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Biological Control of Microbial Pathogens in Edible Mushrooms

  • Gail M. Preston
  • Jaime CarrascoEmail author
  • Francisco J. Gea
  • María J. Navarro
Chapter
Part of the Fungal Biology book series (FUNGBIO)

Abstract

The cultivation of edible mushrooms is susceptible to suffer certain diseases caused by a number of diseases and pests. Fungal, bacterial and mushroom flies conduct to significant reductions of productivity and a substantial impact on mushroom quality. To minimize losses, improve productivity and achieve healthier food, the biological treatment is emerging as a real alternative to reduce the over use of chemical pesticides in this agronomical activity. The present chapter compiles the current knowledge to effectively execute biocontrol of microbial pathogens harmful for the mushroom crops, in the form of bioactive compounds from plant extracts, bacterial strains showing antagonism to the causative agent or nematodes infesting fly larvae. Besides, recommendations in respect to the tools required for the design of integrated management programs for the control of diseases and pests are discussed.

Keywords

Fungi Bacteria Pests Biocontrol agents Bioactive compounds Integrated management 

Notes

Acknowledgement

This article has been funded by the European Union’s Horizon 2020 research and innovation programme under the Marie Sklodowska-Curie grant agreement No 742966. Some of the pictures attached in the text have been kindly loaned by CIES (Antonio Martínez Carrasco).

