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Epidemiology of Fusarium head blight on small-grain cereals
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International Journal of Food Microbiology 119 (2007) 103 – 108 www.elsevier.com/locate/ijfoodmicro
Epidemiology of Fusarium head blight on small-grain cereals Lawrence E. Osborne ⁎, Jeffrey M. Stein 1 South Dakota State University, Plant Science Department 117 Plant Science Bldg, Brookings, SD 57007, USA
Abstract Fusarium head blight (FHB) is one of the most serious diseases affecting wheat and barley worldwide. It is caused by Fusarium graminearum along with F. culmorum, F. avenaceum and other related fungi. These fungi also produce several mycotoxins. Though the disease results in reduced seed quality and yield, the toxins which may accompany the disease are often a more serious problem. Pathogen inoculum is usually very abundant, however production and dispersal of inoculum are weather-sensitive processes. An abundance of colonized substrate (i.e. maize or cereal debris) in a region contributes to airborne inoculum throughout the area. Local residues beneath the cereal crop (i.e. from previous crop) may have a less obvious effect, particularly in regions where long-distance dispersal is likely due to wind conditions. The host is most susceptible to infection at anthesis and shortly thereafter. A warm, moist environment characterized by frequent precipitation or heavy dew is highly favorable to fungal growth, infection and development of disease in head tissues. As the fungus grows, it produces mycotoxins which are water-soluble and may be translocated between tissues or leeched from source tissues. Important epidemiological issues have arisen recently and include an apparent shift in prevalence of Fusarium species on infected heads in Europe toward F. graminearum; and the presence of multiple chemotypes and aggressiveness variants within a species in a region. © 2007 Elsevier B.V. All rights reserved. Keywords: Fusarium head blight; DON; Mycotoxins; Epidemiology; Wheat; Barley
1. Introduction Fusarium head blight (FHB), also called ear blight or scab, is a major fungal disease affecting several gramineous hosts including wheat (Triticum aestivum L.) and barley (Hordeum vulgare L.). The disease occurs throughout much of the world and is associated with several Fusarium spp. including Fusarium graminearum Schwabe (teleomorph: Gibberella zeae (Schwein.) Petch) and F. culmorum (W.G. Smith) Sacc., as well as F. poae (Peck) Wollenw., F. avenaceum (Fr.) Sacc., F. sporotrichoides Scherb., and Microdochium nivale (Fr.) Samuels & I.C. Hallett. While F. graminearum is often the prevalent species in many of the affected regions, the others can be highly pathogenic or are frequently found in association with the disease. These fungi are capable of producing a number of trichothecene mycotoxins including deoxynivalenol (DON) and nivalenol (NIV), as well as zearalenone (ZEA) and monilifor⁎ Corresponding author. Tel.: +1 605 688 5158; fax: +1 605 688 4024. E-mail addresses: [email protected] (L.E. Osborne), [email protected] (J.M. Stein). 1 Tel.: +1 605 688 5540; fax: +1 605 688 4024. 0168-1605/$ - see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.ijfoodmicro.2007.07.032
min (MON), all of which have a range of toxicity to animals (Desjardin, 2006; Leslie and Summerell, 2006; Rotter et al., 1996). Fusarium head blight of wheat appears as blighted head and peduncle tissues which turn brown or tan and senesce prematurely. Symptoms often are accompanied by evidence of the fungus, which may include purple-black perithecia and/or pink sporodochia on heads, especially on glumes. Seed from FHB-affected fields often is shrunken, or shriveled with a characteristically bleached appearance (Andersen, 1948; Goswami and Kistler, 2004; McMullen et al., 1997; Parry et al., 1995). The disease results in direct economic losses including reduced grain yield and quality (aborted or shriveled seed, reduced seed size), and indirect loss due to contamination by mycotoxins leading to rejection or downgrading of grain at marketing (Parry et al., 1995; Snijders, 1990; Sutton, 1982). Additional outcomes have included socially destabilizing economic impacts within FHB-affected regions (McMullen et al., 1997; Nganje et al., 2004; Windels, 2000). Epidemics of FHB (like those of many other disease systems) are strongly influenced by local and regional environment, host factors such as physiological state and
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genetic make-up, and pathogen factors including adaptation and virulence. The objective of this review is to outline the current state of knowledge for FHB and highlight a number of epidemiological issues. A further objective is to discuss some of the pressing issues that have emerged more recently or that have proven especially difficult to deal with experimentally. 2. The pathogen 2.1. Inoculum sources The causal agents of FHB survive and over-winter on or within plant tissue residues including small grain stems and roots as well as maize (Zea mays L.) stalks and ear pieces. The fungi are present and survive in colonized crop residues as mycelium, and may develop saprophytically on residues during the fall, winter, and spring (Sutton, 1982). Pathogen survival is enhanced within reduced tillage systems while tillage (residue burial) speeds decomposition and reduces pathogen reproduction and survival (Khonga and Sutton, 1988; Pereyra et al., 2004). During the early growing season (late May and early June in the Northern Great Plains of the U.S.) F. graminearum produces perithecia in which ascospores are formed (Khonga and Sutton, 1988). All of the associated fungi may produce abundant mycelium as well as conidia, and some of the species produce chlamydospores on and within the crop debris. Among the crop residues, maize stem nodes and grains as well as cereal grains are generally the most prolific sources of inoculum propagules (Gilbert and Fernando, 2004; Guenther and Trail, 2005; Khonga and Sutton, 1988). Inoculum propagules for FHB include both ascospores and conidia and are likely to be found at nearly any time during the adult stages of the cereal crop in the region when the environment falls within the wide range of favorable conditions (Beyer et al., 2005; Brennan et al., 2005; Doohan et al., 2003; Trail et al., 2002; Tshanz et al., 1976). 