Cobweb, a serious pathology in mushroom crops: A review

Jaime Carrasco, María-Jesús Navarro, Francisco J. Gea

Abstract


Cobweb is a fungal disease of commercially cultivated mushrooms. Several members of the ascomycete genus Cladobotryum sp. have been reported as causal agents. White button mushroom is the most frequently cited host, but a wide range of cultivated edible mushrooms suffer cobweb. The pathology causes production losses and reduces the crop surface available. The parasite produces a great number of harmful conidia that can be released easily and distributed throughout the mushroom farm to generate secondary points of infection. To prevent initial outbreaks, hygiene is of primary importance within the facilities dedicated to mushroom cultivation, while additional measures must be implemented to control and reduce cobweb if there is an outbreak, including chemical and biological methods. This review summarizes and discusses the knowledge available on the historic occurrence of cobweb and its impact on commercial mushroom crops worldwide. Causal agents, disease ecology, including the primary source of infection and the dispersal of harmful conidia are also reviewed. Finally, control treatments to prevent the disease from breaking out are discussed.

Keywords


Cladobotryum; fungal disease; dispersal; production losses; edible mushroom; control

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References


Abubaker KS, Sjaarda C, Castle AJ, 2013. Regulation of three genes encoding cell-wall-degrading enzymes of Trichoderma aggressivum during interaction with Agaricus bisporus. Can J Microbiol 59: 417-424. https://doi.org/10.1139/cjm-2013-0173

Adie BAT, 2000. The biology and epidemiology of the cobweb disease pathogen (Cladobotryum spp.) infecting the cultivated mushroom (Agaricus bisporus). PhD thesis, Imperial College, University of London.

Adie BAT, Grogan H, 2000. The liberation of cobweb (Cladobotryum mycophilum) conidia within a mushroom crop. Proc 15th Int Cong on the Science and Cultivation of Edible Fungi, pp: 595-600. Maastricht, Netherlands, 15-19 May.

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. Appl Environ Microbiol 72: 7212-7217. https://doi.org/10.1128/AEM.01369-06

Back CG, Kim YH, Jo WS, Chung H, Jung HY, 2010. Cobweb disease on Agaricus bisporus caused by Cladobotryum mycophilum in Korea. J Gen Plant Pathol 76: 232-235. https://doi.org/10.1007/s10327-010-0236-3

Back CG, Lee CY, Seo GS, Jung HY, 2012. Characterization of species of Cladobotryum which cause cobweb disease in edible mushrooms grown in Korea. Mycobiology 40: 189-194. https://doi.org/10.5941/MYCO.2012.40.3.189

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: 585-595. https://doi.org/10.1111/j.1364-3703.2010.00627.x

Beyer DM, Kremser JJ, 2004. Evaluation of fungicide tolerance and control for three fungal diseases of mushrooms. Mushroom science XVI: Science and cultivation of edible and medicinal fungi, pp. 421-429. Ed by Romaine CP, Keil CB, Rinker DL and Royse DJ. The Pennsylvania State University, USA.

Bhatt N, Singh RP, 2002. Cobweb disease of Agaricus bisporus: incidence, losses and effective management. Indian J Mycol Plant Pathol 22: 178-181.

Bora T, Ozaktan H, 2000. Biological control of some important mushroom diseases in Turkey by fluorescent Pseudomonads. Proc 15th Int Cong on the Science and Cultivation of Edible Fungi, pp: 689-693. Maastricht, Netherlands, 15-19 May.

Calonje M, Mendoza CG, Cabo AP, Bernardo D, Novaes-Ledieu M, 2000. Interaction between the mycoparasite Verticillium fungicola and the vegetative mycelial phase of Agaricus bisporus. Mycol Res104: 988-992. https://doi.org/10.1017/S0953756299002154

Carrasco J, 2016. Estudio de la telaraña del champiñón causada por Cladobotryum mycophilum en cultivos españoles. / Study of mushroom cobweb caused by Cladobotryum mycophilum in Spanish crops. 168 pp. PhD thesis, University of Castilla-La Mancha. http://hdl.handle.net/10578/9752

Carrasco J, Navarro MJ, Santos M, Diánez F, Gea FJ, 2016a. Incidence, identification and pathogenicity of Cladobotryum mycophilum, causal agent of cobweb disease on Agaricus bisporus mushroom crops in Spain. An Appl Biol 168: 214-224. https://doi.org/10.1111/aab.12257

Carrasco J, Navarro MJ, Santos M, Gea FJ, 2016b. Chemical control of mushroom cobweb disease caused by Cladobotryum mycophilum. Mushroom science XIX: Science and cultivation of edible and medicinal fungi, pp 448. Amsterdam (The Netherlands).