References

  1. Aslani MA, Harighi B, Abdollahzadeh J (2018) Screening of endofungal bacteria isolated from wild growing mushrooms as potential biological control agents against brown blotch and internal stipe necrosis diseases of Agaricus bisporus. Biol Control 119:20–26CrossRefGoogle Scholar
  2. Bakkali F, Averbeck S, Averbeck D, Idaomar M (2008) Biological effects of essential oils-a review. Food Chem Toxicol 46(2):446–475PubMedCrossRefGoogle Scholar
  3. Bartlett GR, Keil CBO (1997) Identification and characterization of a permethrin resistance mechanism in populations of the fungus gnat Lycoriella mali (Fitch) (Diptera: Sciaridae). Pest Biochem Physiol 58:173–181CrossRefGoogle Scholar
  4. Berendsen RL, Baars JJ, Kalkhove SI, Lugones LG, Wösten HA, Bakker PA (2010) Lecanicillium fungicola: causal agent of dry bubble disease in white-button mushroom. Mol Plant Pathol 11(5):585–595PubMedGoogle Scholar
  5. Berendsen RL, Kalkhove SI, Lugones LG, Baars JJ, Wösten HA, Bakker PA (2012) Effects of fluorescent Pseudomonas spp. isolated from mushroom cultures on Lecanicillium fungicola. Biol Control 63:210–221CrossRefGoogle Scholar
  6. Beyer DM, Pecchia JA, Paley K (2016) Evaluation of bio-fungicides for the control of fungal diseases on Agaricus bisporus. In: Baars JJP, Sonnenberg AMS (eds) Proceedings of the 19th international society for mushroom science (ISMS) conference, pp 86–90Google Scholar
  7. Carrasco J, Navarro MJ, Santos M, Diánez F, Gea FJ (2016) Incidence, identification and pathogenicity of Cladobotryum mycophilum, causal agent of cobweb disease on Agaricus bisporus mushroom crops in Spain. Ann Appl Biol 168(2):214–224CrossRefGoogle Scholar
  8. Carrasco J, Navarro MJ, Gea FJ (2017) Cobweb, a serious pathology in mushroom crops: a review. Span J Agric Res 15(2):19CrossRefGoogle Scholar
  9. Coles P (2002) Integrated pest management in mushroom production: specific control techniques: exclusion. In: MUSHROOM integrated pest management. The Pennsylvania State University, State College, pp 21–26Google Scholar
  10. Diamantopoulou P, Philippoussis A, Lahouvaris L, Parissopoulos G (2012) The effect of calcium chloride irrigation on yield and quality of Agaricus bisporus. In: Proceeding of the 15th congress of ISMS. Rotterdam, Netherlands. pp. 390–393Google Scholar
  11. Diánez F, Santos M, Boix A, De Cara M, Trillas I, Avilés M, Tello JC (2006) Grape marc compost tea suppressiveness to plant pathogenic fungi: role of siderophores. Compost Sci Util 14(1):48–53CrossRefGoogle Scholar
  12. Dos Santos TL, Belan LL, Zied DC, Dias ES, Alves E (2017) Essential oils in the control of dry bubble disease in white button mushroom. Cienc Rural 47, 05:e20160780Google Scholar
  13. Erler F, Polat E, Demir H, Cetin H, Erdemir T (2009a) Control of the mushroom phorid fly, Megaselia halterata (wood), with plant extracts. Pest Manag Sci 65:144–149PubMedCrossRefGoogle Scholar
  14. Erler F, Polat E, Demir H, Cetin H, Erdemir T (2009b) Evaluation of microbial products for the control of the mushroom phorid fly, Megaselia halterata (wood). J Entomol Sci 44:89–97CrossRefGoogle Scholar
  15. Fletcher JT, Gaze RH (2008) Mushroom pest and disease control:A color handbook. Manson Publishing Ltd. Academic Press, San Diego, p 192Google Scholar
  16. Foulongne-Oriol M, Minvielle N, Savoie JM (2011) QTL for resistance to Trichoderma lytic enzymes and metabolites in Agaricus bisporus. In; Proceedings of the 7th international conference on mushroom biology and mushroom products (ICMBMP7), Arcachon, France. vol 2. pp 17–25Google Scholar
  17. Foulongne-Oriol M, Rodier A, Savoie JM (2012) Relationship between yield components and partial resistance to Lecanicillium fungicola in Agaricus bisporus assessed by QTL mapping. Appl Environ Microbiol 78:2435–2442PubMedPubMedCentralCrossRefGoogle Scholar
  18. Fu Y, Wang X, Li D, Liu Y, Song B, Zhang C et al (2016) Identification of resistance to wet bubble disease and genetic diversity in wild and cultivated strains of Agaricus bisporus. Int J Mol Sci 17(10):1568PubMedCentralCrossRefGoogle Scholar
  19. Gea FJ, Navarro MJ (2017) Mushroom diseases and control. In: Cunha D, Pardo-Gimenez A (eds) Edible and medicinal mushrooms: Technology and applications. Wiley Blackwell Ltd, Chichester, pp 239–259CrossRefGoogle Scholar
  20. Gea FJ, Navarro MJ, Tello JC (2009) Potential application of compost teas of agricultural wastes in the control of the mushroom pathogen Verticillium fungicola. J Plant Dis Protect 116(6):271–273CrossRefGoogle Scholar
  21. Gea FJ, Tello JC, Navarro MJ (2010) Efficacy and effects on yield of different fungicides for control of wet bubble disease of mushroom caused by the mycoparasite Mycogone perniciosa. Crop Prot 29(9):1021–1025CrossRefGoogle Scholar
