Trichoderma virens-Tv4 enhances growth promoter and plant defense-related enzymes of mungbean (Vigna radiata) against soil-borne pathogen Rhizoctonia solani
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ALFI INAYATI
♥
LILIEK SULISTYOWATI
https://orcid.org/0000-0001-5241-1213
LUQMAN QURATA AINI
https://orcid.org/0000-0003-2577-534X
ERIYANTO YUSNAWAN
https://orcid.org/0000-0002-8641-8445
Abstract
Abstract. Inayati A, Sulistyowati L, Aini LQ, Yusnawan E. 2020. Trichoderma virens-Tv4 enhances growth promoter and plant defense-related enzymes of mungbean (Vigna radiata) against soil-borne pathogen Rhizoctonia solani. Biodiversitas 21: 2410-2419. Trichoderma virens has been studied for its ability to control various soil-borne pathogens as well as to induce plant resistance. The ability of T. virens control R. solani and its capability to induce resistance was evaluated in two different genotypes of mungbean (Vigna radiata (L.) R. Wilczek). Plant growth-promoting capability and production of plant defense-related enzymes during plant-pathogen-Trichoderma interaction were investigated. Pathogen infection caused the morphological and biochemical changes as well as increased plant defense enzymes activity such as peroxidase, polyphenol oxidase, PAL, phenolics, and flavonoid compared to control uninoculated plants. T. virens improved mungbean seedling growth in terms of increased total biomass, root weight, and root length as well as improved chlorophyll content and IAA-synthase from leaves and roots. T. virens treatment alone or in the presence of pathogen-induced mungbean defense-related enzymes indicated by the increasing of PO and PPO activity, and higher accumulation of total phenolic and flavonoid content. Although most of plant induced resistance parameters showed low and non-significant in direct single-factor comparison, Pearson’s correlation showed there was a positive correlation between plant growth promoter compounds (IAA and chlorophyll) with plant defense-related enzymes (total phenol, and flavonoid content). T. virens treatment can induce systemic defense response of mungbean seedling directly by increasing the activity of some defense-related enzymes, and indirectly by improving plant health, and promoting plant growth. In conclusion, T. virens-Tv4 has potential to be developed as bio-control agents to control R. solani as well as to induce mungbean resistance.
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References
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Bengyella, L., Waikhom, S. D., Allie, F., & Rey, C. (2015). Virus tolerance and recovery from viral induced-symptoms in plants are associated with transcriptome reprograming. Plant molecular biology, 89(3), 243-252.
Bhattacharya, A., Sood, P., & Citovsky, V. (2010). The roles of plant phenolics in defence and communication during Agrobacterium and Rhizobium infection. J Molecular plant pathology, 11(5), 705-719.
Castillejo, M. Á., Bani, M., & Rubiales, D. (2015). Understanding pea resistance mechanisms in response to Fusarium oxysporum through proteomic analysis. Phytochemistry, 115, 44-58. doi:https://doi.org/10.1016/j.phytochem.2015.01.009
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Howell, C., Stipanovic, R., & Lumsden, R. (1993). Antibiotic production by strains of Gliocladium virens and its relation to the biocontrol of cotton seedling diseases. Biocontrol science and technology, 3(4), 435-441.
Howell, C. R. (2006). Understanding the mechanisms employed by Trichoderma virens to effect biological control of cotton diseases. Phytopathology, 96(2), 178-180.
Kangasjärvi, S., Neukermans, J., Li, S., Aro, E.-M., & Noctor, G. (2012). Photosynthesis, photorespiration, and light signalling in defence responses. Journal of Experimental Botany, 63(4), 1619-1636. doi:10.1093/jxb/err402
Kavitha, R., & Umesha, S. (2008). Regulation of defense-related enzymes associated with bacterial spot resistance in tomato. J Phytoparasitica, 36(2), 144.
Kubalt, K. (2016). The role of phenolic compounds in plant resistance. Biotechnol Food Sci, 80(2), 97-108.
Lichtenthaler, H. K., & Buschmann, C. (2001). Chlorophylls and carotenoids: Measurement and characterization by UV?VIS spectroscopy. J Current protocols in food analytical chemistry, 1(1), F4. 3.1-F4. 3.8.
Løvdal, T., Olsen, K. M., Slimestad, R., Verheul, M., & Lillo, C. (2010). Synergetic effects of nitrogen depletion, temperature, and light on the content of phenolic compounds and gene expression in leaves of tomato. J Phytochemistry, 71(5-6), 605-613.
