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DISEASE | Replant Problems and Soil Sickness
DISEASE/Replant Problems and Soil Sickness
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Further Reading
Figure 7 Susceptibility and resistance to P. mucronatum. The compound leaf of R. corymbifera `Laxa' (left) is heavily rusted, whereas Rosa `Pascali'Õ (right) growing as a scion on the `Laxa' stock, and which has not been `headed back', is unaffected.
collecting fallen rusted leaves is unlikely to be successful. Furthermore, later in the year teliospores are also dispersed, albeit shorter distances, and stick, as stated earlier, to stems and other permanent substrates. Removal of rust-forming galls in the case of P. mucronatum and P. rosae-pimpinellifoliae, however, may help to reduce aeciospore inoculum arising from perennating systemic mycelial infection. Chemical control can be effective and a number of systemic fungicides, e.g. benodanil, oxycarboxin, penconazole, propiconazole and triforine, have given excellent control over the past couple of decades. The latter two have been available to the amateur gardener but have become outclassed or withdrawn for a variety of reasons. Myclobutanil is a readily available systemic fungicide providing protective, curative and eradicant control and, of course, is active against powdery mildew, too. Myclobutanil is an azole compound and this family of chemicals inhibits sterol biosynthesis and therefore disrupts cell membranes of target fungal pathogens. Commercial growers, in the United Kingdom at least, have a wider choice of compounds to choose from including new-generation azoles developed for the cereal market and other compounds too, such as the strobilurins which inhibit cellular respiration in pathogens. In the United Kingdom, subject to the usual restrictions, fungicides approved for use on any growing edible crop, e.g. cereal or top fruit, can be used, at present, on commercial agricultural or horticultural holdings, where no part of the plant is to be consumed by humans or animals. This applies to hardy ornamental nursery stock, and therefore includes roses. See also: Disease: Overview; Botrytis; Black Spot; Downy Mildew; Powdery Mildew. Breeding: Selection Strategies for Disease and Pest Resistance.
Henderson DM (2000) A Check List of the Rust Fungi of the British Isles. Kew, UK: British Mycological Society. Horst RK (1983) Compendium of Rose Diseases. St Paul, MN, USA: American Phytopathological Society. Laundon GF and Rainbow AK (1969a) Phragmidium tuberculatum, CMI Descriptions of Pathogenic Fungi and Bacteria no. 204. Kew, UK: Commonwealth Agricultural Bureaux. Laundon GF and Rainbow AK (1969b) Phragmidium mucronatum, CMI Descriptions of Pathogenic Fungi and Bacteria no. 205. Kew, UK: Commonwealth Agricultural Bureaux. Laundon GF and Rainbow AK (1969c) Phragmidium rosae-pimpinellifoliae, CMI Descriptions of Pathogenic Fungi and Bacteria no. 208. Kew, UK: Commonwealth Agricultural Bureaux. Losing H (1988) Bekampfung von Rosenrost. Deutsche Baumschule 40: 518ÿ519. Shattock RC and Rahbar Bhatti MH (1983) Rust on Laxa stocks. In: Harkness J (ed.) The Rose Annual 1983, pp. 150ÿ162. St Albans, UK: Royal National Rose Society.
Replant Problems and Soil Sickness W Spethmann, University of Hanover, Germany G Otto, Dresden, Germany # 2003, Elsevier Ltd. All Rights Reserved.
Introduction Declines in growth and yield have been observed in roses and several other genera when the same genus has repeatedly been planted in the same location. The degree of decline depends on the plant species, various soil factors, and pests present in the soil. To avoid such replant problems growers tend to move to a new ®eld, fumigate, or cure with hot steam (Figure 1). Crop rotation schedules, allowing planting intervals for the species in question as well as fallow periods, are recommended. The two main causes of replant problems are ®rst, nematodes and second, speci®c replant disease or soil sickness. Both factors will be discussed in this article. At the present time it is not known whether nematodes are connected directly with the speci®c replant disease. The organisms causing speci®c replant disease in roses have not yet been identi®ed, although economic losses are very high. After many years of intensive research in apples, the causal organisms associated with speci®c
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DISEASE/Replant Problems and Soil Sickness
Figure 1 Disinfected soil plots with optimum growth of Rosa corymbifera `Laxa' beside plots with depressed growth caused by soil sickness and nematodes in BoÈnningstedt (Schleswig± Holstein). (Photograph by W. Spethmann.)
replant disease were identi®ed as Actinomycetes. It is possible that these microorganisms could have a similar effect in roses as in apples; therefore the mode of action of these microorganisms in Malus are discussed in detail. Besides nematodes and speci®c replant disease, replant problems could be caused or increased by fungi, lack of mineral substances, trace elements, or soil compaction.
Characteristics and Terminology Some plant species suffer severe damage when grown repeatedly in the same ®eld. This cannot be avoided even by having a long interval before returning with the same crop, especially where species of the Rosaceae family are concerned. The terms `replant disease', `soil sickness' and `soil exhaustion' are often used to describe this problem. The problem is said to be species-speci®c (for apples, for roses, etc.). The persistence of the cause of replant disease can be observed in the soil even decades later, but other factors should also be taken into account. The phenomenon appears to be strictly limited to the ®eld in which the particular crop was grown previously, as especially noted in nurseries which changed the direction in which rows of roses or apple liners were planted. The disease occurs uniformly within entire rows of plants, not in nestlike pockets. Furthermore, it is known that replant disease is reversible. Plants from affected soil which are transplanted into virgin soil will soon recover and grow normally. Typically, replant disease occurs with varying severity in different locations. In some areas serious problems rarely occur or only after several repetitions of the same crop, whereas in other areas a single, short-term planting produces immediate damage for the following crop. Of course, this
particularly applies to nurseries. Steaming or chemical fumigation of the soil will improve the problem. Numerous investigations have suggested a range of theories on the cause of replant problem. They include macro- or micronutrient de®ciencies, nematodes, structural changes in the soil, toxin accumulation and an imbalance in microorganism population. A conclusive explanation of the cause of replant problems has not yet been presented. It has sometimes facetiously been said that ``soil sickness or replant disease is when nobody knows the cause''. The replant problem in roses often results from a combination of soil sickness or replant disease and nematode damage. Many factors may play a role when the same species is planted successively, and this multiplicity of causes has made it dif®cult to diagnose replant problems. Therefore de®nitions need to be precise. Replant problems include all those factors which cause reduced growth and yield when the same species or close relatives are planted repeatedly. One primary cause is nonspeci®c or more or less speci®c pests, such as the nematode Pratylenchus penetrans. Its hosts include over 200 plant species, and therefore it cannot be considered to be an exclusive agent in the context of replant disease. Physical soil factors may cause replant problems, such as soil compaction or waterlogging. Intentional monocropping of the same crop instead of a proper crop rotation programme may give rise to replant problems. De®ciencies in macro- or micronutrients may develop under such conditions. However, this should not be assumed to be the cause of the replant disease, because other plant species will react in a similar way. Neither can the long-term persistence of the problem in one location be explained in such cases. Similar arguments ignore the effect of root excretions or toxic substances formed when the remaining roots decompose after grubbing. Such substances are not expected to remain in the soil for long periods of time. Neither is it expected that the after effects of herbicide applications are a causal agent of replant disease. All these factors have generated various theories on the cause of replant disease. Replant disease or soil sickness is but one factor in this range of considerations. It differs from other factors by having a speci®c effect on one plant species and persisting in the long term. Savory coined the term `speci®c replant disease' and distinguished between `speci®c apple replant disease' and `speci®c peach replant disease' etc. emphasizing the biological species-speci®city. Practical experience provides evidence to support this concept, since pome fruit trees can be grown after stone fruit and vice versa with no replant problems. It also correlates with Klaus's de®nition of `plant speci®city'
DISEASE/Replant Problems and Soil Sickness
which is not necessarily associated with any species in the taxonomic sense. A Malus rootstock taxonomic species may well show different symptoms from a previously cropped Malus of a different species, and other Rosaceae may show reductions in growth when planted after a crop of apple trees. Thus, plant or fruit tree speci®city cannot be considered a true characteristic of replant disease. In spite of these endeavours to de®ne `speci®c replant disease' clearly, the lines of difference today are not clearly drawn. Depending on respective authors' scienti®c ®elds, factors are often cited that are not necessarily associated with the characteristics of replant disease. Opinions on the cause of replant disease are divided at this time. Investigations must continue in order to resolve this problem, as virgin soils in suitable climates become scarcer and scarcer. Fumigation is not an acceptable proposition for environmental reasons. New methods of dealing with this problem cannot be developed until we know its true cause.
Soil Sickness/Replant Disease with Roses Compared with fruit trees, much less is known on replant disease in roses. There is no evidence on whether the phenomenon only occurs during the ®rst few years after replanting, and whether plants can overcome it after a short time on site. It had been assumed that apples could recover from replant disease; however it was found that symptoms continued until the replanted trees were 11 years old. Obvious yield reductions in 36% of the compared ®elds were measured in replant trees during the entire life of these trees compared with those planted on virgin soil. No de®nitive ®gures exist in roses on a `weary' soil. The growth performance of four rose rootstocks in a replant plot was only 21ÿ78% compared with steam-treated soil. In the same experimental study the same four rose stocks replanted on an `apple-weary' soil only attained 41ÿ68% performance compared with steamed soil. Reports on the frequency of replant problems are also quite rare. In a survey of 166 German rose nurseries, about 75% of growers' replies mentioned replant problems, and 60% observed reduced growth. The same order of magnitude was found in 300 replies to a survey on apples. In this survey 85% of respondents did not recommend replanting apples without adequate treatment. Investigations are hampered by the fact that nurseries either avoid replanting or fumigate their soil regularly after one or two crops. Usually ®elds are assumed to be at risk of replant problems, and are given prophylactic treatment.
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Little is known about persistence and reversibility of replant disease in roses. Moreover there is no evidence that transplanting roses from a `sick' soil to a virgin soil will improve the symptoms. One observation prevails for both roses and fruit trees: effective control is only possible with soil fumigation. This indicates that the microorganisms involved are hard to control. There is no conclusive evidence that roses planted after other woody species or following a reverse planting sequence will have reduced performance. It has been observed that apples planted in a former rose nursery plot produced less growth than on virgin soil, and that several Rosaceae species are unsuitable crops when pome or stone fruits follow. These observations, as well as similarities in the replant disease in apples and roses, justify a more detailed description of the research results on the cause of speci®c apple replant disease. The intention is to clarify the factors associated with the replant disease in roses. It may also aid in designing further studies on replant disease in roses.