2.2. Pathogen population and toxicology The pathogen population in the FHB system has been the subject of several recent research papers and reviews (Bottalico and Perrone, 2002; Doohan et al., 2003; Gale, 2003; Goswami and Kistler, 2004; Logrieco et al., 2002; Miedaner et al., 2001; Munkvold, 2003; O'Donnell et al., 2000, 2004; Parry et al., 1995; Xu et al., 2005). In brief, F. graminearum is the predominant FHB pathogen in much of the world, especially in the temperate and warmer regions of the U.S., China, and the southern hemisphere. It can be highly aggressive and often produces abundant mycotoxins, especially DON. Individual strains or populations may characteristically produce acetylated derivatives of DON (3-AcDON, 15-AcDON) or NIV as well as ZEA in association with the disease. The genetic variation within the species is very high and influences aggressiveness, toxin spectrum and abundances, host interaction, sexual and asexual reproduction, and environmental response (Desjardin, 2006). Fusarium culmorum is more frequently found in the cooler regions of the world such as the U.K., Northern Europe
and Canada and is also associated with DON, ZEA, and/or NIV (Desjardin, 2006). A number of other species are frequently reported in association with FHB of wheat and barley, primarily in Europe, including F. poae, F. avenaceum, F. sporotrichoides, and M. nivale. Of the species found in association with FHB of small grains, only F. graminearum and F. culmorum are thought to be highly pathogenic (Brennan et al., 2003; Stack and McMullen, 1985). The other species mentioned are less aggressive on wheat and barley in that they may infect but do not proliferate, or may grow in a superficial or saprophytic manner. The less aggressive or less pathogenic species may still be quite economically important as their development alone, or in conjunction with the stronger pathogens can lead to mycotoxins in grain, even in the absence of major symptom development (Salas et al., 1999). Species such as F. poae also may aid in disease development through early colonization of hosts, prior to F. culmorum or F. graminearum (Sturz and Johnston, 1983). In addition to fungi associated with small grains, the Fusarium population on other crops may impact the epidemiology of FHB. Maize is host to a number of species including F. graminearum, F. culmorum, F. avenaceum, F. poae, F. verticilliodes (Sacc.) Nirenberg (syn. F. moniliforme), F. sporotrichoides and others as ear rots, stalk rots, or as superficial or saprophytic fungi. Many of these species are the same as those infecting wheat and barley, and most are toxigenic. The spores of these fungi are produced on maize debris, and also on ears and other above ground plant parts during the growing season. From those sites, the inoculum can be dispersed to a suitable host or substrate where it may lead to disease, or mycotoxin production, or both. Regions of the world with abundant maize debris, such as the Northern Great Plains of the U.S. are perhaps at greater risk from species such as F. graminearum which thrives on maize and maize residues. It has been suggested that distinct populations of F. graminearum ‘chemotypes’ are establishing themselves in the U.S., indicating the introduction and movement of unique genetic populations (Gale, 2003). Also, for parts of Europe, it has been suggested that F. graminearum is displacing other species such as F. culmorum (Xu et al., 2005), presumably due in part to shortterm climate variation and ecological differences among the fungi, but also perhaps due to differences in aggressiveness and pathogenicity of the various species. 2.3. Pathogen dispersal In the case of FHB caused by F. graminearum, ascospores were once considered to be the primary inoculum propagules arising from residues (Andersen, 1948; Bai and Shaner, 1994; Parry et al., 1995; Sutton, 1982). However, conidia may also be formed in the field on debris colonized by F. graminearum. Of course, conidia are the primary infective particle for species with mainly (or exclusively) asexual development. Previous crop and the amount of crop residue on the soil surface are considered to be major factors in local inoculum levels (Dill Macky and Jones, 2000; Teich and Hamilton, 1985), however long-distance spore dispersal has also been reported (Maldonado-Ramirez et al.,
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2005). Ascospore dispersal is thought to be by air movement, because ascospores are ejected forcibly from perithecia into the air. The ejection distance, however, is very small — up to a few mm (Trail et al., 2005). Dispersal of conidial inoculum is reported to be caused by rain-splash (Horberg, 2002; Paul et al., 2004), a common mechanism for conidiogenous fungi. Wind and insects also are dispersal mechanisms (Parry et al., 1995; Schmale et al., 2005; Sutton, 1982). Ascospores and conidia may retain viability for several days on leaves under field conditions (Jin et al., 2001). The presence of airborne ascospores of F. graminearum is associated with precipitation and other periods of very high relative humidity (RH) in some studies (Horberg, 2002; Paulitz, 1996), but not others (Francl et al., 1999; Thomas et al., 1999). There may be a threshold (N 80% RH) below which ascospore release does not occur (Gilbert and Tekauz, 2000). Recent research suggests that for South Dakota, ascospores and conidia of F. graminearum are more ubiquitous in the air than previously thought (Osborne, 2006). The two spore types were abundant in the air for prolonged periods (up to several days), and may be related to regularity of wind speed and direction (Osborne, unpublished). It is likely that, for the Northern Great Plains region, where maize fields and residue are highly abundant, and no-till cropping systems are common, large quantities of inoculum may be blown from colonies near the soil (on residue), from leaves of maize or cereal plants, or from infected small grain spikes. The wind in this region often is very strong and may blow strongly for days at a time, and is rarely calm. Data from South Dakota indicates that conidial and ascospore inoculum accumulate on both the uppermost and lowermost leaves of the canopy, suggesting that inoculum deposition occurs from above and below (Osborne et al., 2002). Shah et al., (Shah and Bergstrom, 2001; Shah et al., 2000)
