased interest in breeding crops for resistance to insect pests as an alternative to the use of

859

Chapter | 14  Ecology, Epidemiology, and Control of Plant Viruses

TABLE 14.2  Examples of Plants with Resistance to Airborne Vectors That Have Been Associated with Decreased Incidence of Virus Infection Vector

Crop

Gene

Reference

Acyrthosiphon pisum

Alfalfa

Polygenic

Julier et al. (2004)

Aphis craccivora

Peanut

One recessive gene

Herselman et al. (2004)

Aphis gossypii

Melon

Vat gene

Pauquet et al. (2004)

Macrosiphum euphorbiae

Tomato

Mi-1 gene

Vos et al. (1998)

Myzus persicae

Prunus spp.

Rm1 and Rm2 genes dominant

Sauge et al. (2012)

Myzus persicae

Arabidopsis

PAD4 gene

Pegadaraju et al. (2005)

Rhopalosiphon maidis

Soybean

Unknown

Gunasinghe et al. (1998)

Rice

Dominant gene(s)

Sebastian et al. (1996)

Rice

Unknown

Parejarlarn et al. (1984)

Tomato

Mi-1 gene

Vos et al. (1998)

Peanut

Unknown

Amin (1985)

Wheat

Cmc1 dominant gene

Murugan et al. (2011)

Aphids

Leafhopper Nephotettix virescens Plant hopper Niloparvata lugens Whitefly Bemisia tabaci Thrips Frankiniella schilzei Mites Aceria tulipae

pesticide chemicals. This has been due to various factors, including emergence of resistance to insecticides in insects, the costs of developing new pesticides, and increasing concern regarding environmental hazards and the effects on non-target insect species, especially those that predate on vector species. Along with these developments, there has been increased activity in breeding for resistance to invertebrates that are virus vectors. Some virus vectors are not pests in their own right, but others, especially leafhoppers and planthoppers, may be severe pests. In this situation there is a double benefit in achieving a resistant cultivar, sometimes with striking improvements in performance. The subject has been reviewed by Jones (1998), Dogimont et  al. (2010), and Westwood and Stevens (2010). Sources of resistance have been found among most of the airborne vector groups. Some examples are given in Table 14.2. Inheritance of aphid resistance may be monogenic (dominant or recessive genes) or polygenic. Two dominant aphid-resistance genes that have been cloned or mapped

appear to encode NBS-LRR proteins (see Chapter  11, Section III) involved in the specific recognition of aphids. Several aphid-resistance genes confer resistance to other invertebrates; for example, the Mi-1 gene/allele from tomato confers resistance to a biotype of the potato aphid M. euphorbiae as well as to other insects, whiteflies, psyllids, and three species of the root-knot nematodes Meloidogyne (see Dogimont et al., 2010 for details). The basis for resistance to the vectors is not always clearly understood, but some factors have been defined. In general terms, there are two kinds of resistance relevant to the control of vectors. First, physical resistance involves an adverse effect on vector behavior, resulting in decreased colonization. Some specific mechanisms for this form of resistance are: (i) sticky material exuded by glandular trichomes such as those in tomato (Berlinger and Dahan, 1987) or to trichome density which affects the oviposition rate of whitefly (Firdaus et  al., 2011); (ii) heavy leaf pubescence in soybean (Gunasinghe et  al., 1988); (iii) A-type hairs on Solanum betrhaultii which, when ruptured, entrap aphids with their contents and B-type hairs

860

on the same host, which entangle aphids making them struggle more and so rupture more A-type hairs (Tingey and Laubengayer, 1981); (iv) inability of the vector to find the phloem in Agropyron species (Shukle et  al., 1987). However, this effect is not operative with an aphid vector of BYDV in barley (Ullman et al., 1988); (v) interference with the ability of the vector to locate the host plant. For example, in cucurbits with silvery leaves there is a delay of several weeks in the development of 100% infection in the field with CMV and ClYVV (Davis and Shifriss, 1983). This effect may be due to aphids visiting plants with silvery leaves less frequently because of their different lightreflecting properties. Second, antibiosis/nonpreference resistance involves an adverse effect on vector growth, reproduction, and survival after colonization has occurred. Resistance conferred by NBS-LRR genes is an example of this, but there appear to be several other mechanisms. There is evidence that different aphid-resistance genes activate distinct signaling pathways. For example, Mi-1-mediated resistance is dependent upon the salicylic acid (SA) signaling pathway, while the jasmonic acid–responsive gene pathway is predominantly or exclusively induced in Medicago truncatula resistant to the blue-green aphid (Li et al., 2006; Gao et al., 2007). It is thought that aphid saliva contains elicitor proteins that induce defense response both that conferred by NBS-LRR proteins and by other mechanisms. For example, M. persicae saliva-induced resistance in Arabidopsis is independent of known defense signaling pathways involving SA, jasmonate, and ethylene and may induce aphidrepellent glucosinolates (de Vos and Jander, 2009). Combining resistance to a vector with some other control measure may sometimes be useful. For example, in field trials, rice tungro disease was effectively controlled by a combination of insecticide application and moderate resistance of the rice cultivar to the leafhopper vectors (Heinrichs et al., 1986). Sprays would be unnecessary with fully resistant cultivars. There may be various limitations on the use of vectorresistant cultivars: (i) sometimes such resistance provides no protection against viruses. For example, resistance to aphid infestation in cowpea does not provide any protection against CABMV (Atiri et al., 1984); (ii) if a particular virus has several vector species, or if the crop is subject to infection with several viruses, breeding effective resistance against all the possibilities may not be practicable, unless a non-specific mechanism is used (e.g., tomentose leaves); (iii) perhaps the most serious problem is the potential for new vector biotypes to emerge following widespread cultivation of a resistant cultivar (similar to what happens following the use of insecticides), as exemplified by breakdown of resistance to the rice brown planthopper (Nilaparvata lugens) (BPH) (reviewed by Yencho et al., 2000).

Plant Virology

In spite of these difficulties, and the problems associated with the identification of plants with resistance to vectors, it seems certain that substantial efforts will continue to be made to improve and extend the range of crop cultivars with resistance to virus vectors. A combination of resistance to the vector and to the virus will frequently be the goal.

F.  Plant Resistance to Nematodes (reviewed by Fuller et al., 2008) The use of crop varieties that contain either natural resistance genes or that are transformed with anti-nematode genes reduce nematode populations. “Resistance” as applied to nematode control is normally interpreted as meaning the prevention or limitation of nematode multiplication as a result of the expression of specific host genes. Thus, it does not generally protect plants against nematode invasion but results in a failure to produce a functional feeding site able to support development of a reproducing female. There are both natural and transgenic forms of resistance. Some natural sources of resistance are conferred by a single dominant resistance gene (R gene) (see Chapter 11, Section III for R genes) in the host plant that may interact specifically with a corresponding avirulence (Avr) gene in the nematode resulting in the initiation of a cascade of defense responses often culminating in a hypersensitive response. Although some genes, e.g., Mi-1 conferring resistance to Meloidogyne spp. (which, as noted above, also gives resistance to some insect vectors), belong to the same group of R genes as do several genes conferring resistance to plant viruses, there is no evidence yet that they confer resistance to Longidorus or Trichodorus spp. virus-vector nematodes. There is at least one NB-LRR R gene in grape, XiR1 that confers resistance to Xiphinema index, the vector of GFLV (Hwang et al., 2010). This resistance has been transferred to rootstocks but only reduces the translocation of the virus to the scion, delaying infection (reviewed by Oliver and Fuchs, 2011). Other natural sources of nematode resistance are complex traits inherited in a polygenic manner and the genes involved in these resistance mechanisms have not been identified. None of these are reported to give resistance to plant virus vectors. Transgenic resistance to nematodes has been produced using genes encoding proteins that affect nematode feeding (e.g., proteinase inhibitors, lectins, and Bacillus thuringiensis Cry proteins), peptides that disrupt nematode chemoreceptors that identify potential host plants, and RNAi targeted to silence nematode genes (reviewed by Fuller et al., 2008; Li et al., 2011).

861

Chapter | 14  Ecology, Epidemiology, and Control of Plant Viruses

TABLE 14.3  Examples of the Relation Between the Durability of Resistance and the Number of Mutations Required to Obtain Virulent Isolates and Break Resistance Gene

Durability

No. of Amino Acid Changes

Potato Nb

Poor

1

Potato Nx

Poor

1

Tomato Tm-1

Poor

1a

Brassica TuRB01

Moderate

1b

Tomato Tm-2

Moderate

2

Brassica TuRB01 + TuRB04

Good

2c

Tomato Tm-22

Very good

2

Potato Rx-1

Very good

2

Tobacco N

Excellent

>2

Modified from Harrison (2002) with permission of the publishers. a Two different amino acid changes can lead independently to virulence (Meshi et al., 1988) b Jenner et al., 2000. c Jenner et al., 2002.

G.  Factors to Be Considered in Conventional Resistance 1. Durability (reviewed by Lecoq et al., 2004) The major problem with resistance of any sort as a control measure is its durability. How long can it be deployed successfully before a resistance-breaking (virulent) strain of the virus emerges? There are multiple factors, including the virus resistance mechanism, the number of mutations sufficient to generate virulent/aggressive variants, and the effect of these mutations on virus fitness; all can contribute to an estimate of resistance durability. a.  Nature of Resistance Fraser (1992) suggested that recessive resistance resulting from loss of factor(s) essential for virus multiplication in the host plant fits a negative functional model whereas dominant resistance results from active mechanisms (the “positive model”). There is no clear correlation between resistance durability and its mode of inheritance (dominant or recessive genes), although there is a tendency for recessive resistances to be more durable (Fraser, 1992). Thus, according to the negative functional model, it would be difficult for the virus to fulfill the function of this missing factor and according to the positive functional model, resistance-breaking could occur more easily by virus mutations that would suppress a specific recognition between the host resistance factor and the virus avirulence factor. Polygenic resistance is generally quantitative and without clear strain-specific effects and so it is assumed to be

more durable (Lindhout, 2002). Limited data are available on the durability of several other kinds of resistance (e.g., systemic acquired resistance, virus-induced gene silencing). b.  The Avirulence Gene A diverse array of plant viral avirulence (AVR) factors have been characterized (see Table 11.2) showing that many virus-encoded proteins and even non-coding sequences are potential AVR factors. For many virus resistances, mutations responsible for the transition from an avirulent to a virulent strain have been identified using molecular techniques. Therefore, the nature of the AVR gene/sequence does not correlate with the durability of a resistance gene. There is a general trend to an increase in durability of resistance when many mutations are needed to gain virulence (Harrison, 2002). In most cases, resistance that require two or more mutations of the AVR gene show more durability (Table 14.3). c.  Spread and Fitness of Virulent Strains Since most virus resistances can be overcome by virulent strains, a working definition of resistance durability depends on the prevalence and impact of these strains in the field. For some crop plants and viruses, resistance has proved to be remarkably durable. Examples are the resistance to BCMV found in Corbett Refugee bean (Zaumeyer and Meiners, 1975), the multigenic resistance in sugar beet to the BCTV (Duffus, 1987), resistance to TuMV in lettuce (Duffus, 1987; Robbins et  al., 1994), the Pvr4 resistance of pepper (Dogimont et  al., 1996), and the Ry resistance

862

Plant Virology

TABLE 14.4  Solanum Species Containing Sources of Resistance to PLRV Species

Series

Ploidy

Country of Origin

Cultivated or Wild

Tuber Bearing

S. etuberosum

Etuberosa

2x

Chile

Wild

No

S. brevidens

Etuberosa

2x

Argentina, Chile

Wild

No

S. raphanifolium

Megistacroloba

2x

Peru

Wild

Yes

S. chacoense

Yungasensa

2x

Argentina, Bolivia, Paraguay, Uruguay

Wild

Yes

S. acaule

Acaulia

4x

Argentina, Bolivia, Peru

Wild

Yes

S. demissum

Demissa

6x

Mexico

Wild

Yes

S. phureja

Tuberosa

2x

Bolivia, Columbia, Ecuador, Peru, Venezuela

Cultivated

Yes

S. tuberosum ssp. andiginea

Tuberosa

4x

Argentina, Bolivia, Colombia, Ecuador, Peru, Venezuela

Cultivated

Yes

S. tuberosum ssp. tuberosum

Tuberosa

4x

Chile

Cultivated

Yes

From Barker and Waterhouse (1999) with permission of the publishers.

of potato to PVY (Mestre et al., 2000). An explanation of at least some of these examples of durability could be that mutations which modify the domain of the AVR factor that interacts with the resistance factor have a deleterious effect on virus fitness. The importance of assessing the durability of a resistance gene and the fitness of resistance-breaking virus isolates in an agricultural environment is discussed by Lecoq et al. (2004).



●

2.  Sources of Resistant Genotypes Quite frequently, no resistance could be found for particular crops and viruses. For example, no resistance to BWYV was found in 70 cultivars and 500 breeding lines of lettuce (Watts, 1975) but was found later (Maisonneuve et al., 1991). Russell (1960) found no resistance to BYV in 100,000 beet seedlings. In general, there is certainly a need to broaden the search for resistance genes. For example, in the United Kingdom, 22 horticultural crops have no known source of resistance to a total of 25 viruses that are known to affect them (Fraser, 1988). Nevertheless, many effective sources of resistance have been found and are currently in use (for list, see Khetarpal et  al., 1998). In such circumstances, it may be necessary to widen the search for resistance to specific viruses in important crops. There are various approaches to this including: Sometimes certain existing lines or varieties have been found to have a useful degree of resistance, as with the resistance of Corbett refugee bean to BCMV (Zaumeyer and Meiners, 1975). Resistance may not always be uniform, however. For example, even within inbred lines of corn there was variation in resistance to

●



●



●



●

MDMV (Louie et  al., 1976). In cabbage, variation in degree of resistance to TuMV was found between different lines of the same variety (Polak, 1983). Occasionally, useful sources of resistance can be identified by making initial selections from plants showing good growth in otherwise severely infected fields (Cope et al., 1978). With important crops, searches for sources of resistance have been made on a worldwide basis. Timian (1975) tested 4889 entries in the Barley World collection and found 44 that showed no symptoms of infection with BSMV in the field. As another example, sources of resistance to CSSV in Ghana have been found in the upper Amazon region (Legg and Lockwood, 1977), and attempts have been made to combine resistance from various sources (Kenten and Lockwood, 1977). Useful resistance has sometimes been found among a collection of mutants induced by physical or chemical means. For example, Ukai and Yamashita (1984) identified such a barley mutant that was highly resistant to BaYMV. In principle, culture of plant cells as protoplasts offers several possibilities for obtaining new sources of resistance to viruses. However, no commercially successful virus-resistant cultivars have yet been derived by this means. The topic has been reviewed by Shepard (1981). From among wild species. Among the main sources of genetic resistance to pest and pathogens are the centers of origin and regions of diversification of the crop species. In these places, plants have been exposed to selective pressure from the pest or pathogen over long periods of time and thus have developed resistance (Leppik, 1970). This is well illustrated by the Solanum species that contain sources of resistance to PLRV (Table 14.4).

