Disease control by chemical and biological fungicides in cultivated mushrooms: button mushroom, oyster mushroom and shiitake

  • Ivana S Potočnik Institute of Pesticides and Environmental Protection, Banatska 31b, POB 163, 11080 Belgrade
  • Miloš Stepanović Institute of Pesticides and Environmental Protection, Banatska 31b, POB 163, 11080 Belgrade
  • Emil Rekanović Institute of Pesticides and Environmental Protection, Banatska 31b, POB 163, 11080 Belgrade
  • Biljana Todorović Institute of Pesticides and Environmental Protection, Banatska 31b, POB 163, 11080 Belgrade
  • Svetlana Milijašević-Marčić Institute of Pesticides and Environmental Protection, Banatska 31b, POB 163, 11080 Belgrade
Keywords: Fungicides, Biofungicides, Edible mushrooms,

Abstract


The most commonly cultivated basidiomycetes worldwide and in Serbia are button mushroom (Agaricus bisporus), oyster mushroom (Pleurotus sp.) and shiitake (Lentinus edodes). Production of their fruiting bodies is severely afflicted by fungal, bacterial, and viral pathogens that are able to cause diseases which affect yield and quality. Major A. bisporus fungal pathogens include Mycogone perniciosa, Lecanicillium fungicola, and Cladobotryum spp., the causal agents of dry bubble, wet bubble, and cobweb disease, respectively. Various Trichoderma species, the causal agents of green mould, also affect all three kinds of edible mushrooms. Over the past two decades, green mould caused by T. aggressivum has been the most serious disease of button mushroom. Oyster mushroom is susceptible to T. pleurotum and shiitake to T. harzianum. The bacterial brawn blotch disease, caused by Pseudomonas tolaasii, is distributed globally. Disease control on mushroom farms worldwide is commonly based on the use of fungicides. However, evolution of pathogen resistance to fungicides after frequent application, and host sensitivity to fungicides are serious problems. Only a few fungicides are officially recommended in mushroom production: chlorothalonil and thiabendazol in North America and prochloraz in the EU and some other countries. Even though decreased sensitivity levels of L. fungicola and Cladobotryum mycophilum to prochloraz have been detected, disease control is still mainly provided by that chemical fungicide. Considering such resistance evolution, harmful impact to the environment and human health, special attention should be focused on biofungicides, both microbiological products based on Bacillus species and various natural substances of biological origin, together with good programs of hygiene. Introduction of biofungicides has created new possibilities for crop protection with reduced application of chemicals.

Author Biographies

Ivana S Potočnik, Institute of Pesticides and Environmental Protection, Banatska 31b, POB 163, 11080 Belgrade
Laboratory of Applied Phytopathology, Senior Research Associate
Miloš Stepanović, Institute of Pesticides and Environmental Protection, Banatska 31b, POB 163, 11080 Belgrade
Laboratory of Applied Phytopathology, Research Associate
Emil Rekanović, Institute of Pesticides and Environmental Protection, Banatska 31b, POB 163, 11080 Belgrade
Laboratory of Applied Phytopathology, Senior Research Associate
Biljana Todorović, Institute of Pesticides and Environmental Protection, Banatska 31b, POB 163, 11080 Belgrade
Laboratory of Applied Phytopathology, Senior Research Associate
Svetlana Milijašević-Marčić, Institute of Pesticides and Environmental Protection, Banatska 31b, POB 163, 11080 Belgrade
Laboratory of Applied Phytopathology, Senior Research Associate

References

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

Angelini, P., Pagiotti, R., & Granetti, B. (2008). Effect of antimicrobial activity of Melaleuca alternifolia oil on antagonistic potential of Pleurotus species against Trichoderma harzianum in dual culture. World Journal of Microbiology and Biotechnology, 24, 197-202.

Bech, K., & Riber-Rasmussen, C. (1967). Experiments with soil disinfectants for casing material and their effect on yield. Mushroom Science, 6, 515-521.

Beyer, D.M., & Kremser, J.J. (2004). Evaluation of fungicide tolerance and control for three fungal diseases of mushrooms. In: Romaine, C.P., Keil, C.B., Rinker, D.L., Royse, D.J. (Eds), Science and cultivation of edible and medicinal fungi. Mushroom Science XVI. (pp 521-529). Pennsylvania, PA, USA: Penn State University, University Park.

