Sains
Malaysiana 54(8)(2025): 1901-1912
http://doi.org/10.17576/jsm-2025-5408-03
Inhibitory Effect of Trichoderma spp. Causing Green Mold
Disease on the Edible Mushroom Pleurotus
pulmonarius and Pleurotus floridanus
(Kesan Perencatan terhadap
Pertumbuhan Trichoderma spp. yang Menyebabkan
Penyakit Kulat Hijau pada Pleurotus pulmonarius dan Pleurotus
floridanus)
SHAN WAN SWAN1,2, FASEHAH MOHD MULANA1,2, JAYA SEELAN SATHIYA SEELAN1,3 & TAN YEE SHIN1,2,*
1Mushroom Research
Centre, Universiti Malaya, 50603 Kuala
Lumpur, Malaysia
2Institute of Biological
Sciences, Faculty of Science, Universiti Malaya, 50603 Kuala
Lumpur, Malaysia
3Institute for Tropical
Biology and Conservation, Universiti Malaysia Sabah, Jalan
UMS 88400 Kota Kinabalu, Sabah, Malaysia
Diserahkan:
13 Ogos 2024/Diterima: 3 Jun 2025
ABSTRACT
The popular cultivated edible oyster mushrooms in Malaysia, Pleurotus pulmonarius(grey oyster mushroom) and Pleurotus floridanus(white oyster mushroom), are susceptible to green mold disease caused by Trichoderma spp. The decline of the quality and
yield production of the mushrooms up to 100% has been frequently observed due
to infection by Trichoderma. The
objective of this study was to investigate the competitive inhibition of Trichoderma spp. isolated from the farm with Pleurotus spp. Nine strains of Trichoderma were cultured in vitro with Pleurotus on potato dextrose agar and the radial growth as well as
mycelial diameter growth were recorded. The direct plate assay results showed
that T. koningiopsisand T. harzianumwere
the most pathogenic strains against P. pulmonarius and P. floridanus by overgrowing and replacing the mycelia,
respectively, due to space competition and nutrient suppression. The bi-plate
Petri dish approach for assessing contactless inhibition of Trichoderma spp. against Pleurotus spp. demonstrated that T. asperellum, T. ghanense, and T. koningiopsiswere able to cross over the partition and inhibit P. pulmonariusmycelium. Meanwhile, inverted plate assay demonstrated that T. ghanense and T. reeseiinhibited P. pulmonarius mycelia, respectively, indicating contactless inhibition of Pleurotus by Trichoderma. When tested with P. floridanus, only T. ghanensedemonstrated
inhibition in bi-plate Petri dish method and inverted plate assay. In summary, all nine Trichoderma spp. suppressed Pleurotus growth in varying degrees. Thus, besides
competing with mushroom mycelia for nutrients and space, Trichoderma sp.
could also release volatile organic compounds that act without direct contact.
Keywords: Green mold; inhibition; mushroom; pathogenic
ABSTRAK
Kata kunci: Cendawan;
kulat hijau; patogen; perencatan
RUJUKAN
Adebayo, E.A. & Oloke, J. 2017. Oyster mushroom (Pleurotus species); A natural functional food. Journal of Microbiology, Biotechnology and Food Sciences 7: 254-264.
Adebayo, E.A., Oloke, J.K., Yadav, A., Barooah, M. &
Bora, T.C. 2013. Improving yield performance of Pleurotus pulmonarius through hyphal
anastomosis fusion of dikaryons. World
Journal of Microbiology and Biotechnology 29: 1029-1037.
Ajis, A.H., Tan, Y.S. & Chai, L.C. 2024. Green mould contamination of Pleurotus pulmonarius cultivation in
Malaysia: Unravelling causal agents and water source as critical factors. Fungal Biology 128(7): 2197-2206.
Allaga,
H., Zhumakayev, A., Büchner, R., Kocsubé, S., Szűcs, A., Vágvölgyi, C.,
Kredics, L. & Hatvani, L. 2021. Members of the Trichoderma harzianum species complex with mushroom pathogenic
potential. Agronomy 11(12): 2434.
An, X-Y., Cheng, G-H., Gao, H-X., Li, X-F., Yang, Y., Li,
D. & Li, Y. 2022. Phylogenetic
analysis of Trichoderma species
associated with green mold disease on mushrooms and two new pathogens on Ganoderma sichuanense. Journal of Fungi 8(7): 704.
Badalyan,
S., Innocenti, G. & Garibyan, N. 2002. Antagonistic activity of xylotrophic
mushrooms against pathogenic fungi of cereals in dual culture. Phytopathologia Mediterranea 41: 220-225.
Bakratsas,
G., Polydera, A., Katapodis, P. & Stamatis, H. 2021. Recent trends in
submerged cultivation of mushrooms and their application as a source of
nutraceuticals and food additives. Future
Foods 4: 100086.