Chapter | 14  Ecology, Epidemiology, and Control of Plant Viruses

Another example is the identification and introgression of BYDV resistance genes from wild relatives of wheat (Zhang et al., 2009). Three BYDV resistance genes (Bdv2, Bdv3, and Bdv4) were introgressed from Thinopyrum intermedium into wheat using wide crosses combined with techniques to bypass sexual incompatibility such as cell culture, embryo rescue, or genetic modification. By using genetic modification techniques to introduce completely novel genes (see Chapter 15, Section I).

●

3.  Low Seed Transmission The discussion in the previous section was concerned with resistance of the growing plant to virus infection. For those viruses affecting annual crops that are seed transmitted, resistance to seed transmission may be an important method for limiting infection in the field. For example, a single recessive gene conditions resistance to seed transmission of BSMV in barley (Carroll et  al., 1979). The resistance gene, found in an Ethiopian barley called Modjo, was introduced into a new variety, Mobet, with good agronomic qualities and high resistance to seed transmission of Montana isolates of BSMV (Carroll et al., 1983). Resistance to seed transmission has also been found for LMV in lettuce and for some legume viruses. The mechanism of seed transmissibility of PSbMV in pea is described in Chapter 12, Section VII, B, 3.

4.  Adequate Testing of Resistant Material Varieties or lines showing resistance in preliminary trials must then be tested under a range of conditions. Important factors to be considered are strains of the virus, climatic conditions (Thompson and Herbert, 1970), and inoculum pressure (Kenten and Lockwood, 1977).

5.  The Need for Resistance to Multiple Pathogens The difficulties in finding suitable breeding material are compounded when there are strains of not one, but several viruses to consider. Cowpeas in tropical Africa are infected to a significant extent by at least seven different viruses. In such circumstances, a breeding program may use any form of genetic protection that can be found. Sources of resistance, hypersensitivity, or tolerance have been found for five of the viruses (Matthews, 1991). However, several of these viruses have different strains or isolates that may break resistance to other isolates (van Boxtel et  al., 2000). There is of course the further problem of combining these factors with multiple resistances to fungal and bacterial diseases. For example, genetic resistance to TMV, cyst nematodes, root-knot nematodes, and wildfire from Nicotiana repanda has been incorporated into N. tabacum (Gwynn et al., 1986).

863

As discussed in Chapter 15, Section I, genetic modification techniques offer the possibility of introducing protection against multiple viruses.

6. Tolerance Where no source of genetic resistance can be found in the host plant, a search for tolerant varieties or races is sometimes made. However, tolerance is not nearly as satisfactory a solution as genetic resistance for several reasons: (i) the infected tolerant plants may act as a reservoir of infection for other hosts. Thus, it is bad practice to grow tolerant and sensitive varieties together under conditions where spread of virus may be rapid; (ii) large numbers of virus-infected plants may come into cultivation. The genetic constitution of host or virus may change to give a breakdown in the tolerant reaction; (iii) the deployment of tolerant varieties removes the incentive to find immunity to the virus until the tolerance breaks down in an “out of sight, out of mind” attitude; and (iv) virus infection may increase susceptibility to a fungal disease (Chapter 4, Section IX, C). However, tolerant varieties may yield very much better than standard varieties where virus infection causes severe crop losses and where large reservoirs of virus exist under conditions where they cannot be eradicated. Thus, tolerance has, in fact, been widely used (Posnette, 1969). Cultivars of wheat and oats commonly grown in the US Midwest have probably been selected for tolerance to BYDV in an incidental manner, because of the prevalence of the virus (Clement et al., 1986). Tolerance to MSV has been found in maize and rapidly incorporated into highyielding maize populations for use in tropical Africa (Soto et al., 1982). Walkey and Antill (1989) obtained an unusual result with a variety of garlic called Fructidor. The yield of selected stocks was significantly less than that of unselected infected stocks. Salomon (1999) argues that breeding for tolerance has an advantage over breeding for resistance in that the selection pressures for the development of resistance-breaking strains are less. This may be so for fungal and bacterial pathogens, but it is open to questions as to whether this consideration pertains to viruses as well.

V. DISCUSSION It was noted in the introduction to this chapter that the ecology and epidemiology of plant viruses are closely interlinked. Their study is important in two aspects, the control of viruses in the crops and the impact that viruses in the “unnatural” agricultural environment may have on the surrounding ecology. Very little is known about the latter, but with the increasing recognition of the importance of, and the impact that humans are having on, biodiversity, it should be studied more.

864

It is estimated that up to 40% of the potential yield of crops worldwide is lost due to biotic factors and that a significant portion of this loss is due to viruses. In the light of major increases in the world population and the impact of abiotic factors (e.g., climate change) the need to control virus and mitigate crop losses is taking on even more importance. The development of a control program for a virus disease in a crop requires a good diagnosis system for identifying that virus and an understanding of the epidemiology of that virus. It is generally considered that introduction of a good resistance gene(s) is the best control measure, but frequently this is not possible due to non-availability of such gene(s) in sexually compatible species. The use of genetically engineered resistance (see Chapter  15, Section I) is offering the possibility of further sources of resistance genes. However, the durability of resistance genes is often a weak link with resistancebreaking strains of the virus appearing. Once again diagnosis and knowledge of the resistance mechanism can help in minimizing this problem. As good durable resistance is not yet available for most crop–virus combinations, the other approaches of avoiding the virus and controlling the vector have to be used. Selection and deployment of these depend on various intrinsic factors discussed above, the economics of the control measures, on the technological expertise of the farmer, and on food health and public acceptance.

REFERENCES A’Brook, J., 1964. The effect of planting date and spacing on the incidence of groundnut rosette disease and of the vector Aphis craccivora, Koch, at Mokawa, Northern Nigeria. Ann. Appl. Biol. 54, 199–208. A’Brook, J., 1968. The effect of plant spacing on the numbers of aphids trapped over the groundnut crop. Ann. Appl. Biol. 61, 289–294. A’Brook, J., 1973. The effect of plant spacing on the number of aphids trapped over cocksfoot and kale crops. Ann. Appl. Biol. 74, 279–285. Adejare, G.O., Coutts, R.H.A., 1981. Eradication of cassava mosaic disease from Nigerian cassava clones by meristem-tip culture. Plant Cell Tissue Organ. Cult. 1, 25–32. Albiach-Martí, M., Mawassi, M., Gowda, S., Satyanarayana, T., Hilf, M.E., et  al., 2000a. Sequences of Citrus tristeza virus separated in time and space are essentially identical. J. Virol. 74, 6856–6865. Alconero, R., Weeden, N.F., Gonsalves, D., Fox, D.T., 1985. Loss of genetic diversity in pea germplasm by the elimination of individuals infected by pea seedborne mosaic virus. Ann. Appl. Biol. 106, 357–364. Amaku, M., Burattini, M.N., Coutinho, F.A.B., Massad, E., 2010. Modeling the competition between viruses in a complex plant-pathogen system. Phytopathology 100, 1042–1047. Amin, P.W., 1985. Apparent resistance of groundnut cultivar Robut 33-1 to bud necrosis disease. Plant Dis. 69, 718–719. Anagnostou, K., Jahn, M., Perl-Treves, R., 2000. Inheritance and linkage analysis of resistance to zucchini yellow mosaic virus, papaya ring­spot virus and powdery mildew in melon. Euphytica 116, 265–270.

Plant Virology

Anderson, P.K., Cunningham, A.A., Patel, N.G., Morales, F.J., Epstein, P.R., et  al., 2004. Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers. Trends Ecol. Evol. 19, 535–544. Anjaneyulu, A., Bhaktavatsalam, G., 1987. Evaluation of synthetic pyrethroid insecticides for tungro management. Trop. Pest Manag. 33, 323–326. Ashby, J.W., Teh, P.B., Close, R.C., 1979. Symptomatology of subterranean clover red leaf virus and its incidence in some legume crops, weed hosts and certain alate aphids in Canterbury, New Zealand. N. Z. J. Agric. Res. 22, 361–365. Asher, M.J.C., Grimmer, M.K., Mutasa-Goettgens, E.S., 2009. Selection and characterization of resistance to Polymyxa betae, vector of Beet necrotic yellow vein virus, derived from wild sea beet. Plant Pathol. 58, 250–260. Asjes, C.J., 1978. Minerale oliën op lelies om virusverspreiding tegen te gaan. Bloembollencultuur 88, 1046–1047. Asjes, C.J., 1980. Toepassing van minerale olie om verspreiding van hyacintemozaiekvirus in hyacinten tegen te gaan. Bloemboliencultuur 90, 1396–1397. Atiri, G.I., Ekpo, E.J.A., Thottappilly, G., 1984. The effect of aphidresistance in cowpea on infestation and development of Aphis craccivora and the transmission of cowpea aphid-borne mosaic virus. Ann. Appl. Biol. 104, 339–346. Atkinson, T.G., Grant, M.N., 1967. An evaluation of streak mosaic losses in winter wheat. Phytopathology 57, 188–192. Atkinson, T.G., Slykhuis, J.T., 1963. Relation of spring drought, summer rains and high fall temperatures to the wheat streak mosaic epiphytotic in southern Alberta, 1963. Can. Plant Dis. Surv. 43, 154–159. Barbosa, C.J., Pina, J.A., Perez-Panades, J., Bernad, L., Serra, P., et  al., 2005. Mechanical transmission of citrus viroids. Plant Dis. 89, 749–754. Barker, H., Harrison, B.D., 1986. Restricted distribution of potato leafroll virus antigen in resistant potato genotypes and its effect on transmission of the virus by aphids. Ann. Appl. Biol. 109, 595–604. Barker, H., Waterhouse, P.M., 1999. The development of resistance to luteoviruses mediated by host genes and pathogen-derived transgenes. In: Smith, H.G., Barker, H. (Eds.), The Luteoviridae CAB International, Wallingford, UK, pp. 169–210. Barnes, J.M., Trinidad-Correa, R., Orum, T.V., Felix-Gastelum, R., Nelson, M.R., 1999. Landscape ecology as a new infrastructure for improving management of plant viruses and their insect vectors in agroecosystems. Ecosystem Health 5, 26–35. Bawden, F.C., 1964. Plant Viruses and Virus Diseases, fourth ed. Ronald Press, New York, NY. Bayles, R., O’Sullivan, D., Lea, V., Freeman, S., Budge, G., et al., 2007. Controlling Soil-borne cereal mosaic virus in the UK by developing resistant wheat cultivars. HGCA Project Rep. 418, 60. Beemster, A.B.R., 1967. Partial infection with potato virus YN of tubers from primarily infected potato plants. Neth. J. Plant Pathol. 73, 161–164. Beemster, A.B.R., 1979. Acquisition of potato virus YN by Myzus persicae from primarily infected “Bintje” potato plants. Neth. J. Plant Pathol. 85, 75–81. Belliure, B., Amorós-Jiménez, R., Fereres, A., Marcos-García, M.A., 2011. Antipredator behaviour of Myzus persicae affects transmission efficiency of Broad bean wilt virus 1. Virus Res. 159, 206–214. Bennett, C.W., 1963. Highly virulent strains of curly top virus in sugar beet in western United States. J. Am. Soc. Sugar Beet Technol. 12, 515–520.

Chapter | 14  Ecology, Epidemiology, and Control of Plant Viruses

Berlinger, M.J., Daban, R., 1987. Breeding for resistance to virus transmission by whiteflies in tomatoes. Insect Sci. Appl. 8, 783–784. Best, R.J., 1968. Tomato spotted wilt virus. Adv. Virus Res. 13, 65–146. Bittner, H., Schenk, G., Schuster, G., 1987. Chemotherapeutical elimination of potato virus X from potato stem cuttings. J. Phytopathol. 120, 90–92. Blencowe, J.W., Tinsley, T.W., 1951. The influence of density of plant population on the incidence of yellows in sugar beet crops. Ann. Appl. Biol. 38, 395–401. Blum, H., Gross, H.J., Beier, H., 1989. The expression of the TMVspecific 30-kDa protein in tobacco protoplasts is strongly and selectively enhanced by actinomycin. Virology 169, 51–61. Boag, B., 1985. The localised spread of virus-vector nematodes adhering to farm machinery. Nematologica 31, 234–235. Boiteau, G., Singh, M., Lavoie, J., 2009. Crop border and mineral oil sprays used in combination as physical control methods of aphidtransmitted potato virus Y in potato. Pest Manage. Sci. 65, 255–259. Boller, T., Meins, F. (Eds.), 1992. Genes Involved in Plant Defense Springer, Vienna. Borissensko, S., Schuster, G., Schmygla, W., 1985. Obtaining a high percentage of explants with negative serological reactions against viruses by combining potato meristem culture with phytoviral chemotherapy. Phytopathol. Z 114, 185–188. Bottrell, D.G., Barbosa, P., 1998. Manipulating natural enemies by plant varietal selection and modification: a realistic strategy? Annu. Rev. Entomol. 43, 347–367. Bradley, R.H.E., 1956. Effects of depth of stylet penetration on aphid transmission of potato virus Y. Can. J. Microbiol. 2, 539–547. Bradley, R.H.E., Wade, C.V., Wood, F.A., 1962. Aphid transmission of potato virus Y inhibited by oils. Virology 18, 327–328. Broadbent, L., 1957. Investigation of Virus Diseases of Brassica Crops. Cambridge University Press, London, A.R.C. Rep. Ser. No. 14. Broadbent, L., 1962. The epidemiology of tomato mosaic. II. Smoking tobacco as a source of virus. Ann. Appl. Biol. 50, 461–466. Broadbent, L., 1963. The epidemiology of tomato mosaic. III. Cleaning virus from hands and tools. Ann. Appl. Biol. 52, 225–232. Broadbent, L., 1964. The epidemiology of tomato mosaic. VII. The effect of TMV on tomato fruit yield and quality under glass. Ann. Appl. Biol. 54, 209–224. Broadbent, L., 1965. The epidemiology of tomato mosaic. IX. Transmission of TMV by birds. Ann. Appl. Biol. 55, 67–69. Broadbent, L., 1976. Epidemiology and control of tomato mosaic virus. Annu. Rev. Phytopathol. 14, 75–96. Broadbent, L., Fletcher, J.T., 1963. The epidemiology of tomato mosaic. IV. Persistence of the virus on clothing and glasshouse structures. Ann. Appl. Biol. 52, 233–241. Broadbent, L., Gregory, P.H., Tinsley, T.W., 1952. The influence of planting date and manuring on the incidence of virus diseases in potato crops. Ann. Appl. Biol. 39, 509–524. Broadbent, L., Heathcote, G.D., McDermott, N., Taylor, C.E., 1957. The effect of date of planting and of harvesting potatoes on virus infection and on yield. Ann. Appl. Biol. 45, 603–622. Broadbent, L., Green, D.E., Walker, P., 1963. Narcissus virus diseases. Daffodil Tulip Yearbook 28, 154–160. Broadbent, L., Read, W.H., Last, F.T., 1965. The epidemiology of tomato mosaic X. Persistence of TMV infected debris in soil and the effects of soil partial sterilisation. Ann. Appl. Biol. 55, 471–483. Burt, P.E., Heathcote, G.D., Broadbent, L., 1964. The use of insecticides to find when leaf roll and virus Y spread within potato crops. Ann. Appl. Biol. 54, 13–22.