  22. Gea FJ, Santos M, Diánez F, Tello JC, Navarro MJ (2012) Effect of spent mushroom compost tea on mycelial growth and yield of button mushroom (Agaricus bisporus). World J Microbiol Biotechnol 28(8):2765–2769PubMedCrossRefGoogle Scholar
  23. Gea FJ, Carrasco J, Diánez F, Santos M, Navarro MJ (2014) Control of dry bubble disease (Lecanicillium fungicola) in button mushroom (Agaricus bisporus) by spent mushroom substrate tea. Eur J Plant Pathol 138:711–720CrossRefGoogle Scholar
  24. Geels FP, Van de Geijn J, Rutjens AJ (1988) Pests and diseases. In: Griensven V, Interlingua LJLD (eds) The cultivation of mushrooms, Sussex, pp 361–422Google Scholar
  25. Geösel A, Szabó A, Akan O, Szarvas J (2014) Effect of essential oils on mycopathogens of Agaricus bisporus. In: Proceedings of 8th international conference on mushroom biology and mushroom products (ICMBMP8), New Delhi, pp 530–535Google Scholar
  26. Glamočlija J, Sokovic M, Vukojevic J, Milenkovic I, Tesevic V, Van Griensven LJLD (2007) Effect of oregano essential oil on infection of Agaricus bisporus by Mycogone perniciosa in vitro and in the mushroom growing unit. Int J Med Mushrooms 9(3/4):300Google Scholar
  27. Glamočlija J, Sokovic M, Grubisic D, Vukojevic J, Milinekovic I, Ristic M (2009) Antifungal activity of Critmum maritimum essential oil and its components against mushroom pathogen Mycogone perniciosa. Chem Nat Compd 45(1):96–97CrossRefGoogle Scholar
  28. Grewal PS, Richardson PN, Collins G, Edmondson RN (1992) Comparative effects of Steinernema feltiae (Nematoda: Steinernematidae) and insecticides on yield and cropping of the mushroom Agaricus bisporus. Ann Appl Biol 121:511–520CrossRefGoogle Scholar
  29. Jess S, Bingham JFW (2004) Biological control of sciarid and phorid pests of mushroom with predatory mites from the genus Hypoaspis (Acari: Hypoaspidae) and the entomopathogenic nematode Steinernema feltiae. Bull Entomol Res 94:159–167PubMedCrossRefGoogle Scholar
  30. Kanchiswamy CN, Malnoy M, Maffei ME (2015) Bioprospecting bacterial and fungal volatiles for sustainable agriculture. Trends Plant Sci 20:206–211PubMedCrossRefGoogle Scholar
  31. Kim HH, Choo HY, Kaya HK, Lee DW, Lee SM, Jeon HY (2004) Steinernema carpocapsae (Rhabditida: Steinernematidae) as a biological control agent against the fungus gnat Bradysia agrestis (Diptera: Sciaridae) in propagation houses. Biocon Sci Technol 14:171–183CrossRefGoogle Scholar
  32. Kim MH, Park SW, Kim YK (2011) Bacteriophages of Pseudomonas tolaasii for the biological control of brown blotch disease. J Korean Soc Appl Biol Chem 54(1):99–104Google Scholar
  33. Kirk DJ, Keil CB (2001) Factors influencing efficacy of two- entomopathogenic nematodes used for fly control in commercial mushroom crops. Mush News 49:4–17Google Scholar
  34. Koppenhöfer AM, Grewal PS (2005) Compatibility and interactions with agrochemicals and other biocontrol agents. In: Nematodes as biocontrol agents, CABI Eds, pp 363–381CrossRefGoogle Scholar
  35. Kües U, Khonsuntia W, Subba S, Dörnte B (2018) Volatiles in communication of Agaricomycetes. In: Anke T, Schüfflerpp A (eds) Physiology and genetics. Springer, Cham, pp 149–212CrossRefGoogle Scholar
  36. Largeteau ML, Savoie JM (2010) Microbially induced diseases of Agaricus bisporus: biochemical mechanisms and impact on commercial mushroom production. Appl Microbiol Biotechnol 86(1):63–73PubMedCrossRefGoogle Scholar
  37. Leveau JH, Preston GM (2008) Bacterial mycophagy: definition and diagnosis of a unique bacterial–fungal interaction. New Phytol 177(4):859–876PubMedCrossRefGoogle Scholar
  38. Liu C, Sheng J, Chen L, Zheng Y, Lee DYW, Yang Y et al (2015) Biocontrol activity of Bacillus subtilis isolated from Agaricus bisporus mushroom compost against pathogenic fungi. J Agric Food Chem 63:6009–6018PubMedCrossRefGoogle Scholar
  39. Lomax KM (2007) Dew point temperature related to wet mushroom caps. Mushroom News 55(1):4–10Google Scholar
  40. Malpani MO, Rajput PR, Ghodile NG (2012) Effect of medicinally potential plant extracts and isolated ingredients on pathogen damaging mushroom cultivation in Vidarbha region of India. In: Proceeding of the 18th congress of ISMS. Beijing, China, pp 390–393Google Scholar
  41. Marín F, Santos M, Diánez F, Carretero F, Gea FJ, Yau JA, Navarro MJ (2013) Characters of compost teas from different sources and their suppressive effect on fungal phytopathogens. World J Microbiol Biotechnol 29(8):1371–1382PubMedCrossRefGoogle Scholar
  42. Mehrparvar M, Goltapeh EM, Safaie N, Ashkani S, Hedesh RM (2016) Antifungal activity of essential oils against mycelial growth of Lecanicillium fungicola var. fungicola and Agaricus bisporus. Ind Crop Prod 84:391–398CrossRefGoogle Scholar
  43. Milijašević-Marčić S, Stepanović M, Todorović B, Duduk B, Stepanović J, Rekanović E, Potočnik I (2017) Biological control of green mould on Agaricus bisporus by a native Bacillus subtilis strain from mushroom compost. Eur J Plant Pathol 148(3):509–519CrossRefGoogle Scholar