Bhatt, N. & Sing, R.P. (1992). Cobweb disease of Agariucus bisporus: Incidence, losses and effective management. Indian Journal of Mycology and Plant Pathology, 22, 178-181.

Bollen, G.J., & van Zaayen, A. (1975). Resistance to benzimidazole fungicides in pathogenic strains of Verticillium fungicola. Netherlands Journal of Plant Pathology, 81, 157-167.

Bonnen, A.M., & Hopkins, C. (1997). Fungicide resistance and population variation in Verticillium fungicola, a pathogen of the button mushroom, Agaricus bisporus. Mycological Research, 101, 89-96.

Chrysayi-Tokousbalides, M., Kastanias, M.A., Philippoussis, A., & Diamantopoulou, P. (2007). Selective fungitoxicity of famaxadone, tebuconazole and trifloxystrobin between Verticillium fungicola and Agaricus bisporus. Crop Protection, 26, 469-475.

Delp, C.J. (1987). Benzimidazole and releted fungicides. In: H. Lyr (Ed.), Modern selective fungicides: Properties, applications, mechanisms of action (pp 233-244). New York, USA: Longman Scientific and Technical; John Wiley and Sons.

Fletcher, J.T., Connolly, G., Mountfield, E.I., & Jacobs, L. (1980). The disappearance of benomyl from mushroom casing. Annals of Applied Biology, 95, 73-82.

Fletcher, J. T., Hims, M. J., & Hall, R. J. (1983). The control of bubble diseases and cobweb disease of mushrooms with prochloraz. Plant Pathology, 32(2), 123-131.

Forer, L.B., Wuest, P.J., & Wagner, U.R. (1974). Occurrence and economic impact of fungal diseases of mushrooms in Pennsylvania. Plant Diesease Reporter, 54, 987-991.

Gaze, R.H. (1996). The past year. Dactylium or Cobweb. Mushroom Journal, 552, 24-25.

Gaze, R.H., & Fletcher, J.T. (1975). ADAS survey of mushroom diseases and fungicide usage 1974/75. Mushroom Journal, 35, 370-376.

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

Gea, F.J., Tello, J.C., & Honrubia, M. (1996). In vitro sensitivity of Verticillium fungicola to selected fungicides. Mycopathologia, 136, 133-137.

Geels, F.P., Hessen, L.P.W., & van Griensven, L.J.L.D. (2008). Brown discoloration of mushrooms caused by Pseudomonas agarici. Journal of Phytopathology, 140, 249-259.

Grogan, H.M. (2006). Fungicide control of mushroom cobweb disease caused by Cladobotryum strains with different benzimidazole resistance profiles. Pest Management Science, 62(2), 153-161.

Grogan, H.M. (2008). Challenges facing mushroom disease control in the 21st century. In Lelley, J.I., Buswell, J.A. (Eds.), Proceeding of the Sixth International Conference on Mushroom Biology and Mushroom Products (pp 120-127). Bonn, Germany: WSMBMP.

Grogan, H.M., & Gaze, R.H. (2000). Fungicide resistance among Cladobotryum spp. – causal agents of cobweb disease of the edible mushroom Agaricus bisporus. Mycological Research, 104(3), 357-364.

Grogan, H.M., & Jukes, A.A. (2003). Persistence of the fungicides thiabendazole, carbendazim and prochloraz-Mn in mushroom casing soil. Pest Management Science, 59, 1225-1231.

Grogan, H.M., Keeling, C. & Jukes, A.A. (2000). In vivo response of the mushroom pathogen Verticillium fungicola (dry bubble) to prochloraz-manganese. In: Proceedings of Brighton Crop Protection Conference: Pests & Diseases (1, pp 273-278). Farnham, Surrey, UK: BCPC.

Hatvani, L., Kocsub・ S., Menczinger, L., Antal, Z., Szekeres, A., Druzhina, I.S., … Kredics, L. (2008). The green mould disease global threat to the cultivation of oyster mushroom (Pleurotus ostreatus): a review. In: M. Van Greuning (Ed.), Science and cultivation of edible and medicinal fungi: Mushroom Science XVII, Proceeding of the 17th Congress of the International Society for Mushroom Science (CD-ROM, pp 485-495). Cape Town, South Africa: ISMS.