Investigations on the Cause of Speci®c Replant Disease in Apples As there were different opinions about the cause of replant disease in apples, suitable methods were required to exclude or con®rm theories. Attempts were ®rst made to transfer replant disease within the root ball of an apple seedling from a sick soil to virgin soil. The roots, including the ®brous roots, were freed from attached soil particles. Successful transfer was only possible when the ®brous roots were present. This indicates that there was no causal association with nutrient de®ciencies, soil physical factors or toxins in the soil. Further experiments revealed successful transfer when sick soil was freed from visible ®brous roots. A greater percentage of sick soil mixed with virgin soil resulted in increased replant disease. These results suggested a causal association of microorganisms in soil particles and in the ®brous root system. To identify these microorganisms, the temperature levels needed to remove replant disease in steaming practices were varied and compared with the temperature tolerance of groups of microorganisms. This procedure eliminated microscopic fungal microorganisms as a possible cause. Nematodes have a lower temperature tolerance than fungi and can therefore also be excluded. Actinomycetes and other bacteria could not be excluded. Actinomycetes are organisms of the family Actinomycetaceae in the order Actinomycetales. They show a vegetative mycelium, whose hyphae have a diameter lower than 1 mm. In the mycelial hyphae rod-shaped
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DISEASE/Replant Problems and Soil Sickness
or claviform segmentations were found. They are mostly Gram-positive, aerobic and prefer neutral pH. The temperature tolerance of some strains of Actinomycetes isolated from soils with apple replant disease is very close to the critical temperature for replant disease to be removed and therefore it has become the target for further investigations. There are several modes of action whereby Actinomycetes may produce replant disease. An accumulation of Actinomycetes in the rhizosphere may have negative physiologically in¯uence on replanted trees by metabolic substances. Pathogenic Actinomycetes may cause damage to the ®ne roots. Actinomycetes were found in longitudinal sections of ®brous roots from sick soil (Figure 2). These Actinomycetes grow into young light ®brous roots, accumulate in the root cortex, and functionally damage the root. This observation correlates with the appearance of root systems from sick soils. The ®brous roots appear to be brittle, they are brownish, and the total root mass is considerably reduced. Electron micrograph research has con®rmed that the Actinomycetes were indeed phytopathogenic. This was the ®rst plausible explanation of the cause of apple replant disease. However, it was dif®cult to comprehend the failure to ®nd comparable amounts of Actinomycetes in the ®ne roots. Infection occurred as early as 10 days after the formation of ®ne roots, and reached considerable dimensions subsequently. With severe replant disease, Actinomycetes was found to be associated with up to 80% of the ®brous roots. Surprisingly low Actinomycetes counts were found at the end of the growing season, unrelated to the degree of replant disease. There is a connection of the infection rate with host plant metabolic activities. The infection intensity is promoted by auxins and cytokinins. If their ¯ow into the roots is interrupted,
the attack on the ®brous roots is reduced, which means that during a phase of intensive synthesis of growth regulators during the main growth phase, there is a vigorous attack on the ®brous roots. During the second half of the growth period the attack is reduced. These observations help to explain a further phenomenon of replant disease in apple trees. On strongly affected ®elds apple trees display pronounced abatement of growth and yield. Seedlings are reported to produce nothing but rosette shoots. In spite of such impairment, apple trees do not die more frequently than in plantings on virgin soil. Apple tree performance is reduced as a result of damage to the ®brous roots during the main season such that they produce much less shoot growth and fruit yield. In the second half of the season the ®brous roots are only infected by Actinomycetes on a very small scale, so root regeneration takes place and the trees will survive. In longitudinal cuttings of ®brous roots development of sexual stages could be observed only occasionally. Apparently it only started in the weakened cortex of the ®brous roots and proceeded by fragmentation of Actinomycetes hyphae (Figure 3). As damaged root tissue decomposes, the permanent form of Actinomycetes gets into the soil and increases the number of germs locally. Fibrous roots entering these parts of the soil are attacked again and the enrichment of parasitic organisms in the rhizosphere leads to replant disease. This cyclic process is repeated year after year. It is independent of grubbing and this explains why it occurs in existing orchards. This ties in with the fact that replant disease is strictly limited to the extent of a previous orchard or nursery plot. The extent of accumulation of root pathogenic Actinomycetes is a deciding factor for the level of replant disease (Figure 4), which is also said to depend on pH and O2 content.
Figure 2 Actinomycetes in the root cortex of ®brous roots of an apple seedling from a sick soil with the beginnings of damage of the root tissue. (Photograph by G. Otto.)
Figure 3 Permanent forms in catenulate order formed by fragmentation of Actinomycetes hyphae. (Photograph by G. Otto.)
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173
90 80
Frequency (%)
70 60 50 40 30 20 10 0 14 21 28 35 42 A
14 21 28 35 42 B
14 21 28 35 42 C
14 21 28 35 42 D
Figure 4 Frequency of Actinomycetes in rootlets of apple seedlings from soils with increasing degrees (A to D) of soil sickness 2ÿ6 weeks after planting. (Data after Otto G and Winkler H (1993) Acta Horticulturae 324: 53ÿ59.)
The permanent forms of root pathogenic Actinomycetes which cause replant disease with apples are probably ubiquitous in the soil at low microbial levels. Furthermore they can be transferred with their roots from nursery ®elds when planted in another location. As development begins, some growth regulators or other substances get into the soil from root excretions. They act as signal substances on permanent forms of the root pathogenic Actinomycetes and reactivate them. The hyphae of germinating permanent forms either penetrate the epidermis of the ®brous roots or enter across root hairs into the cortex (Figure 5). They injure it to such an extent that entire parts of it disintegrate or die. Only when new ®ne roots could not grow into soil areas without accumulation of Actinomycetes, growth and yield start being reduced. This may explain why high-density plantings which have a greater number of trees per hectare show an effect sooner than extensive orchards which only have a few hundred trees per hectare. It has been suggested that exchanging the soil of the planting hole may overcome replant disease. Any positive results were lost the smaller the volume of exchanged soil had been. Improved performance could only be sustained as long as only the exchanged soil was ®lled with roots. When new root growth reached the sick soil, the enriched Actinomycetes produced a typical growth depression. These ®ndings have led to a new view on replant disease and the need for new discussions. Replant disease in apple is no longer a `speci®c replant disease', but rather a phytopathological problem in the rhizosphere of apple trees. But up to now no conclusive proof has been supplied. Not all authors agree with the Actinomycetes theory, sometimes preferring a multifactor complex of fungi like Phythium or
Figure 5 Hair roots and epidermal cells of ®brous roots of an apple seedling damaged by Actinomycetes. (Photograph by G. Otto.)
Rhizoctonia with bacteria like pseudomonads and Pratylenchus, but investigations could not support this clearly. Investigations over some decades support the Actinomycetes theory for central Europe and the United States, but in other continents different organisms could be prevalent.
Soil Sickness/Replant Disease with Various Rosaceae Species Since it has been established that replant disease with apples is a phytopathological problem, the question arises as to what is the range of hosts for the disease. This question is important because other species of the Rosaceae family are also af¯icted by replant disease. Additionally, negative effects have been seen when apples are grown after pears, or rowan after apples. Therefore an experiment was carried out to ®nd out whether ®brous roots of woody Rosaceae plants on an
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DISEASE/Replant Problems and Soil Sickness
`apple-sick' soil were carrying Actinomycetes. It was noted that ®brous roots of rowan were just as infected as the roots of apple seedlings. Only in pears was the frequency slightly lower than with apples 11 weeks after planting. The appearance in root cortex portions was the same as in apple cortex. In ®brous roots of cherry, plum and rose (Rosa canina) no Actinomycetes were found in these investigations. This led to the conclusion that replant disease cannot be caused by the same pathogen in these species as with apple, pear and rowan. This con®rmed growers' observations that successive planting of pome and stone fruits or vice versa does not result in speci®c replant disease. Further investigations were carried out on ornamental woody plants of the Rosaceae family regarding infestation by Actinomycetes. These trees or shrubs were planted either on previous apple plots or on plots of the same species. Actinomycetes was found in the ®brous roots of all six ornamentals from previous apple plots. The species tested were hawthorn (Crataegus monogyna), Cotoneaster, Japanese quince (Chaenomeles spp.), ®rethorn (Pyracantha spp.), Spiraea and rose (R. glauca) (Figure 6). The frequency of infestation varied, but in Pyracantha it was as high as in apple. With the exception of Spiraea spp., all other woody ornamental Rosaceae carried Actinomycetes when grown in repetition. The frequency of infestation was greater than in ®brous roots in previous apple plantings, except in Chaenomeles, whose symptoms corresponded to those in ®brous apple roots. The trials were not large enough to enable safe conclusions to be made about the infestation of ®brous roots of these species and also to correlate the infestation directly with growth reduction. At any rate, this was the ®rst con®rmation of involvement in Rosaceae of Actinomycetes, which are
Figure 6 Actinomycetes in the root cortex of a ®brous root of Rosa glauca from a sick soil. (Reproduced with permission from Otto G. et al. (1995) Zeitschrift fuÈr P¯anzenkrankheiten und P¯anzenschutz 102(6): 599ÿ605.)
known to cause replant disease. The occurrence of Actinomycetes in ®brous roots of roses is of particular interest here. In R. canina grown on previous apple soil no Actinomycetes were found, whereas R. glauca carried them on both apple soil and in previous rose plots. The Actinomycetes infestation was generally not very great, but it was clearly higher in previous rose soil than in apple plots. This may indicate that different rose rootstock species are af¯icted differently, and they may develop resistance to root pathogenic Actinomycetes. On the other hand the Actinomycetes on different Rosaceae may be different species of this causative agent. Root pathogenic Actinomycetes may have preferred host plants ÿ infestation is roughly similar in apple, rowan and Pyracantha, and lower in pear and other Rosaceae on previous apple plots. It is not yet possible to state this categorically, as only a limited number of cases have been investigated to date. However, it appears safe to claim that the Actinomycetes causing apple replant disease have a host range beyond any Malus species, but which does not include all other Rosaceae.
