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Challenges facing mushroom disease control in the 21st century.

Abstract: Disease outbreaks can severely reduce the yield and productivity of commercial mushroom production. Many mushroom pathogens are resistant to benzimidazole fungicides or are increasingly tolerant to prochloraz. New pathogens have emerged at regular intervals over the years such as Trichoderma aggressivum, Cladobotryum mycophilum Type 2 and Mushroom Virus X (MVX). The number of approved pesticide products has been significantly reduced in Europe, and it is expensive to generate the data required to register potential new products for small users such as the mushroom industry. This combination of circumstances makes controlling disease outbreaks more challenging. Disease control will increasingly depend on effective hygiene measures. Knowledge of disease epidemiology of specific pathogens will provide growers with insight into how they are transmitted and spread within and between crops. Collaboration between research groups at the international level is a way forward.

Introduction

The mushroom industry in Europe has undergone much change in the past 10 to 1.5 years. In Britain and France production has decreased by approximately 50 percent. In the Netherlands and Ireland it has decreased by about 20 percent while in Poland it has increased by 100 percent. In 2006 Poland become the second largest producer of mushrooms in Europe (216,000 tonnes) after The Netherlands (225,000 tonnes) (Grogan, 2008). This changing pattern of production across Europe has resulted in large reductions in grower numbers in many countries. Small inefficient farms have closed and farms remaining have increased output and efficiency.

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Throughout Europe the industry is consolidating into larger, more productive farms with increased mechanization and centralized management. Within this framework, it is essential that a clear disease management strategy be in place to maximize efficiency. Failure to treat disease outbreaks in the early stages can be very costly as untreated areas of disease produce the spores and propagules that will spread the disease throughout the rest of the crop and the farm. Serious outbreaks of disease reduce marketable yield, incur additional costs for disease control chemicals, as well as additional labor to identify and treat disease and to apply chemicals.

In Europe many chemicals are no longer approved for use. In addition there is increased demand from consumers and supermarket retailers for reduced pesticide use so that growers will increasingly have to depend on disease prevention and containment measures to control outbreaks rather than resorting to chemicals. Thus a major challenge for mushroom growers in the 21st century is disease control with few or no chemicals. Other challenges include fungicide resistance among pathogen populations, managing existing available pesticides and the emergence of new pathogens. The mushroom research community in Europe is also facing a reduction in both numbers and funding and will be less able to respond to emerging problems. Collaboration on projects between research groups around the world is the way forward.

Fungicide Resistance

Over time, mushroom pathogens such as Verticillium fungicola, Cladobotryum mycophilum and now Trichoderma aggressivum have developed resistance to the benzimidazole fungicides (Fletcher &Yarham, 1976; Grogan & Gaze, 2000, Romaine et al, 2005). Resistance to benzimidazoles usually requires only a single mutation in a single gene. This has occurred with relative ease for a large number of pathogens, particularly those with many life cycles in a year like Verticillium and Trichoderma. However other pathogens, such as Mycogone perniciosa, have remained sensitive. In Europe the benzimidazole fungicide carbendazim is now withdrawn for use on mushrooms leaving no benzimidazoles approved for controlling sensitive pathogens such as Mycogone.

In many countries the fungicide prochloraz is the only effective chemical to control Verticillium fungicola. In countries where prochloraz is used, Verticillium populations become more tolerant to the active ingredient but this tolerance has not been associated with any major loss of control (Grogan et al 2000, Gea et al, 2005). Elsewhere in agriculture, prochloraz has remained an effective fungicide against a broad range of fungal pathogens despite many years of use and records of increased tolerance in fungal populations similar to that seen in Verticillium. However, significantly increased levels of prochloraz resistance have been detected in some populations of the cereal eyespot pathogen in France and New Zealand (Dyer et al, 2000). Whether or not prochloraz remains effective for Verticillium control will depend on whether resistance is determined by mutation in a single major gene or requires mutations in many genes.