Kosanović, D., Potočnik, I., Duduk, B., Vukojević, J., Stajić, M., Rekanović, E., & Milijašević-Marčić, S. (2013). Trichoderma species on Agaricus bisporus farms in Serbia and their biocontrol. Annals of Applied Biology, 163, 218-230.

Kosanović, D., Potočnik, I., Vukojević, J., Stajić, M., Rekanović, E., Stepanović, M., & Todorović, B. (2015). Fungicide sensitivity of Trichoderma spp. from Agaricus bisporus farm in Serbia. Journal of Environmental Science and Health, Part B: Pesticides, Food Contaminants, and Agricultural Wastes, 50, 607-613.

Krupke, O.A., Castle, A.J., & Rinker, D.L. (2003). The North American mushroom competitor, Trichoderma aggressivum f. aggressivum, produces antifungal compounds in mushroom compost that inhibit mycelial growth of the commercial mushroom Agaricus bisporus. Mycological Research, 107, 1467-1475.

Levanon, D., Danai, O., & Masaphy, S. (1988). Chemical and physical parameters in recycling organic wastes for mushroom production. Biological Wastes, 26, 341-348.

McKay, G. L., Egan, D., Morris, E., & Brown, A.E. (1998). Identification of benzimidazole resistance in Cladobotryum dendroides using a PCR-based method. Mycological Research 102, 671-676.

Milijašević-Marčić, S., Todorović, B. Potočnik, I., Stepanović, M. & Rekanović, E. (2012): First report of Pseudomonas tolaasii on Agaricus bisporus in Serbia. Phytoparasitica, 40, 299-303.

Olivier, J.M., Mamoun, M., & Munsh, P. (1997). Standardization of a method to assess mushroom blotch resistance in cultivated and wild Agaricus bisporus strains. Canadian Journal of Plant Pathology, 19, 36-42.

Papadopoulos, G. (2006). The fate of prochloraz in mushroom casin - PhD thesis, University of Reading, UK.

Potočnik I., Milijašević S., Rekanović E., Todorović B., & Stepanović, M. (2008). Sensitivity of Verticillium fungicola var. fungicola, Mycogone perniciosa and Cladobotryum spp. to fungicides in Serbia. In: M. Van Greuning (Ed.), Science and cultivation of edible and medicinal fungi: Mushroom Science XVII, Proceeding of the

th Congress of the International Society for Mushroom Science (pp 615-627). Cape Town, South Africa: ISMS.

Potočnik I., Vukojević, J., Stajić, M., Rekanović, E., Milijašević, S., Stepanović, M., & Todorović, B. (2009b). Toxicity of fungicides with different modes of action to Cladobotryum dendroides and Agaricus bisporus. Journal of Environmental Science and Health, Part B, 44, 823-827.

Potočnik I., Vukojević, J., Stajić, M., Rekanović, E., Milijašević, S., Todorović, B., & Stepanović, M. (2009a). In vitro toxicity of selected fungicides from the groups of benzimidazoles and demethylation inhibitors to Cladobotryum dendroides and Agaricus bisporus. Journal of Environmental Science and Health, Part B, 44, 365-370.

Potočnik I., Vukojević, J., Stajić, M., Rekanović, E., Stepanović, M., Milijašević, S., & Todorović, B. (2010a). Toxicity of biofungicide Timorex 66 EC to Cladobotryum dendroides and Agaricus bisporus. Crop Protection, 29, 290-294.

Potočnik, I., Vukojević, J., Stajić, M., Tanović, B., & Rekanović, E. (2010b). Sensitivity of Mycogone perniciosa, pathogen of culinary-medicinal button mushroom Agaricus bisporus (J. Lange) Imbach (Agaricomycetideae) to selected fungicides and essential oils. Internаtional Journal of Medicinal Mushrooms, 12(1), 91-98.

Potočnik, I., Vukojević, J., Stajić, M., Tanović, B., & Todorović, B. (2008b). Fungicide sensitivity of selected Verticillium fungicola isolates from Agaricus bisporus farms. Archives of Biological Sciences, 60(1), 151-158.

Potočnik, I., Tanović, B., Milijašević, S., Rekanović, E., & Todorović, B. (2005). Response of the mushroom pathogen Verticillium fungicola (Preuss) Hasebrauk (dry bubble) to some essential oils. (ESNA Meeting, Amiens, France). Revue de Cytologie et de Biologie Végétales – Le Botaniste, 28, 388-392.