Błaszczyk, L., Siwulski, M., Sobieralski, K. &
Frużyńska-Jóźwiak, D. 2013. Diversity
of Trichoderma spp. causing Pleurotus green mould diseases in
Central Europe. Folia Microbiologica 58(4): 325-333.
Chen,
X., Zhou, X., Zhao, J., Tang, X., Pasquali, M., Migheli, Q., Berg, G. &
Cernava, T. 2021. Occurrence of green mold disease on Dictyophora rubrovolvata caused by Trichoderma koningiopsis. Journal
of Plant Pathology 103(3):
981-984.
Choi, I-Y., Joung, G-T., Ryu, J., Choi, J-S. & Choi,
Y-G. 2003. Physiological characteristics of green mold (Trichoderma spp.) isolated from oyster
mushroom (Pleurotus spp.). Mycobiology 31(3): 139-144.
Colavolpe,
M.B., Mejía, S.J. & Albertó, E. 2014. Efficiency of treatments for
controlling Trichoderma spp. during
spawning in cultivation of lignicolous mushrooms. Brazilian Journal of Microbiology 45: 1263-1270.
Dang,
H., Kong, Q., Winchester, W., Wan, X., Lei, Y., Zhang, H., Zhao, Y., Liu, X.,
Xu, B., Zhang, B. & Wang, Z. 2023. Isolation, identification, and
pathogenic effects of Trichoderma spp. from Auricularia auricula. Advanced Composites and Hybrid Materials 6: 96.
Department
of Agriculture. 2022. Industrial Crops
Statistics Malaysia. Putrajaya: Kementerian Pertanian dan Keterjaminan
Makanan.
Effiong, M.E., Umeokwochi, C.P., Afolabi, I.S. &
Chinedu, S.N. 2023. Assessing the nutritional quality of Pleurotus ostreatus (oyster mushroom). Frontiers in Nutrition 10: 1279208.
Food and
Agriculture Organization of the United Nations. 2022. Production/production indices - metadata. FAO Global Statistical
Yearbook.
Grand
View Research. 2022. Market Analysis Report.
Gualtieri, L., Monti, M.M., Mele, F., Russo, A., Pedata,
P.A. & Ruocco, M. 2022. Volatile
organic compound (VOC) profiles of different Trichoderma species and their potential application. Journal of Fungi 8(10): 989.
Hatvani,
L., Antal, Z., Manczinger, L., Szekeres, A., Druzhinina, I.S., Kubicek, C.P.,
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(4): 532-537.
Illuri,
R., Eyeni, M., Kumar, M., Babu, R.S., Prema, P., Nguyen, V.H., Bukhari, N.A.,
Hatamleh, A.A. & Balaji, P. 2022. Bio-prospective potential of Pleurotus djamor and Pleurotus florida mycelial extracts
towards Gram positive and Gram negative microbial pathogens causing infectious
disease. Journal of Infection and Public
Health 15(2): 297-306.
Iqbal,
S., Ashfaq, M., Malik, A., Khan, K. & Mathew, P. 2017. Isolation,
preservation and revival of Trichoderma
viride in culture media. Journal of
Entomology and Zoology Studies 5(3):
1640-1646.
Islam, T., Zakaria, Z., Hamidin, N. & Ishak, M. 2017. Selection and cultivation of oyster mushroom
for the indoor controlled environment in Malaysia and similar ecological
region. MAYFEB Journal of Agricultural
Science 1: 14-22.
Jayalal,
R. & Adikaram, N. 2007. Influence of Trichoderma
harzianum metabolites on the development of green mould disease in the
oyster mushroom. Journal of Science
(Biological Sciences) 36(1):
53-60.
Kamm,
J.A., Buttery, R.G. & Robinson, W.H. 1987. An attractant for mushroom flies
(Diptera: Phoridae). Journal of the New
York Entomological Society 95(1):
19-22.
Kim, S-W., Kim, S., Lee, H-J., Park, J-W. & Ro, H-S.
2013. Isolation of fungal pathogens to an edible
mushroom, Pleurotus eryngii, and
development of specific ITS primers. Mycobiology 41(4): 252-255.
Kredics,
L., Garcia Jimenez, L., Naeimi, S., Czifra, D., Urbán, P., Manczinger, L.,
Vágvölgyi, C. & Hatvani, L. 2010. A challenge to mushroom growers: The
green mould disease of cultivated champignons. In Current Research, Technology and Education Topics in Applied
Microbiology and Microbial Biotechnology, edited by Méndez-Vilas, A. FORMATEX. pp. 295-305.
Krupke,
O., Castle, A. & Rinker, D. 2004. 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(12): 1467-1475.
Lee,
S.H., Jung, H.J., Hong, S.B., Choi, J.I. & Ryu, J.S. 2020. Molecular
markers for detecting a wide range of Trichoderma spp. that might potentially cause green mold in Pleurotus eryngii. Mycobiology 48(4): 313-320.
