Isolation of antagonistic fungi from rhizospheres and its biocontrol activity against different isolates of soil borne fungal pathogens infected legumes
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Abstract. 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 20: 2048-2054. Soilborne diseases caused by Rhizoctonia solani and Fusarium sp. are biotic limits for legume production. Biological controls offer environmental friendly control for these pathogens. This study aimed to isolate and screen Trichoderma from different rhizospheres and to obtain effective Trichoderma isolates to suppress in vitro growth of the soil borne pathogens. The antagonistic inhibitory activity was performed by dual culture method. Seven out of forty indigenous Trichoderma isolates collected from East Java, Indonesia effectively suppressed the growth of different fungal isolates, namely Rhizoctonia solani (R.s1), R. solani (R.s2) as well as Fusarium sp. which infected soybean and mung bean. In vitro study showed different suppression of the pathogens on dual culture tests. The seven isolates inhibited the growth of R. solani (R.s1), R.solani (R.s2) and Fusarium sp. ranging from 90.0 to 99.6%, 72.8 to 82.4%, and 67.9 to 90.8%, respectively. Isolate origin and genetic variability of Trichoderma played an important role in the antagonistic activity. The fast-growing of selected Trichoderma showed their abilities for space occupation and nutrition competition, which involved in the antagonistic activity. The mycelial growth of Trichoderma over pathogens showed hyperparasitism mechanism. In addition, coiling of Trichoderma over hyphal pathogens was observed during microscopic observation. The seven Trichoderma isolates, therefore, are promising as biological control agents against the soil borne fungi infected legumes.
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References
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Agamani P, Bhagat S, Biswas M, Viswanath K. 2017. Effect of volatile and non volatile compounds of Trichoderma spp. against soil borne diseases of chickpea. International Journal of Current Microbiology and Applied Sciences 6(7): 1486-1491.
Ajith PS, Lakshmidevi N. 2010. Effect of volatile and non-volatile compounds from Trichoderma spp. against Colletotrichum capsici incitant of anthracnose on bell peppers. Nature and Science 8(9): 265–269.
Akhter W, Bhuiyan MKA, Sultana F, Hossain MM. 2015. Integrated effect of microbial antagonist, organic amendment and fungicide in controlling seedling mortality (Rhizoctonia solani) and improving yield in pea (Pisum sativum L.). Comptes Rendus Biologies 338(1): 21-28.
Akrami M, Ibrahimov AS, Zafari DM, Valizadeh E. 2009. Control Fusarium rot of bean by combination of by Trichoderma harzianum and Trichoderma asperellum in greenhouse condition. Agricultural Journal 4(3): 121-123.
Borrero C, Trillas M, Delgado A, Avilés M. 2012. Effect of ammonium/nitrate ratio in nutrient solution on control of Fusarium wilt of tomato by Trichoderma asperellum T34. Plant pathology 61(1): 132-139.
Brotman Y, Kapuganti JG, Viterbo A. 2010. Trichoderma. Current Biology 20(9): R390-R391.
Brotman Y, Landau U, Cuadros-Inostroza Á, Takayuki T, Fernie AR, Chet I, et al. 2013. Trichoderma-plant root colonization: escaping early plant defense responses and activation of the antioxidant machinery for saline stress tolerance. PLoS pathogens: 9(3): e1003221.
Cai F, Chen W, Wei Z, Pang G, Li R, Ran W, et al. 2015. Colonization of Trichoderma harzianum strain SQR-T037 on tomato roots and its relationship to plant growth, nutrient availability and soil microflora. Plant and Soil 388(1-2): 337-350.
Christopher DJ, Raj TS, Rani SU, Udhayakumar R. 2010. Role of defense enzymes activity in tomato as induced by Trichoderma virens against Fusarium wilt caused by Fusarium oxysporum f sp. lycopersici. Journal of Biopesticides 3(1): 158.
Datta S, Dey P, Sarkar A, Tarafdar J, Chowdhury A. 2016. Comparison among four triazole fungicides on growth and development of sheath blight of rice pathogen Rhizoctonia solani Kühn AG1-1A. Archives of Phytopathology And Plant Protection 49(9-10): 239-251.
Devi SS, Sreenivasulu Y, Saritha S, Kumar MR, Kumar KP, Sudhakar P. 2012. Molecular diversity of native Trichoderma isolates against Fusarium oxysporum f. sp. lycopersici (Sacc.). a casual agent of Fusarium wilt in tomato (Lycopersicon esculentum Mill.). Archives of Phytopathology and Plant Protection 45(6): 686-698.
