Mycoparasitic Activity of Indigenous Trichoderma virens Strains Against Mungbean Soil Borne Pathogen Rhizoctonia solani: Hyperparasite and Hydrolytic Enzyme Production

Alfi Inayati, Liliek Sulistyowati, Luqman Qurata Aini, Eriyanto Yusnawan

Abstract


Rhizoctonia solani is one of the harmful pathogens on mungbean, which is very challenging to be controlled. T. virens has been studied intensively and has great potency to control R. solani through mycoparasitism. Seven strains of T. virens isolated from various rhizospheres were tested for their mycoparasitic potential by observing their hyperparasitism and the production of hydrolytic enzymes. All strains showed the ability to suppress the growth of R. solani on dual culture assay as well as on culture filtrate test with the inhibition ability from 43.8 to 68.6% on the dual culture assay and from 22.2 to 71.1% on the culture filtrate assay. Inter-fungal interaction, which was observed by an electron microscope, showed hyperparasitic action of T. virens against R. solani involved the formation of the knob-like structure followed by the growth of Trichoderma hyphae inside host mycelia, coiling, lysed cell wall, and swollen of mycelial tips. Mycoparasitism of T. virens also correlated with the synthesis of hydrolytic enzymes, such as cellulase and chitinase, which influenced the overall hyperparasitic ability of T. virens against the pathogen. Based on in vitro assay, the Tv3 strain proposed as a promising strain to control R. solani due to its high growth inhibition and relatively high cellulase and chitinase productionse.

Keywords


Cellulase; Chitinase; Hydrolytic enzyme; Hyperparasite; T. virens

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References


Abou-Taleb, K. A. A., Mashhoor, W. A., Nasr, S. A., Sharaf, M. S., & Abdel-Azeem, H. H. M. (2009). Nutritional and environmental factors affecting cellulase production by two strains of cellulolytic Bacilli. Australian Journal of Basic and Applied Sciences, 3(3), 2429–2436. Retrieved from http://www.ajbasweb.com/old/ajbas/2009/2429-2436.pdf

Agrawal, T., & Kotasthane, A. S. (2012). Chitinolytic assay of indigenous Trichoderma isolates collected from different geographical locations of Chhattisgarh in central India. SpringerPlus, 1, 73. https://doi.org/10.1186/2193-1801-1-73

Angel, L. P. L., Sundram, S., Ping, B. T. Y., Yusof, M. T., & Ismail, I. S. (2018). Profiling of anti-fungal activity of Trichoderma virens 159C involved in biocontrol assay of Ganoderma boninense. Journal of Oil Palm Research, 30(1), 83–93. https://doi.org/10.21894/jopr.2017.0009

Angel, L. P. L., Yusof, M. T., Ismail, I. S., Ping, B. T. Y., Mohamed Azni, I. N. A., Kamarudin, N. H., & Sundram, S. (2016). An in vitro study of the antifungal activity of Trichoderma virens 7b and a profile of its non-polar antifungal components released against Ganoderma boninense. Journal of Microbiology, 54, 732–744. https://doi.org/10.1007/s12275-016-6304-4

Baek, J. M., Howell, C. R., & Kenerley, C. M. (1999). The role of an extracellular chitinase from Trichoderma virens Gv29-8 in the biocontrol of Rhizoctonia solani. Current Genetics, 35, 41–50. https://doi.org/10.1007/s002940050431

Carling, D. E., Baird, R. E., Gitaitis, R. D., Brainard, K. A., & Kuninaga, S. (2002). Characterization of AG-13, a newly reported anastomosis group of Rhizoctonia solani. Phytopathology, 92(8), 893–899. https://doi.org/10.1094/PHYTO.2002.92.8.893

Cattelan, A. J., Hartel, P. G., & Fuhrmann, J. J. (1999). Screening for plant growth-promoting rhizobacteria to promote early soybean growth. Soil Science Society of America Journal, 63(6), 1670–1680. https://doi.org/10.2136/sssaj1999.6361670x