There is evidence to suggest that this polygenic resistance is conferred by a single major gene along with additional minor genes. This complex control mechanism is probably the reason why there is no widespread loss of field performance by prochloraz to date despite shifts in sensitivity. Sexual reproduction within fungal populations can markedly increase the level of resistance in the progeny and increase the likelihood of reduced efficacy. However, as the sexual state of Verticillium has not been encountered so far, the risk of increased resistance due to sexual recombination is reduced.

Fungicide Persistence

Reduced efficacy of fungicides can occur for reasons other than resistance. Benomyl and carbendazim are both known to be susceptible to microbial degradation in soils previously exposed to them (Fletcher et al., 1980, Yarden et al, 1990) and this can lead to reduced control of pathogens. Biodegradation of pesticides is an environmentally desirable trait so that toxic chemicals do not accumulate in the environment, as was the case with DDT. But there has to be a balance between the time frame within which the chemical is effective against the target pathogen and the ultimate degradation of the chemical to non-toxic components.

The current widespread practice of buying in ready made "pristine" casing mixes that have never been treated with fungicides, rather than preparing casing mixes from scratch on the farm from stored stocks of ingredients, will reduce the opportunity for fungicide degrading microbial populations to develop. It is a good idea not to mix old and new batches of casing as old batches that have been stored on the farm can pick up the microbes that flourish in casing elsewhere on the site. If fungicides are generally used on the farm then some casing microbes may have acquired the ability to degrade those fungicides and may be present in the background microbial population on the farm.

Recent research has shown that prochloraz too can be degraded by microbes present in prochloraz-treated casing (Papadopulos, 2006). When the fungicide is applied to casing under laboratory conditions, the concentration of prochloraz remains reasonably high with approximately 50 percent of what was applied still present by day 40 (Figure 1-A). Under normal growing conditions on a mushroom unit however, there was a rapid decline in the concentration of the active ingredient with less than 15 percent remaining by day 45 (Figure 1-B). This will likely lead to reduced efficacy late in the crop cycle but further work is required to determine if this is the case.

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As prochloraz remains one of the few chemicals available to control fungal diseases of mushrooms it is important that we maximize its efficacy through good farm management practices. This is all the more important if more aggressive strains of Verticillium emerge.

Emerging New Pathogens

Mushroom pathogens have evolved alongside mushrooms, originally in the wild, and have successfully migrated to wherever mushrooms are cultivated commercially. Fungal pathogens such as Verticillium, Mycogone, cobweb and Trichoderma have been known since the early days of commercial production (Kligman, 1950). Compost-related pathogens and weed molds have also found a niche in commercial mushroom compost such as truffle, olive green mold and plaster molds. With improvements in technology, hygiene and grower understanding of diseases and how they spread, many of these diseases, particularly compost related ones, are no longer problematical. However, nature is a dynamic force and as mushroom compost improves and mushroom growing becomes more hygienic and precisely controlled, new pathogens have emerged that have overcome some of the obstacles in their way or become adapted to new conditions such as more productive compost, bulk handling of vulnerable Phase III compost or wetter growing conditions. A key question is often "where did the new pathogen come from?" but this question is often difficult to answer. "New" pathogens may be present at low levels within the existing pathogen population or they may be a recently mutated form that confers an advantage, such as fungicide resistance. Table 1 lists a number of new pathogens or new strains of existing pathogens, which have been reported since 1950.
Table 1: Some new mushroom pathogens or pathogen strains reported
since 1950.

Pathogen First Reported Reference

La France Virus 1948 USA Sinden & Hauser (1950)

Pythium artotrogus 1960 USA Fergus et al. (1963)

Pythium oligandrum 1986 UK Fletcher et al. (1990)

Trichoderma aggressivum 1984 Ireland Morris et al. (1995)
var europaeum

Trichoderma aggressivum 1990 Canada Rinker & Alm (2000)
var aggressivum

Cladobotryum mycophilum 1992 Ireland McKay et al. (1999)
Type II

Mushroom Virus X 1996 UK Gaze et al. (2000)


La France virus disease was probably the first major new pathogen which affected mushroom cultivation, impacting severely on the mushroom industry in the United States and United Kingdom the 1960s. Epidemiological research indicated that it was predominately spread by spores from infected mushrooms and also by infected mycelium carried over from one crop to the next (Schisler et al. 1967). Control was achieved by preventing the spread of spores by filtration, not growing flat mushrooms and by cooking out crops at the end of the cycle.