Mahanta, I. B. a. R. (2012). EVALUATION OF PEROXIDASES FROM VARIOUS PLANT SOURCES International Journal of Scientific and Research Publications, 2(5), 1-5.
Ma?olepsza, U., Nawrocka, J., & Szczech, M. (2017). Trichoderma virens 106 inoculation stimulates defence enzyme activities and enhances phenolic levels in tomato plants leading to lowered Rhizoctonia solani infection. Biocontrol science and technology, 27(2), 180-199.
Mandal, S. M., Chakraborty, D., & Dey, S. (2010). Phenolic acids act as signaling molecules in plant-microbe symbioses. J Plant signaling behavior, 5(4), 359-368.
Martínez-Medina, A., Alguacil, M. D. M., Pascual, J. A., & Van Wees, S. C. (2014). Phytohormone profiles induced by Trichoderma isolates correspond with their biocontrol and plant growth-promoting activity on melon plants. Journal of chemical ecology, 40(7), 804-815.
Martínez-Medina, A., Alguacil, M. M., Pascual, J., & van Wees, S. (2014). Phytohormone Profiles Induced by Trichoderma Isolates Correspond with Their Biocontrol and Plant Growth-Promoting Activity on Melon Plants (Vol. 40).
Martínez-Medina, A., Fernández, I., Sánchez-Guzmán, M. J., Jung, S. C., Pascual, J. A., & Pozo, M. J. (2013). Deciphering the hormonal signalling network behind the systemic resistance induced by Trichoderma harzianum in tomato. J Frontiers in plant science, 4, 206.
Martínez-Medina, A., Roldán, A., Albacete, A., & Pascual, J. A. (2011). The interaction with arbuscular mycorrhizal fungi or Trichoderma harzianum alters the shoot hormonal profile in melon plants. Phytochemistry, 72(2-3), 223-229.
Mazzei, P., Vinale, F., Woo, S. L., Pascale, A., Lorito, M., & Piccolo, A. (2016). Metabolomics by H-HRMAS-NMR of tomato plants treated with two secondary metabolites isolated from Trichoderma. J. Agric. Food. Chem, 64, 1021-1055.
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Pérez-Bueno, M. L., Pineda, M., & Barón, M. (2019). Phenotyping Plant Responses to Biotic Stress by Chlorophyll Fluorescence Imaging. Front.Plant.Sci, 10(1135). doi:10.3389/fpls.2019.01135
Phelps, R. H., & Sequeira, L. (1967). Synthesis of indoleacetic acid via tryptamine by a cell-free system from tobacco terminal buds. Plant physiology, 42(8), 1161.
Pieterse, C. M. J., Zamioudis, C., Berendsen, R. L., Weller, D. M., Van Wees, S. C. M., & Bakker, P. A. H. M. (2014). Induced Systemic Resistance by Beneficial Microbes. Annual Review of Phytopathology, 52(1), 347-375. doi:10.1146/annurev-phyto-082712-102340
Shakeri, J., & Foster, H. A. (2007). Proteolytic activity and antibiotic production by Trichoderma harzianum in relation to pathogenicity to insects. Enzyme and Microbial Technology, 40(4), 961-968.
Shoresh, M., & Harman, G. E. (2008). The molecular basis of shoot responses of maize seedlings to Trichoderma harzianum T22 inoculation of the root: a proteomic approach. J Plant physiology, 147(4), 2147-2163.
Shoresh, M., & Harman, G. E. (2010). Differential expression of maize chitinases in the presence or absence of Trichoderma harzianum strain T22 and indications of a novel exo-endo-heterodimeric chitinase activity. BMC plant biology, 10(1), 136.
Shoresh, M., Yedidia, I., & Chet, I. (2005). Involvement of jasmonic acid/ethylene signaling pathway in the systemic resistance induced in cucumber by Trichoderma asperellum T203. J Phytopathology, 95(1), 76-84.
Singh, B., Singh, A., Singh, B., & Singh, H. (2014). T richoderma harzianum elicits induced resistance in sunflower challenged by Rhizoctonia solani. Journal of Applied Microbiology, 116(3), 654-666.