What Are the Future Expectations Regarding Replanting of Roses? There are similarities between apple and rose speci®c replant disease, although signi®cant proof has not yet been supplied. The existence of Actinomycetes in the ®brous roots of R. glauca grown on both previous apple and rose soil is a ®rst clue. Because trials have so far been limited, it cannot be ascertained whether infestation of ®brous roots depends on the growth rhythm during the vegetation period in roses as it does in apples. Thus it has not been de®nitively established whether infestation of ®brous roots occurs in R. canina grown on previous rose or apple plots as it does that in one case, in R. glauca. The investigation date must be carefully checked. This is also true for microscopic checks of four rose rootstocks: it was only in R. multi¯ora that a certain amount of infestation of ®brous roots by Actinomycetes could be established. Perhaps, as with apples, the infection is limited to certain growth periods and therefore would not be detected at every time of investigation. Furthermore, microscopic analysis of the ®ne structures of Actinomycetes in the ®brous roots requires a great deal of knowledge and experience. Of course, the question whether only one or several species of Actinomycetes are involved cannot be resolved. This requires isolation of the Actinomycetes, but this has not yet been accomplished even with apples. So postulates could not be proved until now. Presumably Actinomycetes are obligatory biotrophic
DISEASE/Replant Problems and Soil Sickness
organisms whose isolation and pure culture are very dif®cult. The literature does not present de®nitive statements on the persistence of replant disease and its reversibility. There are no indications about the soil factors which promote the disease or its occurrence even before grubbing in the range of still-developing roots. Finally there has not been any conclusive evidence about the extent of reactions of rootstocks to replanting after rose cultivation. Tests have indicated that there is more than just nematode damage when roses are cultivated repeatedly. Only steam sterilization or fumigation is effective at preventing this with roses ÿ as with apples. This indicates that the cause must also be microorganisms in roses as well. The occasional occurrence of Actinomycetes in ®brous roots of roses is an indication of this. However, replant disease in roses possibly may be caused by other factors, such as have been proposed with stone fruit trees. Actinomycetes have not been detected in Prunus mahaleb, although repeated cultivation results in severe growth depression. The development of a prognostic system for replant problems would be very important for the commercial rose grower. If root pathogenic Actinomycetes are the main cause of replant disease in rose ®elds, it will be crucial to develop new methods of controlling this organism. Strategies may include the application of antagonistic microorganisms. Using antagonistic plant species for intercropping may also be valuable.
Nematodes as Important Causal Agents of Replant Problems In most nursery soils different species of nematodes are present (Figure 7). In rose nursery plots with replant
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problems, 50ÿ1500 nematodes, mainly Pratylenchus penetrans, were counted in 250 cm3 soil. Other species observed were P. crenatus and P. neglectus. The damaging effects of the latter two species, as well as those of the genera Tylenchorhynchus, Paratylenchus, Trichodorus and Rotylenchus, have not yet been well documented. A large number of Paratylenchus were counted only on aeolic loess soil. Differences between locations give rise to variations in the range of genera. Investigations on a loess ®eld showed differences between rose species regarding the ratios of Pratylenchus and Paratylenchus. Whereas in R. canina `PfaÈnders' and R. corymbifera `Laxa' approximately the same proportions of both genera were found, in R. rugosa and R. acicularis the genus Paratylenchus was prevalent (Table 1). One- or two-times rose cropping resulted in increasing Pratylenchus populations, while three- or fourtimes cropping reduced the number of Pratylenchus in favour of other nematode genera. The optimum conditions for Pratylenchus are found at pH 5.5ÿ 5.8, but at pH 6.7 the population decreases considerably. High soil temperatures (418 C) or high precipitation levels are reported to have a negative effect on Pratylenchus development. The largest proportion of nematodes (about 80%) is found in the upper 30-cm layer, and during the growing season they are found to a depth of 60 cm (Figure 8). From April until the summer season varying populations of Pratylenchus were counted in the soil surface layer (30 cm): from October they decreased, but at a depth of 60ÿ90 cm nematode density increases, indicating that part of the population retreats to deeper soil layers in the autumn. In the plant roots Pratylenchus could only be found from July onwards. Until October the ®gures rose to
Longidorus spp. Aphelenchoides spp. Globodera spp. Meloidogyne spp. Xiphinema spp. Rotylenchus spp. Helicotylenchus spp. Trichodorus spp. Paratylenchus spp. Tylenchorhynchus spp. Pratylenchus spp. 0
10
20
30 40 50 Frequency (%)
60
70
80
Figure 7 Frequency of nematodes found in nursery soils in the SchleswigÿHolstein area (Germany) 1986ÿ1994 (n 638). (Data after LoÈsing H (1995) PhD thesis, University of Berlin, Germany.)
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DISEASE/Replant Problems and Soil Sickness
Table 1 Number of Pratylenchus and Paratylenchus nematodes (in 250 cm3) in sandy soil plots in BoÈnningstedt (BoÈ) (Schleswigÿ Holstein) after a culture of R. corymbifera `Laxa' and in loamy loess soil plots in Ruthe (Hanover) after a 3-year culture of some Rosa species (Kloczko and Spethmann) Plot
Pratylenchus spp.
Paratylenchus spp.
7 May
23 Jun
4 Aug
10 Sep
27 Oct
7 May
23 Jun
4 Aug
10 Sep
27 Oct
BoÈ BoÈ BoÈ BoÈ BoÈ BoÈ BoÈ BoÈ BoÈ BoÈ
1 3 4 5 6 9 10 12 13 15
24 12 6 6 24 72 0 24 6 24
120 30 141 189 0 102 27 246 12 51
30 18 42 48 0 21 21 9 45 39
69 107 27 54 3 237 45 231 3 120
159 54 Ð 33 3 504 39 63 3 30
0 0 0 0 0 0 6 0 0 6
0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0 0 0
0 3 0 0 0 0 0 0 0 51
0 0 0 0 0 0 0 0 0 27
R. R. R. R. R. R. R. R. R. R.
canina `PfaÈnders' corymbifera `Laxa' acicularis micrantha rugosa nitida arvensis canina rubiginosa glauca
0 30 24 24 30 30 0 6 18 18
48 60 9 18 3 0 0 15 6 12
3 0 15 3 6 0 3 3 0 3
45 24 12 3 9 Ð 0 9 6 6
24 36 3 36 3 6 Ð Ð 6 24
0 48 24 18 48 0 6 0 0 0
8 39 24 3 18 18 0 3 3 0
0 0 0 0 66 0 0 0 0 0
3 18 18 0 81 Ð 0 3 0 0
52 Ð 27 9 45 0 Ð Ð 6 0
Data from Kloczko M and Spethmann W (1994) Untersuchungen uÈber SchaÈden durch Nematoden an Rosen in Baumschulen. Taspo Gartenbaumagazin 3(5): 10ÿ11.
200 Depth of soil layer 0–30 cm 180
Depth of soil layer 30–60 cm Depth of soil layer 60–90 cm
Number of Pratylenchus spp. per 250 cm³ soil
160 140 120 100 80 60 40 20 0 3 Apr
15 May
25 Jun 29 Jul Date of sampling
9 Sep
29 Oct
Figure 8 Number of Pratylenchus spp. per 250 cm3 soil dependent on date of sampling and depth of the soil layer. (Unpublished data of M. Kloczko and W. Spethmann.)
a maximum of 4500 nematodes per 5 g roots. As roses are suitable host plants, the number of Pratylenchus increased in the successive year. Even after one rose crop, the number may increase to such an extent that damage becomes evident in the following rose crop.
The number of nematodes is considerably in¯uenced by the preceding crop (Figure 9). Cereals, maize and legumes as a preceding crop increase the number of Pratylenchus nematodes. A preceding crop of conifers, deciduous trees or shrubs, e.g., fruit plants, slightly
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177
900 Mean number of nematodes per 250 cm3 soil
800 700 600 500
Paratylenchus spp. Tylenchorhynchus spp. Pratylenchus spp.
400 300 200 100 0
Broadleaved
Conifers
Roses
Maize
Grain crops
Grass
Green manure
Figure 9 In¯uence of the preceding crop on the number of Pratylenchus spp., Tylenchorhynchus spp. and Paratylenchus spp. in the SchleswigÿHolstein nursery area (Germany) (n 506). (Data after LoÈsing H (1995) PhD thesis, University of Berlin, Germany.)
2
3.5 3 2.5 2
1.5
1.5
1
1 0.5
0.5 0
20 40 60 80 Pratylenchus penetrans per 5 g roots
0 100
Figure 10 Plant and root fresh weight and total root length of R. corymbifera `Laxa' dependent on concentration of Pratylenchus penetrans per 5 g roots. (Unpublished data of M. Kloczko and W. Spethmann.)
increases the number. Reduced Pratylenchus numbers are observed after a fallow period and a Tagetes crop, particularly T. patula and T. erecta. These species are speci®cally used to control nematode pests (see Insects and other Animals: Nematodes).
Visual Nematode Damage Nematode damage on roses is caused not only by Pratylenchus penetrans, but also by P. vulnus, P. thornei and Meloidogyne hapla, and possibly also by P. crenatus and P. neglecta (in greenhouses). Experimental data on their damaging effects are only available on P. penetrans. A comparison of roses on nematode locations with roses from `clean' plots shows reduced growth. Localized, nest-like reduced growth or blanks are usually typical of nematodes. Rosette shoot formation, i.e. decreasing length of internodes, reduced leaf number, reduction in root length and fresh weight
Fresh weight per plant (g)
2.5
0
4
4 Plant fresh weight Root fresh weight Total root length
Total root length
Plant and root fresh weight (g)
3
3.5 3 2.5 2 1.5 1 0.5 0 0 1000 2000 3000 4000 5000 6000 Number of Pratylenchus spp. per 5 g root fresh weight
Figure 11 Rose plant fresh weight dependent on the number of Pratylenchus in the roots per 5 g root fresh weight (open marks disinfected plots). (Unpublished data of M. Kloczko and W. Spethmann.)
of plants, are typical characteristics (Figure 10). The germination of rose seed is often inhibited. The extent of the damage increases with increasing numbers of nematodes: however, damage remains constant with 1000 nematodes per 5 g roots (Figure 11). It remains to be seen whether other growthinhibiting factors supplement the nematode effects. To ®nd out whether that is the case, inoculations were carried out in a greenhouse. The materials chosen were Pratylenchus isolated from R. corymbifera `Laxa' roots which were mixed into the TKS substrate (peat and sand mixture) at rates of 0ÿ1500 nematodes in 250 g substrate. Two-week-old seedlings of R. micrantha, R. obtusifolia and R. tomentosa were planted, and the presence of Pratylenchus resulted in an infection in all cases. Increasing inoculum densities caused increasing root infection, depending on the species. In R. micrantha almost 800 nematodes per 5 g roots were counted, but in R. obtusifolia only 200 could be found (Figure 12).
DISEASE/Replant Problems and Soil Sickness
The damage depended on inoculum density, as could be shown by inoculation of R. corymbifera `Laxa' (Figure 13). Growth reductions became more severe between 30 and 300 nematodes per 5 g, but above that level, only slightly more damage was observed. As regards the number of nematodes in the substrate, damage only increased at rates between 50 and 750 nematodes per 250 g soil. This con®rms results obtained in the ®eld. The threshold of de®nitive damage is 250 nematodes in 250 g soil; the critical threshold is seen to be 700ÿ800 nematodes. Depending on where the investigation is carried out, these ®gures are lower or, in a few cases, higher. The results con®rm that different rose species have different susceptibility to nematodes. The search for
Number of Pratylenchus penetrans per 5 g root
800 R. obtusifolia R. tomentosa R. micrantha
700 600 500 400 300 200 100 0
0
500 1000 1500 Density of inoculum
3000
Figure 12 Number of Pratylenchus per 5 g root fresh weight dependent on the density of the inoculum (Pratylenchus penetrans) per 500 g substrate. (Data after Spethmann W (1993) Rosenjahrbuch Verein Deutscher Rosenfreunde 1993: 67ÿ82.)