Doley K, Jite, PK. 2012. In-vitro efficacy of Trichoderma viride against Sclerotium rolfsii and Macrophomina phaseolina. Notulae Scientia Biologicae 4(4): 39.
Dubey SC, Suresh M, Singh B. 2007. Evaluation of Trichoderma species against Fusarium oxysporum f. sp. ciceris for integrated management of chickpea wilt. Biological control 40(1): 118-127.
Fiorentino N, Ventorino V, Woo SL, Pepe O, De Rosa A, Gioia L, Romano I, Nadia L, Napolitano M, Colla G. 2018. Trichoderma-based biostimulants modulate rhizosphere microbial populations and improve N uptake efficiency, yield, and nutritional quality of leafy vegetables. Frontiers in Plant Science 9(743): 1-15.
Gajera H, Savaliya DD, Patel S, Golakiya B. 2015. Trichoderma viride induces pathogenesis related defense response against rot pathogen infection in groundnut (Arachis hypogaea L.). Infection, Genetics and Evolution 34: 314-325.
Gams W, Bissett J. 1998. Morphology and identification of Trichoderma. In C. P. Kubicek & G. E. Harman (Eds.), Trichoderma & Gliocladium (Vol. 1, pp. 3-34): Taylor & Francis.
Harman GE, Howell CR, Viterbo A, Chet I, Lorito M. 2004. Trichoderma species-opportunistic, avirulent plant symbionts. Nature reviews microbiology 2(1): 43.
Hasanah U, Riwayati R, Idramsa I, Prasetya E. 2017. Molecular identification of endophytic fungi from bark of raru (Cotylelobium melanoxylon) that produce the antibacterial compounds. Biosaintifika: Journal of Biology & Biology Education 9(3): 380-386.
Jahan N, Sultana S, Adhikary S, Rahman S, Yasmin S. 2013. Evaluation of the growth performance of Trichoderma harzianum (Rifai.) on different culture media. IOSR Journal of Agriculture and Veterinary Science (IOSR-JAVS) 3(4): 44-50.
Jayalakshmi S, Raju S, Rani SU, Benagi V, Sreeramulu K. 2009. Trichoderma harzianum L1 as a potential source for lytic enzymes and elicitor of defense responses in chickpea (Cicer arietinum L.) against wilt disease caused by Fusarium oxysporum f. sp. ciceri. Australian Journal of Crop Science 3(1): 44.
John NS, Anjanadevi I, Nath VS, Sankar SA, Jeeva ML, John KS, Misra RJ. 2015. Characterization of Trichoderma isolates against Sclerotium rolfsii, the collar rot pathogen of Amorphophallus–A polyphasic approach. Biological control 90: 164-172.
John RP, Tyagi R, Prévost D, Brar SK, Pouleur S, Surampalli R. 2010. Mycoparasitic Trichoderma viride as a biocontrol agent against Fusarium oxysporum f. sp. adzuki and Pythium arrhenomanes and as a growth promoter of soybean. Crop protection 29(12): 1452-1459.
Küçük Ç, Kývanç M. 2008. Mycoparasitism in the biological control of Gibberella zeae and Aspergillus ustus by Trichoderma harzianum strains. Journal of Agricultural Technology 4: 49-55.
Mahmoud AF, Abdalla OA. 2018. Biocontrol efficacy of Trichoderma spp. against sesame wilt caused by Fusarium oxysporum f. sp. sesami. Archives of Phytopathology and Plant Protection: 1-11.
Mayo S, Gutierrez S, Malmierca MG, Lorenzana A, Campelo MP, Hermosa R,Casquero PA. 2015. Influence of Rhizoctonia solani and Trichoderma spp. in growth of bean (Phaseolus vulgaris L.) and in the induction of plant defense-related genes. Frontiers in Plant Science 6 (685): 1-11
Mishra B, Mishra RK, Mishra R, Tiwari AK, Yadav RS, Dikshit A. 2011. Biocontrol efficacy of Trichoderma viride isolates against fungal plant pathogens causing disease in Vigna radiata L. Archives of Applied Science Research 3(2): 361-369.
Moosa A, Sahi ST, Haq IU, Farzand A, Khan SA, Javaid K. 2017. Antagonistic potential of Trichoderma isolates and manures against Fusarium wilt of tomato. International Journal of Vegetable Science 23(3): 207-218.
Morsy EM, Abdel-Kawi K, Khalil M. 2009. Efficiency of Trichoderma viride and Bacillus subtilis as biocontrol agents gainst Fusarium solani on tomato plants. Egyptian Journal of Phytopathology 37(1): 47-57.