865

Büttner, C., Nienhaus, F., 1989. Virus contamination of soils in forest ecosystems of the Federal Republic of Germany. Eur. J. For. Pathol. 19, 47–53. Büttner, C., Jacobi, V., Koenig, R., 1987. Isolation of carnation Italian ringspot virus from a creek in a forested area southwest of Bonn. J. Phytopathol. 118, 131–134. Canto, T., Aranda, M.A., Fereres, A., 2009. Climate change effects on physiology and population processes of hosts and vectors that influence the spread of hemipteran-borne plant viruses. Global Change Biol. 15, 1884–1894. Carriére, Y., Ellers-Kirk, C., Hartfield, K., Larocque, G., Degain, B., et al., 2012. Large-scale, spatially-explicit test of the refuge strategy for delaying insecticide resistance. Proc. Natl. Acad. Sci. USA 109, 775–780. Carroll, T.W., 1983. Certification schemes against barley stripe mosaic. Seed Sci. Technol. 11, 1033–1042. Carroll, T.W., Gossel, P.L., Hockett, E.A., 1979. Inheritance of resistance to seed transmission of barley stripe mosaic virus in barley. Phytopathology 69, 431–433. Carroll, T.W., Hockett, E.A., Zaske, S.K., 1983. Registration of mobet barley germplasm. Crop Sci. 23, 599–600. Catherall, P.L., Jones, A.T., Hayes, J.D., 1970. Inheritance and effectiveness of genes in barley that condition tolerance to barley yellow dwarf virus. Ann. Appl. Biol. 65, 153–161. Cervantes, F.A., Alvarez, J.M., 2011. Within plant distribution of Potato virus Y in hairy nightshade (Solanum sarrachoides): an inoculum source affecting PVY aphid transmission. Virus Res. 159, 194–200. Chakraborty, S., Newton, A.C., 2011. Climate change, plant diseases and food security. Plant Pathol. 60, 2–14. Chan, M.S., Jeger, M.J., 1994. An analytical model of plant virus disease dynamics with roguing and replanting. J. Appl. Ecol. 31, 413–427. Chancellor, T.C.B., Holt, J., Villareal, S., Tiongco, E.R., Venn, J., 2006. Spread of plant virus disease to new plantings: a case study of rice tungro disease. Adv. Virus Res. 66, 1–29. Chavez, P., Zorogastua, P., Chuquillanqui, C., Salazar, L.F., Mares, V., et  al., 2009. Assessing Potato yellow vein virus (PYVV) infection using remotely sensed data. Int. J. Pest Manage. 55, 251–256. Cho, J.J., Mau, R.F.L., German, T.L., Hartman, R.W., Yudin, L.S., et al., 1989. A multidisciplinary approach to management of tomato spotted wilt virus in Hawaii. Plant Dis. 73, 375–383. Clement, D.L., Lister, R.M., Foster, J.E., 1986. ELISA-based studies on the ecology and epidemiology of barley yellow dwarf virus in Indiana. Phytopathology 76, 86–92. Clinch, P., Loughnane, J.B., Murphy, P.A., 1938. A study of the infiltration of viruses into seed potato stocks in the field. Sci. Proc. R. Dublin Soc. 22, 18–31. Cock, L.J., 1968. Virus diseases of lettuce. NAAS Q. Rev. 79, 126–138. Cohen, S.S., 1981. Reducing the spread of aphid-transmitted viruses in peppers by coarse-net cover. Phytoparasitica 9, 69–76. Cohen, S.S., Marco, S., 1973. Reducing the spread of aphid-transmitted viruses in peppers by trapping the aphids on sticky yellow polyethylene sheets. Phytopathology 63, 1207–1209. Colvin, J., Omongo, C.A., Govindappa, M.R., Stevenson, P.C., Maruthi, M.N., et  al., 2006. Host-plant viral infection effects on arthropodvector population growth, development and behaviour: management and epidemiological implications. Adv. Virus Res. 67, 419–452. Conti, M., 1972. Investigations on the epidemiology of maize rough dwarf virus. I. Overwintering of virus in its planthopper vector. Actas Congr. Uniao Fitopatol. Mediterr. 3, 11–17.

866

Conti, M., Masenga, V., 1977. Identification and prevalence of pepper viruses in northwest Italy. Phytopathol. Z 90, 212–222. Converse, R.H., Tanne, E., 1984. Heat therapy and stolon apex culture to eliminate mild yellow-edge virus from Hood strawberry. Phytopathology 74, 1315–1316. Cooper, I., Jones, R.A.C., 1996. Wild plants and viruses: under-investigated ecosystems. Adv. Virus Res. 67, 1–47. Cooper, I., Jones, R.A.C., 2006. Wild plants and viruses: under-investigated ecosystems. Adv. Virus Res. 67, 1–47. Cooper, J.I., 1971. The distribution in Scotland of tobacco rattle virus and its nematode vectors in relation to soil type. Plant Pathol. 20, 51–58. Cooper, J.I., Harrison, B.D., 1973. Distribution of potato mop top virus in Scotland in relation to soil and climate. Plant Pathol. 22, 73–78. Cope, W.A., Walker, S.K., Lucas, L.T., 1978. Evaluation of selected white clover clones for resistance to viruses in the field. Plant Dis. Rep. 62, 267–270. Córdoba-Selles, M.D.C., García-Rández, A., Alfaro-Fernández, A., Jorda-Gutiérrez, C., 2007. Seed transmission of pepino mosaic virus and efficacy of tomato seed disinfection treatments. Plant Dis. 91, 1250–1254. Cotten, J., 1979. The effectiveness of soil sampling for virus-vector nematodes in MAFF certification schemes for fruit and hops. Plant Pathol. 28, 40–44. Coutts, R.H.A., 1986. New threats to crops from changing farm practices. Nature 322, 594. Covey, S.N., Turner, D.S., Lucy, A.P., Saunders, K., 1990. Host regulation of the cauliflower mosaic virus multiplication cycle. Proc. Natl. Acad. Sci. USA 87, 1633–1637. Dahal, G., Hibino, H., Saxena, R.C., 1990a. Association of leafhopper feeding behaviour with transmission of rice tungro to susceptible and resistant rice cultivars. Phytopathology 80, 371–377. Dahal, G., Hibino, H., Cabunagan, R.C., Tionco, E.M., Flores, Z.M., et  al., 1990b. Changes in cultivar reaction due to changes in “virulence” of the leafhopper vector. Phytopathology 80, 659–665. Dale, J.L., 1987. Banana bunchy top: an economically important tropical plant virus disease. Adv. Virus Res. 33, 301–325. Dale, J.L., Harding, R.M., 1998. Banana bunchy top disease: current and future strategies for control. In: Hadidi, A., Khetarpal, R.K., Koganezawa, H. (Eds.), Plant Virus Disease Control APS Press, St. Paul, MN, pp. 659–669. Davis, R.F., Shifriss, O., 1983. Natural virus infection in silvery and nonsilvery lines of Cucurbita pepo. Plant Dis. 67, 379–380. Dawson, W.O., Boyd, C., 1987a. Modifications of nucleic acid precursors that inhibit plant virus multiplication. Phytopathology 77, 477–480. de Bokx, J.A. (Ed.), 1972. Viruses of Potatoes and Seed-Potato Production Pudoc, Wageningen. de Fazio, G., Kudamatsu, M., Vicente, M., 1980. Virazole pretreatments for the prevention of tomato spotted wilt virus (TSWV) systemic infection in tobacco plants Nicotiana tabacum, L. “White Burley”. Fitopatol. Bras. 5, 343–394. de Vos, M., Jander, G., 2009. Myzus persicae (green peach aphid) salivary components induce defense responses in Arabidopsis thaliana. Plant Cell Environ. 32, 1548–1560. de Vos, M., Cheng, W.Y., Summers, H.E., Raguso, R.A., Jander, G., 2010. Alarm pheromone habituation in Myzus persicae has fitness consequences and causes extensive gene expression changes. Proc. Natl. Acad. Sci. USA 107, 14673–14678.

Plant Virology

de Wijs, J.J., 1980. The characteristics of mineral oils in relation to their inhibitory activity on the aphid transmission of potato virus Y. Neth. J. Plant Pathol. 86, 291–300. Dedryver, C.-A., Le Ralec, A., Fabre, F., 2010. The conflicting relationships between aphids and men: a review of aphid damage and control strategies. C.R. Biol. 333, 539–553. Dewar, A.M., Smith, H.G., 1999. Forty years of forecasting virus yellow incidence in sugar beet. In: Smith, H.G., Barker, H. (Eds.), The Luteoviridae CAB International, Wallingford, UK, pp. 231–243. Diaz, B.M., Fereres, A., 2007. Ultraviolet-blocking materials as a physical barrier to control insect pests and plant pathogens in protected crops. Pest Technol. 1, 85–95. Diekmann, M., Putter, C.A., 1996. FAO/IPGRI Technical Guidelines for the Safe Movement of Germplasm. No. 15, Musa, second ed. Food and Agriculture Organization of the United Nations/International Plant Genetic Resource Institute, Rome. Diener, T.O., 1987. Biological properties. In: Diener, T.O. (Ed.), The Viroids, Plenum Press, New York, NY, pp. 9–35. Dijkstra, J., de Jager, C.P., 1998. Practical Plant Pathology: Protocols and Exercises. Springer-Verlag, Berlin. Dinant, S., Lot, H., 1992. Lettuce mosaic virus. Plant Pathol. 41, 528–542. Dogimont, C., Palloix, A., Daubèze, A.M., Marchoux, G., Gebré Selassié, K., et al., 1996. Genetic analysis of broad spectrum resistance to potyviruses using doubled haploid lines of pepper (Capsicum annuum L.). Euphytica 88, 231–239. Dogimont, C., Bendahmane, A., Chovelon, V., Boissot, N., 2010. Host plant resistance to aphids in cultivated crops: genetic and molecular bases and interactions with aphid populations. C.R. Biol. 333, 566–573. Domashevskiy, A.V., Miyoshi, H., Goss, D.J., 2012. Inhibition of pokeweed antivirus protein (PAP) by Turnip mosaic virus genome-linked protein (VPg). J. Biol. Chem. 287, 29729–29738. Doncaster, J.P., Gregory, P.H., 1948. The spread of virus diseases in the potato crop. G. B. Agric. Res. Counc. Rep. Ser. 7, 1–189. Douthit, L.B., McGuire, J.M., 1975. Some effects of temperature on Xiphinema americanum and infection of cucumber by tobacco ringspot virus. Phytopathology 65, 134–138. Duffus, J.E., 1987. Durability of resistance. Ciba Found. Symp. 133, 196–199. Duffy, S., Seah, Y.M., 2010. 98% identical, 100% wrong: per cent nucleotide identity can lead plant virus epidemiology astray. Philos. Trans. R. Soc. B Biol. Sci. 365, 1891–1897. Ebbels, D.L., 1979. A historical review of certification schemes for vegetatively propagated crops in England and Wales. ADAS Q. Rev. 32, 21–58. Egan, B.T., Hall, P., 1983. Monitoring the Fiji disease epidemic in sugar cane at Bundaberg, Australia. In: Plumb, R.T., Thresh, J.M. (Eds.), Plant Virus Epidemiology Blackwell, Oxford, pp. 287–296. Escriu, F., Fraile, A., Garcia-Arenal, F., 2000. Evolution of virulence in natural populations of the satellite RNA of cucumber mosaic virus. Phytopathology 90, 480–485. Evans, A.C., 1954. Groundnut rosette disease in Tanganyika. I. Field studies. Ann. Appl. Biol. 41, 189–206. Faccioli, G., Marani, F., 1998. Virus elimination by meristem tip culture and tip micrografting. Breeding for resistance to plant viruses. In: Hadidi, A., Khetarpal, R.K., Koganezawa, H. (Eds.), Plant Virus Disease Control APS Press, St. Paul, MN, pp. 346–380. Faccioli, G., Rubies-Autonell, C., 1982. PVX and PVY distribution in potato meristem tips and their eradication by the use of thermotherapy and meristem-tip culture. Phytopathol. Z 103, 66–75.

Chapter | 14  Ecology, Epidemiology, and Control of Plant Viruses

Fahn, A., 1985. Plant Anatomy. Pergamon Press. Fargette, D., Fauquet, C., Thouvenel, J.-C., 1985. Field studies on the spread of African cassava mosaic. Ann. Appl. Biol. 106, 285–294. Fargette, D., Konaté, G., Fauquet, C., Muller, E., Peterschmitt, M., et al., 2006. Molecular ecology and emergence of tropical plant viruses. Annu. Rev. Phytopathol. 44, 235–260. Fereres, A., Moreno, A., 2009. Behavioural aspects influencing plant virus transmission by homopterous insects. Virus Res. 141, 158–168. Finlay, K.J., Luck, J.E., 2011. Response of the bird cherry-oat aphid (Rhopalosiphun padi) to climate change in relation to its pest status, vectoring potential and function in a crop-vector-virus pathosystem. Agric. Ecosys. Environ. 144, 405–421. Firdaus, S., van Heusden, A., Harpenas, A., Supena, E.D.J., Visser, R.G.F., et al., 2011. Identification of silverleaf whitefly resistance in pepper. Plant Breed. 130, 708–714. Foster, J.A., Hadidi, A., 1998. Exclusion of viruses. In: Hadidi, A., Khetarpal, R.K., Koganezawa, H. (Eds.), Plant Virus Disease Control APS Press, St. Paul, MN, pp. 208–229. Francki, R.I.B., Miles, R., 1985. Mechanical transmission of sowbane mosaic virus carried on pollen from infected plants. Plant Pathol. 34, 11–19. Fraser, R.S.S., 1988. Virus recognition and pathogenicity: implications for resistance mechanisms and breeding. Pest. Sci. 23, 267–275. Fraser, R.S.S., 1992. The genetics of plant–virus interactions: implications for plant breeding. Euphytica 63, 175–185. Frazier, N.W., Voth, V., Bringhurst, R.S., 1965. Inactivation of two strawberry viruses in plants grown in a natural high temperature environment. Phytopathology 53, 1203–1205. Frison, E.A., Ng, S.Y., 1981. Elimination of sweet potato virus disease agents by meristem tip culture. Trop. Pest Manag. 27, 452–454. Fuller, V.L., Lilley, C.J., Urwin, P.E., 2008. Nematode resistance. New Phytol. 180, 27–44. Fulton, R.W., 1986. Practices and precautions in the use of cross protection for plant virus disease control. Annu. Rev. Phytopathol. 24, 67–81. Gaborjanyi, R., Pasztor, L., Papp, M., Szabo, J., Mesterhazy, A., et  al., 2003. Use of remote sensing to detect virus infected wheat plants in the field. Cereal Res. Comm. 31, 113–120. Gallard, A., Mallet, R., Chevalier, M., Grapin, A., 2011. Limited elimination of two viruses by cryotherapy of pelargonium apices related to virus distribution. Cryo Letters 32, 111–122. Gallitelli, D., Vovlas, C., Martelli, G., Montasser, M.S., Tousignant, M.E., et  al., 1991. Satellite-mediated protection of tomato against cucumber mosaic virus: II. Field test under natural epidemic conditions in southern Italy. Plant Dis. 75, 93–95. Gao, L.L., Anderson, J.P., Klingler, J.P., Nair, R.M., Edwards, O.R., et al., 2007. Involvement of the octadecanoid pathway in bluegreen aphid resistance in Medicago truncatula. Mol. Plant Microbe Interact. 20, 82–93. Garnsey, S.M., Randles, J.W., 1987. Biological interactions and agricultural implications of viroids. In: Semancik, J.S. (Ed.), Viroids and Viroid-Like Pathogens CRC Press, Boca Raton, FL, pp. 127–160. Garnsey, S.M., Gottwald, T.R., Yokomi, R.K., 1998. Control strategies for citrus tristeza virus. In: Hadidi, A., Khetarpal, R.K., Koganezawa, H. (Eds.), Plant Virus Disease Control APS Press, St. Paul, MN, pp. 639–658. Garrett, K.A., Hulbert, S.H., Leach, J.E., Travers, S.E., 2006. Ecological genomics and epidemiology. Eur. J. Plant Pathol. 115, 35–51. Garrett, K.A., Forbes, G.A., Savary, S., Skelsey, P., Sparks, A.H., et  al., 2011. Complexity in climate-change impacts: an analytical framework for effects mediated by plant disease. Plant Pathol. 60, 15–30.

