Abstract
Agaricus bisporus, called as button mushroom, constitutes majority of the cultivated mushrooms in the world. Green mould, caused by Trichoderma species, is a destructive fungal disease causing epidemics in A. bisporus cultivation. In 2015, 2016 and 2017, a total of 71 samples including compost, casing soil and mushroom tissues were collected from mushroom farms in Antalya Province, Turkey. Of 24 Trichoderma isolates obtained, 13 were identified as Trichoderma aggressivum f. aggressivum (Th4). To date, Th4 is known to occur in North America, but it was also reported in Hungary in 2017. In addition, to our knowledge, this is the first record of occurrence of Th4 on button mushroom in Turkey. In the present study, in vitro and in vivo experiments were also conducted to examine aggressiveness of the Trichoderma isolates on A. bisporus. In vitro experiments, based on confrontation tests, it was found that mycelial growth of A. bisporus was inhibited up to 71.99% and 58.71% in the presence of Th4 and Th1 isolates, respectively. In vivo experiments, biomass and morphological features (cap weight, stipe weight and so on) of the mushrooms in the treatments were compared with controls. Th4 isolates caused 95.06% mean reduction in biomass. Th4 and Th1 isolates significantly affected all the examined morphological features. The study revealed that Th4 and Th1 isolates had significant (P < 0.01) inhibitory influence on A. bisporus growth in vitro and in vivo. But, aggressiveness of the Th4 isolates was significantly much higher than that of the Th1 isolates.
Similar content being viewed by others
References
Abubaker KS (2010) Cell wall degrading enzymes and interaction between Trichoderma aggressivum and Agaricus bisporus. A thesis for the degree of doctor of philosophy. Brock University St. Catharines, Ontario, Canada
Abd-Elsalam KA, Almohimeed I, Moslem MA, Bahkali AH (2010) M13-microsatellite PCR and rDNA sequence markers for identification of Trichoderma (Hypocreaceae) species in Saudi Arabian soil. Genet Mol Res 9(4):2016–2024. https://doi.org/10.4238/vol9-4gmr908
Anonymous (2019) Mushroom cultivation, history and mysticism. https://pajarostreet.com/Food/FoodInfo/Mushrooms/history.html. Accessed 22 July 2019
Anastasi A, Varese GC, Marchisio VF (2005) Isolation and identification of fungal communities in compost and vermicompost. Mycologia 97(1):33–34. https://doi.org/10.1080/15572536.2006.11832836
Beyer DM, Wuest PJ, Kremser JJ (2000) Evaluation of epidemiological factors and mushroom substrate characteristics influencing the occurrence and development of Trichoderma green mold. In: Van Griensven (ed) Science and cultivation of edible fungi. Balkema, Rotterdam, pp 633–640
Błaszczyk L, Popiel D, Chełkowski J, Koczyk G, Samuels GJ, Sobieralski K, Siwulski M (2011) Species diversity of trichoderma in Poland. J Appl Genet 52(2):233–243. https://doi.org/10.1007/s13353-011-0039-z
Błaszczyk L, Siwulski M, Sobieralski K, Frużyńska-Jóźwiak D (2013) Diversity of Trichoderma spp. causing Pleurotus green mould diseases in Central Europe. Folia Microbiol 58:325–333. https://doi.org/10.1007/s12223-012-0214-6
Carbone I, Kohn LM (1999) A method for designing primer sets for speciation studies in filamentous Ascomycetes. Mycologia 91:553–556
Castle A, Speranzini D, Rghei N, Alm G, Rinker D, Bissett J (1998) Morphological and molecular identification of trichoderma isolates on North American mushroom farms. Appl Environ Microbiol 64(1):133–137