Luković,
J., Milijašević-Marčić, S., Hatvani, L., Kredics, L.,
Szűcs, A., Vágvölgyi, C., Duduk, N., Vico, I. & Potočnik, I.
2020. Sensitivity of Trichoderma strains from edible mushrooms to the fungicides prochloraz and metrafenone. Journal of Environmental Science and Health,
Part B 56(1): 54-63.
Manjit, S., Kamal, S. & Sharma, V.P. 2021. Status and trends in world mushroom
production-III-world production of different mushroom species in 21st century. Mushroom Research 29(2): 75.
Mumpuni,
A., Sharma, H.S.S. & Brown, A.E. 1998. Effect of metabolites produced by Trichoderma harzianum biotypes and Agaricus bisporus on their respective
growth radii in culture. Applied and
Environmental Microbiology 64(12):
5053-5056.
Naser,
A., Aljanabi, H., Al-Mashhady, F.R., Al-Janabi, J. & Al-Shujairi, A. 2022.
Antagonistic activities of bioagent fungi Trichoderma
harzianum and Pleurotus ostreatus against three species of Fusarium in
cucumber plants. Asia-Pacific Journal of
Molecular Biology and Biotechnology 30(1): 12-21.
Park,
M.S., Bae, K.S. & Yu, S.H. 2006. Two new species of Trichoderma associated with green mold of oyster mushroom
cultivation in Korea. Mycobiology 34(3): 111-113.
Ponnusamy,
A., Ajis, A.H., Tan, Y.S. & Chai, L.C. 2021. Dynamics of fungal and
bacterial microbiome associated with green‐mould contaminated sawdust
substrate of Pleurotus pulmonarius (grey oyster mushroom). Journal of
Applied Microbiology 132(3):
2131-2143.
Qiu, Z.,
Wu, X., Zhang, J. & Huang, C. 2017. High temperature enhances the ability
of Trichoderma asperellum to infect Pleurotus ostreatus mycelia. PLoS ONE 12(10): e0187055.
Rosmiza, M., Davies, W., Aznie, R., Jabil, M. &
Mazdi, M. 2016. Prospects for increasing commercial mushroom
production in Malaysia: Challenges and opportunities. Mediterranean Journal of Social Sciences 7(1): 406-415.
Ruangwong,
O-U., Wonglom, P., Suwannarach, N., Kumla, J., Thaochan, N., Chomnunti, P.,
Pitija, K. & Sunpapao, A. 2021. Volatile organic compound from Trichoderma asperelloides TSU1: Impact
on plant pathogenic fungi. Journal of
Fungi 7(3): 187.
Samuels,
G.J., Ismaiel, A., Mulaw, T.B., Szakacs, G., Druzhinina, I.S., Kubicek, C.P.
& Jaklitsch, W.M. 2012. The Longibrachiatum clade of Trichoderma: A revision with new species. Fungal Diversity 55:
77-108.
Šašić
Zorić, L., Janjušević, L., Djisalov, M., Knežić, T., Vunduk, J.,
Milenković, I. & Gadjanski, I. 2023. Molecular approaches for
detection of Trichoderma green mold
disease in edible mushroom production. Biology 12(2): 299.
Sharma,
S.R. & Vijay, B.Y. 1996. Yield loss in Pleurotus spp. caused by Trichoderma viride. Mushroom Research 5: 19-22.
Sobieralski,
K., Siwulski, M., Kommon-Żelazowska, M., Błaszczyk, L., Sas-Golak, I.
& Frużyńska-Jóźwiak, D. 2012. Impact of Trichoderma pleurotum and T.
pleuroticola isolates on yielding of Pleurotus
ostreatus (FR.) Kumm. Journal of
Plant Protection Research 52(1):
165-168.
Sood,
M., Kapoor, D., Kumar, V., Sheteiwy, M.S., Ramakrishnan, M., Landi, M.,
Araniti, F. & Sharma, A. 2020. Trichoderma:
The “secrets” of a multitalented biocontrol agent. Plants 9(6): 762.
Toral, L., Rodriguez Gonzalez, M.A., Martínez-Checa, F.,
Montaño, A., Cortés Delgado, A., Smolinska, A., Llamas, I. & Sampedro, I.
2021. Identification of volatile organic compounds in
extremophilic bacteria and their effective use in biocontrol of postharvest
fungal phytopathogens. Frontiers in
Microbiology 12: 773092.
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.
Wang, M.
& Zhao, R. 2023. A review on nutritional advantages of edible mushrooms and
its industrialization development situation in protein meat analogues. Journal of Future Foods 3(1): 1-7.
Wang,
X-M., Zhang, J., Wu, L-H., Zhao, Y-L., Li, T., Li, J-Q., Wang, Y-Z. & Liu,
H-G. 2014. A mini-review of chemical composition and nutritional value of
edible wild-grown mushroom from China. Food
Chemistry 151: 279-285.
*Pengarang
untuk surat-menyurat; email: tanyeeshin@um.edu.my