Root fresh weight (g) Plant fresh weight (g) Total root length (m)
3.5 3 2.5
Demarcation of Replant Disease and Nematode Damage Since for places showing replant problems it could not been determined whether the replant problems are caused by replant disease, nematodes, or both, various tests have been developed. One such test, developed for apples, is direct evidence comparing growth in treated and untreated soil. Shoot growth in untreated soil was compared with that in steamed soil or in soil fumigated with Dazomet and Metham-sodium compounds. Evidence of exclusive nematode damage can be obtained by comparison with an aldicarb nematicide-treated soil. The growth difference indicates how serious the replant disease is. Based on the tests developed for apple, a test for Rosa was introduced which helps to estimate the proportions of the two causes ÿ replant disease and nematodes. In this test R. corymbifera `Laxa' seedling growth is assessed in untreated soil, soil partially heat-treated at 50 C, and soil fully heat-treated at 100 C. Since nematodes are destroyed at 45ÿ50 C, the comparison of a partially treated soil and an untreated soil demonstrates how much damage is caused by factors other than nematodes. On the average of several tests, the 50 C steaming results in a growth increment of 45ÿ90% compared to untreated soil; after full treatment at 100 C the biomass increment is around 300% higher (Figure 14 and Table 2). This demonstrates that replant disease is an important factor in addition to nematode injury in the development 10 9 8 7 6 5 4 3 2 1 0
Fresh weight (g)
Plant and root fresh weight (g) and total root length (m)
4
resistant rose species or rootstocks therefore appears promising. In the survey on replant problems the most serious damage was observed with R. corymbifera `Laxa' and R. canina `PfaÈnders', while minimal damage was seen with R. canina `Inermis', `Pollmers' and R. multi¯ora.
2 1.5 1 0.5 0 0
50
100 200 400 800 1600 Concentration of Pratylenchus penetrans per 500 g substrate
Figure 13 Plant and root fresh weight and total root length of R. corymbifera `Laxa' dependent on concentration of Pratylenchus penetrans per 500 g substrate. (Unpublished data of M. Kloczko and W. Spethmann.)
16 Root fresh weight Plant fresh weight Total root length
14 12 10 8 6 4
Root length (m)
178
2 0 °C (untreated)
100 °C 50 °C (partly disinfected) (disinfected)
0
Figure 14 Plant and root fresh weight and total root length of R. corymbifera `Laxa' dependent on part and total disinfection (mean of 15 plots). (Data after Kloczko M and Spethmann W (1994) Taspo Gartenbaumagazin 3(5): 10ÿ11.)
DISEASE/Replant Problems and Soil Sickness
of replant problems. Another test, carried out with Rosa raised in vitro (`The Fairy' and `Komet') is based on the same principle. The in vitro plants are grown in the respective substrates and growth is compared after 4 weeks.
Measures to Control Nematodes Treatments with nematicides (e.g. Temik 5 G) or fumigants (Basamid) result in a clear reduction in the nematode population (Figure 15). The increasing withdrawal of pesticides has led to a search for alternative methods. Inserting a complete fallow period in the crop rotation could considerably reduce the nematode count. Steaming at 450 C is quite effective, but is expensive. As mentioned above, inserting a crop of Tagetes patula and T. erecta (10 kg haÿ1 of seed) reduces the nematode population and is already practiced over large surface areas (Figure 16). The problem here is the slow initial development which allows weeds to ¯ourish in competition with the Tagetes. Herbicides or mechanical weeding is indispensable. With T. erecta pre- and postemergence treatments
179
with Afalon and Goltix WG are compatible with roses; in pre-emergence Tenoran, Bandur or Stomp SC is effective. For T. patula Goltix WG is considered to be compatible. The cultivar T. minuta `Nemanon', however, produces only minimal nematicidal effect, and Phacelia is likewise unsuitable as a crop before roses. Some authors claim that sun¯owers have a positive effect, while others refute this. It makes sense to use rootstocks that suffer less damage. Of the two main rootstocks, `Laxa' and `Inermis', the latter shows less damage, particularly its smallfruited selection. `Heinsohns Rekord' also produces minimal damage symptoms. Growth reduction has not been found with R. multi¯ora `Stachellos' and R. carolina. The search for resistant species needs to be intensi®ed to provide basic material for breeding nematode-resistant rootstocks. Regarding the cause of speci®c replant disease in roses many questions remain. Will further investigations give more evidence for the contribution of Actinomycetes? Are other organisms like fungi concerned? Are nematodes a separate phytopathological problem, or are they a contributing part of
Table 2 Percentage of reduction of plant and root fresh weight and total root length by nematodes and speci®c soil sickness (100% total reduction compared with plants growing in disinfected soil) Soil of nursery Reduction of plant fresh weight (%) plots Nematodes Soil sickness
Reduction of root fresh weight (%)
Reduction of total root length (%)
Nematodes
Soil sickness
Nematodes
Soil sickness
BoÈnningstedt Klei Mehlen Ruthe (loess)
30 45 47 39
70 54 53 61
16 38 40 49
84 62 60 51
39 43 32 46
61 57 68 54
450
8000
400
7000
350 300 250 200 150
6000 5000 4000 3000
100
2000
50
1000 0
T D era is in bo fe l 1 ct 9 io 89 n 19 Te T 89 D r is ab em in o ik fe l 1 ct io 988 n 1 Ta 988 ge R te ye s g O ras il ra s di C R sh al os ci um e F s cy all an ow Ph am ac el M ide ia us / B ta en rd Ph ton ac it e C Lu lia lo p ve in rg s ra ss
0
Plant fresh weight
Number of Pratylenchus per 250 cm3 soil
Data from Kloczko M and Spethmann W (1994) Untersuchungen uÈber SchaÈden durch Nematoden an Rosen in Baumschulen. Taspo Gartenbaumagazin 3(5): 10ÿ11.
Figure 15 Number of Pratylenchus per 250 cm3 soil (shaded bars) and rose plants fresh weight (g) (solid circles) of the total plot after different disinfection treatments or cash crops. (Data modi®ed after Strassburger T (1992) PhD thesis, University of Kiel, Germany.)
180
DISEASE/Viruses
Increase or decrease of Pratylenchus penetrans per 100 cm3 soil
100 50 0 – 50 – 100
3 Dec 90 (B) 19 Apr 91 (B) 1995 (A)
– 150 – 200 – 250
Tagetes Tagetes patula erecta
Fallow
Tagetes Phacelia Oil ‘Nemanon’ radish
Figure 16 Increase or decrease of Pratylenchus penetrans (per 100 cm3 soil) in percent after different cultures of fallow. (Data after LoÈsing H (1995) PhD thesis, University of Berlin, Germany (A) and unpublished data of M. Kloczko and W. Spethmann (B).)
a multifactor complex together with bacteria or fungi, maybe as vectors? Many investigations must be undertaken to clear up the problem. See also: Breeding: Selection Strategies for Disease and Pest Resistance. Disease: Bactericides and Fungicides. Insects and other Animals: Nematodes. Integrated Pest Management. Morphology and Anatomy: Roots. Rootstocks: Usage of Rootstocks.
Further Reading Dauck H and Spethmann W (1991) Der BodenmuÈdigkeit auf der Spur: Eine bundesweite Umfrage zu Nachbauproblemen bei Rosen. Deutsche Baumschule 43(4): 164ÿ167. Dressler H (1997) Untersuchungen zur Besiedlung von Rosenwurzeln durch Bakterien im Hinblick auf BodenmuÈdigkeit. PhD Thesis, University of Hanover, Germany. Hoestra H (1968) Replant diseases of apple in the Netherlands. Mededelingen Landbouwhogeschool 68: 13. KruÈssmann G (1997) Die Baumschule. Berlin: Paul Parey Verlag. LoÈsing H (1995) Bedeutung und integrierte BekaÈmpfung wandernder Nematoden (Pratylenchus spp.) als eine Ursache von NachbauschaÈden bei Rosen in der Baumschulproduktion. PhD Thesis, University of Berlin, Germany. Maeseneer de J (1967) Biologie en Bestrijding van Pratylenchus penetrans en P. crenatus. PhD Thesis, Rijksfaculteit der Landbouwwetenschapen, Ghent, Belgium. Mazzola M and Gu Yu Huan (2000) Phyto-management of microbial community structure to enhance growth of apple in replant soils. Acta Horticulturae 532: 73ÿ78. Oostenbrink M (1961) Nematode damage and `speci®c sickness' in Rosa, Malus and Laburnum. Tijdschrift over Planteziekten 67: 264ÿ272.
Otto G (2000) BodenmuÈdigkeit. In: Friedrich G and Fischer M (eds.) Physiologische Grundlagen des Obstbaues, 3rd edn, pp. 281ÿ296. Stuttgart, Germany: Eugen Ulmer. Otto G and Winkler H (1993) Soil fumigation for controlling replant problems in apple orchards. Acta Horticulturae 324: 53ÿ59. Otto G and Winkler H (1998) In¯uence of root pathogenic actinomycetes on the trimming of the rootlets of some species of Rosaceae with root hairs. Acta Horticulturae 477: 49ÿ54. Otto G, Winkler H and Szabo K (1993a) In¯uence of growth regulators on the infection of rootlets of apple seedlings in SARD soils by actinomycetes. Acta Horticulturae 363: 101ÿ107. Otto G, Winkler H and Szabo K (1994) Proof of actinomycetes in rootlets of species of Rosaceae from a SARD soil: a contribution to the speci®city of replant diseases. Acta Horticulturae 363: 43ÿ48. Savory BM (1966) Speci®c Replant Diseases. Farnham, UK: Commonwealth Agricultural Bureaux. Spethmann W and Dauck H (1992) Forschungskonzepte zum Nachbauproblem bei Rosen. Gartenbaumagazin 1(7): 18ÿ20. Strassburger T (1992) Alternative Verfahren zur Beseitigung von Nachbauproblemen in Baumschulen. PhD thesis, University of Keil, Germany. Szabo K, Winkler H, Petzold H and Marwitz R (1998) Evidence for the pathogenicity of Actinomycetes in rootlets of apple seedlings from soils conductive to speci®c apple replant disease. Acta Horticulturae 477: 55ÿ65. Tagliavini M, Utkhede R and Zucconi F (eds.) ( 1990) Symposium on soil sickness and replant diseases in fruit trees. Acta Horticulturae 324: 1ÿ109.
Viruses M S Szyndel, Warsaw Agricultural University, Poland # 2003, Elsevier Ltd. All Rights Reserved.