Although Trichoderma species such as T. koningii and T. viride were long associated with mushroom cultivation, their impact on production was relatively minor. In the mid 1980s and 1990s Trichoderma aggressivum emerged as an aggressive compost mold that decimated mushroom production if it got into freshly spawned Phase II compost. It had a higher temperature optimum than other Trichoderma spp. and grew rapidly on carbohydrates in the grain supporting the mushroom spawn. Once T. aggressivum encountered mushroom cultivation facilities it found a niche ideally suited to its characteristics: it is a successful fungus producing enzymes capable of growing on carbohydrate rich substrates with a fast growth rate and temperature optimum close to that of Agaricus. Poor hygiene at Phase II emptying and/or spawning either through ineffective disinfection of equipment or through the ingress of contaminated air into spawning halls is the likely route of entry into a crop or Phase III tunnel. Initially, benzimida-zole fungicides applied to the spawn gave good control of the problem but in the states resistance has now emerged leaving improved hygiene as the only option to control this pathogen (Romaine et al. 2005).

Fungicide resistance appears to have been the trigger for the emergence of another new pathogen in the 1990s. Up until then, Cladobotryum dendroides was an occasional pathogen of crops, usually late in the cycle, but in the 1990s serious cobweb epidemics started to occur, first in Europe then later in Australia and United States. Close examination of the organisms associated with the epidemics revealed that C. dendroides was not the major cause but a fungicide-resistant strain of C. mycophilum (McKay et al. 1999). Although benzimidazole-sensitive C. mycophilum was also occasionally recorded from diseased crops, most of the problems were associated with benzimidazole-resistant isolates. These appeared to differ in many respects to the normal C. mycophilum in having a faster growth rate, more profuse and earlier sporulation, no distinct odor and spores which were regularly two, three and four-celled rather than the two celled spores characteristic of C. myco-philum (Adie, 2000, Grogan & Gaze, 2000).

The widespread use of benzimidazole fungicides to control cobweb and other diseases would have facilitated the emergence of a resistant strain. The shift at this time to using wetter casings, made from freshly harvested deep-dug peats, would have provided an ideal moist environment for cobweb spores to germinate. Epidemiological research indicated that the disease was spread very rapidly through mushroom houses when sporulating areas of disease were disturbed by watering or when applying salt to kill it. Control can be achieved however by carefully covering diseased areas with a damp paper towel prior to salting so as to prevent spores from entering the air stream (Adie et al., 2006).

Mushroom Virus X (MVX) is an enigmatic disease that emerged in the late 1990s causing crop delay, pinning disruption, poor quality and occasionally brown or off-colored mushrooms. The symptoms were consistently associated with a variable number of viral dsRNAs (Gaze et al, 2000). It is difficult and time consuming to characterize the exact aetiology of MVX-associated cropping problems, however the symptoms are transmitted in conjunction with MVX dsRNAs (Grogan et al., 2005).

MVX is unlike La France virus in that La France is most problematical when virus infected spores or mycelium infect the crop at spawning and is less problematical if infection takes place later. In contrast, epidemiological research indicates that MVX infected mycelium can cause severe effects when minute quantities of infected mycelium are introduced at either spawning or casing. Further experiments indicate that the expression of the brown mushroom symptom most often occurs when infection takes place within a narrow window of opportunity. Early infection of a crop often produces no brown mushroom symptoms whereas infection of a crop at casing time produces the brown symptomatic mushrooms more consistently. This suggests a complex interaction between the infective agent (dsRNAs?) and the actively differentiating tissue within the mushroom cap.

The absence of symptomatic mushrooms in an "infected" crop means that ultimate control of the problem may be compromised, as growers will be unaware that there is a potential problem on the farm. MVX was brought under control in Britain through improvements in farm hygiene aimed at preventing the contamination of crops with potentially infected spores and mycelial debris at spawning or casing. In Ireland, however the brown mushroom symptom still persists and the transient nature of its expression indicates that there is still a reservoir of infective material within the industry.