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studied spatial patterns of incidence and concluded that they were random with respect to the inoculum on residue beneath the canopy, supporting the hypothesis of external airborne inoculum. Rain-splash dispersal may not be as important as wind in the Northern Great Plains, but is important for dispersal of FHB inoculum in regions with less turbulence or air-mass movement. Rain-splash is hypothesized to enable conidial inoculum to move up leaf-to-leaf and eventually to susceptible spikes (Horberg, 2002; Jenkinson and Parry, 1994; Paul et al., 2004). Whether propagules become airborne due to wind, or due to rain-splash, environmental conditions play a critical role in the production of spores, as well as their dispersal. 3. Climate and ecology Each fungus in the FHB disease system has somewhat different biological and environmental requirements (Table 1) which can, in part, explain why the frequencies of these species varies by location. For example, F. graminearum grows well over a wide range of temperatures up to 30 °C and is associated with the warmer regions of the world, whereas F. poae, which is a more efficient pathogen at lower temperatures (i.e. 20 °C) is found more frequently in temperate climates. Most of the species can be found in much of the geographical area affected by FHB, but individual species usually dominate a specific region and F. graminearum dominates in a majority of regions. Table 1 lists a number of fungal development processes and some of the optimum environmental parameters for each species. To summarize, F. graminearum reproduces over a very wide range of temperatures and moisture conditions. Relative to other species, F. graminearum is favored in warmer, wetter conditions, in terms of conidial production and infection rates. However,
Table 1 Environmental factors affecting fungal development Pathogen species F. graminearum
Source F. culmorum
F. poae
F. avenaceum
M. nivale
20 °C (10–30 °C)
20 °C (10–30 °C)
Brennan et al. (2003)
26 °C
(Xu, 2003; Sung and Cook, 1981) Sung and Cook (1981)
18 °C; 72 h (10–35 °C, 8–72 h)
Rossi et al. (2001)
Reported optimum temperature or moisture (tested range) Mycelial growth Sporulation (conidia) Conidia germination Infection frequency by conidia Perithecial maturation Ascospore release Ascospore germination Infection by ascospores Wheat seedling inhibition
25 °C (10–30 °C)
20–25 °C (10–30 °C)
32 °C; − 0.14 MPa
32 °C; − 1.5 MPa
28 °C; − 1.5 MPa
100% 0 to − 6.0 MPa (delay when drier) 29 °C; N48 h incr. with time (10–35 °C, 8–72 h) 20–24 °C; − 0.45 MPa inhib. when wetter 16 °C
100% 0 to −6.0 MPa (delay when drier) 26.5 °C; 72 h (10–35 °C, 8–72 h)
100% 0 to − 6.0 MPa (delay when drier) 29 °C; 72 h 25 °C; 24–48 h (10–35 °C, 8–72 h)
–
20–25 °C (10–30 °C)
–
–
–
(Dufault et al., 2006; Sung and Cook, 1981) Sutton (1982)
4 h; at − 2.0 MPa 24 h at − 6.0 MPa (0 to − 8.0 MPa) Increases in rate to 35 °C
–
–
–
–
Lu et al. (2001)
25 °C (10–30 °C)
25 °C (10–30 °C)
20 °C (10–30 °C)
25 °C (10–30 °C)
15 °C (10–30 °C)
Brennan et al. (2003)
Sung and Cook (1981)
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cooler conditions favor perithecial development (Dufault et al., 2006) and ascospore release, with the latter being inhibited by prolonged high humidity (Sung and Cook, 1981). Infection by F. graminearum also occurs across a broader range of temperatures than for the other species, and infection may occur more rapidly as well (Rossi et al., 2001). Taken together, these reports suggest that F. graminearum is more broadly adapted to environmental variability than the other species, which is consistent with the dominance of F. graminearum in the FHB system. In addition to the environmental influence on pathogen populations, niche availability also is a major factor in pathogen abundance. In the U.S., particularly in the Great Plains, cereal production generally accompanies row crop production of maize and soybeans. These crops often are rotated in a field over successive seasons and zero tillage and reduced tillage systems have become more popular. South Dakota is among the leaders in the U.S. in adoption of zero tillage, increasing from ∼120,000 hectares in the mid-1980's to N 2,000,000 hectares in 2004 (USDANRCS, 2005). Pereyra et al. (Pereyra et al., 2004) showed that these residues can harbor perithecia and produce ascospores even after two years on the soil surface. The increased production of maize and the dramatic increase in maize and other residues that remain on the soil surface provide a large increase in the niche available to fungi such as F. graminearum. Maize and small grains are good hosts for Fusarium spp., especially F. graminearum, and the colonization of these hosts in their senescent stages leads to a large reservoir of fungal biomass capable of producing ascospores and conidia from the surface residues. 4. Host factors The abundance of fungal niches both during and after the growing season coupled with a broadly (environmentally) adapted group of pathogenic species makes the FHB disease system difficult to manage and to predict. However, the role of the host as a component of the disease system cannot be overlooked. Host factors of importance include genetic resistance to the pathogen and also physiological condition of the host as influenced by nutrition, hydration, and age. The host response to infection and disease development varies widely. Genetic resistance to FHB is generally expressed as a quantitative trait, presumably due to many minor genes and few major ones conferring the resistance and as such, there is wide variation in phenotypic reaction and environmental response. Resistance is often described with a classification system based on observable characters, e.g. visible symptoms, or other quantifiable disease reaction (such as DON concentration). Schroeder and Christensen (1963), described two phenotypic measures of disease resistance, commonly referred to as Type I (resistance to initial infection) and Type II (resistance to spreading within affected tissues). Mesterhazy (2003) reviewed these and several other mechanisms including resistance to toxins (termed Type V). In most types of wheat and barley, genetic resistance to FHB has been identified in germplasm stocks. In bread wheat, the most common source of resistance in commercial lines is probably ‘Sumai-3’, which provides quantitative Type II resistance. In barley, resistance is