867

Gay, J.D., Johnson, A.W., Chalfant, R.B., 1973. Effects of a trap crop on the introduction and distribution of cowpea virus by soil and insect vectors. Plant Dis. Rep. 57, 684–688. Gebhardt, C., Valkonen, J.P., 2001. Organization of genes controlling disease resistance in the potato genome. Annu. Rev. Phytopathol. 39, 79–102. Georghiou, G.P., Saito, T. (Eds.), 1983. Pest Resistance to Pesticides Plenum Press, New York, NY. Gerpa, C.P., 1984. Applied and theoretical aspects of virus adsorption to surfaces. Adv. Appl. Microbiol. 30, 133–168. Gibbs, A.J., 1962. Lucerne mosaic virus in British lucerne crops. Plant Pathol. 11, 167–171. Gibson, R.W., Rice, A.D., 1986. The combined use of mineral oils and pyrethroids to control plant viruses transmitted non- and semi-persistently by Myzus persicae. Ann. Appl. Biol. 109, 465–472. Gibson, R.W., Pickett, J.A., Dawson, G.W., Rice, A.D., Stribley, M.F., 1984. Effects of aphid alarm pheromone derivatives and related compounds on non- and semi-persistent plant virus transmission by Myzus persicae. Ann. Appl. Biol. 104, 203–209. Gonsalves, D., 1998. Control of papaya ringspot virus in papaya: a case study. Annu. Rev. Phytopathol. 36, 415–437. Gooding, G.V., 1975. Inactivation of tobacco mosaic virus on tomato seed with trisodium orthophosphate and sodium hypochlorite. Plant Dis. Rep. 59, 770–772. Gregory, P.H., 1948. The multiple-infection transformation. Ann. Appl. Biol. 35, 412–417. Grisham, M.P., Johnson, R.M., Zimba, P.V., 2010. Detecting sugarcane yellow leaf virus infection in asymptomatic leaves with hyperspectral remote sensing and associated leaf pigment changes. J. Virol. Meth. 167, 140–145. Grogan, R.G., Welch, J.E., Bardin, R., 1952. Common lettuce mosaic and its control by use of disease free seed. Phytopathology 42, 573–578. Grout, B.W., 1999. Meristem-tip culture for propagation and virus elimination. Methods Mol. Biol. 111, 115–125. Grumet, R., Kabelka, E., McQueen, S., Wai, T., Humphrey, R., 2000. Characterization of sources of resistance to the watermelon strain of papaya ringspot virus in cucumber: allelism and co-segregation with other potyvirus resistances. Theor. Appl. Genet. 101, 463–472. Gunasinghe, U.B., Irwin, M.E., Karnpmeier, G.E., 1988. Soybean leaf pubescence affects aphid vector transmission and field spread of soybean mosaic virus. Ann. Appl. Biol. 112, 259–272. Guy, P.L., 1988. Pasture ecology of barley yellow dwarf viruses at Sanford, Tasmania. Plant Pathol. 37, 546–550. Guy, P.L., Webster, D.E., Davis, L., 1998. Pests of non-indigenous organisms: hidden costs of introduction. Trends Ecol. Evol. 13, 111. Gwynn, G.R., Reilly, K.R., Komn, J.J., Burk, L.G., Reed, S.M., 1986. Genetic resistance to tobacco mosaic virus, cyst nematodes root-knot nematodes and wildfire from Nicotiana repanda incorporated into N. tabacum. Plant Dis. 70, 958–962. Hadidi, A., Khetarpal, R.K., Koganezawa, H. (Eds.), 1998. Plant Virus Disease Control APS Press, St. Paul, MN. Hammond, J., 1982. Plantago as a host of economically important viruses. Adv. Virus Res. 27, 103–140. Hampton, R.O., 1966. Probabilities of failing to detect prune dwarf virus in cherry trees by bud indexing. Phytopathology 56, 650–652. Hampton, R.O., 1988. Health status (virus) of native North American Humulus lupulus in the natural habitat. J. Phytopathol. 123, 353–362. Hansen, A.J., 1989. Antiviral chemicals for plant disease control. Crit. Rev. Plant Sci. 8, 45–88.

868

Hansen, A.J., Lane, W.D., 1985. Elimination of apple chlorotic leafspot virus from apple shoot cultures by ribavirin. Plant Dis. 69, 134–135. Hardy, V.G., Teakle, D.S., 1992. Transmission of sowbane mosaic virus by Thrips tabaci in the presence and absence of virus-carrying pollen. Ann. Appl. Biol. 121, 315–320. Harlan, J.R., 1976. Diseases as a factor in plant evolution. Annu. Rev. Phytopathol. 14, 31–51. Harrington, R., Dewar, A.M., George, B., 1989. Forecasting the incidence of virus yellows in sugar beet in England. Ann. Appl. Biol. 114, 459–469. Harrison, B.D., 2002. Virus variation in relation to resistance breaking in plants. Euphytica 124, 181–192. Harrison, B.D., Winslow, R.D., 1961. Laboratory and field studies on the relation of arabis mosaic virus to its nematode vector Xiphinema diversicaudatum Micoletzky. Ann. Appl. Biol. 49, 621–633. Hartman, R.D., 1974. Dasheen mosaic virus and other phytopathogens eliminated from caladium, taro and cocoyam by culture of shoot tips. Phytopathology 64, 237–240. Harveson, R.M., Rush, C.M., Wheeler, T.A., 1996. The spread of beet necrotic yellow vein virus from point source inoculations as influenced by irrigation and tillage. Phytopathology 86, 1242–1247. Heard, A.J., Chapman, P.F., 1986. A field study of the pattern of local spread of ryegrass mosaic virus in mown grassland. Ann. Appl. Biol. 108, 341–345. Heathcote, G.D., 1973. Beet mosaic—declining disease in England. Plant Pathol. 22, 42–45. Heathcote, G.D., Broadbent, L., 1961. Local spread of potato leaf roll and Y viruses. Eur. Potato J. 4, 138–143. Heijbroek, W., 1988. Dissemination of rhizomania by soil, beet seeds and stable manure. Neth. J. Plant Pathol. 94, 9–15. Hein, A., 1971. Zur Wirkung von Öl auf die Virusübertragung durch Blattäiuse. Phytopathol. Z 71, 42–48. Hein, A., 1987. A contribution to the effect of fungicides and additives for formulation on the rhizomania infection of sugar beets (beet necrotic yellow vein virus). J. Plant Dis. Prot. 94, 250–259. Heinrichs, E.A., Rapusas, H.R., Aquino, G.B., Palis, F., 1986. Integration of host plant resistance and insecticides in the control of Nephotettix virescens (Homoptera: Cicadellidae), a vector of rice tungro virus. J. Econ. Entomol. 79, 437–443. Helliot, B., Swennen, R., Poumay, Y., Frison, E., Lepoivre, P., et  al., 2003a. Ultrastructural changes associated with cryopreservation of banana (Musa spp.) highly proliferating meristems. Plant Cell Rep. 21, 690–698. Helliot, B., Panis, B., Frison, E., De Clercq, E., Swennen, R., et  al., 2003b. The acyclic nucleoside phosphonate alalogues, adefovir, tenofovir and PMEDAP efficiently eliminate banana streak virus from banana (Musa spp.). Antiviral Res. 59, 121–126. Herselman, L., Thwaites, R., Kimmins, F.M., Courtois, B., van der Merwe, J.P.A., et  al., 2004. Identification and mapping of AFLP markers linked to peanut (Arachis hypogaea L.) resistance to the aphid vector of groundnut rosette disease. Theor. Appl. Genet. 109, 1426–1433. Heuss, K., Liu, Q., Hammerschlag, F.A., Hammond, R.W., 1999. A cDNA probe detects Prunus necrotic ringspot virus in three peach cultivars after micrografting and in peach shots following long-term culture at 4 degrees C. HortScience 34, 346–347. Hewitt, W.B., Chiarappa, L. (Eds.), 1977. Plant Health and Quarantine in International Transfer of Genetic Resources CRC Press, Boca Raton, FL.

Plant Virology

Hodge, S., Hardie, J., Powell, G., 2011. Parasitoids aid dispersal of a nonpersistently transmitted plant virus by disturbing the aphid vector. Agric. Forest Entomol. 13, 83–88. Hollings, M., 1965. Disease control through virus-free stock. Annu. Rev. Phytopathol. 3, 367–396. Holmes, F.O., 1955. Elimination of spotted wilt virus from dahlias by propagation of tip cuttings. Phytopathology 45, 224–226. Holt, J., Chancellor, T.C.B., 1997. A model of plant virus disease epidemics in asynchronously-planted cropping systems. Plant Pathol. 46, 490–501. Holt, J., Jeger, M.J., Thresh, J.M., Otim-Nape, G.W., 1997. An epidemiological model incorporating vector population dynamics applied to African cassava mosaic virus disease. J. Appl. Ecol. 34, 793–806. Hooks, C.R.R., Fereres, A., 2006. Protecting crops from non-persistently aphid-transmitted viruses: a review on the use of barrier plants as a management tool. Virus Res. 120, 1–16. Howell, W.E., Mink, G.I., 1971. The relationship between volunteer sugarbeets and occurrence of beet mosaic and beet western yellow viruses in Washington beet fields. Plant Dis. Rep. 55, 676–678. Howell, W.E., Mink, G.I., 1977. The role of weed hosts, volunteer carrots, and overlapping growing seasons in the epidemiology of carrot thin leaf and carrot motley dwarf viruses in central Washington. Plant Dis. Rep. 61, 217–222. Howell, W.E., Mink, G.I., 1988. Natural spread of cherry rugose mosaic disease and two prunus necrotic ringspot virus biotypes in a central Washington sweet cherry orchard. Plant Dis. 72, 636–640. Hudak, K.A., Wang, P., Tumer, N.E., 2000. A novel mechanism for inhibition of translation by pokeweed antiviral protein: depurination of the capped RNA template. RNA 6, 369–380. Hudak, K.A., Bauman, J.D., Tumer, N.E., 2002. Pokeweed antiviral protein binds to the cap structure of eukaryotic mRNA and depurinates the mRNA downstream of the cap. RNA 8, 1148–1159. Hughes, J.d.’A., Ollennu, L.A.A., 1994. Mild strain protection of cocoa in Ghana against cocoa swollen shoot virus—a review. Plant Pathol. 43, 442–457. Hull, R., 1964. Spread of groundnut rosette virus by Aphis craccivora (Koch). Nature 202, 213–214. Hull, R., 1965. Virus diseases of sweet peas in England. Plant Pathol. 14, 150–153. Hull, R., 1991. Introduction: plant viral pathogenesis. Semin. Virol. 2, 79–80. Hullé, M., d’Acier, A.C., Bankhead-Dronnet, S., Harrington, R., 2010. Aphids in the face of global changes. C.R. Biol. 333, 497–503. Hwang, C.-F., Xu, K., Hu, R., Zhou, R., Riaz, S., et  al., 2010. Cloning and characterization of XiR1, a locus responsible for dagger nematode resistance in grape. Theor. Appl. Genet. 121, 789–799. Hyman, B.C., 1996. Molecular systematic and population biology of phytonematodes: some unifying principles. Fund. Appl. Nematol. 19, 309–313. IPCC, 2007. Summary for policymakers. In: Solomon, S., Qin, D., Manning, M., Xhen, Z., Marquis, M. (Eds.), Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel for Climate Change Cambridge University Press, Cambridge. Irwin, M.E., 1999. Implications of movement in developing and deploying integrated pest management strategies. Agric. Forest Meteorol. 97, 235–248. Irwin, M.E., Ruesink, W.G., 1986. Vector intensity: a product of propensity and activity. In: McClean, G.D., Garrett, R.G., Ruesink, W.G. (Eds.), Plant Virus Epidemics Academic Press, Orlando, FL, pp. 13–33.