Recent research from France (Largeteau & Savoie, 2008) indicates that some Verticillium fungicola var. fungicola isolates in Europe are more aggressive than others, however V. fungicola var aleophilum from American appears to be more aggressive than European isolates (Largeteau et al. 2004). A Verticillium fungicola isolate identified in Mexico in 2002 appears to be var. fungicola, like European isolates, and the authors raise the question about the possibility of it having been introduced into Mexico on machinery originating in Europe. The spread of pathogens from one continent to another through imported goods and machinery is not new but as international trade increases, it increases the risk of unwanted introductions of pathogens.

Recently a highly aggressive Verticillium isolate has been isolated in Australia that does not appear to be controlled by prochloraz (A. Clift, pers. comm.). It remains to be seen if more aggressive Verticillium isolates become mores wide-spread in the mushroom growing world. In the absence of an effective fungicide to control an aggressive Verticillium strain more care will be needed in identifying initial outbreaks of the disease and dealing with them quickly before any watering is done. Verticillium spores are readily dispersed in water and are spread by water splashed onto the surrounding casing, structures and growing room floors. Contaminated floor debris will become integrated into the dust fraction on the farm and could be spread further by wind and air movements. Power washing dirty areas near casing storage areas or when casing is in operation will facilitate the spread of contaminated debris in the fine mist generated by power washing. Thus water use needs to be critically evaluated when severe outbreaks of Verticillium occur.

Conclusions

As the mushroom industry is faced with fewer chemicals to control disease outbreaks, and with new and evolving pathogens emerging, growers increasingly will be reliant on rapid identification and containment of disease outbreaks as the first line of defence. Epidemiological research produced by mushroom scientists around the world will be invaluable as a source of information on the best way specific pathogens are spread and transmitted around a farm. Ultimately, excellent hygiene standards (disinfection, cook-out, foot-dips, door-seals, filters, fly-control) will be required across the board, every day for every crop, to prevent a build-up of pathogen propagules around the farm.

New chemicals will be few and far between, given the rigorous costs and requirements for registering new products and the increasing consumer- and retailer-driven demands for reduced pesticide use. Biological control products are likely to be more acceptable but may not be as effective as traditional chemicals. Collaborative research projects between the major mushroom producing countries may be a way forward to identify and register any products that appear to offer some benefit. The recently formed International Mushroom Diagnostic group aims to share knowledge on mushroom disease diagnostics and this group is an excellent forum to progress international collaborative projects and to disseminate knowledge.

References

Adie, B.A.T. (2000). The biology and epidemiology of Cobweb disease

pathogen (Cladobotryum spp. infecting the cultivated mushroom (Agaricus bisporus). Ph.D. Thesis, Imperial College, University of London, UK.

Adie, B.A.T., Grogan, H., Archer, S. & Mills, P. (2006). Temporal and spatial dispersal of Cladobotryum conidia in the controlled environment of a mushroom growing room. Appl. Env. Microbiol 72, 7212-7217.

Dyer, P.S., Hansen, J., Delaney, A. & Lucas, J.A. (2000). Genetic control of Resistance to the sterol 14a-Demethylase inhibitor fungicide prochloraz in the cereal eyespot pathogen Tapesia yallundae. Appl. Env. Microbiol. 66, 4599-4604.

Fergus, C.L., Sinden, J.W., Schisler, L.C & Sigel, E.M. (1963). Possible detrimental effect of Pythium artotrogos on the cultivated mushroom. Phytopathology 53, 1360-1362.

Fletcher, J.Y. & Yarham, D.J. 1976. The incidence of benomyl tolerance in Verticillium fungicola, Mycogone perniciosa and Hypomyces rosellus in mushroom crops. Ann. Appl Biol 84, 343-353.

Fletcher, J.T., Connolly, G., Mountfield, EX & Jacobs, L. (1980). The disappearance of benomyl from mushroom casing. Ann. Appl. Biol. 95, 73-82.

Fletcher, J.T., Smewin, B.J. & O'Brien, A. (1990) Pythium oligandrum associated with a cropping disorder of Agaricus bisporus. Plant Pathology 39, 603-605.