less well developed in commercial lines, and it may take 5 to 10 years for improved resistance to appear in production fields (Legge et al., 2004). Wheat is generally considered to be most susceptible at or near anthesis (growth stage 10.51 on the Feekes scale (Large, 1954), when anthers are mature and beginning to senesce. The anthers are thought to provide nutrients and possibly stimulate fungal growth through other mechanisms. For example, maize pollen stimulates germination of F. graminearum and increases foliar infection of maize (Naik and Busch, 1978), suggesting that wheat pollen might similarly stimulate fungal germination and infection. Fungal spores may come into contact with wheat or barley heads at any time after head emergence, and under proper environments will germinate. Inoculation prior to flowering may result in reduced disease compared to inoculation after flowering, up to the early milk-stage of kernel development (Bergstrom et al., pers. comm.). Pre-heading inoculation may be important in barley as the crop usually flowers while still in the boot stage and would be highly susceptible even before heads are exposed (McCallum and Tekauz, 2002). We have observed barley heads which emerged from the boot stage fully infected and colonized with the fungus. This observation suggests that infection occurred either through the apparently healthy boot sheath, or that spores were washed into the boot sheath prior to head emergence. If inoculum contacts host tissues late in the development of the grain, infection and major visual symptoms may not develop to the same extent as with early anthesis infections; however the effects on toxin production and concentration in the grain are not well understood. F. graminearum can superficially colonize head and leaf tissues and sporulate abundantly in a favorable high-humidity environment (S. Ali, pers. comm., 2003; Osborne and Jin, unpublished data, 2002). The impact that superficial or quasi-pathogenic fungal development has on disease or grain yield and quality is also not well understood. 5. Non-pathogenic fungal development Because of the impact that mycotoxins have on small grain quality, it is important to remember that there is some risk to the crop even in the absence of major symptom development. Many of the fungi mentioned are weak pathogens on wheat spikes or are poorly pathogenic during certain developmental stages of the host. Yet all of these fungi can survive as saprophytes and some may colonize tissues without parasitizing them (Ali and Francl, 2001). Grain in storage is also susceptible to fungal colonization and continued contamination by fungal metabolites. Therefore, even in the absence of visually detectable symptoms on a crop, it is possible to find mycotoxins at harvest, and that fungi may continue to grow and produce additional mycotoxins if grain is improperly stored. 6. Conclusions Most scientists agree that management of FHB will require an integrated approach (Krupinsky et al., 2002). Components of integrated management could include cultural practices to avoid
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Paul, P.A., El-Allaf, S.M., Lipps, P.E., Madden, L.V., 2004. Rain splash dispersal of Gibberella zeae within wheat canopies in Ohio. Phytopathology 94, 1342–1349. Paulitz, T.C., 1996. Diurnal release of ascospores by Gibberella zeae in inoculated wheat plots. Plant Disease 80, 674–678. Pereyra, S.A., Dill Macky, R., Sims, A.L., 2004. Survival and inoculum production of Gibberella zeae in wheat residue. Plant Disease 88, 724–730. Rossi, V., Ravanetti, A., Pattori, E., Giosue, S., 2001. Influence of temperature and humidity on the infection of wheat spikes by some fungi causing Fusarium head blight. Journal of Plant Pathology 83, 189–198. Rotter, B.A., Prelusky, D.B., Pestka, J.J., 1996. Toxicology of deoxynivalenol (vomitoxin). Journal of Toxicology and Environmental Health 48, 1–34. Salas, B., Steffenson, B.J., Casper, H.H., Tacke, B., Prom, L.K., Fetch Jr., T.G, Swhwarz, P.B., 1999. Fusarium species pathogenic to barley and their associated mycotoxins. Plant Disease 83, 667–674. Schmale III, D.G., Shah, D.A., Bergstrom, G.C., 2005. Spatial patterns of viable spore deposition of Gibberella zeae in wheat fields. Phytopathology 95, 472–479. Schroeder, H.W., Christensen, J.J, 1963. Factors affecting resistance of wheat to scab caused by Gibberella zeae. Phytopathology 53, :831. Shah, D.A., Bergstrom, G.C., 2001. Spatial patterns of Fusarium head blight in New York wheat fields in 2000 and 2001. Proc. 2000 National Fusarium Head Blight Forum. Michigan State Univ., Erlanger, KY. Shah, D.A., Stockwell, C.A., Kawamoto, S.O., Bergstrom, G.C., 2000. Spatial patterns of Fusarium head blight in New York wheat fields during the epidemic of 2000. Proc. 2000 National Fusarium Head Blight Forum. Michigan State Univ., Erlanger, KY. Snijders, C.H.A., 1990. Fusarium head blight and mycotoxin contamination of wheat, a review. Netherlands Journal of Plant Pathology 96, 187–198. Stack, R.W, McMullen, M.P., 1985. Head blighting potential of Fusarium species associated with spring wheat heads. Canadian Journal of Plant Pathology 7, 79–82. Sturz, A.V., Johnston, H.W., 1983. Early colonization of the ears of wheat and barley by Fusarium poae. Canadian Journal of Plant Pathology 5, 107–110.