Introduction Plant viruses are infectious, intracellular, submicroscopic, spherical or rod-shaped particles. They are composed of only a single type of nucleic acid surrounded by protein coat. The parasitism of viruses occurs at the molecular, intracellular level, where virus particles copy themselves using the replicative system of a plant cell. Most plant viruses may induce a wide variety of disease symptoms although infection may sometimes be symptomless. Viruses, as infectious agents, can be transmitted from diseased to healthy
169
Further Reading
Figure 7 Susceptibility and resistance to P. mucronatum. The compound leaf of R. corymbifera `Laxa' (left) is heavily rusted, whereas Rosa `Pascali'Õ (right) growing as a scion on the `Laxa' stock, and which has not been `headed back', is unaffected.
collecting fallen rusted leaves is unlikely to be successful. Furthermore, later in the year teliospores are also dispersed, albeit shorter distances, and stick, as stated earlier, to stems and other permanent substrates. Removal of rust-forming galls in the case of P. mucronatum and P. rosae-pimpinellifoliae, however, may help to reduce aeciospore inoculum arising from perennating systemic mycelial infection. Chemical control can be effective and a number of systemic fungicides, e.g. benodanil, oxycarboxin, penconazole, propiconazole and triforine, have given excellent control over the past couple of decades. The latter two have been available to the amateur gardener but have become outclassed or withdrawn for a variety of reasons. Myclobutanil is a readily available systemic fungicide providing protective, curative and eradicant control and, of course, is active against powdery mildew, too. Myclobutanil is an azole compound and this family of chemicals inhibits sterol biosynthesis and therefore disrupts cell membranes of target fungal pathogens. Commercial growers, in the United Kingdom at least, have a wider choice of compounds to choose from including new-generation azoles developed for the cereal market and other compounds too, such as the strobilurins which inhibit cellular respiration in pathogens. In the United Kingdom, subject to the usual restrictions, fungicides approved for use on any growing edible crop, e.g. cereal or top fruit, can be used, at present, on commercial agricultural or horticultural holdings, where no part of the plant is to be consumed by humans or animals. This applies to hardy ornamental nursery stock, and therefore includes roses. See also: Disease: Overview; Botrytis; Black Spot; Downy Mildew; Powdery Mildew. Breeding: Selection Strategies for Disease and Pest Resistance.
Henderson DM (2000) A Check List of the Rust Fungi of the British Isles. Kew, UK: British Mycological Society. Horst RK (1983) Compendium of Rose Diseases. St Paul, MN, USA: American Phytopathological Society. Laundon GF and Rainbow AK (1969a) Phragmidium tuberculatum, CMI Descriptions of Pathogenic Fungi and Bacteria no. 204. Kew, UK: Commonwealth Agricultural Bureaux. Laundon GF and Rainbow AK (1969b) Phragmidium mucronatum, CMI Descriptions of Pathogenic Fungi and Bacteria no. 205. Kew, UK: Commonwealth Agricultural Bureaux. Laundon GF and Rainbow AK (1969c) Phragmidium rosae-pimpinellifoliae, CMI Descriptions of Pathogenic Fungi and Bacteria no. 208. Kew, UK: Commonwealth Agricultural Bureaux. Losing H (1988) Bekampfung von Rosenrost. Deutsche Baumschule 40: 518ÿ519. Shattock RC and Rahbar Bhatti MH (1983) Rust on Laxa stocks. In: Harkness J (ed.) The Rose Annual 1983, pp. 150ÿ162. St Albans, UK: Royal National Rose Society.
Replant Problems and Soil Sickness W Spethmann, University of Hanover, Germany G Otto, Dresden, Germany # 2003, Elsevier Ltd. All Rights Reserved.
Introduction Declines in growth and yield have been observed in roses and several other genera when the same genus has repeatedly been planted in the same location. The degree of decline depends on the plant species, various soil factors, and pests present in the soil. To avoid such replant problems growers tend to move to a new ®eld, fumigate, or cure with hot steam (Figure 1). Crop rotation schedules, allowing planting intervals for the species in question as well as fallow periods, are recommended. The two main causes of replant problems are ®rst, nematodes and second, speci®c replant disease or soil sickness. Both factors will be discussed in this article. At the present time it is not known whether nematodes are connected directly with the speci®c replant disease. The organisms causing speci®c replant disease in roses have not yet been identi®ed, although economic losses are very high. After many years of intensive research in apples, the causal organisms associated with speci®c
170
DISEASE/Replant Problems and Soil Sickness
Figure 1 Disinfected soil plots with optimum growth of Rosa corymbifera `Laxa' beside plots with depressed growth caused by soil sickness and nematodes in BoÈnningstedt (Schleswig± Holstein). (Photograph by W. Spethmann.)
replant disease were identi®ed as Actinomycetes. It is possible that these microorganisms could have a similar effect in roses as in apples; therefore the mode of action of these microorganisms in Malus are discussed in detail. Besides nematodes and speci®c replant disease, replant problems could be caused or increased by fungi, lack of mineral substances, trace elements, or soil compaction.
Characteristics and Terminology Some plant species suffer severe damage when grown repeatedly in the same ®eld. This cannot be avoided even by having a long interval before returning with the same crop, especially where species of the Rosaceae family are concerned. The terms `replant disease', `soil sickness' and `soil exhaustion' are often used to describe this problem. The problem is said to be species-speci®c (for apples, for roses, etc.). The persistence of the cause of replant disease can be observed in the soil even decades later, but other factors should also be taken into account. The phenomenon appears to be strictly limited to the ®eld in which the particular crop was grown previously, as especially noted in nurseries which changed the direction in which rows of roses or apple liners were planted. The disease occurs uniformly within entire rows of plants, not in nestlike pockets. Furthermore, it is known that replant disease is reversible. Plants from affected soil which are transplanted into virgin soil will soon recover and grow normally. Typically, replant disease occurs with varying severity in different locations. In some areas serious problems rarely occur or only after several repetitions of the same crop, whereas in other areas a single, short-term planting produces immediate damage for the following crop. Of course, this
particularly applies to nurseries. Steaming or chemical fumigation of the soil will improve the problem. Numerous investigations have suggested a range of theories on the cause of replant problem. They include macro- or micronutrient de®ciencies, nematodes, structural changes in the soil, toxin accumulation and an imbalance in microorganism population. A conclusive explanation of the cause of replant problems has not yet been presented. It has sometimes facetiously been said that ``soil sickness or replant disease is when nobody knows the cause''. The replant problem in roses often results from a combination of soil sickness or replant disease and nematode damage. Many factors may play a role when the same species is planted successively, and this multiplicity of causes has made it dif®cult to diagnose replant problems. Therefore de®nitions need to be precise. Replant problems include all those factors which cause reduced growth and yield when the same species or close relatives are planted repeatedly. One primary cause is nonspeci®c or more or less speci®c pests, such as the nematode Pratylenchus penetrans. Its hosts include over 200 plant species, and therefore it cannot be considered to be an exclusive agent in the context of replant disease. Physical soil factors may cause replant problems, such as soil compaction or waterlogging. Intentional monocropping of the same crop instead of a proper crop rotation programme may give rise to replant problems. De®ciencies in macro- or micronutrients may develop under such conditions. However, this should not be assumed to be the cause of the replant disease, because other plant species will react in a similar way. Neither can the long-term persistence of the problem in one location be explained in such cases. Similar arguments ignore the effect of root excretions or toxic substances formed when the remaining roots decompose after grubbing. Such substances are not expected to remain in the soil for long periods of time. Neither is it expected that the after effects of herbicide applications are a causal agent of replant disease. All these factors have generated various theories on the cause of replant disease. Replant disease or soil sickness is but one factor in this range of considerations. It differs from other factors by having a speci®c effect on one plant species and persisting in the long term. Savory coined the term `speci®c replant disease' and distinguished between `speci®c apple replant disease' and `speci®c peach replant disease' etc. emphasizing the biological species-speci®city. Practical experience provides evidence to support this concept, since pome fruit trees can be grown after stone fruit and vice versa with no replant problems. It also correlates with Klaus's de®nition of `plant speci®city'
DISEASE/Replant Problems and Soil Sickness
which is not necessarily associated with any species in the taxonomic sense. A Malus rootstock taxonomic species may well show different symptoms from a previously cropped Malus of a different species, and other Rosaceae may show reductions in growth when planted after a crop of apple trees. Thus, plant or fruit tree speci®city cannot be considered a true characteristic of replant disease. In spite of these endeavours to de®ne `speci®c replant disease' clearly, the lines of difference today are not clearly drawn. Depending on respective authors' scienti®c ®elds, factors are often cited that are not necessarily associated with the characteristics of replant disease. Opinions on the cause of replant disease are divided at this time. Investigations must continue in order to resolve this problem, as virgin soils in suitable climates become scarcer and scarcer. Fumigation is not an acceptable proposition for environmental reasons. New methods of dealing with this problem cannot be developed until we know its true cause.
Soil Sickness/Replant Disease with Roses Compared with fruit trees, much less is known on replant disease in roses. There is no evidence on whether the phenomenon only occurs during the ®rst few years after replanting, and whether plants can overcome it after a short time on site. It had been assumed that apples could recover from replant disease; however it was found that symptoms continued until the replanted trees were 11 years old. Obvious yield reductions in 36% of the compared ®elds were measured in replant trees during the entire life of these trees compared with those planted on virgin soil. No de®nitive ®gures exist in roses on a `weary' soil. The growth performance of four rose rootstocks in a replant plot was only 21ÿ78% compared with steam-treated soil. In the same experimental study the same four rose stocks replanted on an `apple-weary' soil only attained 41ÿ68% performance compared with steamed soil. Reports on the frequency of replant problems are also quite rare. In a survey of 166 German rose nurseries, about 75% of growers' replies mentioned replant problems, and 60% observed reduced growth. The same order of magnitude was found in 300 replies to a survey on apples. In this survey 85% of respondents did not recommend replanting apples without adequate treatment. Investigations are hampered by the fact that nurseries either avoid replanting or fumigate their soil regularly after one or two crops. Usually ®elds are assumed to be at risk of replant problems, and are given prophylactic treatment.
171
Little is known about persistence and reversibility of replant disease in roses. Moreover there is no evidence that transplanting roses from a `sick' soil to a virgin soil will improve the symptoms. One observation prevails for both roses and fruit trees: effective control is only possible with soil fumigation. This indicates that the microorganisms involved are hard to control. There is no conclusive evidence that roses planted after other woody species or following a reverse planting sequence will have reduced performance. It has been observed that apples planted in a former rose nursery plot produced less growth than on virgin soil, and that several Rosaceae species are unsuitable crops when pome or stone fruits follow. These observations, as well as similarities in the replant disease in apples and roses, justify a more detailed description of the research results on the cause of speci®c apple replant disease. The intention is to clarify the factors associated with the replant disease in roses. It may also aid in designing further studies on replant disease in roses.