Rahayu M. 2014. Identification and pathogenicity of pathogen responsible for aerial blight disease of soybean. Journal of Experimental Biology 2: 2S.
Rao GS, Reddy NNR, Surekha C. 2015. Induction of plant systemic resistance in Legumes Cajanus cajan, Vigna radiata, Vigna mungo against plant pathogens Fusarium oxysporum and Alternaria alternata–a Trichoderma viride mediated reprogramming of plant defense mechanism. International Journal of Recent Scientific Research 6(5): 4270-4280.
Rosmana A, Samuels GJ, Ismaiel A, Ibrahim ES, Chaverri P, Herawati Y, Asman A. 2015. Trichoderma asperellum: A dominant endophyte species in cacao grown in Sulawesi with potential for controlling vascular streak dieback disease. Tropical Plant Pathology 40(1): 19-25.
Saravanakumar K, Yu C, Dou K, Wang M, Li Y, Chen J. 2016. Synergistic effect of Trichoderma-derived antifungal metabolites and cell wall degrading enzymes on enhanced biocontrol of Fusarium oxysporum f. sp. cucumerinum. Biological control 94: 37-46.
Setyawan B, Rouf A, Setiono. 2014. Evaluation of Trichoderma spp. isolates combination for biological control of white root disease in rubber. In Purwono, Soeharto, Juarini, S. Wardoyo, Sumarwoto, O. S. Padmini (eds.) Proceeding of National Seminar of Sustainable Bioindustry Agriculture (pp. 239-246). UPN Veteran Yogyakarta, 11 December 2014. [Indonesian]
Setyorini SD, Yusnawan E. 2014. Fungi associated with wilt disease on mung bean germplasm. In Purwono, Soeharto, Juarini, S. Wardoyo, Sumarwoto, O. S. Padmini (eds.) Proceeding of National Seminar of Sustainable Bioindustry Agriculture (pp. 255-262). UPN Veteran Yogyakarta, 11 December 2014. [Indonesian]
Sharfuddin C, Mohanka R. 2012. In vitro antagonism of indigenous Trichoderma isolates against phytopathogen causing wilt of lentil. International Journal of Life Science & Pharma Research 2: 195-202.
Sundaramoorthy S, Balabaskar P. 2013. Biocontrol efficacy of Trichoderma spp. against wilt of tomato caused by Fusarium oxysporum f. sp. lycopersici. Journal of Applied Biology & Biotechnology 1(03): 36-40.
Tapwal A, Singh U, Singh G, Garg S, & Kumar R. 2011. In vitro antagonism of Trichoderma viride against five phytopathogens. Pest Technology 5(1): 59-62.
Woo SL, Ruocco M, Vinale F, Nigro M, Marra R, Lombardi N, Pascale A, Lanzuise S, Manganiello G, Lorito M. 2014. Trichoderma-based products and their widespread use in agriculture. The Open Mycology Journal 8(1): 71-126.
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.
Agamani P, Bhagat S, Biswas M, Viswanath K. 2017. Effect of volatile and non volatile compounds of Trichoderma spp. against soil borne diseases of chickpea. International Journal of Current Microbiology and Applied Sciences 6(7): 1486-1491.
Ajith PS, Lakshmidevi N. 2010. Effect of volatile and non-volatile compounds from Trichoderma spp. against Colletotrichum capsici incitant of anthracnose on bell peppers. Nature and Science 8(9): 265–269.
Akhter W, Bhuiyan MKA, Sultana F, Hossain MM. 2015. Integrated effect of microbial antagonist, organic amendment and fungicide in controlling seedling mortality (Rhizoctonia solani) and improving yield in pea (Pisum sativum L.). Comptes Rendus Biologies 338(1): 21-28.
Akrami M, Ibrahimov AS, Zafari DM, Valizadeh E. 2009. Control Fusarium rot of bean by combination of by Trichoderma harzianum and Trichoderma asperellum in greenhouse condition. Agricultural Journal 4(3): 121-123.
Borrero C, Trillas M, Delgado A, Avilés M. 2012. Effect of ammonium/nitrate ratio in nutrient solution on control of Fusarium wilt of tomato by Trichoderma asperellum T34. Plant pathology 61(1): 132-139.
Brotman Y, Kapuganti JG, Viterbo A. 2010. Trichoderma. Current Biology 20(9): R390-R391.