Surekha, C., Neelapu, N., Prasad, B. S., & Ganesh, P. S. (2014). Induction of defense enzymes and phenolic content by Trichoderma viride in Vigna mungo infested with Fusarium oxysporum and Alternaria alternata. J Int J Agr Sci Res, 4(4), 31-40.
Team, R. J. R., Inc., Boston, MA URL http://www. rstudio. com. (2015). RStudio: integrated development for R. 42, 14.
Thakker, J. N., Patel, S., & Dhandhukia, P. C. (2012). Induction of defense-related enzymes in banana plants: Effect of live and dead pathogenic strain of Fusarium oxysporum f. sp. cubense. J ISRN biotechnology, 2013.
Treutter, D. (2005). Significance of flavonoids in plant resistance and enhancement of their biosynthesis. Plant biology, 7(06), 581-591.
Tucci, M., Ruocco, M., De Masi, L., De Palma, M., & Lorito, M. (2011). The beneficial effect of Trichoderma spp. on tomato is modulated by the plant genotype. Molecular plant pathology, 12(4), 341-354.
Van der Ent, S., Van Wees, S. C., & Pieterse, C. M. (2009). Jasmonate signaling in plant interactions with resistance-inducing beneficial microbes. J Phytochemistry, 70(13-14), 1581-1588.
Whipps, J. M., & Lumsden, R. D. (2001). Commercial use of fungi as plant disease biological control agents: status and prospects. Fungal biocontrol agents: progress, problems and potential, 9-22.
Woo, S., Scala, F., Ruocco, M., & Lorito, M. (2006). The molecular biology of the interactions between Trichoderma spp., phytopathogenic fungi, and plants. J Phytopathology, 96(2), 181-185.
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. doi:10.1371/journal.pone.0179957
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Ata, A., El-Samman, M., Moursy, M. A., & Mostafa, M. (2008). Inducing resistance against rust disease of sugar beet by certain chemical compounds. J Egyptian Journal of Phytopathology, 36, 113-132.
Bekkara, F., Jay, M., Viricel, M. R., & Rome, S. (1998). Distribution of phenolic compounds within seed and seedlings of two Vicia faba cvs differing in their seed tannin content, and study of their seed and root phenolic exudations. J Plant Soil, 203(1), 27-36.
Bengyella, L., Waikhom, S. D., Allie, F., & Rey, C. (2015). Virus tolerance and recovery from viral induced-symptoms in plants are associated with transcriptome reprograming. Plant molecular biology, 89(3), 243-252.
Bhattacharya, A., Sood, P., & Citovsky, V. (2010). The roles of plant phenolics in defence and communication during Agrobacterium and Rhizobium infection. J Molecular plant pathology, 11(5), 705-719.
Castillejo, M. Á., Bani, M., & Rubiales, D. (2015). Understanding pea resistance mechanisms in response to Fusarium oxysporum through proteomic analysis. Phytochemistry, 115, 44-58. doi:https://doi.org/10.1016/j.phytochem.2015.01.009
Constabel, C. P., & Barbehenn, R. (2008). Defensive roles of polyphenol oxidase in plants. In S. A. (Ed.), Induced Plant Resistance to Herbivory (pp. 253-270). Dordrecht: Springer.
Contreras-Cornejo, H. A., Macías-Rodríguez, L., Cortés-Penagos, C., & López-Bucio, J. (2009). Trichoderma virens, a plant beneficial fungus, enhances biomass production and promotes lateral root growth through an auxin-dependent mechanism in Arabidopsis. Plant physiology, 149(3), 1579-1592.
Dogbo, D., Gogbeu, S., N’zue, B., Ya, K., Zohouri, G., Mamyrbekova-Bekro, J., & Bekro, Y.-A. (2012). Comparative activities of phenylalanine ammonia-lyase and tyrosine ammonia-lyase and phenolic compounds accumulated in cassava elicited cell. J African Crop Science Journal, 20(2), 85-94.
Duba, A., Goriewa-Duba, K., Wachowska, U., G?owacka, K., & Wiwart, M. (2019). The Associations between Leaf Morphology, Phenylalanine Ammonia Lyase Activity, Reactive Oxygen Species, and Fusarium Resistance in Selected Species of Wheat with Different Ploidy Levels. Plants, 8(10), 360.
Dubey, S. C., Tripathi, A., & Tak, R. (2018). Expression of defense-related genes in mung bean varieties in response to Trichoderma virens alone and in the presence of Rhizoctonia solani infection. 3 Biotech, 8(10), 432.