Rekanović, E., Milijašević, S., Todorović, B., & Potočnik, I. (2007). Posibilities of biological and chemical control of Verticillium Wilt in pepper. Phytoparasitica, 35, 436-441.

Rinker, D.L., & Alm, G. (2008). Management of casing Trichoderma using fungicides. In: M. Van Greuning (Ed.), Science and cultivation of edible and medicinal fungi: Mushroom Science XVII, Proceeding of the 17th Congress of the International Society for Mushroom Science (pp. 496-509). Cape Town, South Africa: ISMS.

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

Romaine, C.P., Royse, D.J., & Schlagnhaufer, C. (2008). Emergence of benzimidazole-resistant green mould Trichoderma aggressivum, on cultivated Agaricus bisporus in North America. In: M. Van Greuning (Ed.), Science and cultivation of edible and medicinal fungi: Mushroom Science XVII, Proceeding of the 17th Congress of the International Society for Mushroom Science (pp 510-523). Cape Town, South Africa: ISMS.

Savoie, J.-M., Iapicco, R., & Largeteau-Mamoun, M.L. (2001). Factors influencing the competitive saprophytic ability of Trichoderma harzianum Th2 in mushroom (Agaricus bisporus) compost. Mycological Research, 105, 1348-1356.

Soković, M., & van Griensven, J.L.D. (2006). Antimicrobial activity of essential oils and their components against the three major pathogens of the cultivated button mushroom, Agaricus bisporus. European Journal of Plant Pathology, 116, 211-224.

Soković, M., Vukojević, J., Marin, P., Brkić, D., Vajs, V., & van Griensven, J.L.D. (2009). Chemical composition of essential oils of Thymus and Mentha species and their antifungal activities. Molecules, 14, 238-249.

Solomon, J.M., Beelman, R.B., & Bartley, C.E. (1991). Addition of calcium chloride and stabilized chlorine dioxide to irrigation water to improve quality and shelf life of Agaricus bisporus. Mushroom Science, 13, 695-701.

Tanović, B., Potočnik, I., Delibašić, G., Ristić, M., Kostić, M., & Marković, M. (2009). In vitro effect of essential oils from aromatic and medicinal plants on mushroom pathogens: Verticillium fungicola var. fungicola, Mycogone perniciosa, and Cladobotryum sp. Archives of Biological Sciences, 61(2), 231-238.

Todorović, B., Milijašević-Marčić, S., Potočnik, I., Stepanović, M., Rekanović, E., Nikolić-Bujanović, Lj., & Čekerevac, M. (2012): In vitro activity of antimicrobial agents against Pseudomonas tolaasii, pathogen of cultivated button mushroom. Journal of Environmental Science and Health, Part B: Pesticides, Food Contaminants & Agricultural Wastes, 47(3), 175-179.

van Zaayen, A. (1979). Daconil and intermediate mushroom cultivars. Champignoncultuur, 23, 217.

van Zaayen, A., & van Adrichem, J.C.J. (1982). Prochloraz for control of fungal pathogens of cultivated mushrooms. Netherlands Journal of Plant Pathology, 88(5), 203-213.

Védie, R., & Rousseau, T. (2008). Serenade biofungicide: une innovation mjeure dans les champignonnières françaises pour lutter contre Trichoderma aggressivum, agent de la moisissure verte du compost. La Lettre du CTC, 21, 1-2.

Visscher, H.R. (1988). Casing soil. In van Griensven, L.J.L.D. (Ed.), The cultivation of mushrooms (pp. 73-90). Waalwijk, Holland: Grafidrukkerij Waalwijk.

Ware, W.M. (1933). Annual Report, Department of Mycology. Journal of South Eastern Agricultural College (Wye, Kent, UK), 31, 13-21.

Wong, W.C., & Preece, T.F. (1987). Sources of Verticillium fungicola on a commercial mushroom farm in England. Plant Pathology, 36(4), 577-582.

Woo, S.L., di Benedetto, P., Senatore, M., Abadi, K., Gigante, S., Soriente, I., ... Lorito, M. (2004). Identification and charactrization of Trichoderma species aggressive to Pleurotus in Italy. Journal of Zhejiang University (Agriculture and Life Sciences), 30, 469-470.

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

Zare, R., & Gams, W. (2008). A revision of the Verticillium fungicola species complex and its affinity with the genus Lecanicillium. Mycological Research, 112, 811-824.

Published
2016/02/18
Section
Review Paper