Sutton, J.C., 1982. Epidemiology of wheat head blight and maize ear rot caused by Fusarium graminearum. Canadian Journal of Plant Pathology 4, 195. Sung, J.-M., Cook, R.G., 1981. Effect of water potential on reproduction and spore germination by Fusarium roseum ‘Graminearum’, ‘Culmorum’, and ‘Avenaceum’. Phytopathology 71, 499–504. Teich, A.H., Hamilton, J.R., 1985. Effect of cultural practices, soil phosphorus, potassium, and pH on the incidence of fusarium head blight and deoxynivalenol levels in wheat. Applied and Environmental Microbiol 49, 1429–1431. Thomas, D., Buechley, G., Shaner, G., 1999. Epidemiology of Fusarium head blight of wheat in Indiana. Proc. 1999 National Fusarium Head Blight Forum. Michigan State Univ., Sioux Falls, SD. Trail, F., Xu, H., Loranger, R., Gadoury, D., 2002. Physiological and environmental aspects of ascospore discharge in Gibberella zeae (anamorph Fusarium graminearum). Mycologia 94, 181. Trail, F., Gaffoor, I., Vogel, S., 2005. Ejection mechanics and trajectory of the ascospores of Gibberella zeae (anamorph Fusarium graminearum). Fungal Genetics and Biology 42, 528–533. Tshanz, A.T., Horst, R.K., Nelson, P.E., 1976. The effect of environment on sexual reproduction of Gibberella zeae. Mycologia 68, 327–340. USDA-NRCS, 2005. Acres under no-till farming on all planted cropland acres in South Dakota. ftp://ftp-fc.sc.egov.usda.gov/SD/www/News/2005% 2520Releases/2_11_05_SDNo-TillAcresTREND.jpg. Last accessed May 3, 2007. Windels, C.E., 2000. Economic and social impacts of Fusarium head blight: changing farms and rural communities in the Northern Great Plains. Phytopathology 90, 17–21. Xu, X., 2003. Effects of environmental conditions on the development of Fusarium ear blight. European Journal of Plant Pathology 109, 683–689. Xu, X.M., Parry, D.W., Nicholson, P., Thomsett, M.A., Simpson, D., Edwards, S.G., Cooke, B.M., Doohan, F.M., Brennan, J.M., Moretti, A., Tocco, G., Mule, G., Hornok, L., Giczey, G., Tatnell, J., 2005. Predominance and association of pathogenic fungi causing Fusarium ear blight in wheat in four European countries. European Journal of Plant Pathology 112, 143–154.
International Journal of Food Microbiology 119 (2007) 103 – 108 www.elsevier.com/locate/ijfoodmicro
Epidemiology of Fusarium head blight on small-grain cereals Lawrence E. Osborne ⁎, Jeffrey M. Stein 1 South Dakota State University, Plant Science Department 117 Plant Science Bldg, Brookings, SD 57007, USA
Abstract Fusarium head blight (FHB) is one of the most serious diseases affecting wheat and barley worldwide. It is caused by Fusarium graminearum along with F. culmorum, F. avenaceum and other related fungi. These fungi also produce several mycotoxins. Though the disease results in reduced seed quality and yield, the toxins which may accompany the disease are often a more serious problem. Pathogen inoculum is usually very abundant, however production and dispersal of inoculum are weather-sensitive processes. An abundance of colonized substrate (i.e. maize or cereal debris) in a region contributes to airborne inoculum throughout the area. Local residues beneath the cereal crop (i.e. from previous crop) may have a less obvious effect, particularly in regions where long-distance dispersal is likely due to wind conditions. The host is most susceptible to infection at anthesis and shortly thereafter. A warm, moist environment characterized by frequent precipitation or heavy dew is highly favorable to fungal growth, infection and development of disease in head tissues. As the fungus grows, it produces mycotoxins which are water-soluble and may be translocated between tissues or leeched from source tissues. Important epidemiological issues have arisen recently and include an apparent shift in prevalence of Fusarium species on infected heads in Europe toward F. graminearum; and the presence of multiple chemotypes and aggressiveness variants within a species in a region. © 2007 Elsevier B.V. All rights reserved. Keywords: Fusarium head blight; DON; Mycotoxins; Epidemiology; Wheat; Barley
1. Introduction Fusarium head blight (FHB), also called ear blight or scab, is a major fungal disease affecting several gramineous hosts including wheat (Triticum aestivum L.) and barley (Hordeum vulgare L.). The disease occurs throughout much of the world and is associated with several Fusarium spp. including Fusarium graminearum Schwabe (teleomorph: Gibberella zeae (Schwein.) Petch) and F. culmorum (W.G. Smith) Sacc., as well as F. poae (Peck) Wollenw., F. avenaceum (Fr.) Sacc., F. sporotrichoides Scherb., and Microdochium nivale (Fr.) Samuels & I.C. Hallett. While F. graminearum is often the prevalent species in many of the affected regions, the others can be highly pathogenic or are frequently found in association with the disease. These fungi are capable of producing a number of trichothecene mycotoxins including deoxynivalenol (DON) and nivalenol (NIV), as well as zearalenone (ZEA) and monilifor⁎ Corresponding author. Tel.: +1 605 688 5158; fax: +1 605 688 4024. E-mail addresses: [email protected] (L.E. Osborne), [email protected] (J.M. Stein). 1 Tel.: +1 605 688 5540; fax: +1 605 688 4024. 0168-1605/$ - see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.ijfoodmicro.2007.07.032
min (MON), all of which have a range of toxicity to animals (Desjardin, 2006; Leslie and Summerell, 2006; Rotter et al., 1996). Fusarium head blight of wheat appears as blighted head and peduncle tissues which turn brown or tan and senesce prematurely. Symptoms often are accompanied by evidence of the fungus, which may include purple-black perithecia and/or pink sporodochia on heads, especially on glumes. Seed from FHB-affected fields often is shrunken, or shriveled with a characteristically bleached appearance (Andersen, 1948; Goswami and Kistler, 2004; McMullen et al., 1997; Parry et al., 1995). The disease results in direct economic losses including reduced grain yield and quality (aborted or shriveled seed, reduced seed size), and indirect loss due to contamination by mycotoxins leading to rejection or downgrading of grain at marketing (Parry et al., 1995; Snijders, 1990; Sutton, 1982). Additional outcomes have included socially destabilizing economic impacts within FHB-affected regions (McMullen et al., 1997; Nganje et al., 2004; Windels, 2000). Epidemics of FHB (like those of many other disease systems) are strongly influenced by local and regional environment, host factors such as physiological state and