Brotman Y, Landau U, Cuadros-Inostroza Á, Takayuki T, Fernie AR, Chet I, et al. 2013. Trichoderma-plant root colonization: escaping early plant defense responses and activation of the antioxidant machinery for saline stress tolerance. PLoS pathogens: 9(3): e1003221.
Cai F, Chen W, Wei Z, Pang G, Li R, Ran W, et al. 2015. Colonization of Trichoderma harzianum strain SQR-T037 on tomato roots and its relationship to plant growth, nutrient availability and soil microflora. Plant and Soil 388(1-2): 337-350.
Christopher DJ, Raj TS, Rani SU, Udhayakumar R. 2010. Role of defense enzymes activity in tomato as induced by Trichoderma virens against Fusarium wilt caused by Fusarium oxysporum f sp. lycopersici. Journal of Biopesticides 3(1): 158.
Datta S, Dey P, Sarkar A, Tarafdar J, Chowdhury A. 2016. Comparison among four triazole fungicides on growth and development of sheath blight of rice pathogen Rhizoctonia solani Kühn AG1-1A. Archives of Phytopathology And Plant Protection 49(9-10): 239-251.
Devi SS, Sreenivasulu Y, Saritha S, Kumar MR, Kumar KP, Sudhakar P. 2012. Molecular diversity of native Trichoderma isolates against Fusarium oxysporum f. sp. lycopersici (Sacc.). a casual agent of Fusarium wilt in tomato (Lycopersicon esculentum Mill.). Archives of Phytopathology and Plant Protection 45(6): 686-698.
Doley K, Jite, PK. 2012. In-vitro efficacy of Trichoderma viride against Sclerotium rolfsii and Macrophomina phaseolina. Notulae Scientia Biologicae 4(4): 39.
Dubey SC, Suresh M, Singh B. 2007. Evaluation of Trichoderma species against Fusarium oxysporum f. sp. ciceris for integrated management of chickpea wilt. Biological control 40(1): 118-127.
Fiorentino N, Ventorino V, Woo SL, Pepe O, De Rosa A, Gioia L, Romano I, Nadia L, Napolitano M, Colla G. 2018. Trichoderma-based biostimulants modulate rhizosphere microbial populations and improve N uptake efficiency, yield, and nutritional quality of leafy vegetables. Frontiers in Plant Science 9(743): 1-15.
Gajera H, Savaliya DD, Patel S, Golakiya B. 2015. Trichoderma viride induces pathogenesis related defense response against rot pathogen infection in groundnut (Arachis hypogaea L.). Infection, Genetics and Evolution 34: 314-325.
Gams W, Bissett J. 1998. Morphology and identification of Trichoderma. In C. P. Kubicek & G. E. Harman (Eds.), Trichoderma & Gliocladium (Vol. 1, pp. 3-34): Taylor & Francis.
Harman GE, Howell CR, Viterbo A, Chet I, Lorito M. 2004. Trichoderma species-opportunistic, avirulent plant symbionts. Nature reviews microbiology 2(1): 43.
Hasanah U, Riwayati R, Idramsa I, Prasetya E. 2017. Molecular identification of endophytic fungi from bark of raru (Cotylelobium melanoxylon) that produce the antibacterial compounds. Biosaintifika: Journal of Biology & Biology Education 9(3): 380-386.
Jahan N, Sultana S, Adhikary S, Rahman S, Yasmin S. 2013. Evaluation of the growth performance of Trichoderma harzianum (Rifai.) on different culture media. IOSR Journal of Agriculture and Veterinary Science (IOSR-JAVS) 3(4): 44-50.
Jayalakshmi S, Raju S, Rani SU, Benagi V, Sreeramulu K. 2009. Trichoderma harzianum L1 as a potential source for lytic enzymes and elicitor of defense responses in chickpea (Cicer arietinum L.) against wilt disease caused by Fusarium oxysporum f. sp. ciceri. Australian Journal of Crop Science 3(1): 44.
John NS, Anjanadevi I, Nath VS, Sankar SA, Jeeva ML, John KS, Misra RJ. 2015. Characterization of Trichoderma isolates against Sclerotium rolfsii, the collar rot pathogen of Amorphophallus–A polyphasic approach. Biological control 90: 164-172.
John RP, Tyagi R, Prévost D, Brar SK, Pouleur S, Surampalli R. 2010. Mycoparasitic Trichoderma viride as a biocontrol agent against Fusarium oxysporum f. sp. adzuki and Pythium arrhenomanes and as a growth promoter of soybean. Crop protection 29(12): 1452-1459.