Carrasco, J, Navarro, MJ, Santos, M, Gea, FJ, 2017. Effect of five fungicides with different modes of action on cobweb disease (Cladobotryum mycophilum) and mushroom yield. An Appl Biol: 10.1111/aab.12352.

Chakwiya A, Van der Linde EJ, Korsten, L, 2015. In vitro sensitivity testing of Cladobotryum mycophilum to carbendazim and prochloraz manganese. S Afr J Sci: 111, 1-7. https://doi.org/10.17159/sajs.2015/20140408

De Hoog GS, 1978. Notes on some fungicolus hyphomycetes and their relatives. Persoonia 10: 33-81.

Desrumeaux B, 2005. Cobweb disease: an overview. Pest and diseases. Mushroom business 15: 16-17.

Eicker A, 1984. A report on the use of thiabendazole for the control of fungal pathogens of cultivated mushroom. S. Afr. J. Bot 3: 179-183. https://doi.org/10.1016/S0022-4618(16)30049-3

Eicker, A, Peng JT, Chen ZC, 1990. A Pseudohansfordia-disease of sawdust-cultivated Auricularia mesenterica in Taiwan. Bot Bull Acad Sinica 31: 205-210.

Feng Y, Blunt JW, Cole AL, Cannon JF, Robinson WT, Munro MH, 2003. Two novel cytotoxic cyclodepsipeptides from a mycoparasitic Cladobotryum sp. J Org Chem 68: 2002-2005. https://doi.org/10.1021/jo0263059

Fletcher JT, Allan J, Seymour GK, 2004, Managing cobweb disease in Australia. Proc 16th Int Cong on the Science and Cultivation of Edible Fungi, pp: 711-715. Miami, FL. U.S.A.

Fletcher JT, Gaze RH, 2008. Mushroom pest and disease control: a color handbook. Ed. Manson Publishing Ltd. Academic Press, San Diego. 192 pp.

FRAC (2016) FRAC Code List ©*2016: Fungicides sorted by mode of action (including FRAC Code numbering). http://www.frac.info/publications/downloads

Gams W, Hoozemans ACM, 1970. Cladobotryum-konidienformen von Hypomyces-arten. Persoonia 6: 95-110.

Gea FJ, Navarro MJ, Tello JC, 2005. Reduced sensitivity of the mushroom pathogen Verticillium fungicola to prochloraz-manganese in vitro. Mycol Res 109: 741-745. https://doi.org/10.1017/S095375620500242X

Gea FJ, Navarro MJ, Suz LM, 2011. First Report of Cladobotryum mycophilum causing cobweb on cultivated king oyster mushroom in Spain. Plant Dis 95: 1030. https://doi.org/10.1094/PDIS-03-11-0255

Gea FJ, Navarro MJ, Carrasco J, González AJ, Suz LM 2012. First report of cobweb on white button mushroom (Agaricus bisporus) in Spain caused by Cladobotryum mycophilum. Plant Dis 96: 1067. https://doi.org/10.1094/PDIS-02-12-0120-PDN

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: 711-720. https://doi.org/10.1007/s10658-013-0344-y

Gea FJ, Carrasco J, Suz LM. Navarro MJ, 2017. Characterization and pathogenicity of Cladobotryum mycophilum in Spanish Pleurotus eryngii mushroom crops and their sensitivity to fungicides. Eur J Plant Pathol 147:129-139. https://doi.org/10.1007/s10658-016-0986-7

Geösel A, 2011. The cultivation opportunities and complex comparison survey of Agaricus blazei (Murrill), 21pp. Doctoral dissertation, Budapesti Corvinus Egyetem.