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genetic make-up, and pathogen factors including adaptation and virulence. The objective of this review is to outline the current state of knowledge for FHB and highlight a number of epidemiological issues. A further objective is to discuss some of the pressing issues that have emerged more recently or that have proven especially difficult to deal with experimentally. 2. The pathogen 2.1. Inoculum sources The causal agents of FHB survive and over-winter on or within plant tissue residues including small grain stems and roots as well as maize (Zea mays L.) stalks and ear pieces. The fungi are present and survive in colonized crop residues as mycelium, and may develop saprophytically on residues during the fall, winter, and spring (Sutton, 1982). Pathogen survival is enhanced within reduced tillage systems while tillage (residue burial) speeds decomposition and reduces pathogen reproduction and survival (Khonga and Sutton, 1988; Pereyra et al., 2004). During the early growing season (late May and early June in the Northern Great Plains of the U.S.) F. graminearum produces perithecia in which ascospores are formed (Khonga and Sutton, 1988). All of the associated fungi may produce abundant mycelium as well as conidia, and some of the species produce chlamydospores on and within the crop debris. Among the crop residues, maize stem nodes and grains as well as cereal grains are generally the most prolific sources of inoculum propagules (Gilbert and Fernando, 2004; Guenther and Trail, 2005; Khonga and Sutton, 1988). Inoculum propagules for FHB include both ascospores and conidia and are likely to be found at nearly any time during the adult stages of the cereal crop in the region when the environment falls within the wide range of favorable conditions (Beyer et al., 2005; Brennan et al., 2005; Doohan et al., 2003; Trail et al., 2002; Tshanz et al., 1976). 2.2. Pathogen population and toxicology The pathogen population in the FHB system has been the subject of several recent research papers and reviews (Bottalico and Perrone, 2002; Doohan et al., 2003; Gale, 2003; Goswami and Kistler, 2004; Logrieco et al., 2002; Miedaner et al., 2001; Munkvold, 2003; O'Donnell et al., 2000, 2004; Parry et al., 1995; Xu et al., 2005). In brief, F. graminearum is the predominant FHB pathogen in much of the world, especially in the temperate and warmer regions of the U.S., China, and the southern hemisphere. It can be highly aggressive and often produces abundant mycotoxins, especially DON. Individual strains or populations may characteristically produce acetylated derivatives of DON (3-AcDON, 15-AcDON) or NIV as well as ZEA in association with the disease. The genetic variation within the species is very high and influences aggressiveness, toxin spectrum and abundances, host interaction, sexual and asexual reproduction, and environmental response (Desjardin, 2006). Fusarium culmorum is more frequently found in the cooler regions of the world such as the U.K., Northern Europe
and Canada and is also associated with DON, ZEA, and/or NIV (Desjardin, 2006). A number of other species are frequently reported in association with FHB of wheat and barley, primarily in Europe, including F. poae, F. avenaceum, F. sporotrichoides, and M. nivale. Of the species found in association with FHB of small grains, only F. graminearum and F. culmorum are thought to be highly pathogenic (Brennan et al., 2003; Stack and McMullen, 1985). The other species mentioned are less aggressive on wheat and barley in that they may infect but do not proliferate, or may grow in a superficial or saprophytic manner. The less aggressive or less pathogenic species may still be quite economically important as their development alone, or in conjunction with the stronger pathogens can lead to mycotoxins in grain, even in the absence of major symptom development (Salas et al., 1999). Species such as F. poae also may aid in disease development through early colonization of hosts, prior to F. culmorum or F. graminearum (Sturz and Johnston, 1983). In addition to fungi associated with small grains, the Fusarium population on other crops may impact the epidemiology of FHB. Maize is host to a number of species including F. graminearum, F. culmorum, F. avenaceum, F. poae, F. verticilliodes (Sacc.) Nirenberg (syn. F. moniliforme), F. sporotrichoides and others as ear rots, stalk rots, or as superficial or saprophytic fungi. Many of these species are the same as those infecting wheat and barley, and most are toxigenic. The spores of these fungi are produced on maize debris, and also on ears and other above ground plant parts during the growing season. From those sites, the inoculum can be dispersed to a suitable host or substrate where it may lead to disease, or mycotoxin production, or both. Regions of the world with abundant maize debris, such as the Northern Great Plains of the U.S. are perhaps at greater risk from species such as F. graminearum which thrives on maize and maize residues. It has been suggested that distinct populations of F. graminearum ‘chemotypes’ are establishing themselves in the U.S., indicating the introduction and movement of unique genetic populations (Gale, 2003). Also, for parts of Europe, it has been suggested that F. graminearum is displacing other species such as F. culmorum (Xu et al., 2005), presumably due in part to shortterm climate variation and ecological differences among the fungi, but also perhaps due to differences in aggressiveness and pathogenicity of the various species. 2.3. Pathogen dispersal In the case of FHB caused by F. graminearum, ascospores were once considered to be the primary inoculum propagules arising from residues (Andersen, 1948; Bai and Shaner, 1994; Parry et al., 1995; Sutton, 1982). However, conidia may also be formed in the field on debris colonized by F. graminearum. Of course, conidia are the primary infective particle for species with mainly (or exclusively) asexual development. Previous crop and the amount of crop residue on the soil surface are considered to be major factors in local inoculum levels (Dill Macky and Jones, 2000; Teich and Hamilton, 1985), however long-distance spore dispersal has also been reported (Maldonado-Ramirez et al.,