Küçük Ç, Kývanç M. 2008. Mycoparasitism in the biological control of Gibberella zeae and Aspergillus ustus by Trichoderma harzianum strains. Journal of Agricultural Technology 4: 49-55.
Mahmoud AF, Abdalla OA. 2018. Biocontrol efficacy of Trichoderma spp. against sesame wilt caused by Fusarium oxysporum f. sp. sesami. Archives of Phytopathology and Plant Protection: 1-11.
Mayo S, Gutierrez S, Malmierca MG, Lorenzana A, Campelo MP, Hermosa R,Casquero PA. 2015. Influence of Rhizoctonia solani and Trichoderma spp. in growth of bean (Phaseolus vulgaris L.) and in the induction of plant defense-related genes. Frontiers in Plant Science 6 (685): 1-11
Mishra B, Mishra RK, Mishra R, Tiwari AK, Yadav RS, Dikshit A. 2011. Biocontrol efficacy of Trichoderma viride isolates against fungal plant pathogens causing disease in Vigna radiata L. Archives of Applied Science Research 3(2): 361-369.
Moosa A, Sahi ST, Haq IU, Farzand A, Khan SA, Javaid K. 2017. Antagonistic potential of Trichoderma isolates and manures against Fusarium wilt of tomato. International Journal of Vegetable Science 23(3): 207-218.
Morsy EM, Abdel-Kawi K, Khalil M. 2009. Efficiency of Trichoderma viride and Bacillus subtilis as biocontrol agents gainst Fusarium solani on tomato plants. Egyptian Journal of Phytopathology 37(1): 47-57.
Rahayu M. 2014. Identification and pathogenicity of pathogen responsible for aerial blight disease of soybean. Journal of Experimental Biology 2: 2S.
Rao GS, Reddy NNR, Surekha C. 2015. Induction of plant systemic resistance in Legumes Cajanus cajan, Vigna radiata, Vigna mungo against plant pathogens Fusarium oxysporum and Alternaria alternata–a Trichoderma viride mediated reprogramming of plant defense mechanism. International Journal of Recent Scientific Research 6(5): 4270-4280.
Rosmana A, Samuels GJ, Ismaiel A, Ibrahim ES, Chaverri P, Herawati Y, Asman A. 2015. Trichoderma asperellum: A dominant endophyte species in cacao grown in Sulawesi with potential for controlling vascular streak dieback disease. Tropical Plant Pathology 40(1): 19-25.
Saravanakumar K, Yu C, Dou K, Wang M, Li Y, Chen J. 2016. Synergistic effect of Trichoderma-derived antifungal metabolites and cell wall degrading enzymes on enhanced biocontrol of Fusarium oxysporum f. sp. cucumerinum. Biological control 94: 37-46.
Setyawan B, Rouf A, Setiono. 2014. Evaluation of Trichoderma spp. isolates combination for biological control of white root disease in rubber. In Purwono, Soeharto, Juarini, S. Wardoyo, Sumarwoto, O. S. Padmini (eds.) Proceeding of National Seminar of Sustainable Bioindustry Agriculture (pp. 239-246). UPN Veteran Yogyakarta, 11 December 2014. [Indonesian]
Setyorini SD, Yusnawan E. 2014. Fungi associated with wilt disease on mung bean germplasm. In Purwono, Soeharto, Juarini, S. Wardoyo, Sumarwoto, O. S. Padmini (eds.) Proceeding of National Seminar of Sustainable Bioindustry Agriculture (pp. 255-262). UPN Veteran Yogyakarta, 11 December 2014. [Indonesian]
Sharfuddin C, Mohanka R. 2012. In vitro antagonism of indigenous Trichoderma isolates against phytopathogen causing wilt of lentil. International Journal of Life Science & Pharma Research 2: 195-202.
Sundaramoorthy S, Balabaskar P. 2013. Biocontrol efficacy of Trichoderma spp. against wilt of tomato caused by Fusarium oxysporum f. sp. lycopersici. Journal of Applied Biology & Biotechnology 1(03): 36-40.
Tapwal A, Singh U, Singh G, Garg S, & Kumar R. 2011. In vitro antagonism of Trichoderma viride against five phytopathogens. Pest Technology 5(1): 59-62.
Woo SL, Ruocco M, Vinale F, Nigro M, Marra R, Lombardi N, Pascale A, Lanzuise S, Manganiello G, Lorito M. 2014. Trichoderma-based products and their widespread use in agriculture. The Open Mycology Journal 8(1): 71-126.
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.
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