Contreras-Cornejo, H. A., Macías-Rodríguez, L., Herrera-Estrella, A., & López-Bucio, J. (2014). The 4-phosphopantetheinyl transferase of Trichoderma virens plays a role in plant protection against Botrytis cinerea through volatile organic compound emission. Plant and Soil, 379, 261–274. https://doi.org/10.1007/s11104-014-2069-x

Dennis, C., & Webster, J. (1971). Antagonistic properties of species-groups of Trichoderma: I. Production of non-volatile antibiotics. Transactions of the British Mycological Society, 57(1), 25–39. https://doi.org/10.1016/S0007-1536(71)80077-3

Djunaedy, A. (2008). Aplikasi fungisida sistemik dan pemanfaatan mikoriza dalam rangka pengendalian patogen tular tanah pada tanaman kedelai (Glycine max L.). Embryo, 5(2), 149–157. Retrieved from https://scholar.google.co.id/scholar?hl=en&as_sdt=0,5&cluster=11437799408234141220

El-Hadi, A. A., El-Nour, S. A., Hammad, A., Kamel, Z., & Anwar, M. (2014). Optimization of cultural and nutritional conditionsfor carboxymethylcellulase productionby Aspergillus hortai. Journal of Radiation Research and Applied Sciences, 7(1), 23–28. https://doi.org/10.1016/j.jrras.2013.11.003

Florencio, C., Couri, S., & Farinas, C. S. (2012). Correlation between agar plate screening and solid-state fermentation for the prediction of cellulase production by Trichoderma strains. Enzyme Research, 2012(793708), 1–7. https://doi.org/10.1155/2012/793708

Inayati, A., Sulistyowati, L., Aini, L. Q., & Yusnawan, E. (2019). Antifungal activity of volatile organic compounds from Trichoderma virens. In AIP Conference Proceedings (p. 080012). AIP Publishing LLC. https://doi.org/10.1063/1.5115750

Li, M. F., Li, G. H., & Zhang, K. Q. (2019). Non-volatile metabolites from Trichoderma spp. Metabolites, 9(3), 58. https://doi.org/10.3390/metabo9030058

Meena, M., Swapnil, P., Zehra, A., Aamir, M., Dubey, M. K., Goutam, J., & Upadhyay, R. S. (2017). Beneficial microbes for disease suppression and plant growth promotion. In D. Singh, H. Singh, & R. Prabha (Eds.), Plant-Microbe Interactions in Agro-Ecological Perspectives (pp. 395–432). Singapore: Springer. https://doi.org/10.1007/978-981-10-6593-4_16

Meena, M., Swapnil, P., Zehra, A., Dubey, M. K., & Upadhyay, R. S. (2017). Antagonistic assessment of Trichoderma spp. by producing volatile and non-volatile compounds against different fungal pathogens. Archives of Phytopathology and Plant Protection, 50(13–14), 629–648. https://doi.org/10.1080/03235408.2017.1357360

Mohiddin, F. A., Khan, M. R., Khan, S. M., & Bhat, B. H. (2010). Why Trichoderma is considered super hero (super fungus) against the evil parasites? Plant Pathology Journal, 9(3), 92–102. https://doi.org/10.3923/ppj.2010.92.102

Monfil, V. O., & Casas-Flores, S. (2014). Molecular mechanisms of biocontrol in Trichoderma spp. and their applications in agriculture. In V. K. Gupta, M. Schmoll, A. Herrera-Estrella, R. S. Upadhyay, I. Druzhinina, & M. G. Tuohy (Eds.), Biotechnology and Biology of Trichoderma (pp. 429–453). Elsevier. https://doi.org/10.1016/B978-0-444-59576-8.00032-1

Muis, A. (2007). Pengelolaan penyakit busuk pelepah (Rhizoctonia solani Kuhn.) pada tanaman jagung. Jurnal Litbang Pertanian, 26(3), 100–103. Retrieved from http://203.190.37.42/publikasi/p3263072.pdf