Chapter | 14  Ecology, Epidemiology, and Control of Plant Viruses

Jaag, H.M., Nagy, P.D., 2010. The combined effect of environmental and host factors on the emergence of viral RNA recombinants. PLoS Pathog. 6, e1001156. Jacobsen, B.J., 1997. Role of plant pathology in integrated pest management. Annu. Rev. Phytopathol. 35, 373–391. Jacquemond, M., Tepfer, M., 1998. Breeding for resistance to plant viruses. In: Hadidi, A., Khetarpal, R.K., Koganezawa, H. (Eds.), Plant Virus Disease Control APS Press, St. Paul, MN, pp. 94–120. Jeger, M.J., Chan, M.S., 1995. Theoretical aspects of epidemics—uses of analytical models to make strategic management decisions. Can. J. Plant Pathol. 17, 109–114. Jeger, M.J., van den Bosch, F., Madden, L.V., Holt, J., 1998. A model for analyzing plant–virus transmission characteristics and the epidemic development. J. Math. Appl. Med. Biol. 15, 1–18. Jeger, M.J., Chen, Z., Powell, G., Hodge, S., van den Bosch, F., 2011a. Interactions in a host plant-virus-vector-parasitoid system: modelling the consequences for virus transmission and disease dynamics. Virus Res. 159, 183–193. Jeger, M.J., van den Bosch, F., Madden, L.V., 2011b. Modelling virusand host-limitation in vectored plant disease epidemics. Virus Res. 159, 215–222. Jenner, C.E., Sánchez, F., Nettleship, S.B., Foster, G.D., Ponz, F., et al., 2000. The cylindrical inclusion gene of Turnip mosaic virus encodes a pathogenic determinant to the Brassica resistance gene TuRB01. Mol. Plant Microbe Interact. 13, 1102–1108. Jenner, C.E., Tomimura, K., Ohshima, K., Hughes, S.L., Walsh, J.A., 2002. Mutations in Turnip mosaic virus P3 and cylindrical inclusion proteins are separately required to overcome two Brassica napus resistance genes. Virology 300, 50–59. Johnson, E.M., Valleau, W.D., 1946. Field strains of tobacco mosaic virus. Phytopathology 36, 112–116. Johnson, J., Ogden, W.B., 1929. The overwintering of tobacco mosaic virus. Wis. Agric. Exp. Stn. Bull. 95, 1–25. Johnson, S.J., 1995. Insect migration in North America: Synoptic-scale transport in a highly seasonal environment. In: Drake, V.A., Gatehouse, A.G. (Eds.), Insect Migration: Tracking Resources Through Space and Time, Cambridge University Press, Cambridge, pp. 31–66. Johnstone, G.R., Koen, T.B., Conley, H.L., 1982. Incidence of yellows in sugar beet as affected by variation in plant density and arrangement. Bull. Entomol. Res. 72, 289–294. Jones, A.T., 1998. Control of virus infection in crops through breeding plants for vector resistance. In: Hadidi, A., Khetarpal, R.K., Koganezawa, H. (Eds.), Plant Virus Disease Control APS Press, St. Paul, MN, pp. 41–55. Jones, R.A.C., 2004. Using epidemiological information to develop effective integrated virus disease management strategies. Virus Res. 100 (5), 30. Jones, R.A.C., 2006. Control of plant virus diseases. Adv. Virus Res. 67, 205–244. Jones, R.A.C., 2009. Plant virus emergence and evolution: origins, new encounter scenarios, factors driving emergence, effects of changing world conditions, and prospects for control. Virus Res. 141, 113–130. Jones, R.A.C., Harrison, B.D., 1972. Ecological studies on potato moptop virus in Scotland. Ann. Appl. Biol. 71, 47–57. Jones, R.A.C., Salam, M.U., Maling, T.J., Diggle, A.J., Thackray, D.J., 2010. Principles of predicting plant virus disease epidemics. Annu. Rev. Phytopathol. 48, 179–203. Julier, B., Bournoville, R., Landre, B., Ecalle, C., Carre, S., 2004. Genetic analysis of lucerne (Medicago sativa L.) seedling resistance to pea aphid (Acyrthosiphon pisum Harris). Euphytica 138, 133–139.

869

Khan, M.A., Mukhopadhyay, S., 1985. Studies on the effect of some alternative cultural methods on the incidence of yellow vein mosaic virus (YVMV) disease of okra (Abelmoschus esculentus (L.) Moench.). Indian J. Virol. 1, 69–72. Kahn, R.P., 1976. Aseptic plantlet culture to improve the phytosanitary aspects of plant introduction for asparagus. Plant Dis. Rep. 60, 459–461. Kahn, R.P., 1989. Plant Protection and Quarantine, vols. 1–3. CRC Press, Boca Raton, FL. Kahn, R.P., Monroe, R.L., 1970. Viruses isolated from arborescent Datura species from Bolivia, Ecuador and Columbia. Plant Dis. Rep. 54, 675–677. Kang, B.-C., Yeam, I., Jahn, M.M., 2005. Genetics of plant virus resistance. Annu. Rev Phytopathol. 43, 581–621. Kassanis, B., Varma, A., 1967. The production of virus-free clones of some British potato varieties. Ann. Appl. Biol. 59, 447–450. Keesing, F., Belden, L.K., Daszak, P., Dobson, A., Harvell, C.D., et  al., 2010. Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468, 647–652. Kenten, R.H., Lockwood, G., 1977. Studies on the possibility of increasing resistance to cocoa swollen-shoot virus by breeding. Ann. Appl. Biol. 85, 71–78. Kerlan, C., Robert, Y., Perennec, P., Guillery, E., 1987. Survey of the level of infection by PVY-O and control methods developed in France for potato seed production. Potato Res. 30, 651–667. Khetarpal, R.K., Maisonneuve, B., Maury, Y., Chalhoab, B., Dianant, S., et al., 1998. Breeding for resistance to plant viruses. In: Hadidi, A., Khetarpal, R.K., Koganezawa, H. (Eds.), Plant Virus Disease Control APS Press, St. Paul, MN, pp. 14–32. Kimble, K.A., Grogan, R.G., Greathead, A.S., Paulus, A.O., House, J.K., 1975. Development, application and comparison of methods for indexing lettuce seed for mosaic virus in California. Plant Dis. Rep. 59, 461–464. Klein, M., Harpaz, I., 1970. Heat suppression of plant-virus propagation in the insect vector’s body. Virology 41, 72–76. Klein, R.E., Wyatt, S.D., Kaiser, W.J., 1988. Incidence of bean common mosaic virus in USDA Phaseolus germplasm collection. Plant Dis. 72, 301–302. Koenig, R., 1986. Plant viruses in rivers and takes. Adv. Virus Res. 31, 321–333. Koenig, R., An, D., Lesemann, D.-E., Burgermeister, W., 1988. Isolation of carnation ringspot virus from a canal near a sewage plant: cDNA hybridization analysis, serology, and cytopathology. J. Phytopathol. 121, 346–356. Koenig, R., Pfeilstetter, E., Kegler, H., Lesemann, D.E., 2004. Isolation of two strains of a new tombusvirus (Havel river virus, HaRV) from surface waters in Germany. Eur. J. Plant Pathol. 110, 429–433. Kontzog, H.G., Kleinhempel, H., Kegler, H., 1988. Detection of plant pathogenic viruses in waters. Arch. Phytopathol. Pflanzenschutz 24, 171–172. Kopp, M., Rouster, I., Fritig, B., Darvill, A., Albersheim, P., 1989. Host– pathogen interactions. XXXII. A fungal glucan preparation protects Nicotiana against infection by viruses. Plant Physiol. 90, 208–216. Krczal, G., 1998. Virus certification of ornamental plants—the European strategy. Breeding for resistance to plant viruses. In: Hadidi, A., Khetarpal, R.K., Koganezawa, H. (Eds.), Plant Virus Disease Control APS Press, St. Paul, MN, pp. 277–287. Kunert, G., Reinhold, C., Gershenzon, J., 2010. Constitutive emission of the aphid alarm pheromone, (E)-beta-farnesene, from plants does not serve as a direct defense against aphids. BMC Ecol. 10, 23.

870

Lanter, J.M., McQuire, J.M., Goode, M.J., 1982. Persistence of tomato mosaic virus in tomato debris and soil under field conditions. Plant Dis. Rep. 66, 552–555. Larsen, R.C., Kurowski, C.J., Miklas, P.N., 2010. Two independent quantitative trait loci are responsible for novel resistance to Beet curly top virus in common bean landrace G122. Phytopathology 100, 972–978. Lecoq, H., 1998. Control of plant virus diseases by cross protection. In: Hadidi, A., Khetarpal, R.K., Koganezawa, H. (Eds.), Plant Virus Disease Control APS Press, St. Paul, MN, pp. 33–40. Lecoq, H., 1999. Epidemiology of cucurbit aphid-borne yellows virus. In: Smith, H.G., Barker, H. (Eds.), The Luteoviridae CAB International, Wallingford, UK, pp. 243–248. Lecoq, H., Moury, B., Desbiez, C., Palloix, A., Pitrat, M., 2004. Durable virus resistance in plants through conventional approaches: a challenge. Virus Res. 100, 31–39. Legarrea, S., Karnieli, A., Fereres, A., Weintraub, P.G., 2010. Comparison of UV-absorbing nets in pepper crops: spectral properties, effects on plants and pest control. Photochem. Photobiol. 86, 324–330. Legg, J.T., Lockwood, G., 1977. Evaluation and use of a screening method to aid selection of cocoa (Theobroma cacao) with field resistance to cocoa swollen-shoot virus in Ghana. Ann. Appl. Biol. 86, 241–248. Lei, J.D., Agrios, G.N., 1986. Mechanisms of resistance in corn to maize dwarf mosaic virus. Phytopathology 76, 1034–1040. Leppik, E.E., 1970. Gene centers of plants as sources of disease resistance. Annu. Rev. Phytopathol. 8, 323–344. Lewis, T., Dibley, G.C., 1970. Air movement near windbreaks and a hypothesis of the mechanism of the accumulation of airborne insects. Ann. Appl. Biol. 66, 477–484. Li, J.R., Todd, T.C., Lee, J., Trick, H.N., 2011. Biotechnological application of functional genomics towards plant-parasitic nematode control. Plant Biotechnol. J. 9, 936–944. Li, Q., Xie, Q.G., Smith-Becker, J., Navarre, D.A., Kaloshian, I., 2006. Mi-1-mediated aphid resistance involves salicylic acid and mitogenactivated protein kinase signaling cascades. Mol. Plant Microbe Interact. 19, 655–664. Lindhout, P., 2002. The perspectives of polygenic resistance in breeding for durable resistance. Euphytica 124, 217–229. Logan, A.E., Zettler, F.W., 1985. Rapid in vitro propagation of virusindexed gladioli. Acta Hortic. 164, 169–180. Louie, R., Findley, W.R., Knoke, J.K., 1976. Variation in resistance within corn inbred lines to infection by maize dwarf mosaic virus. Plant Dis. Rep. 60, 838–842. Lovisolo, O., 1985. International transport of flowers, foliage, nursery stock and ornamental plants in Europe and the Mediterranean basin. Acta Hortic. 164, 139–151. Lozoya-Saldaña, H., Abello, F., de la Garcia, G., 1996. Electrotherapy and shoot tip culture eliminate potato virus X in potatoes. Am. Potato J. 73, 149–154. Luhn, C.F., Goheen, A.C., 1970. Viruses in early California grape vines. Plant Dis. Rep. 54, 1055–1056. Luo, H., Wylie, S.J., Coutts, B., Jones, R.A.C., Jones, M.G.K., 2011. A virus of an isolated indigenous flora spreads naturally to an introduced crop species. Ann. Appl. Biol. 159, 339–347. Madden, L.V., Campbell, C.L., 1986. Descriptions of virus disease epidemics in time and space. In: McLean, G.D., Garrett, R.G., Ruesink, W.G. (Eds.), Plant Virus Epidemics Academic Press, Orlando, FL, pp. 273–293.

Plant Virology

Madden, L.V., Paul, P.A., 2011. Meta-analysis for evidence synthesis in plant pathology: an overview. Phytopathology 101, 16–30. Madden, L.V., Louie, R., Knoke, J.K., 1987a. Temporal and spatial analysis of maize dwarf mosaic epidemics. Phytopathology 77, 148–156. Madden, L.V., Pirone, T.P., Raccah, B., 1987b. Analysis of spatial patterns of virus-diseased tobacco plants. Phytopathology 77, 1409–1417. Madden, L.V., Jeger, M.J., van den Bosch, F., 2000. A theoretical assessment of the effects of vector–virus transmission mechanism on plant virus disease epidemics. Phytopathology 90, 576–594. Madriz, J.A., de Miranda, J.R., Cabezas, E., Oliva, M., Hernandez, M., et  al., 1998. Echinocloa hoja blanca and rice hoja blanca viruses occupy distinct ecological niches. J. Phytopathol. 146, 305–308. Maisonneuve, B., Chovelon, V., Lot, H., 1991. Inheritance of resistance to beet western yellows virus in Lactuca virosa L. HortScience 26, 1543–1545. Maling, T., Diggle, A.J., Thackray, D.J., Siddique, K.H.M., Jones, R.A.C., 2010. An epidemiological model for externally acquired vector-borne viruses applied to beet western yellows virus in Brassica napus crops in a Mediterranean-type environment. Crop Pasture Sci. 61, 132–144. Malmstrom, C.M., Melcher, U., Bosque-Pérez, N.A., 2011. The expanding field of plant virus ecology: historical foundations, knowledge gaps and future directions. Virus Res. 159, 84–94. Manwan, I., Sama, S., Rizvi, S.A., 1985. Use of varietal rotation in the management of tungro disease in Indonesia. Indones. Agric. Res. Dev. J. 7, 43–48. Manwan, I., Sama, S., Rizvi, S.A., 1987. Management strategy to control rice tungro in Indonesia Proceeding of the Workshop on Rice Tungro Virus. Ministry of Agriculture, AARD-Maros Research Institution for Food Crops, Maros, Indonesia, pp. 91–97. Markham, R., Smith, K.M., 1949. Studies on the virus of turnip yellow mosaic. Parasitology 39, 330–342. Markham, R., Matthews, R.E.F., Smith, K.M., 1948. Testing potato stocks for virus X. Farming February, 40–46. Marrou, J., Messian, C.-M., Migliori, A., 1967. Méthode de contrôle de l’état sanitaire des graines de laitice. Ann. Epiphyt. 18, 227–238. Marrou, J., Quiot, J.B., Dutuil, M., Labonne, G., Leclant, F., et al., 1979. Ecology and epidemiology of cucumber mosaic virus. III. Interest of the exposure of bait plants in the study of cucumber mosaic virus dissemination. Ann. Phytopathol. 11, 291–306. Masmoudi, K., Duby, C., Suhas, M., Guo, J.Q., Guyot, L., et  al., 1994. Quality-control of pea seed for pea seed-borne mosaic virus. Seed Sci. Technol. 22, 407–414. Matthews, R.E.F., 1949. Studies on potato virus X. I. Types of change in potato virus X infections. Ann. Appl. Biol. 36, 448–459. Matthews, R.E.F., 1953. Incorporation of 8-azaguanine into nucleic acid of tobacco mosaic virus. Nature 171, 1065–1066. Matthews, R.E.F., 1981. Plant Virology, second ed. Academic Press, New York, NY. Matthews, R.E.F., 1991. Plant Virology, third ed. Academic Press, London. Maury, Y., Bossennec, J.-M., Boudazin, G., Hampton, R., Pietersen, G., et  al., 1987. Factors influencing ELISA evaluation of transmission of pea seed-borne mosaic virus in infected pea seed: seed-group size and seed decortication. Agronomie 7, 225–230. Maury, Y., Duby, C., Khetarpal, R.K., 1998. Seed certification for viruses. Breeding for resistance to plant viruses. In: Hadidi, A., Khetarpal,