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2005). Ascospore dispersal is thought to be by air movement, because ascospores are ejected forcibly from perithecia into the air. The ejection distance, however, is very small — up to a few mm (Trail et al., 2005). Dispersal of conidial inoculum is reported to be caused by rain-splash (Horberg, 2002; Paul et al., 2004), a common mechanism for conidiogenous fungi. Wind and insects also are dispersal mechanisms (Parry et al., 1995; Schmale et al., 2005; Sutton, 1982). Ascospores and conidia may retain viability for several days on leaves under field conditions (Jin et al., 2001). The presence of airborne ascospores of F. graminearum is associated with precipitation and other periods of very high relative humidity (RH) in some studies (Horberg, 2002; Paulitz, 1996), but not others (Francl et al., 1999; Thomas et al., 1999). There may be a threshold (N 80% RH) below which ascospore release does not occur (Gilbert and Tekauz, 2000). Recent research suggests that for South Dakota, ascospores and conidia of F. graminearum are more ubiquitous in the air than previously thought (Osborne, 2006). The two spore types were abundant in the air for prolonged periods (up to several days), and may be related to regularity of wind speed and direction (Osborne, unpublished). It is likely that, for the Northern Great Plains region, where maize fields and residue are highly abundant, and no-till cropping systems are common, large quantities of inoculum may be blown from colonies near the soil (on residue), from leaves of maize or cereal plants, or from infected small grain spikes. The wind in this region often is very strong and may blow strongly for days at a time, and is rarely calm. Data from South Dakota indicates that conidial and ascospore inoculum accumulate on both the uppermost and lowermost leaves of the canopy, suggesting that inoculum deposition occurs from above and below (Osborne et al., 2002). Shah et al., (Shah and Bergstrom, 2001; Shah et al., 2000)
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studied spatial patterns of incidence and concluded that they were random with respect to the inoculum on residue beneath the canopy, supporting the hypothesis of external airborne inoculum. Rain-splash dispersal may not be as important as wind in the Northern Great Plains, but is important for dispersal of FHB inoculum in regions with less turbulence or air-mass movement. Rain-splash is hypothesized to enable conidial inoculum to move up leaf-to-leaf and eventually to susceptible spikes (Horberg, 2002; Jenkinson and Parry, 1994; Paul et al., 2004). Whether propagules become airborne due to wind, or due to rain-splash, environmental conditions play a critical role in the production of spores, as well as their dispersal. 3. Climate and ecology Each fungus in the FHB disease system has somewhat different biological and environmental requirements (Table 1) which can, in part, explain why the frequencies of these species varies by location. For example, F. graminearum grows well over a wide range of temperatures up to 30 °C and is associated with the warmer regions of the world, whereas F. poae, which is a more efficient pathogen at lower temperatures (i.e. 20 °C) is found more frequently in temperate climates. Most of the species can be found in much of the geographical area affected by FHB, but individual species usually dominate a specific region and F. graminearum dominates in a majority of regions. Table 1 lists a number of fungal development processes and some of the optimum environmental parameters for each species. To summarize, F. graminearum reproduces over a very wide range of temperatures and moisture conditions. Relative to other species, F. graminearum is favored in warmer, wetter conditions, in terms of conidial production and infection rates. However,
Table 1 Environmental factors affecting fungal development Pathogen species F. graminearum
Source F. culmorum
F. poae
F. avenaceum
M. nivale
20 °C (10–30 °C)
20 °C (10–30 °C)
Brennan et al. (2003)
26 °C
(Xu, 2003; Sung and Cook, 1981) Sung and Cook (1981)
18 °C; 72 h (10–35 °C, 8–72 h)
Rossi et al. (2001)
Reported optimum temperature or moisture (tested range) Mycelial growth Sporulation (conidia) Conidia germination Infection frequency by conidia Perithecial maturation Ascospore release Ascospore germination Infection by ascospores Wheat seedling inhibition
25 °C (10–30 °C)
20–25 °C (10–30 °C)
32 °C; − 0.14 MPa
32 °C; − 1.5 MPa
28 °C; − 1.5 MPa
100% 0 to − 6.0 MPa (delay when drier) 29 °C; N48 h incr. with time (10–35 °C, 8–72 h) 20–24 °C; − 0.45 MPa inhib. when wetter 16 °C
100% 0 to −6.0 MPa (delay when drier) 26.5 °C; 72 h (10–35 °C, 8–72 h)
100% 0 to − 6.0 MPa (delay when drier) 29 °C; 72 h 25 °C; 24–48 h (10–35 °C, 8–72 h)
–
20–25 °C (10–30 °C)
–
–
–
(Dufault et al., 2006; Sung and Cook, 1981) Sutton (1982)
4 h; at − 2.0 MPa 24 h at − 6.0 MPa (0 to − 8.0 MPa) Increases in rate to 35 °C
–
–
–
–
Lu et al. (2001)
25 °C (10–30 °C)
25 °C (10–30 °C)
20 °C (10–30 °C)
25 °C (10–30 °C)
15 °C (10–30 °C)
Brennan et al. (2003)
Sung and Cook (1981)