  44. Moquet F, Desmerger C, Mamoun M, Ramos-Guedes-Lafargue M, Olivier JM (1999) A quantitative trait locus of Agaricus bisporus resistance to Pseudomonas tolaasii is closely linked to natural cap color. Fungal Genet Biol 28:34–42PubMedCrossRefGoogle Scholar
  45. Navarro MJ, Gea FJ (2014) Entomopathogenic nematodes for the control of phorid and sciarid flies in mushroom crops. Pesq Agropec Bras 49(1):11–17CrossRefGoogle Scholar
  46. Navarro MJ, Carrasco J, Gea FJ (2014) Chemical and biological control of diptera in Spanish mushroom crops. In: Proceedings of 8th international conference on mushroom biology and mushroom products (ICMBMP8), New Delhi, pp 549–5556Google Scholar
  47. Navarro MJ, Gea FJ, Gonzalez AJ (2018) Identification, incidence and control of bacterial blotch disease in mushroom crops by management of environmental conditions. Sci Hort 2018 229:10–18CrossRefGoogle Scholar
  48. Pandin C, Le Coq D, Deschamps J, Védie R, Rousseau T, Aymerich S, Briandet R (2018) Complete genome sequence of Bacillus velezensis QST713: a biocontrol agent that protects Agaricus bisporus crops against the green mould disease. J Biotechnol 278:10–19PubMedCrossRefGoogle Scholar
  49. Payapanon A, Suthirawut S, Shompoosang S, Tsuchiya K, Furuya N, Roongrawee P et al (2011) Increase in yield of the straw mushroom (Vovariella volvacea) by supplement with Paenibacillus and Bacillus to the compost. J Fac Agric Kyushu U 56:249–254Google Scholar
  50. Potočnik I, Vukojević J, Stajić M, Rekanović E, Stepanović M, Milijašević S, Todorović B (2010) Toxicity of biofungicide Timorex 66 EC to Cladobotryum dendroides and Agaricus bisporus. Crop Prot 29:290–294CrossRefGoogle Scholar
  51. Regnier T, Combrinck S (2010) In vitro and in vivo screening of essential oils for the control of wet bubble disease of Agaricus bisporus. S African J Bot 76:681–685CrossRefGoogle Scholar
  52. Savoie JM, Foulongne-Oriol M, Barroso G, Callac P (2013) Genetics and genomics of cultivated mushrooms, application to breeding of agarics. In: Kempken F (ed) The mycota, agricultural applications, vol 11. Springer, Berlin, pp 3–33CrossRefGoogle Scholar
  53. Shamshad A (2010) The development of integrated pest management for the control of mushroom sciarid flies, Lycoriella ingenua (Dufour) and Bradysia ocellaris (Comstock), in cultivated mushrooms. Pest Manag Sci 66:1063–1074PubMedCrossRefGoogle Scholar
  54. Shamshad A, Clift AD, Mansfield S (2008) Toxicity of six commercially formulated insecticides and biopesticides to third instar larvae of mushroom sciarid, Lycoriella ingenua Dufour (Diptera: Sciaridae), in New South Wales, Australia. Aus J Entomol 47:256–260CrossRefGoogle Scholar
  55. Smith JE (2002) Dimilin resistance in mushroom sciarids. Mushroom J 626:15Google Scholar
  56. Soković M, Van Griensven LJ (2006) Antimicrobial activity of essential oils and their components against the three major pathogens of the cultivated button mushroom, Agaricus bisporus. Eur J Plant Pathol 116(3):211–224CrossRefGoogle Scholar
  57. Soler-Rivas C, Jolivet S, Arpin N, Olivier JM, Wichers HJ (1999) Biochemical and physiological aspects of brown blotch disease of Agaricus bisporus. FEMS Microbiol Rev 23(5):591–614PubMedCrossRefGoogle Scholar
  58. Sonnenberg AS, Baars JJ, Gao W, Visser RG (2017) Developments in breeding of Agaricus bisporus var. bisporus: progress made and technical and legal hurdles to take. Appl Microbiol Biot 101(5):1819–1829CrossRefGoogle Scholar
  59. Stanojević O, Milijašević-Marčić S, Potočnik I, Stepanović M, Dimkić I, Stanković S, Berić T (2016) Isolation and identification of Bacillus spp. from compost material, compost and mushroom casing soil active against Trichoderma spp. Arch Biol Sci 68:845–852CrossRefGoogle Scholar
  60. Tajalipour S, Hassanzadeh N, Khabbaz Jolfaee H, Heydari A, Ghasemi A (2014) Biological control of mushroom brown blotch disease using antagonistic bacteria. Biocontrol Sci Tech 24:473–484CrossRefGoogle Scholar
  61. Tanović B, Potočnik I, Stanisavljević B, Đorđević M, Rekanović E (2006) Response of Verticillium fungicola var. fungicola, Mycogone perniciosa and Cladobotryum sp. mushroom pathogens to some essential oils. Pestic Phytomed 21(3):231–237Google Scholar
  62. 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. Arch Biol Sci 61(2):231–237CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Gail M. Preston
    • 1
  • Jaime Carrasco
    • 1
    Email author
  • Francisco J. Gea
    • 2
  • María J. Navarro
    • 2
  1. 1.Department of Plant SciencesUniversity of OxfordOxfordUK
  2. 2.Centro de Investigación Experimentación y Servicios del Champiñón (CIES)CuencaSpain

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