Geösel A, Szabó A, Akan O, Szarvas J, 2014. Effect of essential oils on mycopathogens of Agaricus bisporus. Proc 8th Conf of Mushroom Biology and Mushroom Products, pp. 530-535. Mushroom society of India (Solan) (Eds.). New Delhi, India.

Grogan HM, 2006. Fungicide control of mushroom cobweb disease caused by Cladobotryum strains with different benzimidazole resistance profiles. Pest Manag Sci 62: 153-161. https://doi.org/10.1002/ps.1133

Grogan HM, Gaze RH, 2000. Fungicide resistance among Cladobotryum spp. – causal agents of cobweb disease of the edible mushroom Agaricus bisporus. Mycol Res 104: 357-364. https://doi.org/10.1017/S0953756299001197

Howard RJ, Garland JA, Seaman WL, 1994. Chapter 26. Mushrooms. Diseases and pests of vegetable crops in Canada: an illustrated compendium, pp. 363-379. Entomological Society of Canada & Canadian Phytopathological Society. Ottawa, Ontario.

Kim HK, Seok SJ, Kim JP, Moon BJ, Terashita T, 1999. Occurrence of disease caused by Cladobotryum varium on Flammulina velutipes in Korea. Korean J Mycol. 27: 415-419.

Kim MK, Lee, YH, Cho KM, Lee JY, 2012. First report of cobweb disease caused by Cladobotryum mycophilum on the edible mushroom Pleurotus eryngii in Korea. Plant Dis 96: 1374. https://doi.org/10.1094/PDIS-01-12-0015-PDN

Kim MK, Lee YH, Cho KM, 2014. Fungicide sensitivity and characterization of cobweb disease on a Pleurotus eryngii mushroom crop caused by Cladobotryum mycophilum. Plant Pathol J 30: 82-89. https://doi.org/10.5423/PPJ.OA.09.2013.0098

Kirschner R, Arnold GR, Cheejen C, 2007. Cladobotryum semicirculare sp. nov. (Hyphomycetes) from commercially grown Ganoderma tsugae in Taiwan and other basidiomycota in Cuba. Sydowia 59: 114-124.

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. Ann Appl Biol 163: 218-230. https://doi.org/10.1111/aab.12048

Krupke OA, Castle AJ, Rinker DL, 2003. The North American mushroom competitor, Trichoderma aggressivum f. aggressivum, produces antifungal compounds in mushroom compost that inhibits mycelial growth of the commercial mushroom Agaricus bisporus. Mycol. Res. 107: 1467–1475. https://doi.org/10.1017/S0953756203008621

Lane CR, Cooke RC, Burden LJ, 1991. Ecophysiology of Dactylium dendroides – the causal agent of cobweb mould. Proc 14th Int Cong on the Science and Cultivation of Edible Fungi, pp. 365-372. Ed. T.J. Elliott. Rotterdam, The Netherlands.

Largeteau ML, Savoie JM, 2010. Microbially induced diseases of Agaricus bisporus: biochemical mechanisms and impact on commercial mushroom production. Appl Microbiol Biotechnol 86: 63-73. https://doi.org/10.1007/s00253-010-2445-2

Mckay GJ, Egan D, Morris E, Brown AE, 1998. Identification of benzimidazole resistance in Cladobotryum dendroides using a PCR-based method. Mycol Res 102: 671–676. https://doi.org/10.1017/S095375629700542X

Mckay GJ, Egan D, Morris E, Scott C, Brown AE, 1999. Genetic and morphological characterization of Cladobotryum species causing cobweb disease of mushrooms. Appl Environ Microbiol 65: 606-610.

Mignucci JS, Hernández-Bacó C, Rivera-Vargas L, Betancourt C, Alameda M, 2000. Diseases and pests research on oyster mushrooms (Pleurotus spp.) in Puerto Rico. IJMS 3: 21-26.