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cooler conditions favor perithecial development (Dufault et al., 2006) and ascospore release, with the latter being inhibited by prolonged high humidity (Sung and Cook, 1981). Infection by F. graminearum also occurs across a broader range of temperatures than for the other species, and infection may occur more rapidly as well (Rossi et al., 2001). Taken together, these reports suggest that F. graminearum is more broadly adapted to environmental variability than the other species, which is consistent with the dominance of F. graminearum in the FHB system. In addition to the environmental influence on pathogen populations, niche availability also is a major factor in pathogen abundance. In the U.S., particularly in the Great Plains, cereal production generally accompanies row crop production of maize and soybeans. These crops often are rotated in a field over successive seasons and zero tillage and reduced tillage systems have become more popular. South Dakota is among the leaders in the U.S. in adoption of zero tillage, increasing from ∼120,000 hectares in the mid-1980's to N 2,000,000 hectares in 2004 (USDANRCS, 2005). Pereyra et al. (Pereyra et al., 2004) showed that these residues can harbor perithecia and produce ascospores even after two years on the soil surface. The increased production of maize and the dramatic increase in maize and other residues that remain on the soil surface provide a large increase in the niche available to fungi such as F. graminearum. Maize and small grains are good hosts for Fusarium spp., especially F. graminearum, and the colonization of these hosts in their senescent stages leads to a large reservoir of fungal biomass capable of producing ascospores and conidia from the surface residues. 4. Host factors The abundance of fungal niches both during and after the growing season coupled with a broadly (environmentally) adapted group of pathogenic species makes the FHB disease system difficult to manage and to predict. However, the role of the host as a component of the disease system cannot be overlooked. Host factors of importance include genetic resistance to the pathogen and also physiological condition of the host as influenced by nutrition, hydration, and age. The host response to infection and disease development varies widely. Genetic resistance to FHB is generally expressed as a quantitative trait, presumably due to many minor genes and few major ones conferring the resistance and as such, there is wide variation in phenotypic reaction and environmental response. Resistance is often described with a classification system based on observable characters, e.g. visible symptoms, or other quantifiable disease reaction (such as DON concentration). Schroeder and Christensen (1963), described two phenotypic measures of disease resistance, commonly referred to as Type I (resistance to initial infection) and Type II (resistance to spreading within affected tissues). Mesterhazy (2003) reviewed these and several other mechanisms including resistance to toxins (termed Type V). In most types of wheat and barley, genetic resistance to FHB has been identified in germplasm stocks. In bread wheat, the most common source of resistance in commercial lines is probably ‘Sumai-3’, which provides quantitative Type II resistance. In barley, resistance is
less well developed in commercial lines, and it may take 5 to 10 years for improved resistance to appear in production fields (Legge et al., 2004). Wheat is generally considered to be most susceptible at or near anthesis (growth stage 10.51 on the Feekes scale (Large, 1954), when anthers are mature and beginning to senesce. The anthers are thought to provide nutrients and possibly stimulate fungal growth through other mechanisms. For example, maize pollen stimulates germination of F. graminearum and increases foliar infection of maize (Naik and Busch, 1978), suggesting that wheat pollen might similarly stimulate fungal germination and infection. Fungal spores may come into contact with wheat or barley heads at any time after head emergence, and under proper environments will germinate. Inoculation prior to flowering may result in reduced disease compared to inoculation after flowering, up to the early milk-stage of kernel development (Bergstrom et al., pers. comm.). Pre-heading inoculation may be important in barley as the crop usually flowers while still in the boot stage and would be highly susceptible even before heads are exposed (McCallum and Tekauz, 2002). We have observed barley heads which emerged from the boot stage fully infected and colonized with the fungus. This observation suggests that infection occurred either through the apparently healthy boot sheath, or that spores were washed into the boot sheath prior to head emergence. If inoculum contacts host tissues late in the development of the grain, infection and major visual symptoms may not develop to the same extent as with early anthesis infections; however the effects on toxin production and concentration in the grain are not well understood. F. graminearum can superficially colonize head and leaf tissues and sporulate abundantly in a favorable high-humidity environment (S. Ali, pers. comm., 2003; Osborne and Jin, unpublished data, 2002). The impact that superficial or quasi-pathogenic fungal development has on disease or grain yield and quality is also not well understood. 5. Non-pathogenic fungal development Because of the impact that mycotoxins have on small grain quality, it is important to remember that there is some risk to the crop even in the absence of major symptom development. Many of the fungi mentioned are weak pathogens on wheat spikes or are poorly pathogenic during certain developmental stages of the host. Yet all of these fungi can survive as saprophytes and some may colonize tissues without parasitizing them (Ali and Francl, 2001). Grain in storage is also susceptible to fungal colonization and continued contamination by fungal metabolites. Therefore, even in the absence of visually detectable symptoms on a crop, it is possible to find mycotoxins at harvest, and that fungi may continue to grow and produce additional mycotoxins if grain is improperly stored. 6. Conclusions Most scientists agree that management of FHB will require an integrated approach (Krupinsky et al., 2002). Components of integrated management could include cultural practices to avoid
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