Investigations on the Cause of Speci®c Replant Disease in Apples As there were different opinions about the cause of replant disease in apples, suitable methods were required to exclude or con®rm theories. Attempts were ®rst made to transfer replant disease within the root ball of an apple seedling from a sick soil to virgin soil. The roots, including the ®brous roots, were freed from attached soil particles. Successful transfer was only possible when the ®brous roots were present. This indicates that there was no causal association with nutrient de®ciencies, soil physical factors or toxins in the soil. Further experiments revealed successful transfer when sick soil was freed from visible ®brous roots. A greater percentage of sick soil mixed with virgin soil resulted in increased replant disease. These results suggested a causal association of microorganisms in soil particles and in the ®brous root system. To identify these microorganisms, the temperature levels needed to remove replant disease in steaming practices were varied and compared with the temperature tolerance of groups of microorganisms. This procedure eliminated microscopic fungal microorganisms as a possible cause. Nematodes have a lower temperature tolerance than fungi and can therefore also be excluded. Actinomycetes and other bacteria could not be excluded. Actinomycetes are organisms of the family Actinomycetaceae in the order Actinomycetales. They show a vegetative mycelium, whose hyphae have a diameter lower than 1 mm. In the mycelial hyphae rod-shaped
172
DISEASE/Replant Problems and Soil Sickness
or claviform segmentations were found. They are mostly Gram-positive, aerobic and prefer neutral pH. The temperature tolerance of some strains of Actinomycetes isolated from soils with apple replant disease is very close to the critical temperature for replant disease to be removed and therefore it has become the target for further investigations. There are several modes of action whereby Actinomycetes may produce replant disease. An accumulation of Actinomycetes in the rhizosphere may have negative physiologically in¯uence on replanted trees by metabolic substances. Pathogenic Actinomycetes may cause damage to the ®ne roots. Actinomycetes were found in longitudinal sections of ®brous roots from sick soil (Figure 2). These Actinomycetes grow into young light ®brous roots, accumulate in the root cortex, and functionally damage the root. This observation correlates with the appearance of root systems from sick soils. The ®brous roots appear to be brittle, they are brownish, and the total root mass is considerably reduced. Electron micrograph research has con®rmed that the Actinomycetes were indeed phytopathogenic. This was the ®rst plausible explanation of the cause of apple replant disease. However, it was dif®cult to comprehend the failure to ®nd comparable amounts of Actinomycetes in the ®ne roots. Infection occurred as early as 10 days after the formation of ®ne roots, and reached considerable dimensions subsequently. With severe replant disease, Actinomycetes was found to be associated with up to 80% of the ®brous roots. Surprisingly low Actinomycetes counts were found at the end of the growing season, unrelated to the degree of replant disease. There is a connection of the infection rate with host plant metabolic activities. The infection intensity is promoted by auxins and cytokinins. If their ¯ow into the roots is interrupted,
the attack on the ®brous roots is reduced, which means that during a phase of intensive synthesis of growth regulators during the main growth phase, there is a vigorous attack on the ®brous roots. During the second half of the growth period the attack is reduced. These observations help to explain a further phenomenon of replant disease in apple trees. On strongly affected ®elds apple trees display pronounced abatement of growth and yield. Seedlings are reported to produce nothing but rosette shoots. In spite of such impairment, apple trees do not die more frequently than in plantings on virgin soil. Apple tree performance is reduced as a result of damage to the ®brous roots during the main season such that they produce much less shoot growth and fruit yield. In the second half of the season the ®brous roots are only infected by Actinomycetes on a very small scale, so root regeneration takes place and the trees will survive. In longitudinal cuttings of ®brous roots development of sexual stages could be observed only occasionally. Apparently it only started in the weakened cortex of the ®brous roots and proceeded by fragmentation of Actinomycetes hyphae (Figure 3). As damaged root tissue decomposes, the permanent form of Actinomycetes gets into the soil and increases the number of germs locally. Fibrous roots entering these parts of the soil are attacked again and the enrichment of parasitic organisms in the rhizosphere leads to replant disease. This cyclic process is repeated year after year. It is independent of grubbing and this explains why it occurs in existing orchards. This ties in with the fact that replant disease is strictly limited to the extent of a previous orchard or nursery plot. The extent of accumulation of root pathogenic Actinomycetes is a deciding factor for the level of replant disease (Figure 4), which is also said to depend on pH and O2 content.
Figure 2 Actinomycetes in the root cortex of ®brous roots of an apple seedling from a sick soil with the beginnings of damage of the root tissue. (Photograph by G. Otto.)
Figure 3 Permanent forms in catenulate order formed by fragmentation of Actinomycetes hyphae. (Photograph by G. Otto.)
DISEASE/Replant Problems and Soil Sickness
173
90 80
Frequency (%)
70 60 50 40 30 20 10 0 14 21 28 35 42 A
14 21 28 35 42 B
14 21 28 35 42 C
14 21 28 35 42 D
Figure 4 Frequency of Actinomycetes in rootlets of apple seedlings from soils with increasing degrees (A to D) of soil sickness 2ÿ6 weeks after planting. (Data after Otto G and Winkler H (1993) Acta Horticulturae 324: 53ÿ59.)
The permanent forms of root pathogenic Actinomycetes which cause replant disease with apples are probably ubiquitous in the soil at low microbial levels. Furthermore they can be transferred with their roots from nursery ®elds when planted in another location. As development begins, some growth regulators or other substances get into the soil from root excretions. They act as signal substances on permanent forms of the root pathogenic Actinomycetes and reactivate them. The hyphae of germinating permanent forms either penetrate the epidermis of the ®brous roots or enter across root hairs into the cortex (Figure 5). They injure it to such an extent that entire parts of it disintegrate or die. Only when new ®ne roots could not grow into soil areas without accumulation of Actinomycetes, growth and yield start being reduced. This may explain why high-density plantings which have a greater number of trees per hectare show an effect sooner than extensive orchards which only have a few hundred trees per hectare. It has been suggested that exchanging the soil of the planting hole may overcome replant disease. Any positive results were lost the smaller the volume of exchanged soil had been. Improved performance could only be sustained as long as only the exchanged soil was ®lled with roots. When new root growth reached the sick soil, the enriched Actinomycetes produced a typical growth depression. These ®ndings have led to a new view on replant disease and the need for new discussions. Replant disease in apple is no longer a `speci®c replant disease', but rather a phytopathological problem in the rhizosphere of apple trees. But up to now no conclusive proof has been supplied. Not all authors agree with the Actinomycetes theory, sometimes preferring a multifactor complex of fungi like Phythium or
Figure 5 Hair roots and epidermal cells of ®brous roots of an apple seedling damaged by Actinomycetes. (Photograph by G. Otto.)
Rhizoctonia with bacteria like pseudomonads and Pratylenchus, but investigations could not support this clearly. Investigations over some decades support the Actinomycetes theory for central Europe and the United States, but in other continents different organisms could be prevalent.
Soil Sickness/Replant Disease with Various Rosaceae Species Since it has been established that replant disease with apples is a phytopathological problem, the question arises as to what is the range of hosts for the disease. This question is important because other species of the Rosaceae family are also af¯icted by replant disease. Additionally, negative effects have been seen when apples are grown after pears, or rowan after apples. Therefore an experiment was carried out to ®nd out whether ®brous roots of woody Rosaceae plants on an
174
DISEASE/Replant Problems and Soil Sickness
`apple-sick' soil were carrying Actinomycetes. It was noted that ®brous roots of rowan were just as infected as the roots of apple seedlings. Only in pears was the frequency slightly lower than with apples 11 weeks after planting. The appearance in root cortex portions was the same as in apple cortex. In ®brous roots of cherry, plum and rose (Rosa canina) no Actinomycetes were found in these investigations. This led to the conclusion that replant disease cannot be caused by the same pathogen in these species as with apple, pear and rowan. This con®rmed growers' observations that successive planting of pome and stone fruits or vice versa does not result in speci®c replant disease. Further investigations were carried out on ornamental woody plants of the Rosaceae family regarding infestation by Actinomycetes. These trees or shrubs were planted either on previous apple plots or on plots of the same species. Actinomycetes was found in the ®brous roots of all six ornamentals from previous apple plots. The species tested were hawthorn (Crataegus monogyna), Cotoneaster, Japanese quince (Chaenomeles spp.), ®rethorn (Pyracantha spp.), Spiraea and rose (R. glauca) (Figure 6). The frequency of infestation varied, but in Pyracantha it was as high as in apple. With the exception of Spiraea spp., all other woody ornamental Rosaceae carried Actinomycetes when grown in repetition. The frequency of infestation was greater than in ®brous roots in previous apple plantings, except in Chaenomeles, whose symptoms corresponded to those in ®brous apple roots. The trials were not large enough to enable safe conclusions to be made about the infestation of ®brous roots of these species and also to correlate the infestation directly with growth reduction. At any rate, this was the ®rst con®rmation of involvement in Rosaceae of Actinomycetes, which are
Figure 6 Actinomycetes in the root cortex of a ®brous root of Rosa glauca from a sick soil. (Reproduced with permission from Otto G. et al. (1995) Zeitschrift fuÈr P¯anzenkrankheiten und P¯anzenschutz 102(6): 599ÿ605.)
known to cause replant disease. The occurrence of Actinomycetes in ®brous roots of roses is of particular interest here. In R. canina grown on previous apple soil no Actinomycetes were found, whereas R. glauca carried them on both apple soil and in previous rose plots. The Actinomycetes infestation was generally not very great, but it was clearly higher in previous rose soil than in apple plots. This may indicate that different rose rootstock species are af¯icted differently, and they may develop resistance to root pathogenic Actinomycetes. On the other hand the Actinomycetes on different Rosaceae may be different species of this causative agent. Root pathogenic Actinomycetes may have preferred host plants ÿ infestation is roughly similar in apple, rowan and Pyracantha, and lower in pear and other Rosaceae on previous apple plots. It is not yet possible to state this categorically, as only a limited number of cases have been investigated to date. However, it appears safe to claim that the Actinomycetes causing apple replant disease have a host range beyond any Malus species, but which does not include all other Rosaceae.
What Are the Future Expectations Regarding Replanting of Roses? There are similarities between apple and rose speci®c replant disease, although signi®cant proof has not yet been supplied. The existence of Actinomycetes in the ®brous roots of R. glauca grown on both previous apple and rose soil is a ®rst clue. Because trials have so far been limited, it cannot be ascertained whether infestation of ®brous roots depends on the growth rhythm during the vegetation period in roses as it does in apples. Thus it has not been de®nitively established whether infestation of ®brous roots occurs in R. canina grown on previous rose or apple plots as it does that in one case, in R. glauca. The investigation date must be carefully checked. This is also true for microscopic checks of four rose rootstocks: it was only in R. multi¯ora that a certain amount of infestation of ®brous roots by Actinomycetes could be established. Perhaps, as with apples, the infection is limited to certain growth periods and therefore would not be detected at every time of investigation. Furthermore, microscopic analysis of the ®ne structures of Actinomycetes in the ®brous roots requires a great deal of knowledge and experience. Of course, the question whether only one or several species of Actinomycetes are involved cannot be resolved. This requires isolation of the Actinomycetes, but this has not yet been accomplished even with apples. So postulates could not be proved until now. Presumably Actinomycetes are obligatory biotrophic
DISEASE/Replant Problems and Soil Sickness
organisms whose isolation and pure culture are very dif®cult. The literature does not present de®nitive statements on the persistence of replant disease and its reversibility. There are no indications about the soil factors which promote the disease or its occurrence even before grubbing in the range of still-developing roots. Finally there has not been any conclusive evidence about the extent of reactions of rootstocks to replanting after rose cultivation. Tests have indicated that there is more than just nematode damage when roses are cultivated repeatedly. Only steam sterilization or fumigation is effective at preventing this with roses ÿ as with apples. This indicates that the cause must also be microorganisms in roses as well. The occasional occurrence of Actinomycetes in ®brous roots of roses is an indication of this. However, replant disease in roses possibly may be caused by other factors, such as have been proposed with stone fruit trees. Actinomycetes have not been detected in Prunus mahaleb, although repeated cultivation results in severe growth depression. The development of a prognostic system for replant problems would be very important for the commercial rose grower. If root pathogenic Actinomycetes are the main cause of replant disease in rose ®elds, it will be crucial to develop new methods of controlling this organism. Strategies may include the application of antagonistic microorganisms. Using antagonistic plant species for intercropping may also be valuable.