Chang R (1996) Functional properties of edible mushrooms. Nutr Rev 54:91–93. https://doi.org/10.1111/j.1753-4887.1996.tb03825.x
Chen X, Romaine CP, Tan Q, Schlagnhaufer B, Ospina-Giraldo MD, Royse DJ, Huff DR (1999) PCR-based genotyping of epidemic and preepidemic trichoderma isolates associated with green mold of Agaricus bisporus. Appl Environ Microbiol 65(6):2674–2678
Chen X, Ospina-Giraldo MD, Wilkinson V, Royse DJ, Romaine CP (2003) Resistance of pre- and post-epidemic strains of Agaricus bisporus to Trichoderma aggressivum f. aggressivum. Plant Dis 87:1457–1461. https://doi.org/10.1094/PDIS.2003.87.12.1457
Cloonan KR, Andreadis SS, Chen H, Jenkins NE, Baker TC (2016) Attraction, oviposition and larval survival of the fungus gnat, Lycoriella ingenua, on fungal species isolated from adults, larvae, and mushroom compost. PLoS ONE 11(12):e0167074. https://doi.org/10.1371/journal.pone.0167074
Cumagun CJR, Manalo JO, Salcedo-Bacalangco NA, Ilag LL (2009) Cellulose decomposing ability of trichoderma in relation to their saprophytic survival. Arch Phytopathol Plant Protect 42(7):698–704. https://doi.org/10.1080/03235400701492731
Eastburn DM, Butler EE (1991) Effects of soil moisture and temperature on the saprophytic ability of Trichoderma harzianum. Mycologia 83(3):257–263. https://doi.org/10.1080/00275514.1991.12026009
Górski R, Sobieralski K, Siwulski M, Frąszczak B, Sas-Golak I (2014) The effect of trichoderma isolates, from family mushroom growing farms, on the yield of four Agaricus bisporus (Lange) Imbach strains. J Plant Protect Res 54(1):102–105. https://doi.org/10.2478/jppr-2014-0016
Hatvani L, Antal Z, Manczinger L, Szekeres A, Druzhinina IS, Kubicek CP, Nagy A, Nagy E, Vágvölgyi C, Kredics L (2007) Green mold diseases of Agaricus and Pleurotus spp. are caused by related but phylogenetically different Trichoderma species. Phytopathology 97:532–537. https://doi.org/10.1094/PHYTO-97-4-0532
Hatvani L, Kredics L, Allaga H, Manczinger L, Vágvölgyi C, Kuti K, Geösel A (2017) First report of Trichoderma aggressivum f. aggressivum green mold on Agaricus bisporus in Europe. Plant Dis 101(6):1052. https://doi.org/10.1094/PDIS-12-16-1783-PDN
Hermosa MR, Grondona I, Monte E (1999) Isolation of Trichoderma harzianum Th2 from commercial mushroom compost in Spain. Plant Dis 83(6):591. https://doi.org/10.1094/PDIS.1999.83.6.591B
Jaklitsch WM, Komon M, Kubicek CP, Druzhinina IS (2005) Hypocrea voglmayrii sp. nov. from the Austrian Alps represents a new phylogenetic clade in Hypocrea/Trichoderma. Mycologia 97:1365–1378
Jayalal RGU, Adikaram NKB (2007) Influence of Trichoderma harzianum metabolites on the development of green mould disease in the oyster mushroom. Cey J Sci (Bio Sci) 36(1):53–60
Jiang Y, Wang J-L, Chen J, Mao L-J, Feng X-X, Zhang C-L, Lin F-C (2016) Trichoderma biodiversity of agricultural fields in East China reveals a gradient distribution of species. PLoS ONE 11(8):e0160613. https://doi.org/10.1371/journal.pone.0160613
Kim CS, Park MS, Kim SC, Maekawa N, Yu SH (2012) Identification of trichoderma, a competitor of shiitake mushroom (Lentinula edodes), and competition between Lentinula edodes and Trichoderma species in Korea. Plant Pathol J 28(2):137–148. https://doi.org/10.5423/PPJ.OA.02.2011.0030
Kertesz MA, Thai M (2018) Compost bacteria and fungi that influence growth and development of Agaricus bisporus and other commercial mushrooms. Appl Microbiol Biotechnol 102(4):1639–1650. https://doi.org/10.1007/s00253-018-8777-z