Chapter | 14  Ecology, Epidemiology, and Control of Plant Viruses

R.K., Koganezawa, H. (Eds.), Plant Virus Disease Control APS Press, St. Paul, MN, pp. 237–248. Mazzi, D., Dorn, S., 2012. Movement of insect pests in agricultural landscapes. Ann. Appl. Biol. 160, 97–113. McElhany, P., Real, L.A., Power, A.G., 1995. Vector preference and disease dynamics—a study of barley yellow dwarf virus. Ecology 76, 444–457. McKinney, H.H., 1929. Mosaic diseases in the Canary Islands, West Africa and Gibraltar. J. Agric. Res. 39, 557–578. McLean, G.D., Burl, J.R., Thomas, D.W., Sproul, A.N., 1982. The use of reflective mulch to reduce the incidence of watermelon mosaic virus in Western Australia. Crop Prot. 1, 491–496. Meehl, G., Stocker, T., Collin, W., Friedlingstein, P., Gaye, A. (Eds.), 2007. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change Cambridge University Press, Cambridge. Meshi, T., Motoyoshi, F., Adachi, A., Watanabe, Y., Takamatsu, N., et al., 1988. Two concomitant base substitutions in the putative replicase genes of tobacco mosaic virus confer the ability to overcome the effects of a tomato resistance gene, Tm-1. EMBO J. 7, 1575–1581. Mestre, P., Brigneti, G., Baulcombe, D.C., 2000. An Ry-mediated resistance response requires the intact active site of the NIa proteinase from potato virus Y. Plant J. 23, 653–661. Mink, G.I., Wample, R., Howell, W.E., 1998. Heat treatment of perennial plants to eliminate phytoplasmas, viruses and viroids while maintaining plant survival. Breeding for resistance to plant viruses. In: Hadidi, A., Khetarpal, R.K., Koganezawa, H. (Eds.), Plant Virus Disease Control APS Press, St. Paul, MN, pp. 332–345. Mirik, M., Jones, D.C., Price, J.A., Workneh, F., Ansley, R.J., et al., 2011. Satellite remote sensing of wheat infected by wheat streak mosaic virus. Plant Dis. 95, 4–12. Molinari, S., 2011. Natural genetic and induced plant resistance, as a control strategy to plant-parasitic nematodes alternative to pesticides. Plant Cell Rep. 30, 311–323. Montasser, M.S., Tousignant, M., Kaper, J.M., 1991. Satellite-mediated protection against cucumber mosaic virus: I. Greenhouse experiments and simulated epidemic conditions in the field. Plant Dis. 75, 86–92. Montasser, M.S., Tousignant, M.E., Kaper, J.M., 1998. Viral satellite RNAs for the prevention of cucumber mosaic virus (CMV) disease in field-grown pepper and melon plants. Plant Dis. 82, 1298–1303. Moore, S.M., Manore, C.A., Bokil, V.A., Borer, E.T., Hosseini, P.R., 2011. Spatiotemporal model of barley and cereal yellow dwarf virus transmission dynamics with seasonality and plant competition. Bull. Mathemat. Biol. 73, 2707–2730. Moreira, A., Jones, R.A.C., Fribourg, C.E., 1978. A resistance breaking strain of potato virus X that does not cause local lesions in Gomphrena globose. Proc. Int. Congr. Plant Pathol., 56. 3rd, Abstract. Moreno, P., Ambos, S., Albiach-Marti, M.R., Guerri, J., Pena, L., 2008. Plant diseases that changed the World—Citrus tristeza virus: a pathogen that changed the course of the citrus industry. Mol. Plant Pathol. 9, 251–268. Moury, B., Desbiez, C., Jacquemond, M., Lecoq, H., 2006. Genetic diversity of plant viral populations: towards hypothesis testing in molecular epidemiology. Adv. Virus Res., 49. Mukherjee, S.S., Lough, T., Hopcroft, D.H., Castello, J.D., 2012. New tombusviruses isolated from surface waters in New Zealand. Austral. Plant Pathol. 41, 79–84.

871

Mukhopadhyay, S., Chowdhury, A.K., 1973. Some epidemiological aspects of tungro virus disease of rice in West Bengal. Int. Rice Commun. Newsl. 22, 44–57. Mullin, R.H., Smith, S.H., Frazier, N.W., Schlegel, D.E., McCall, S.R., 1974. Meristem culture frees strawberries of mild yellow edge, pallidosis and mottle diseases. Phytopathology 64, 1425–1429. Murant, A.F., Lister, R.M., 1967. Seed-transmission in the ecology of nematode-borne viruses. Ann. Appl. Biol. 59, 63–76. Murant, A.F., Taylor, C.E., 1965. Treatment of soil with chemicals to prevent transmission of tomato black ring and raspberry ringspot viruses by Longidorus elongatus (de Man). Ann. Appl. Biol. 55, 227–237. Murphy, J.F., Zehnder, G.W., Schuster, D.J., Sikora, E.J., Polston, J.E., et al., 2000. Plant growth-promoting rhizobacterial mediated protection of tomato against tomato mottle virus. Plant Dis. 84, 779–784. Murugan, M., Cardona, P.S., Duraimurugan, P., Whitfield, A.E., Schneweis, D., et  al., 2011. Wheat curl mite resistance: interactions of the mite feeding with wheat streak mosaic virus infection. J. Econ. Entomol. 104, 1406–1414. Nagaich, B.B., Upadhya, M.D., Prakash, O., Singh, S.J., 1968. Cytoplasmically determined expression of symptoms of potato virus X crosses between species of Capsicum. Nature 220, 1341–1342. Nameth, S.T., Dodds, J.A., Paulus, A.O., Laemmien, F.F., 1986. Cucurbit viruses of California: an ever-changing problem. Plant Dis. 70, 8–11. Navarro, L., Llacer, G., Cambra, M., Arregui, J.M., Juarez, J., 1983. Shoot-tip grafting in vitro for elimination of viruses in peach plants (Prunus persica Batsch). Acta Hortic. 130, 185–192. Nutter, F.W., 1997. Quantifying the temporal dynamics of plant virus epidemics: a review. Crop Protect 16, 603–618. Ohta, S., Kuniga, T., Nishikawa, F., Yamasaki, A., Endo, T., et al., 2011. Evaluation of novel antiviral agents in the elimination of Satsuma dwarf virus (SDV) by semi-micrografting in citrus. J. Japan. Soc. Hort. Sci. 80, 145–149. Oliver, J.E., Fuchs, M., 2011. Tolerance and resistance to viruses and their vectors in Vitis sp.: a virologist’s perspective of the literature. Am. J. Enolog. Viticult. 62, 438–451. Orr, C.C., Newton, O.H., 1971. Distribution of nematodes by wind. Plant Dis. Rep. 55, 61–63. Osborne, J.L., Loxdale, H.D., Woiwod, I.P., 2002. Monitoring insect dispersal: methods and approaches. In: Bullock, J.M., Kenward, R.E., Hails, R.S. (Eds.), Dispersal Ecology: The 42nd Symposium of the British Ecological Society Held at the University of Reading, 2–5 April 2001 Blackwell Science, Malden, MA, pp. 24–49. Paduch-Cichal, E., Kryczynski, S., 1987. A low-temperature therapy and meristem-tip culture for eliminating four viroids from infected plants. J. Phytopathol. 118, 341–346. Paludan, N., 1985. Spread of viruses by a recirculating water supply in soilless culture. Phytoparasitica 13, 276. Palukaitis, P., Roossinck, M.J., 1996. Spontaneous change of a benign satellite RNA of cucumber mosaic virus to a pathogenic variant. Nature Biotech. 14, 1264–1268. Parejarlarn, A., Lapis, D.B., Hibino, H., 1984. Reaction of rice varieties to rice ragged stunt virus (RSV) infection by three known plant hopper (BPH) biotypes. Int. Rice Res. Newsl. 9, 7–8. Park, W.M., Lee, G.P., Ryu, K.H., Park, K.W., 1999. Transmission of tobacco mosaic virus in recirculating hydroponic system. Scientia Hortic. 79, 217–226. Paunovic, S., Ruzic, D., Vujovic, T., Milenkovic, S., Ievremovic, D., 2007. In vitro production of plum pox virus-free plums by chemotherapy with riboflavin. Biotech. Biotechnol. Equipment 21, 417–421.

872

Pauquet, J., Burget, E., Hagen, L., Chovelon. V., Le Menn, A. et  al. (2004). Map-based cloning of the Vat gene from melon conferring resistance to both aphid colonization and aphid transmission of several viruses. In: Lebeda, A., Paris, H.S. (Eds.), Progress in Cucurbit Genetics and Breeding Research—Proceedings of the 8th EUCARPIA Meeting on Cucurbit Genetics and Breeding Olomouc, Czech Republic, pp. 325–329. Pegadaraju, V., Knepper, C., Reese, J.C., Shah, J., 2005. Premature leaf senescence modulated by the Arabidopsis thaliana PAD4 gene is associated with defense against the phloem feeding green peach aphid. Plant Physiol. 139, 1927–1934. Perring, T.M., Gruenhagen, N.M., Farrar, C.A., 1999. Management of plant viral diseases through chemical control of insect vectors. Annu. Rev. Entomol. 44, 457–481. Perry, J.N., 1998. Measures of spatial pattern for counts. Ecology 79, 1008–1017. Piazzolla, P., Palmieri, F., Nuzzaci, M., 1989. Infectivity studies on cucumber mosaic virus treated with a clay material. J. Phytopathol. 127, 291–295. Piron, P.G.M., 1986. New aphid vectors of potato virus YN. Neth. J. Plant Pathol. 92, 223–229. Polak, J., 1983. Variability of resistance of white cabbage to turnip mosaic virus. Tagungsber. Akad. Landwirtschaftswiss. D.D.R 216, 331–335. Posnette, A.F., 1969. Tolerance of virus infection in crop plants. Rev. Appl. Mycol. 48, 113–118. Posnette, A.F., Todd, J.M.C.A., 1955. Virus diseases of cacao in West Africa. IX. Strain variation and interference in virus 1 A. Ann. Appl. Biol. 43, 433–453. Power, A.G., 1996. Competition between viruses in a complex plant– pathogen. Ecology 77, 1004–1010. Preil, W., Koenig, R., Engelhardt, M., Meier-Dinkel, A., 1982. Elimination of poinsettia mosaic virus (PoiMV) I and poinsettia cryptic virus (PoiCV) from Euphorbia pulcherrima Willd by cell suspension culture. Phytopathol. Z 105, 193–197. Proctor, V.W., 1968. Long-distance dispersal of seeds by retention in digestive tracts of birds. Science 160, 321–322. Proeseler, G., Kastirr, U., 1988. Research into the effect of fungicides against Polymyxa graminis Led. as vector of barley yellow mosaic virus. Nachrichten bl. Pflanzenschutzdienst DDR 42, 116–117. Provvidenti, R., 1990. Inheritance of resistance to pea mosaic virus in Pisum sativum. J. Hered. 81, 143–145. Provvidenti, R., Alconero, R., 1988. Inheritance of resistance to a third pathotype of pea seed-borne mosaic virus in Pisum sativum. J. Hered. 79, 76–77. Pryor, T., Ellis, J., 1993. The genetic complexity of fungal resistance genes in plants. Adv. Plant Pathol. 10, 281–305. Quiot, J.B., Devergne, J.C., Marchoux, G., Cardin, L., Douine, L., 1979. Ecology and epidemiology of cucumber mosaic virus (CMV) in South East France. VI. Distribution of two CMV groups in weeds. Ann. Phytopathol. 11, 349–357. Raski, D.J., Hewitt, W.B., 1963. Plant-parasitic nematodes as vectors of plant viruses. Phytopathology 53, 39–47. Rast, A.T.B., 1975. Variability of tobacco mosaic vines in relation to control of tomato mosaic in glasshouse tomato crops by resistance breeding and cross protection. Agric. Res. Rep. (Wageningen) 834, 1–76. Raybould, A.F., Maskell, A.F., Edwards, M.L., Cooper, J.I., Gray, A.J., 1999. The prevalence and spatial distribution of viruses in natural populations of Brassica oleracea. New Phytol. 141, 265–275.

Plant Virology

Real, L.A., McElhany, P., 1996. Spatial pattern and process in plant– pathogen interactions. Ecology 77, 1011–1025. Reynaud, B., Delatte, H., Peterschmitt, M., Fargette, D., 2009. Effects of temperature increase on the epidemiology of three major vectorborne viruses. Eur. J. Plant Pathol. 123, 269–280. Reynolds, D.R., Riley, J.R., Armes, N.J., Cooter, R.J., Tucker, M.R., et  al., 1997. Techniques for quantifying insect migration. In: Dent, D.R., Walton, M.P. (Eds.), Methods in Ecological and Agricultural Entomology CAB International, Wallingford, UK, pp. 111–145. Reynolds, D.R., Chapman, J.W., Harrington, R., 2006. The migration of insect vectors of plant and animal viruses. Adv. Virus Res. 67, 453–517. Riley, J.R., Cheng, X.-N., Zhang, X.-X., Reynolds, D.R., Xu, G.-M., et al., 1991. The long distance migration of Nilaparvata lugens (Stål) (Delphacidae) in China: Radar observations of mass return flight in the autumn. Ecol. Entomol. 16, 471–489. Riley, J.R., Reynolds, D.R., Smith, A.D., Rosenberg, L.J., Cheng, X.-N., et  al., 1994. Observations on the autumn migration of Nilaparvata lugens (Homoptera: Delphacidae) and other pests in east central China. Bull. Ent. Res. 84, 389–402. Robbins, M.A., Witsenboer, H., Michelmore, R.W., Laliberte, J.-F., Fortin, M.G., 1994. Genetic mapping of turnip mosaic virus resistance in Lactuca sativa. Theor. Appl. Genet. 89, 583–589. Robert, Y., 1999. Epidemiology of potato leafroll disease. In: Smith, H.G., Barker, H. (Eds.), The Luteoviridae CAB International, Wallingford, UK, pp. 221–231. Rocha-Peña, M.A., Lee, R.F., Lastra, R., Niblett, C.L., Ochoacorona, F.M., et al., 1995. Citrus tristeza virus and its aphid vector Toxoptera citricida: threats to citrus production in the Caribbean and Central and North America. Plant Dis. 79, 437–444. Rochow, W.F., 1979. Field variants of barley yellow dwarf virus: detection and fluctuation during twenty years. Phytopathology 69, 655–660. Rønde Kristensen, H., 1983. European fights against fruit tree viruses as organised by EPPO and EEC. Acta Hortic. 130, 19–29. Roos, J., Hopkins, R., Kvarnheden, A., Dixelius, C., 2011. The impact of global warming on plant diseases and insect vectors in Sweden. Eur. J. Plant Pathol. 129, 9–19. Roossinck, M.J., 2013. Plant virus ecology. PLoS Pathog. 9, e1003304. Roossinck, M.J., Saha, P., Wiley, G.B., Quan, J., White, J.D., et al., 2010. Ecogenomics: using massively parallel pyrosequencing to understand virus ecology. Mol. Ecol. 19, 81–88. Rose, D.J.W., 1974. The epidemiology of maize streak disease in relation to population densities of Cicadulina spp. Ann. Appl. Biol. 76, 199–207. Ross, J.P., Butler, A.K., 1985. Distribution of bean pod mottle virus in soybeans in North Carolina. Plant Dis. 69, 101–103. Russell, G.E., 1958. Sugar beet yellows: a preliminary study of the distribution and interrelationships of viruses and virus strains found in East Anglia 1955–57. Ann. Appl. Biol. 46, 393–398. Russell, G.E., 1960. Breeding for resistance to sugar beet yellows. Br. Sugar Beet Rev. 28, 163–170. Russell, G.E., 1966. The control of Alternaria species on leaves of sugar beet infected with yellowing viruses. II. Experiments with two yellowing viruses and virus-tolerant sugar beet. Ann. Appl. Biol. 57, 425–434. Rydén, K., Gerhardson, B., 1978. Rödklövermosaikvirus sprids med slättermaskiner. Vaextskyddsnotiser 42, 112–115. Salazar, L.F., Jones, R.A.C., 1975. Some studies on the distribution and incidence of potato mop-top virus in Peru. Am. Potato J. 52, 143–150.