Nematodes as Important Causal Agents of Replant Problems In most nursery soils different species of nematodes are present (Figure 7). In rose nursery plots with replant
175
problems, 50ÿ1500 nematodes, mainly Pratylenchus penetrans, were counted in 250 cm3 soil. Other species observed were P. crenatus and P. neglectus. The damaging effects of the latter two species, as well as those of the genera Tylenchorhynchus, Paratylenchus, Trichodorus and Rotylenchus, have not yet been well documented. A large number of Paratylenchus were counted only on aeolic loess soil. Differences between locations give rise to variations in the range of genera. Investigations on a loess ®eld showed differences between rose species regarding the ratios of Pratylenchus and Paratylenchus. Whereas in R. canina `PfaÈnders' and R. corymbifera `Laxa' approximately the same proportions of both genera were found, in R. rugosa and R. acicularis the genus Paratylenchus was prevalent (Table 1). One- or two-times rose cropping resulted in increasing Pratylenchus populations, while three- or fourtimes cropping reduced the number of Pratylenchus in favour of other nematode genera. The optimum conditions for Pratylenchus are found at pH 5.5ÿ 5.8, but at pH 6.7 the population decreases considerably. High soil temperatures (418 C) or high precipitation levels are reported to have a negative effect on Pratylenchus development. The largest proportion of nematodes (about 80%) is found in the upper 30-cm layer, and during the growing season they are found to a depth of 60 cm (Figure 8). From April until the summer season varying populations of Pratylenchus were counted in the soil surface layer (30 cm): from October they decreased, but at a depth of 60ÿ90 cm nematode density increases, indicating that part of the population retreats to deeper soil layers in the autumn. In the plant roots Pratylenchus could only be found from July onwards. Until October the ®gures rose to
Longidorus spp. Aphelenchoides spp. Globodera spp. Meloidogyne spp. Xiphinema spp. Rotylenchus spp. Helicotylenchus spp. Trichodorus spp. Paratylenchus spp. Tylenchorhynchus spp. Pratylenchus spp. 0
10
20
30 40 50 Frequency (%)
60
70
80
Figure 7 Frequency of nematodes found in nursery soils in the SchleswigÿHolstein area (Germany) 1986ÿ1994 (n 638). (Data after LoÈsing H (1995) PhD thesis, University of Berlin, Germany.)
176
DISEASE/Replant Problems and Soil Sickness
Table 1 Number of Pratylenchus and Paratylenchus nematodes (in 250 cm3) in sandy soil plots in BoÈnningstedt (BoÈ) (Schleswigÿ Holstein) after a culture of R. corymbifera `Laxa' and in loamy loess soil plots in Ruthe (Hanover) after a 3-year culture of some Rosa species (Kloczko and Spethmann) Plot
Pratylenchus spp.
Paratylenchus spp.
7 May
23 Jun
4 Aug
10 Sep
27 Oct
7 May
23 Jun
4 Aug
10 Sep
27 Oct
BoÈ BoÈ BoÈ BoÈ BoÈ BoÈ BoÈ BoÈ BoÈ BoÈ
1 3 4 5 6 9 10 12 13 15
24 12 6 6 24 72 0 24 6 24
120 30 141 189 0 102 27 246 12 51
30 18 42 48 0 21 21 9 45 39
69 107 27 54 3 237 45 231 3 120
159 54 Ð 33 3 504 39 63 3 30
0 0 0 0 0 0 6 0 0 6
0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0 0 0
0 3 0 0 0 0 0 0 0 51
0 0 0 0 0 0 0 0 0 27
R. R. R. R. R. R. R. R. R. R.
canina `PfaÈnders' corymbifera `Laxa' acicularis micrantha rugosa nitida arvensis canina rubiginosa glauca
0 30 24 24 30 30 0 6 18 18
48 60 9 18 3 0 0 15 6 12
3 0 15 3 6 0 3 3 0 3
45 24 12 3 9 Ð 0 9 6 6
24 36 3 36 3 6 Ð Ð 6 24
0 48 24 18 48 0 6 0 0 0
8 39 24 3 18 18 0 3 3 0
0 0 0 0 66 0 0 0 0 0
3 18 18 0 81 Ð 0 3 0 0
52 Ð 27 9 45 0 Ð Ð 6 0
Data from Kloczko M and Spethmann W (1994) Untersuchungen uÈber SchaÈden durch Nematoden an Rosen in Baumschulen. Taspo Gartenbaumagazin 3(5): 10ÿ11.
200 Depth of soil layer 0–30 cm 180
Depth of soil layer 30–60 cm Depth of soil layer 60–90 cm
Number of Pratylenchus spp. per 250 cm³ soil
160 140 120 100 80 60 40 20 0 3 Apr
15 May
25 Jun 29 Jul Date of sampling
9 Sep
29 Oct
Figure 8 Number of Pratylenchus spp. per 250 cm3 soil dependent on date of sampling and depth of the soil layer. (Unpublished data of M. Kloczko and W. Spethmann.)
a maximum of 4500 nematodes per 5 g roots. As roses are suitable host plants, the number of Pratylenchus increased in the successive year. Even after one rose crop, the number may increase to such an extent that damage becomes evident in the following rose crop.
The number of nematodes is considerably in¯uenced by the preceding crop (Figure 9). Cereals, maize and legumes as a preceding crop increase the number of Pratylenchus nematodes. A preceding crop of conifers, deciduous trees or shrubs, e.g., fruit plants, slightly
DISEASE/Replant Problems and Soil Sickness
177
900 Mean number of nematodes per 250 cm3 soil
800 700 600 500
Paratylenchus spp. Tylenchorhynchus spp. Pratylenchus spp.
400 300 200 100 0
Broadleaved
Conifers
Roses
Maize
Grain crops
Grass
Green manure
Figure 9 In¯uence of the preceding crop on the number of Pratylenchus spp., Tylenchorhynchus spp. and Paratylenchus spp. in the SchleswigÿHolstein nursery area (Germany) (n 506). (Data after LoÈsing H (1995) PhD thesis, University of Berlin, Germany.)
2
3.5 3 2.5 2
1.5
1.5
1
1 0.5
0.5 0
20 40 60 80 Pratylenchus penetrans per 5 g roots
0 100
Figure 10 Plant and root fresh weight and total root length of R. corymbifera `Laxa' dependent on concentration of Pratylenchus penetrans per 5 g roots. (Unpublished data of M. Kloczko and W. Spethmann.)
increases the number. Reduced Pratylenchus numbers are observed after a fallow period and a Tagetes crop, particularly T. patula and T. erecta. These species are speci®cally used to control nematode pests (see Insects and other Animals: Nematodes).
Visual Nematode Damage Nematode damage on roses is caused not only by Pratylenchus penetrans, but also by P. vulnus, P. thornei and Meloidogyne hapla, and possibly also by P. crenatus and P. neglecta (in greenhouses). Experimental data on their damaging effects are only available on P. penetrans. A comparison of roses on nematode locations with roses from `clean' plots shows reduced growth. Localized, nest-like reduced growth or blanks are usually typical of nematodes. Rosette shoot formation, i.e. decreasing length of internodes, reduced leaf number, reduction in root length and fresh weight
Fresh weight per plant (g)
2.5
0
4
4 Plant fresh weight Root fresh weight Total root length
Total root length
Plant and root fresh weight (g)
3
3.5 3 2.5 2 1.5 1 0.5 0 0 1000 2000 3000 4000 5000 6000 Number of Pratylenchus spp. per 5 g root fresh weight
Figure 11 Rose plant fresh weight dependent on the number of Pratylenchus in the roots per 5 g root fresh weight (open marks disinfected plots). (Unpublished data of M. Kloczko and W. Spethmann.)
of plants, are typical characteristics (Figure 10). The germination of rose seed is often inhibited. The extent of the damage increases with increasing numbers of nematodes: however, damage remains constant with 1000 nematodes per 5 g roots (Figure 11). It remains to be seen whether other growthinhibiting factors supplement the nematode effects. To ®nd out whether that is the case, inoculations were carried out in a greenhouse. The materials chosen were Pratylenchus isolated from R. corymbifera `Laxa' roots which were mixed into the TKS substrate (peat and sand mixture) at rates of 0ÿ1500 nematodes in 250 g substrate. Two-week-old seedlings of R. micrantha, R. obtusifolia and R. tomentosa were planted, and the presence of Pratylenchus resulted in an infection in all cases. Increasing inoculum densities caused increasing root infection, depending on the species. In R. micrantha almost 800 nematodes per 5 g roots were counted, but in R. obtusifolia only 200 could be found (Figure 12).
DISEASE/Replant Problems and Soil Sickness
The damage depended on inoculum density, as could be shown by inoculation of R. corymbifera `Laxa' (Figure 13). Growth reductions became more severe between 30 and 300 nematodes per 5 g, but above that level, only slightly more damage was observed. As regards the number of nematodes in the substrate, damage only increased at rates between 50 and 750 nematodes per 250 g soil. This con®rms results obtained in the ®eld. The threshold of de®nitive damage is 250 nematodes in 250 g soil; the critical threshold is seen to be 700ÿ800 nematodes. Depending on where the investigation is carried out, these ®gures are lower or, in a few cases, higher. The results con®rm that different rose species have different susceptibility to nematodes. The search for
Number of Pratylenchus penetrans per 5 g root
800 R. obtusifolia R. tomentosa R. micrantha
700 600 500 400 300 200 100 0
0
500 1000 1500 Density of inoculum
3000
Figure 12 Number of Pratylenchus per 5 g root fresh weight dependent on the density of the inoculum (Pratylenchus penetrans) per 500 g substrate. (Data after Spethmann W (1993) Rosenjahrbuch Verein Deutscher Rosenfreunde 1993: 67ÿ82.)