Mukherjee, M., Mukherjee, P. K., Horwitz, B. A., Zachow, C., Berg, G., & Zeilinger, S. (2012). Trichodermaplant- pathogen interactions: Advances in genetics of biological control. Indian Journal of Microbiology, 52(4), 522–529. https://doi.org/10.1007/s12088-012-0308-5

Nakkeeran, S., Vinodkumar, S., Priyanka, R., & Renukadevi, P. (2018). Mode of action of Trichoderma spp. in biological control of plant diseases. In Biocontrol of Soil Borne Pathogens and Hematodes (pp. 81–95). New Delhi, IN: Jeya Publishing house. Retrieved from https://www.researchgate.net/publication/329177943_Mode_of_Action_of_Trichoderma_Spp_in_Biological_Control_of_Plant_Diseases

Olaniyi, O. O., & Oyesiji, Y. V. (2015). Stimulatory effect of physicochemical factors on the expression of cellulase by Trichoderma viride NSPRT23. Microbiology Journal, 5, 58–67. https://doi.org/10.3923/mj.2015.58.67

Potprommanee, L., Wang, X. Q., Han, Y. J., Nyobe, D., Peng, Y. P., Huang, Q., … Chang, K. L. (2017). Characterization of a thermophilic cellulase from Geobacillus sp. HTA426, an efficient cellulaseproducer on alkali pretreated of lignocellulosic biomass. PLoS ONE, 12(4), e0175004. https://doi.org/10.1371/journal.pone.0175004

Qualhato, T. F., Lopes, F. A. C., Steindorff, A. S., Brandão, R. S., Jesuino, R. S. A., & Ulhoa, C. J. (2013). Mycoparasitism studies of Trichoderma species against three phytopathogenic fungi: Evaluation of antagonism and hydrolytic enzyme production. Biotechnology Letters, 35, 1461–1468. https://doi.org/10.1007/s10529-013-1225-3

Rahayu, M. (2014). Identification and pathogenecity of pathogen responsible for aerial blight disease of soybean. Journal of Experimental Biology and Agricultural Sciences, 2(2S), 279–285. Retrieved from http://www.jebas.org/wp-content/uploads/2014/09/Rahayu-JEBAS.pdf

Rahayu, M. (2016). Patologi dan teknis pengujian kesehatan benih tanaman aneka kacang. Buletin Palawija, 14(2), 78–88. Retrieved from http://balitkabi.litbang.pertanian.go.id/wp-content/uploads/2017/11/5-Muji-rahayu-14_2.pdf

RStudio Team. (2015). RStudio: Integrated development for R. Boston, MA: RStudio, Inc.. Retrieved from https://support.rstudio.com/hc/en-us/articles/206212048-Citing-RStudio

Shahriarinour, M., Abd Wahab, M. N., Ariff, A., & Mohamad, R. (2011). Screening, isolation and selection of cellulolytic fungi from oil palm empty fruit bunch fibre. Biotechnology, 10(1), 108–113. https://doi.org/10.3923/biotech.2011.108.113

Smitha, C., Finosh, G. T., Rajesh, R., & Abraham, P. K. (2014). Induction of hydrolytic enzymes of phytopathogenic fungi in response to Trichoderma viride influence biocontrol activity. International Journal of Current Microbiology and Applied Sciences, 3(9), 1207–1217. Retrieved from https://www.ijcmas.com/vol-3-9/C.Smitha,et al.pdf

Soesanto, L., Mugiastuti, E., Rahayuniati, R. F., Manan, A., Dewi, R. S. (2018). Compatibility test of four Trichoderma spp. isolates on several synthetic pesticides. AGRIVITA Journal of Agricultural Science, 40(3), 481-489. https://doi.org/10.17503/agrivita.v40i3.1126

Strakowska, J., Błaszczyk, L., & Chełkowski, J. (2014). The significance of cellulolytic enzymes produced by Trichoderma in opportunistic lifestyle of this fungus. Journal of Basic Microbiology, 54(S1), S2–S13. https://doi.org/10.1002/jobm.201300821