Chapter | 14  Ecology, Epidemiology, and Control of Plant Viruses

Salomon, R., 1999. The evolutionary advantage of breeding for tolerance over resistance against viral plant disease. Israel J. Plant Sci. 47, 135–139. Sama, S., Hasanuddin, A., Manwan, I., Cabunagan, R.C., Hibino, H., 1991. Integrated management of rice tungro disease in South Sulawesi. Crop Protect. 10, 34–40. Sanchez-Navarro, J.A., Canizares, M.C., Cano, E.A., Pallas, V., 2007. Plant tissue distribution and Chemicals inactivation of six carnation viruses. Crop Protect. 26, 1049–1054. Sarra, S., Oevering, P., Guindo, S., Peters, D., 2004. Wind-mediated spread of Rice yellow mottle virus (RYMV) in irrigated rice crops. Plant Pathol. 53, 148–153. Sauge, M.-H., Lambert, P., Pascal, T., 2012. Co-localisation of host plant resistance QTLs affecting the performance and feeding behaviour of the aphid Myzus persicae in the peach tree. Heredity 108, 292–301. Saxena, R.C., Khan, Z.R., 1985. Electronically recorded disturbances in feeding behaviour of Nephotettix virescens (Homoptera: Cicadellidae) on neem oil-treated rice plants. J. Econ. Entomol. 78, 222–226. Sayama, H., Sato, T., Kominato, M., Natsuaki, T., Kaper, J.M., 1993. Field testing of a satellite-containing attenuated strain of cucumber mosaic virus for tomato protection in Japan. Phytopathology 83, 405–410. Schnitzler, W.H., 2004. Pest and disease management of soilless culture. Acta Hortic. 648, 191–203. Scholten, O.E., Lange, W., 2000. Breeding for resistance to rhizomania in sugar beet: a review. Euphytica 112, 219–231. Schwarz, D., Beuch, U., Bandte, M., Fakhro, A., Buttner, C., et al., 2010. Spread and interaction of Pepino mosaic virus (PepMV) and Pythium aphanidermatum in a closed nutrient solution recirculation system: effects on tomato growth and yield. Plant Pathol. 59, 443–452. Sebastian, L.S., Ikeda, R., Huang, N., Inbe, T., Coffman, W.R., et  al., 1996. Molecular mapping of resistance to rice tungro spherical virus and green leafhopper. Phytopathology 86, 25–30. Selsky, M.I., Black, L.M., 1962. Effect of high and low temperatures on the survival of wound-tumor virus in sweet clover. Virology 16, 190–198. Shaw, M.W., Osborne, T.M., 2011. Geographic distribution of plant pathogens in response to climate change. Plant Pathol. 60, 31–43. Shepard, J.F., 1981. Protoplasts as sources of disease resistance in plants. Annu. Rev. Phytopathol. 19, 145–166. Shepherd, R.J., 1972. Transmission of viruses through seed and pollen. In: Kado, C.I., Agrawal, H.O. (Eds.), Principles and Techniques in Plant Virology Van Nostrand-Reinhold, Princeton, NJ, pp. 267–292. Shepherd, R.J., Hills, F.J., 1970. Dispersal of beet yellows and beet mosaic viruses in the inland valleys of California. Phytopathology 60, 798–804. Shukla, D.D., Schmelzer, K., 1973. Studies on viruses and virus disease of cruciferous plants. XIV. Cucumber mosaic virus in ornamental and wild species. Acta Phytopathol. Acad. Sci. Hung. 8, 149–155. Shukla, D.D., Schmelzer, K., 1975. Studies on viruses and virus diseases of cruciferous plants. XIX. Analysis of the results obtained with ornamental and wild species. Acta Phytopathol. Acad. Sci. Hung. 10, 217–229. Shukla, V.D., Anjaneyulu, A., 1981. Plant spacing to reduce rice tungro incidence. Plant Dis. 65, 584–586. Shukla, V.D., Anjaneyulu, A., 1982. Evaluation of systemic insecticides to reduce tungro disease incidence in rice nursery. Indian Phytopathol. 35, 502–504.

873

Shukle, R.H., Lampe, D.J., Lister, R.M., Foster, J.E., 1987. Aphid feeding behaviour: relationship to barley yellow dwarf virus resistance in Agropyron species. Phytopathology 77, 725–729. Sidwell, R.W., Huffman, J.H., Khare, G.P., Allen, L.B., Witkowski, J.T., et  al., 1972. Broad-spectrum antiviral activity of virazole: 1-betad-ribofuranosyl-1,2,4-triazole-3-carboxamide. Science 177, 705–706. Simpkins, I., Walkey, D.G.A., Neely, H.A., 1981. Chemical suppression of virus in cultured plant tissues. Ann. Appl. Biol. 99, 161–169. Slack, S.A., Singh, R.P., 1998. Control of viruses affecting potatoes through seed potato certification programs. Breeding for resistance to plant viruses. In: Hadidi, A., Khetarpal, R.K., Koganezawa, H. (Eds.), Plant Virus Disease Control APS Press, St. Paul, MN, pp. 249–260. Slykhuis, J.T., 1974. Differentiation of transmission and incubation temperatures for wheat spindle streak mosaic virus. Phytopathology 64, 554–557. Slykhuis, J.T., Andrews, J.E., Pittmann, U.J., 1957. Relation of date of seeding winter wheat in southern Alberta to losses from wheat streak mosaic, root rot and rust. Can. J. Plant Sci. 37, 113–127. Smith, C.R., Tousignant, M.E., Geletka, L.M., Kaper, J.M., 1992. Competition between cucumber mosaic virus satellite RNAs in tomato seedlings and protoplasts: a model for satellite-mediated control of tomato necrosis. Plant Dis. 76, 1270–1274. Smith, H.C., 1967. The effect of aphid numbers and stage of plant growth in determining tolerance to barley yellow dwarf virus in cereals. N. Z. J. Agric. Res. 10, 445–466. Smith, H.G., 1986. Fodder beet clamps as a source of virus yellows. Br. Sugar Beet Rev. 54, 38–39. Smith, H.G., Barker, H. (Eds.), 1999. The Luteoviridae CAB International, Wallingford, UK. Smith, M.C., Holt, J., Kenyon, L., Foot, C., 1998. Quantitative epidemiology of banana bunchy top virus disease and its control. Plant Pathol. 47, 177–187. Smith, P.R., 1983. The Australian Fruit Variety Foundation and its role in supplying virus-tested planting material to the fruit industry. Acta Hortic. 130, 263–266. Sol, H.H., 1963. Some data on the occurrence of rattle virus at various depths in the soil and on its transmission. Tijdschr. Plantenziekten 69, 208–214. Soler, S., Prohens, J., Lopez, C., Aramburu, J., Galipienso, L., et  al., 2010. Viruses infecting tomato in Valencia, Spain: occurrence, distribution and effect of seed origin. J. Phytopathol. 158, 797–805. Solomon-Blackburn, R.M., Barker, H., 2001. Breeding virus resistant potatoes (Solanum tuberosum): a review of traditional and molecular approaches. Heredity 86, 17–35. Soto, P.E., Buddenhagen, I.W., Asnani, V.L., 1982. Development of streak virus-resistant maize populations through improved challenge and selection methods. Ann. Appl. Biol. 100, 539–546. Spak, J., Holy, A., Pavingerova, D., Votruba, I., Spakova, V., et al., 2010. New in vitro method for evaluating antivirus activity of acyclic nucleoside phosphonates against plant viruses. Antiviral Res. 88, 296–303. Spak, J., Votruba, I., Pavingerova, D., Holy, A., Spakova, V., et al., 2011. Antiviral activity of tenofovir against cauliflower mosaic virus and its metabolism in Brassica pekinensis plants. Antiviral Res. 92, 378–381. Steddom, K., Heidel, G., Jones, D., Rush, C.M., 2003. Remote detection of rhizomania in sugar beets. Phytopathology 93, 720–726. Stevens, M., Hull, R., Smith, H.G., 1997. Comparison of ELISA and RT-PCR for the detection of beet yellows closterovirus in plants and aphids. J. Virol. Methods 68, 9–16.

874

Stirling, G.R., 1999. Increasing the adoption of sustainable, integrated management strategies for soilborne diseases of high-value annual crops. Aust. J. Plant Pathol. 28, 72–79. Stobbs, L.W., McNeill, B.H., 1980. Increase of tobacco mosaic virus in graft-inoculated TMV resistant tomatoes. Can. J. Plant Pathol. 2, 217–221. Stubbs, L.L., 1956. Motley dwarf virus disease of carrot in California. Plant Dis. Rep. 40, 763–764. Sweet, J.B., 1975. Soil-borne viruses occurring in nursery soils and infecting some ornamental species of Rosaceae. Ann. Appl. Biol. 79, 49–54. Sweet, J.B., 1980. Hedgerow hawthorn (Crataegus spp.) and blackthom (Prunus spinosa) as hosts of fruit tree viruses in Britain. Ann. Appl. Biol. 94, 83–90. Szatmari-Goodman, G., Nault, L.R., 1983. Tests of oil sprays for suppression of aphid-borne maize dwarf mosaic virus in Ohio sweet corn. J. Econ. Entomol. 76, 144–149. Tanzi, M., Betti, L., De Jager, C.P., Canova, A., 1986. Isolation of an attenuated virus mutant obtained from a TMV pepper strain after treatment with nitrous acid. Phytopathol. Mediterr 25, 119–124. Tatchell, G.M., Plumb, R.T., Carter, N., 1988. Migration of alate morphs of the bird cherry aphis (Rhopalosiphum padi) and implications for the epidemiology of barley yellow dwarf virus. Ann. Appl. Biol. 112, 1–11. Taylor, C.E., Thomas, P.R., 1968. The association of Xiphinema diversicaudatum (Micoletsky) with strawberry latent ringspot and arabis mosaic viruses in a raspberry plantation. Ann. Appl. Biol. 62, 147–157. Thackray, D.J., Diggle, A.J., Jones, R.A.C., 2009. BYDV PREDICTOR: a simulation model to predict aphid arrival, epidemics of Barley yellow dwarf virus and yield losses in wheat crops in a Mediterraneantype environment. Plant Pathol. 58, 186–202. Thomas, J.E., Smith, M.K., Kessling, A.F., Hamill, S.D., 1995. Inconsistent transmission of banana bunchy top virus in micropropagated bananas and its implications for germplasm screening. Aust. J. Agric. Res. 46, 663–671. Thompson, D.L., Hebert, T.T., 1970. Development of maize dwarf mosaic symptoms in eight phytotron environments. Phytopathology 60, 1761–1764. Thomson, A.D., 1976. Virus diseases of Solanum laciniatum Ait. in New Zealand. N. Z. J. Agric. Res. 19, 521–527. Thresh, J.M., 1958. The spread of virus diseases in Cacao. West Afr. Cacao Res. Inst. Tech. Bull. 5, 1–36. Thresh, J.M., 1966. Field experiments on the spread of blackcurrant reversion virus and its gall mite vector (Phytoptus ribis Nal). Ann. Appl. Biol. 58, 219–230. Thresh, J.M., 1980. The origins and epidemiology of some important plant viruses diseases In: Coaker, T.H. (Ed.), Applied Virology, vol. VII Academic Press, London, pp. 1–65. Thresh, J.M., 1983. Progress curves of plant virus disease. Adv. Appl. Biol. 8, 1–85. Thresh, J.M., 1988. Rice viruses and “the green revolution”. Aspects Appl. Biol. 17, 187–194. Thresh, J.M., 1989a. Insect-borne viruses of rice and the green revolution. Trop. Pest Manag. 35, 264–272. Thresh, J.M., 2006a. Plant virus epidemiology: the concept of host genetic vulnerability. Adv. Virus Res. 67, 89–125. Thresh, J.M., 2006b. Control of tropical virus diseases. Adv. Virus Res. 67, 245–295.

Plant Virology

Thresh, J.M., 2008. Insect-borne viruses of rice and the Green Revolution. Trop. Pest Manag. 35 (3). Thresh, J.M., Otim-Nape, G.W., 1994. Strategies for controlling African cassava mosaic geminivirus. Adv. Vector Dis. Res. 10, 215–236. Tian, B., Yang, J., Zhang, K.Q., 2007. Bacteria used in the biological control of plant-parasitic nematodes: populations, mechanisms of action and future prospects. FEMS Microbiol. Ecol. 61, 197–213. Tien, P., Wu, G., 1991. Satellite RNA for the biocontrol of plant disease. Adv. Virus Res. 39, 321–339. Tien, P., Zhang, X., Qiu, B., Qin, B., Wu, G., 1987. Satellite RNA for the control of plant diseases caused by cucumber mosaic virus. Ann. Appl. Biol. 111, 143–152. Timian, R.G., 1974. The range of symbiosis of barley and barley stripe mosaic virus. Phytopathology 64, 342–345. Timian, R.G., 1975. Barley stripe mosaic virus and the world collection of barleys. Plant Dis. Rep. 59, 984–988. Tingey, W.M., Laubengayer, J.E., 1981. Defense against the green peach aphid and potato leafhopper by glandular trichomes of Solanum berthaultii. J. Econ. Entomol. 74, 721–725. Todd, J.M., 1958. Spread of potato virus X over a distance. Potato Virus Dis., 132–143. Todd, J.M., 1961. The incidence and control of aphid-borne potato virus diseases in Scotland. Eur. Potato J. 4, 316–329. Tomita, R., Murai, J., Miura, Y., Ishihara, H., Liu, S., et  al., 2008. Fine zapping and DNA fiber FISH analysis locates the tobamovirus resistance gene L3 of Capsicum chinense in a 400-kb region of R-like genes cluster embedded in highly repetitive sequences. Theor. Appl. Genet. 117, 1107–1118. Tomlinson, J.A., 1981. Chemotherapy of plant viruses and virus diseases. In: Harris, K.F., Maramorosch, K. (Eds.), Pathogens, Vectors and Plant Diseases: Approaches to Control Academic Press, New York, NY, pp. 23–44. Tomlinson, J.A., Faithfull, E.M., 1979. Effects of fungicides and surfactants on the zoospores of Olpidium brassicae. Ann. Appl. Biol. 93, 13–19. Tomlinson, J.A., Faithfull, E.M., 1984. Studies on the occurrence of tomato bushy stunt virus in English rivers. Ann. Appl. Biol. 104, 485–495. Tomlinson, J.A., Walker, V.M., 1973. Further studies on seed transmission in the ecology of some aphid-transmitted viruses. Ann. Appl. Biol. 73, 293–298. Tomlinson, J.A., Carter, A.L., Dale, W.T., Simpson, C.J., 1970. Weed plants as sources of cucumber mosaic virus. Ann. Appl. Biol. 66, 11–16. Tomlinson, J.A., Faithfull, E.M., Ward, C.M., 1976. Chemical suppression of the symptoms of two virus diseases. Ann. Appl. Biol. 84, 31–41. Tomlinson, J.A., Faithfull, E., Flemett, T.H., Beards, G., 1982. Isolation of infective tomato barley stunt virus after passage through the human alimentary tract. Nature 300, 637–638. Toussaint, A., Dekegel, D., Vanheule, G., 1984. Distribution of Odontoglossum ringspot virus in apical meristems of infected Cymbidium cultivars. Physiol. Plant Pathol. 25, 297–305. Toussaint, A., Kummert, J., Maroquin, C., Lebrun, A., Roggemans, J., 1993. Use of virazole to eradicate odontoglossu, ringspot virus from in vitro cultures of Cymbidium Sw. Plant Cell Tiss. Org. Cult. 32, 303–309. Toyoda, H., Oishi, Y., Matsuda, Y., Chatani, K., Hirai, T., 1985. Resistance mechanism of cultured plant cells to tobacco mosaic virus. IV. Changes in tobacco mosaic virus concentrations in soma-