Mitova MI, Lang G, Blunt JW, Cummings NJ, Cole AL, Robinson WT, Munro, MH, 2006. Cladobotric acids AF: new cytotoxic polyketides from a New Zealand Cladobotryum sp. J Org Chem 71: 492-497. https://doi.org/10.1021/jo051883l

Põldmaa K, 2011. Tropical species of Cladobotryum and Hypomyces producing red pigments. Stud Mycol 68: 1–34. https://doi.org/10.3114/sim.2011.68.01

Potočnik I, Rekanović E, Milijašević S, Todorović B, 2008. Morphological and pathogenic characteristics of the fungus Cladobotryum dendroides, the causal agent of cobweb disease of the cultivated mushroom Agaricus bisporus in Serbia. Pestic Fitomed 23: 175-181. https://doi.org/10.2298/PIF0803175P

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: 290-294. https://doi.org/10.1016/j.cropro.2009.07.016

Pyck N, Grogan H, 2015. Fungal diseases of mushrooms and their control, 6 pp. Factsheet 04/15. Mush TV Publications.

Rogerson CT, Samuels GJ, 1993. Polyporicolous species of Hypomyces. Mycologia. 85: 271-272. https://doi.org/10.2307/3760461

Rogerson CT, Samuels GJ, 1994. Agaricicolous species of Hypomyces. Mycologia. 86: 839-866. https://doi.org/10.2307/3760597

Royse DJ, 2014. A global perspective on the high five: Agaricus, Pleurotus, Lentinula, Auricularia & Flammulina. Proc 8th Conf on Mushroom Biology and Mushroom Products, pp. 1-6. Mushroom society of India (Solan) (Eds.). New Delhi, India.

Sakemi S, Bordner J, Decosta DL, Dekker KA, Hirai H, Inagaki T, Kim Y, Sugiura A, Sutcliffe, JA, Tachikawa K, Truesdell S, Wong JW, Yoshikawa N, Kojima Y, 2002. CJ-15,696 and its analogs, new furopyridine antibiotics from the fungus Cladobotryum varium: fermentation, isolation, structural elucidation, biotransformation and antibacterial activities. J Antibiot 55: 6-18. https://doi.org/10.7164/antibiotics.55.6

Savić M, Aneđelković I, Duvnjak D, Matijasević D, Avramović A, Nikšić M, 2012. The fungistatic activity of organic selenium and its application to the production of cultivated mushrooms Agaricus bisporus and Pleurotus spp. Arch Biol Sci 64: 1455-1463. https://doi.org/10.2298/ABS1204455S

Sawada D, Ohmasa M, Fukuda M, Masuno K, Koide H, Tsunoda S, Nakamura K, 2005. Disinfection of some pathogens of mushroom cultivation by photocatalytic treatment. Mycoscience 46: 54-60. https://doi.org/10.1007/S10267-004-0211-Y

Schwinn FJ, Morton HV., 1990 Antiresistance strategies: design and implementation in practice. Managing Resistance to Agrochemicals, pp. 170-183. Ed. Green M.B., LeBaron H.M. and Moberg W.K. American Chemical Society. Washington DC. https://doi.org/10.1021/bk-1990-0421.ch011

Seth PK, Dar GM, 1989. Studies on Cladobotryum dendroides (Bull: Merat) W. Gams et Hoozem, causing cobweb disease of Agaricus bisporus and its control. Mushroom Sci 12: 711-723.

Ślusarski C, Uliński Z, Szumigaj-Tarnowska J, Miszczak A, 2012. Preliminary appraisal of the new preparations for protection of the white button mushroom against fungal diseases. Prog Plant Prot 52: 4.

Tamm H, Põldmaa K, 2013. Diversity, host associations and phylogeography of temperate aurofusarin-producing Hypomyces/Cladobotryum including causal agents of cobweb disease of cultivated mushrooms. Fungal Biol 117: 348-367. https://doi.org/10.1016/j.funbio.2013.03.005

Wang GZ, Guo MP, Bian YB, 2015. First report of Cladobotryum protrusum causing cobweb disease on the edible mushroom Coprinus comatus. Plant Dis 99: 287-287. https://doi.org/10.1094/PDIS-07-14-0757-PDN

Zuo B, Lu BH, Liu XL, Wang Y, Ma GL, Gao J, 2016. First report of Cladobotryum mycophilum causing cobweb on Ganoderma lucidum cultivated in Jilin province, China. Plant Dis 100: 1239. https://doi.org/10.1094/PDIS-12-15-1431-PDN




DOI: 10.5424/sjar/2017152-10143