Kosanović D, Potǒcnik I, Duduk B, Vukojević J, Stajić M, Rekanović E, Milijaˇsević-Marčić S (2013) Trichoderma species on Agaricus bisporus farms in Serbia and their biocontrol. Ann Appl Bio 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 inhibit mycelial growth of the commercial mushroom Agaricus bisporus. Mycol Res 107(12):1467–1475. https://doi.org/10.1017/S0953756203008621
Mamoun ML, Savoie J-M, Olivier JM (2000) Interactions between the pathogen Trichoderma harzianum Th2 and Agaricus bisporus in mushroom compost. Mycologia 92(2):233–240. https://doi.org/10.1080/00275514.2000.12061150
Mattila P, Suonpää K, Piironen V (2000) Functional properties of edible mushrooms. Nutrition 16(7–8):694–696. https://doi.org/10.1111/j.1753-4887.1996.tb03825.x
Mirkhani F, Alaei H (2015) Species diversity of indigenous Trichoderma from alkaline pistachio soils in Iran. Mycologia Iranica 2(1):22–37. https://doi.org/10.22043/MI.2015.14264
Mumpuni A, Sharma HSS, Brown AE (1998) Effect of metabolites produced by Trichoderma harzianum biotypes and Agaricus bisporus on their respective growth radii in culture. Appl Environ Mic 64(12):5053–5056
Muthumeenakshi S, Mills PR, Brown AE, Seaby DA (1994) Intraspecific molecular variation among Trichoderma harzianum isolates colonizing mushroom compost in the British Isles. Microbiology 140:769–777
Muthumeenakshi S, Brown AE, Mills PR (1998) Genetic comparison of the aggressive weed mould strains of Trichoderma harzianum from mushroom compost in North America and the British Isles. Mycol Res 102(4):385–390. https://doi.org/10.1017/S0953756297004759
Nazir N, Miraz JH, Akhtar N, Bajwa R, Nasim G (2007) Some studies on thermophilic and thermotolerant fungi from Lahore. Pakistan Mycopath 5(2):95–100
Noble R, Fermor TR, Lincoln S, Dobrovin-Pennington A, Evered C, Mead A, Li R (2003) Primordia initiation of mushroom (Agaricus bisporus) strains on axenic casing materials. Mycologia 95(4):620–629
O’Brien M, Kavanagh K, Grogan H (2017) Detection of Trichoderma aggressivum in bulk phase III substrate and the effect of T. aggressivum inoculum, supplementation and substrate-mixing on Agaricus bisporus yields. Eur J P Patho 147(1):199–209. doi:10.1007/s10658-016-0992-9
Ospina-Giraldo MD, Royse DJ, Thon MR, Chen X, Romaine CP (1998) Phylogenetic relationships of Trichoderma harzianum causing mushroom green mold in Europe and North America to other species of Trichoderma from world-wide sources. Mycologia 90(1):76–81
Ospina-Giraldo MD, Royse DJ, Chen X, Romaine CP (1999) Molecular phylogenetic analyses of biological control strains of Trichoderma harzianum and other biotypes of Trichoderma spp. associated with mushroom green mold. Phytopathology 89:308–313. https://doi.org/10.1094/PHYTO.1999.89.4.308
Potočnik I, Stepanović M, Rekanović E, Todorović B, Milijašević-Marčić S (2015) Disease control by chemical and biological fungicides in cultivated mushrooms: button mushroom, oyster mushroom and shiitake. Pestic Phytomed (Belgrade) 30(4):201–208. https://doi.org/10.2298/PIF1504201P
Rainey PB (1989) A new laboratory medium for the cultivation of Agaricus bisporus. New Zealand Nat Sci 16:109–112
Samuels GJ, Dodd SL, Gams W, Castlebury LA, Petrini O (2002) Trichoderma species associated with the green mold epidemic of commercially grown Agaricus bisporus. Mycologia 94(1):146–170
Seaby DA (1996a) Differentiation of Trichoderma taxa associated with mushroom production. Plant Path 45:905–912. https://doi.org/10.1111/j.1365-3059.1996.tb02901.x