Syed, S., Riyaz-Ul-Hassan, S., & Johri, S. (2013). A novel cellulase from an endophyte, Penicillium sp. NFCCI 2862. American Journal of MicrobiologicalResearch, 1(4), 84–91. https://doi.org/10.12691/ajmr-1-4-4

Veena, D., Priya, H. R., Raheesa, M. K., & Divya, J. (2014). Soilborne diseases in crop plants and their management. Research & Reviews: Journal of Agriculture and Allied Sciences, 3(2), 12–18. Retrieved from http://www.rroij.com/open-access/soilborne-diseases-in-crop-plantsand-their-management.php?aid=33851

Vipul, K., Mohammad, S., Mukesh, S., Anuradha, S., Sonika, P., & Manoj, K. M. (2015). Screening of Trichoderma species for virulence efficacy on seven most predominant phytopathogens. African Journal of Microbiology Research, 9(11), 793–799. https://doi.org/10.5897/ajmr2014.7342

Viterbo, A., & Horwitz, B. A. (2010). Mycoparasitism. In K. Borkovich & D. J. Ebbole (Eds.), Cellular and Molecular Biology of Filamentous Fungi (pp. 679–693). Washington, DC: ASM Press. Retrieved from https://books.google.co.id/books?id=fwSsBAAAQBAJ

Wang, K.-D., Borrego, E. J., Kenerley, C. M., Kolomiets, M. V. (2020). Oxylipins other than jasmonic acid are xylem-resident signals regulating systemic resistance induced by Trichoderma virens in maize. The Plant Cell, 32(1), 166-185. https://doi.org/10.1105/tpc.19.00487

Wu, Q., Sun, R., Ni, M., Yu, J., Li, Y., Yu, C., … Chen, J. (2017). Identification of a novel fungus, Trichoderma asperellum GDFS1009, and comprehensive evaluation of its biocontrol efficacy. PLoS ONE, 12(6), e0179957. https://doi.org/10.1371/journal.pone.0179957

Xue, C. Y., Zhou, R. J., Li, Y. J., Xiao, D., & Fu, J. F. (2018). Cell-wall-degrading enzymes produced in vitro and in vivo by Rhizoctonia solani, the causative fungus of peanut sheath blight. PeerJ, 6, e5580. https://doi.org/10.7717/peerj.5580

You, J., Zhang, J., Wu, M., Yang, L., Chen, W., & Li, G. (2016). Multiple criteria-based screening of Trichoderma isolates for biological control of Botrytis cinerea on tomato. Biological Control, 101, 31–38. https://doi.org/10.1016/j.biocontrol.2016.06.006

Yusnawan, E., Inayati, A., & Baliadi, Y. (2019). Isolation of antagonistic fungi from rhizospheres and its biocontrol activity against different isolates of soil borne fungal pathogens infected legumes. Biodiversitas Journal of Biological Diversity, 20(7), 2048–2054. https://doi.org/10.13057/biodiv/d200735

Zehra, A., Dubey, M. K., Meena, M., & Upadhyay, R. S. (2017). Effect of different environmental conditions on growth and sporulation of some Trichoderma species. Journal of Environmental Biology, 38(March), 197–203. https://doi.org/10.22438/jeb/38/2/MS-251

Zhang, F., Ge, H., Zhang, F., Guo, N., Wang, Y., Chen, L., … Li, C. (2016). Biocontrol potential of Trichoderma harzianum isolate T-aloe against Sclerotinia sclerotiorum in soybean. Plant Physiology and Biochemistry, 100, 64–74. https://doi.org/10.1016/j.plaphy.2015.12.017

Zhang, S., Gan, Y., & Xu, B. (2014). Efficacy of Trichoderma longibrachiatum in the control of Heterodera avenae. BioControl, 59, 319–331. https://doi.org/10.1007/s10526-014-9566-y

Zheng, A., Lin, R., Zhang, D., Qin, P., Xu, L., Ai, P., … Li, P. (2013). The evolution and pathogenic mechanisms of the rice sheath blight pathogen. Nature Communications, 4, 1424. https://doi.org/10.1038/ncomms2427




DOI: http://doi.org/10.17503/agrivita.v0i0.2514

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