Root fresh weight (g) Plant fresh weight (g) Total root length (m)
3.5 3 2.5
Demarcation of Replant Disease and Nematode Damage Since for places showing replant problems it could not been determined whether the replant problems are caused by replant disease, nematodes, or both, various tests have been developed. One such test, developed for apples, is direct evidence comparing growth in treated and untreated soil. Shoot growth in untreated soil was compared with that in steamed soil or in soil fumigated with Dazomet and Metham-sodium compounds. Evidence of exclusive nematode damage can be obtained by comparison with an aldicarb nematicide-treated soil. The growth difference indicates how serious the replant disease is. Based on the tests developed for apple, a test for Rosa was introduced which helps to estimate the proportions of the two causes ÿ replant disease and nematodes. In this test R. corymbifera `Laxa' seedling growth is assessed in untreated soil, soil partially heat-treated at 50 C, and soil fully heat-treated at 100 C. Since nematodes are destroyed at 45ÿ50 C, the comparison of a partially treated soil and an untreated soil demonstrates how much damage is caused by factors other than nematodes. On the average of several tests, the 50 C steaming results in a growth increment of 45ÿ90% compared to untreated soil; after full treatment at 100 C the biomass increment is around 300% higher (Figure 14 and Table 2). This demonstrates that replant disease is an important factor in addition to nematode injury in the development 10 9 8 7 6 5 4 3 2 1 0
Fresh weight (g)
Plant and root fresh weight (g) and total root length (m)
4
resistant rose species or rootstocks therefore appears promising. In the survey on replant problems the most serious damage was observed with R. corymbifera `Laxa' and R. canina `PfaÈnders', while minimal damage was seen with R. canina `Inermis', `Pollmers' and R. multi¯ora.
2 1.5 1 0.5 0 0
50
100 200 400 800 1600 Concentration of Pratylenchus penetrans per 500 g substrate
Figure 13 Plant and root fresh weight and total root length of R. corymbifera `Laxa' dependent on concentration of Pratylenchus penetrans per 500 g substrate. (Unpublished data of M. Kloczko and W. Spethmann.)
16 Root fresh weight Plant fresh weight Total root length
14 12 10 8 6 4
Root length (m)
178
2 0 °C (untreated)
100 °C 50 °C (partly disinfected) (disinfected)
0
Figure 14 Plant and root fresh weight and total root length of R. corymbifera `Laxa' dependent on part and total disinfection (mean of 15 plots). (Data after Kloczko M and Spethmann W (1994) Taspo Gartenbaumagazin 3(5): 10ÿ11.)
DISEASE/Replant Problems and Soil Sickness
of replant problems. Another test, carried out with Rosa raised in vitro (`The Fairy' and `Komet') is based on the same principle. The in vitro plants are grown in the respective substrates and growth is compared after 4 weeks.
Measures to Control Nematodes Treatments with nematicides (e.g. Temik 5 G) or fumigants (Basamid) result in a clear reduction in the nematode population (Figure 15). The increasing withdrawal of pesticides has led to a search for alternative methods. Inserting a complete fallow period in the crop rotation could considerably reduce the nematode count. Steaming at 450 C is quite effective, but is expensive. As mentioned above, inserting a crop of Tagetes patula and T. erecta (10 kg haÿ1 of seed) reduces the nematode population and is already practiced over large surface areas (Figure 16). The problem here is the slow initial development which allows weeds to ¯ourish in competition with the Tagetes. Herbicides or mechanical weeding is indispensable. With T. erecta pre- and postemergence treatments
179
with Afalon and Goltix WG are compatible with roses; in pre-emergence Tenoran, Bandur or Stomp SC is effective. For T. patula Goltix WG is considered to be compatible. The cultivar T. minuta `Nemanon', however, produces only minimal nematicidal effect, and Phacelia is likewise unsuitable as a crop before roses. Some authors claim that sun¯owers have a positive effect, while others refute this. It makes sense to use rootstocks that suffer less damage. Of the two main rootstocks, `Laxa' and `Inermis', the latter shows less damage, particularly its smallfruited selection. `Heinsohns Rekord' also produces minimal damage symptoms. Growth reduction has not been found with R. multi¯ora `Stachellos' and R. carolina. The search for resistant species needs to be intensi®ed to provide basic material for breeding nematode-resistant rootstocks. Regarding the cause of speci®c replant disease in roses many questions remain. Will further investigations give more evidence for the contribution of Actinomycetes? Are other organisms like fungi concerned? Are nematodes a separate phytopathological problem, or are they a contributing part of
Table 2 Percentage of reduction of plant and root fresh weight and total root length by nematodes and speci®c soil sickness (100% total reduction compared with plants growing in disinfected soil) Soil of nursery Reduction of plant fresh weight (%) plots Nematodes Soil sickness
Reduction of root fresh weight (%)
Reduction of total root length (%)
Nematodes
Soil sickness
Nematodes
Soil sickness
BoÈnningstedt Klei Mehlen Ruthe (loess)
30 45 47 39
70 54 53 61
16 38 40 49
84 62 60 51
39 43 32 46
61 57 68 54
450
8000
400
7000
350 300 250 200 150
6000 5000 4000 3000
100
2000
50
1000 0
T D era is in bo fe l 1 ct 9 io 89 n 19 Te T 89 D r is ab em in o ik fe l 1 ct io 988 n 1 Ta 988 ge R te ye s g O ras il ra s di C R sh al os ci um e F s cy all an ow Ph am ac el M ide ia us / B ta en rd Ph ton ac it e C Lu lia lo p ve in rg s ra ss
0
Plant fresh weight
Number of Pratylenchus per 250 cm3 soil
Data from Kloczko M and Spethmann W (1994) Untersuchungen uÈber SchaÈden durch Nematoden an Rosen in Baumschulen. Taspo Gartenbaumagazin 3(5): 10ÿ11.
Figure 15 Number of Pratylenchus per 250 cm3 soil (shaded bars) and rose plants fresh weight (g) (solid circles) of the total plot after different disinfection treatments or cash crops. (Data modi®ed after Strassburger T (1992) PhD thesis, University of Kiel, Germany.)
180
DISEASE/Viruses
Increase or decrease of Pratylenchus penetrans per 100 cm3 soil
100 50 0 – 50 – 100
3 Dec 90 (B) 19 Apr 91 (B) 1995 (A)
– 150 – 200 – 250
Tagetes Tagetes patula erecta
Fallow
Tagetes Phacelia Oil ‘Nemanon’ radish
Figure 16 Increase or decrease of Pratylenchus penetrans (per 100 cm3 soil) in percent after different cultures of fallow. (Data after LoÈsing H (1995) PhD thesis, University of Berlin, Germany (A) and unpublished data of M. Kloczko and W. Spethmann (B).)
a multifactor complex together with bacteria or fungi, maybe as vectors? Many investigations must be undertaken to clear up the problem. See also: Breeding: Selection Strategies for Disease and Pest Resistance. Disease: Bactericides and Fungicides. Insects and other Animals: Nematodes. Integrated Pest Management. Morphology and Anatomy: Roots. Rootstocks: Usage of Rootstocks.
Further Reading Dauck H and Spethmann W (1991) Der BodenmuÈdigkeit auf der Spur: Eine bundesweite Umfrage zu Nachbauproblemen bei Rosen. Deutsche Baumschule 43(4): 164ÿ167. Dressler H (1997) Untersuchungen zur Besiedlung von Rosenwurzeln durch Bakterien im Hinblick auf BodenmuÈdigkeit. PhD Thesis, University of Hanover, Germany. Hoestra H (1968) Replant diseases of apple in the Netherlands. Mededelingen Landbouwhogeschool 68: 13. KruÈssmann G (1997) Die Baumschule. Berlin: Paul Parey Verlag. LoÈsing H (1995) Bedeutung und integrierte BekaÈmpfung wandernder Nematoden (Pratylenchus spp.) als eine Ursache von NachbauschaÈden bei Rosen in der Baumschulproduktion. PhD Thesis, University of Berlin, Germany. Maeseneer de J (1967) Biologie en Bestrijding van Pratylenchus penetrans en P. crenatus. PhD Thesis, Rijksfaculteit der Landbouwwetenschapen, Ghent, Belgium. Mazzola M and Gu Yu Huan (2000) Phyto-management of microbial community structure to enhance growth of apple in replant soils. Acta Horticulturae 532: 73ÿ78. Oostenbrink M (1961) Nematode damage and `speci®c sickness' in Rosa, Malus and Laburnum. Tijdschrift over Planteziekten 67: 264ÿ272.
Otto G (2000) BodenmuÈdigkeit. In: Friedrich G and Fischer M (eds.) Physiologische Grundlagen des Obstbaues, 3rd edn, pp. 281ÿ296. Stuttgart, Germany: Eugen Ulmer. Otto G and Winkler H (1993) Soil fumigation for controlling replant problems in apple orchards. Acta Horticulturae 324: 53ÿ59. Otto G and Winkler H (1998) In¯uence of root pathogenic actinomycetes on the trimming of the rootlets of some species of Rosaceae with root hairs. Acta Horticulturae 477: 49ÿ54. Otto G, Winkler H and Szabo K (1993a) In¯uence of growth regulators on the infection of rootlets of apple seedlings in SARD soils by actinomycetes. Acta Horticulturae 363: 101ÿ107. Otto G, Winkler H and Szabo K (1994) Proof of actinomycetes in rootlets of species of Rosaceae from a SARD soil: a contribution to the speci®city of replant diseases. Acta Horticulturae 363: 43ÿ48. Savory BM (1966) Speci®c Replant Diseases. Farnham, UK: Commonwealth Agricultural Bureaux. Spethmann W and Dauck H (1992) Forschungskonzepte zum Nachbauproblem bei Rosen. Gartenbaumagazin 1(7): 18ÿ20. Strassburger T (1992) Alternative Verfahren zur Beseitigung von Nachbauproblemen in Baumschulen. PhD thesis, University of Keil, Germany. Szabo K, Winkler H, Petzold H and Marwitz R (1998) Evidence for the pathogenicity of Actinomycetes in rootlets of apple seedlings from soils conductive to speci®c apple replant disease. Acta Horticulturae 477: 55ÿ65. Tagliavini M, Utkhede R and Zucconi F (eds.) ( 1990) Symposium on soil sickness and replant diseases in fruit trees. Acta Horticulturae 324: 1ÿ109.
Viruses M S Szyndel, Warsaw Agricultural University, Poland # 2003, Elsevier Ltd. All Rights Reserved.
Introduction Plant viruses are infectious, intracellular, submicroscopic, spherical or rod-shaped particles. They are composed of only a single type of nucleic acid surrounded by protein coat. The parasitism of viruses occurs at the molecular, intracellular level, where virus particles copy themselves using the replicative system of a plant cell. Most plant viruses may induce a wide variety of disease symptoms although infection may sometimes be symptomless. Viruses, as infectious agents, can be transmitted from diseased to healthy