Seaby DA (1996b) Investigation of the epidemiology of green mould of mushroom (Agaricus bisporus) compost caused by Trichoderma harzianum. Plant Path 45:913–923. https://doi.org/10.1111/j.1365-3059.1996.tb02902.x
Savoie J-M, Iapicco R, Largeteau-Mamoun ML (2001) Factors infuencing the competitive saprophytic ability of Trichoderma harzianum Th2 in mushroom (Agaricus bisporus) compost. Mycol Res 105(11):1348–1356. https://doi.org/10.1017/S0953756201004993
Sharma HSS, Kilpatrick M, Ward F, Lyons G, Burns L (1999) Colonization of phase II compost by biotypes of Trichoderma harzianum and their effect on mushroom yield and quality. Appl Mic Biotech 51(5):572–578. https://doi.org/10.1007/s002530051434
Sharma SR, Kumar S, Sharma VP (2007) Diseases and competitor moulds of mushrooms and their management. Technical Bulletin, National Research Centre for Mushroom (Indian Council of Agricultural Research), Chambaghat, pp 1–81
Sharma KK, Singh US (2014) Cultural and morphological characterization of rhizospheric isolates of fungal antagonist Trichoderma. J Appl Nat Sci 6(2):451–456. https://doi.org/10.31018/jans.v6i2.481
Sobieralski K, Siwulski M, Frużyńska-Jóźwiak D, Górski R (2009) Impact of Trichoderma aggressivum f. europaeum Th2 on the yielding of Agaricus bisporus. Phytopathologia 53:5–10
Sobieralski K, Siwulski M, Blaszczyk L, Fruzynska-Józwiak D, Lisiecka J (2012) The effect of infestation with isolates of Trichoderma sp. on mycelium growth and yielding in single-spore heterokaryotic cultures of Agaricus bisporus (Lange) Imbach. Acta Sci Pol Hortorum Cultus 11(6):47–57
Szczech M, Staniaszek M, Habdas H, Uliński Z, Szymański J (2008) Trichoderma spp. the cause of green mold on Polish mushroom farms. Veg Crop Res Bull 69:105–114. https://doi.org/10.2478/v10032-008-0025-0
Valverde ME, Hernández-Pérez T, Paredes-López O (2015) Edible mushrooms: improving human health and promoting quality life. Int J Micro 2015:1–14. https://doi.org/10.1155/2015/376387
Vinale F, Sivasithambaram K, Ghisalberti LE, Marra R, Woo SL, Lortio M (2008) Trichoderma-plant pathogen interactions. S Bio. Biochem 40(1):1–10. https://doi.org/10.1016/j.soilbio.2007.07.002
Wang G, Cao X, Ma X, Guo M, Liu C, Yan L, Bian Y (2016) Diversity and effect of Trichoderma spp associated with green mold disease on Lentinula edodes in China. MicrobiologyOpen 5(4):709–718. https://doi.org/10.1002/mbo3.364
Williams J, Clarkson JM, Mills PR, Cooper RM (2003) Saprotrophic and mycoparasitic components of aggressiveness of Trichoderma harzianum groups toward the commercial mushroom Agaricus bisporus. Appl Environ Microbiol 69(7):4192–4199. https://doi.org/10.1128/AEM.69.7.4192-4199.2003
White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR Protocols: a guide to methods and applications,. Academic Press, Inc. New York, pp 315–322
Acknowledgements
This study was supported by General Directorate of Agricultural Research and Policies with the project (No: TAGEM/BSAD/16/7/02/03).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflicts of interest
There is no any conflict of interest with the study.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Aydoğdu, M., Kurbetli, İ., Kitapçı, A. et al. Aggressiveness of green mould on cultivated mushroom (Agaricus bisporus) in Turkey. J Plant Dis Prot 127, 695–708 (2020). https://doi.org/10.1007/s41348-020-00328-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s41348-020-00328-8