Chapter | 14  Ecology, Epidemiology, and Control of Plant Viruses

clonal tobacco callus tissues and production of virus-free plantlets. Phytopathol. Z. 114, 126–133. Traoré, O., Pinel-Galzi, A., Sorho, F., Sarra, S., Rakotomalala, M., et al., 2009. A reassessment of the epidemiology of Rice yellow mottle virus following recent advances in field and molecular studies. Virus Res. 141, 258–267. Ukai, Y., Yamashita, A., 1984. Induced mutation for resistance to barley yellow mosaic virus. Jpn. Agric. Res. Quart. 17, 255–259. Urban, L.A., Sherwood, J.L., Rezende, J.A.M., Melcher, U., 1990. Examination of mechanisms of cross protection in non-transgenic plants. In: Fraser, R.S.S. (Ed.), Recognition and Response in Plant– Virus Interactions Springer, Berlin, pp. 415–426. Ullman, D.E., Qualset, C.O., McLean, D.L., 1988. Feeding responses of Rhopalosiphum padi (Homoptera: Aphidae) to barley yellow dwarf virus resistant and susceptible barley varieties. Environ. Entomol. 17, 988–991. Valleau, W.D., 1946. Breeding tobacco varieties resistant to mosaic. Phytopathology 36, 412. van Boxtel, J., Singh, B.B., Thottappilly, G., Maule, A.J., 2000. Resistance of cowpea (Vigna unguiculata (L.) Walp.) breeding lines to blackeye cowpea mosaic and cowpea aphid-borne potyvirus isolates under experimental conditions. J. Plant Dis. Protect. 107, 197–204. van den Bosch, F., McRoberts, N., van den Berg, F., Madden, L.V., 2008. The basic reproduction number of plant pathogens: matrix approaches to complex dynamics. Phytopathology 98, 239–249. van der Plank, J.E., 1946. A method for estimating the number of random groups of adjacent diseased plants in a homogeneous field. Trans. R. Soc. S. Afr. 31, 269–278. van der Plank, J.E., 1948. The relation between the size of fields and the spread of plant disease into them. Part I. Crowd diseases. Emp. J. Exp. Agric. 16, 134–142. van Hoof, H.A., 1977. Determination of the infection pressure of potato virus YN. Neth. J. Plant Pathol. 83, 123–127. van Hoof, H.A., Silver, C.N., 1976. Natural elimination of tobacco rattle virus in tulip “Apeldoorn”. Neth. J. Plant Pathol. 82, 255–256. van Oosten, H.J., Meijneke, C.A.R., Peerbooms, H., 1983. Growth, yield and fruit quality of virus-infected and virus-free golden delicious apple trees 1968–1982. Acta Hortic. 130, 213–217. Vandermoten, S., Mescher, M.C., Francis, F., Haubruge, E., Verheggen, F.J., 2012. Aphid alarm pheremone: an overview of current knowledge on biosynthesis and functions. Insect Biochem. Mol. Biol. 42, 155–163. Vanderveken, J.J., 1977. Oils and other inhibitors of nonpersistent virus transmission. In: Harris, K.F., Maramorosch, K. (Eds.), Aphids as Virus Vectors Academic Press, New York, NY, pp. 435–454. Verma, H.N., Baranwal, V.K., Srivastava, S., 1998. Breeding for resistance to plant viruses. In: Hadidi, A., Khetarpal, R.K., Koganezawa, H. (Eds.), Plant Virus Disease Control APS Press, St. Paul, MN, pp. 154–162. Vetten, H.J., Allen, D.J., 1983. Effects of environment and host on vector biology and incidence of two whitefly-spread diseases of legumes in Nigeria. Ann. Appl. Biol. 102, 219–227. Vos, P., Simons, G., Jesse, T., Wijbrandi, J., Heinen, L., et al., 1998. The tomato Mi-1 gene confers resistance to both root-knot nematodes and potato aphids. Nat. Biotechnol. 16, 1365–1369. Walkey, D.G.A., 1968. The production of virus-free rhubarb by apical tipculture. J. Hortic. Sci. 43, 283–287. Walkey, D.G.A., 1985. Applied Plant Virology. Heinemann, London. Walkey, D.G.A., 1991. Applied Plant Virology, second ed. Chapman & Hall, London.

875

Walkey, D.G.A., Antill, D.N., 1989. Agronomic evaluation of virusfree and virus-infected garlic (Allium sativum L). J. Hortic. Sci. 64, 53–60. Walkey, D.G.A., Cooper, J., 1976. Heat inactivation of cucumber mosaic virus in cultured tissues of Stellaria media. Ann. Appl. Biol. 84, 425–428. Walkey, D.G.A., Dance, M.C., 1979. The effect of oil sprays on aphid transmission of turnip mosaic, beet yellows, bean common mosaic and bean yellow mosaic viruses. Plant Dis. Rep. 63, 877–881. Walkey, D.G.A., Freeman, G.H., 1977. Inactivation of cucumber mosaic virus in cultured tissues of Nicotiana rustica by diurnal alternating periods of high and low temperature. Ann. Appl. Biol. 87, 375–382. Walkey, D.G.A., Webb, M.J.W., Bolland, C.J., Miller, A., 1987. Production of virus-free garlic (Allium sativum L.) and shallot (Allium ascalonicum L.) by meristem tip culture. J. Hortic. Sci. 62, 211–220. Walkey, D.G.A., Lecoq, H., Collier, R., Dobson, S., 1992. Studies on the control of zucchini yellow mosaic virus in courgettes by mild strain protection. Plant Pathol. 41, 762–771. Wallin, J.R., Loonan, D.V., 1971. Low-level jet winds, aphid vectors, local weather and barley yellow dwarf virus outbreaks. Phytopathology 61, 1068–1070. Walsh, J.A., 1998. Chemical control of fungal vectors of plant viruses. In: Hadidi, A., Khetarpal, R.K., Koganezawa, H. (Eds.), Plant Virus Disease Control APS Press, St. Paul, MN, pp. 196–207. Walsh, J.A., Tomlinson, J.A., 1985. Viruses infecting winter oilseed rape (Brassica napus ssp. oleifera). Ann. Appl. Biol. 107, 485–495. Wang, A., Krishnaswamy, S., 2012. Eukaryotic translation initiation factor 4E-mediated recessive resistance to plant viruses and its utility in crop improvement. Mol. Plant Pathol. 13, 795–803. Wang, P.G., Tumer, N.E., 2000. Virus resistance mediated by ribosome inactivating proteins. Adv. Virus Res. 55, 325–355. Wang, Q., Valkonen, J.P.T., 2009. Cryotherapy of shoot tips: novel pathogen eradication method. Trends Plant Sci. 14, 119–122. Wang, Q., Cuellar, W.J., Rajamäki, M.-L., Hirata, Y., Valkonen, J.P.T., 2008. Combined thermotherapy and cryotherapy for efficient virus eradication: relation of virus distribution, subcellular changes, cell survival and viral RNA degradation in shoot tips. Mol. Plant Pathol. 9, 237–250. Wang, R.Y., Pirone, T.P., 1996. Mineral oil interferes with retention of tobacco etch potyvirus in the stylets of Myzus persicae. Phytopathology 86, 820–823. Wang, Y.B., Li, H.C., Si, Y., Zhang, H., Guo, H.M., et  al., 2012. Microarray analysis of broad-spectrum resistance derived from an indica cultivar Rathu Heenati. Planta 235, 829–840. Waterworth, H.E., 1998. Certification for plant viruses: an overview. Breeding for resistance to plant viruses. In: Hadidi, A., Khetarpal, R.K., Koganezawa, H. (Eds.), Plant Virus Disease Control APS Press, St. Paul, MN, pp. 325–331. Watson, M.A., Heathcote, G.D., Lauckner, F.B., Sowray, P.A., 1975. The use of weather data and counts of aphids in the field to predict the incidence of yellowing viruses of sugar-beet crops in England in relation to the use of insecticides. Ann. Appl. Biol. 81, 181–198. Watts, L.E., 1975. The response of various breeding lines of lettuce to beet western yellows virus. Ann. Appl. Biol. 81, 393–397. Webley, D.P., Stone, L.E.W., 1972. Field experiments on potato aphids and virus spread in south Wales 1966/9. Ann. Appl. Biol. 72, 197–203.

876

Werker, A.R., Dewar, A.M., Harrington, R., 1998. Modelling the incidence of virus yellows in sugar beet in the UK in relation to the numbers of migrating Myzus persicae. J. Appl. Ecol. 35, 811–818. Westwood, J.H., Stevens, M., 2010. Resistance to aphid vectors of virus disease. Adv. Virus Res. 76, 179–210. Wetter, C., 1975. Tabakmosaikvirus und Para-Tabakmosaikvirus in Zigaretten. Naturwissenshaften 62, 533. Wetter, C., Bernard, M., 1977. Identifizierung, Reinigung und serologischer Nachweis von Tabakmosaikvirus und Par-Tabakmosaikvirus aus Zigaretten. Phytopathol. Z 90, 257–267. Whalen, M.C., Stall, R.E., Staskawicz, B.J., 1988. Characterisation of a gene from a tomato pathogen determining hypersensitive resistance in non-host species and genetic analysis of this resistance in bean. Proc. Natl. Acad. Sci. USA 85, 6743–6747. White, J.L., 1982. Regeneration of virus-free plants from yellowgreen areas and TMV-induced enations of Nicotiana tomentosa. Phytopathology 72, 866–867. White, R.F., Antoniw, J.F., 1983. Direct control of virus diseases. Crop Prot. 2, 259–271. Wohlers, P., 1981. Effects of (E)-beta-farnesene on dispersal behavior of the pea aphid Acyrthosiphon pisum. Entomol. Exp. Appl. 29, 117–124. Wood, G.A., 1983. Problems associated with the introduction of virusand mycoplasma-free apple trees to New Zealand orchards. Acta Hortic. 130, 257–262. Wood, G.A., Hall, H.K., 2001. Source of Raspberry bushy dwarf virus in Rubus in New Zealand, and the infectibility of some newer cultivars to this virus. N. Z. J Crop Hort. Sci. 29, 177–186. Wu, G., Kang, L., Tien, P., 1989. The effect of satellite RNA on crossprotection among cucumber mosaic virus strains. Ann. Appl. Biol. 114, 489–496. Wu, R.Y., Su, H.J., 1991. Regeneration of healthy banana plantlets from banana bunchy top-infected tissues cultures at high temperature. Plant Pathol. 40, 4–7. Wutscher, H.K., Shull, A.V., 1975. Machine-hedging of citrus trees and transmission of exocortis and xyloporosis viruses. Plant Dis. Rep. 59, 368–369. Wyatt, S.D., Seybert, L.J., Mink, G., 1988. Status of the barley yellow dwarf problem of winter wheat in eastern Washington. Plant Dis. 72, 110–113.

Plant Virology

Xu, P., Chen, F., Mannas, J.P., Feldman, T., Sumner, L.W., et  al., 2008. Virus infection improves drought tolerance. New Phytol. 180, 911–921. Yassin, A.M., 1983. A review of factors influencing control strategies against tomato leafcurl virus disease in The Sudan. Trop. Pest Manag. 29, 253–256. Yeh, S.-D., Gonsalves, D., Wang, H.-L., Namba, R., Chiu, R.-J., 1988. Control of papaya ringspot virus by cross protection. Plant Dis. 72, 375–380. Yencho, G.C., Cohen, M.B., Byrne, P.F., 2000. Applications of tagging and mapping insect resistance loci in plants. Annu. Rev. Entomol. 45, 393–422. Yi-Li, R., Wen-Li, C., Rui-Fen, L., 1981. Studies on the rice virus vector small brown planthopper Laodelphax striatella Fallen. Acta Entomol. Sin. 24, 290. Yu, X.-Q., Jia, J.-L., Zhang, C.-L., Li, X.-D., Wang, Y.-J., 2010. Phylogenetic analyses of an isolate from potato in 1985 revealing potato virus X was introduced to China via multiple events. Virus Genes 40, 447–451. Zasada, I.A., Halbrendt, J.M., Kokalis-Burelle, N., LaMondia, J., McKenry, M.V., et  al., 2010. Managing nematodes without methyl bromide. Annu. Rev. Phytopathol. 48, 311–328. Zaumeyer, W.J., Meiners, J.P., 1975. Disease resistance in beans. Annu. Rev. Phytopathol. 13, 313–334. Zettler, F.W., Hartman, R.D., 1987. Dasheen mosaic virus as a pathogen of cultivated aroids and control of the virus by tissue culture. Plant Dis. 71, 958–963. Zeyen, R.J., Stromberg, E.L., Kuehnast, E.L., 1987. Long range aphid transport hypothesis for maize dwarf mosaic virus: history and distribution in Minnesota, USA. Ann. Appl. Biol. 111, 325–336. Zhang, X.-S., Holt, J., Colvin, J., 2001. Synergism between plant viruses: a mathematical analysis of the epidemiological implications. Plant Pathol. 50, 732–746. Zhang, Z., Lin, Z., Xin, Z., 2009. Research progress in BYDV resistance genes derived from wheat and its wild relatives. J. Genet. Genom. 36, 567–573. Zink, F.W., Grogan, R.G., Welch, J.E., 1956. The effect of percentage of seed transmission upon subsequent spread of lettuce mosaic virus. Phytopathology 46, 622–624.