Gaze, R.H., Calvo-Bado, L., Challen, M.P., Adie, B.A.T. & Romaine, C.P. (2000). A new virus disease of Agaricus bisporus? Mush. Sci. XV, 701-705.

Gea, F.J., Navarro, M.J. & Tello, J.C. 2005. Reduced sensitivity of the mushroom pathogen Verticillium fungicola to prochloraz-manganese in vitro. Mycol Res. 109, 741-745

Grogan, H.M. 2008. Changes and challenges for the Irish mushroom Industry. Mushroom Business 28, 22-23.

Grogan, H.M. & Gaze, R.H. 2000. Fungicide resistance among Cladobotryum spp. - causal agents of cobweb disease of the edible mushroom Agaricus bisporus. Mycol. Res. 104, 357-364.

Grogan, H. M., Keeling, C. & Jukes, A. A. (2000). In vivo response of the mushroom pathogen Verticillium fungicola (dry bubble) to prochloraz-manganese. Proceedings Brighton Crop Protection Conference - Pests and Diseases 2000, pp 273-278.

Grogan, H.M., Gaze, R.H. & Holcroft, S. (2005). Viral dsRNAs in Agaricus bisporus: Transmission, symptom expression and control. Acta Edulis Fungi, 12, 363-367.

Kligman, A.M. (1950). Handbook of Mushroom Culture. 2nd Edition. J.B. Swayne, Publisher, Kennet Square, Pennsylvania, USA.

Largeteau, M., Mata, G., Savoie, J.M. (2004). Verticillium fungicola v fungicola affects Agaricus bisporus cultivation in Mexico. FEMS Microbiol. Lets 236, 191-196.

Largeteau, M. and Savoie, J.M. (2008) Effect of the fungal pathogen Verticillium fungicola on fruiting initiation of its host, Agaricus bisporus. Mycol. Res. 112, In press.

McKay, G.J., Egan, D., Morris, E., Scott, C. & Brown, A.E. (1999). Genetic and morphological characterization of Cladobotryum species causing Cobweb disease of mushrooms. Appl. Env. Microbiol 65, 606-610.

Morris, E., Doyle, O. & Clancy, K.J. (1995). A profile of Trichoderma species. Mushroom compost production. Mush. Sci. XVI 611-618.

Papadopoulos, G. (2006). The fate of prochloraz in mushroom casing. Ph.D. Thesis, University of Reading, UK.

Rinker, D.L. & Alm, G. (2000). Management of green mould disease in Canada. Mush. Sci. XV, 617-623.

Romaine, C.P.D, Royse, D.J. & Schlagnhaufer. (2005). Superpathogenic Trichoderma resistant to TopsinM found in Pennsylvania and Delaware. Mush. News 53, 6-9.

Schisler, L.C., Sinden, J.W. & Sigel, E.M. (1967). Etiology, symptomology and epidemiology of a virus disease of cultivated mushrooms. Phytopathology 57, 519-526.

Sinden, J.W. & Hauser, E. 1950. Report on two new mushroom diseases. Mush. Sci I. 96-100.

Yarden, O., Salomon, R., Katan, J. & Aharonson, N. (1990). Involvement of fungi and bacteria in enhanced and nonenhanhanced biodegradation of carbendazim and other benzimidazole compounds in soil. Can. J. Microbiol, 36, 15-23.

Footnote: Teagasc is the agriculture and food development authority in Ireland. Its mission is to support science-based innovation in the agri-food sector and the broader bioeconomy that will underpin profitability, competitiveness and sustainability.

Helen Grogan Ph. D.

Teagasc Kinsealy Research Center

Dublin, Ireland heten.grogan@teagasc.ie

Presented at the 6th International Conference on Mushroom Biology & Mushroom Products

Bonn, Germany, Sept. 29 - Oct. 3, 2008

Editor's Note: Prochloraz is a chemical never registered for use in the United States.
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Title Annotation:pest control
Author:Grogan, Helen
Publication:Mushroom News
Date:Apr 1, 2009
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