Durairaj, K., Velmurugan, P., Park, J.-H., Chang, W.-S., Park, Y.-J., Senthilkumar, P., . . . Oh, B.-T. (2018). Characterization and assessment of two biocontrol bacteria against Pseudomonas syringae wilt in Solanum lycopersicum and its genetic responses. Microbiological Research, 206, 43-49. doi:https://doi.org/10.1016/j.micres.2017.09.003
Harman, G. E. (2011). Multifunctional fungal plant symbionts: new tools to enhance plant growth and productivity. New Phytologist, 189(3), 647-649.
Harman, G. E., Herrera-Estrella, A. H., Horwitz, B. A., & Lorito, M. (2012). Trichoderma-from basic biology to biotechnology. J Microbiology-Reading, 158(1), 1.
Harman, G. E., Howell, C. R., Viterbo, A., Chet, I., & Lorito, M. (2004). Trichoderma species — opportunistic, avirulent plant symbionts. Nature Reviews Microbiology, 2, 43. doi:10.1038/nrmicro797
Hermosa, R., Viterbo, A., Chet, I., & Monte, E. (2012). Plant-beneficial effects of Trichoderma and of its genes. J Microbiology, 158(1), 17-25.
Hoagland, R. E. (1990). Biochemical responses of plants to pathogens. In R. E. Hoagland (Ed.), Microbes and Microbial Products as Herbicides (Vol. 439): ACS Publications.
Howell, C. (2003). Mechanisms employed by Trichoderma species in the biological control of plant diseases: the history and evolution of current concepts. Plant Disease, 87(1), 4-10.
Howell, C., Stipanovic, R., & Lumsden, R. (1993). Antibiotic production by strains of Gliocladium virens and its relation to the biocontrol of cotton seedling diseases. Biocontrol science and technology, 3(4), 435-441.
Howell, C. R. (2006). Understanding the mechanisms employed by Trichoderma virens to effect biological control of cotton diseases. Phytopathology, 96(2), 178-180.
Kangasjärvi, S., Neukermans, J., Li, S., Aro, E.-M., & Noctor, G. (2012). Photosynthesis, photorespiration, and light signalling in defence responses. Journal of Experimental Botany, 63(4), 1619-1636. doi:10.1093/jxb/err402
Kavitha, R., & Umesha, S. (2008). Regulation of defense-related enzymes associated with bacterial spot resistance in tomato. J Phytoparasitica, 36(2), 144.
Kubalt, K. (2016). The role of phenolic compounds in plant resistance. Biotechnol Food Sci, 80(2), 97-108.
Lichtenthaler, H. K., & Buschmann, C. (2001). Chlorophylls and carotenoids: Measurement and characterization by UV?VIS spectroscopy. J Current protocols in food analytical chemistry, 1(1), F4. 3.1-F4. 3.8.
Løvdal, T., Olsen, K. M., Slimestad, R., Verheul, M., & Lillo, C. (2010). Synergetic effects of nitrogen depletion, temperature, and light on the content of phenolic compounds and gene expression in leaves of tomato. J Phytochemistry, 71(5-6), 605-613.
Mahanta, I. B. a. R. (2012). EVALUATION OF PEROXIDASES FROM VARIOUS PLANT SOURCES International Journal of Scientific and Research Publications, 2(5), 1-5.
Ma?olepsza, U., Nawrocka, J., & Szczech, M. (2017). Trichoderma virens 106 inoculation stimulates defence enzyme activities and enhances phenolic levels in tomato plants leading to lowered Rhizoctonia solani infection. Biocontrol science and technology, 27(2), 180-199.
Mandal, S. M., Chakraborty, D., & Dey, S. (2010). Phenolic acids act as signaling molecules in plant-microbe symbioses. J Plant signaling behavior, 5(4), 359-368.
Martínez-Medina, A., Alguacil, M. D. M., Pascual, J. A., & Van Wees, S. C. (2014). Phytohormone profiles induced by Trichoderma isolates correspond with their biocontrol and plant growth-promoting activity on melon plants. Journal of chemical ecology, 40(7), 804-815.
Martínez-Medina, A., Alguacil, M. M., Pascual, J., & van Wees, S. (2014). Phytohormone Profiles Induced by Trichoderma Isolates Correspond with Their Biocontrol and Plant Growth-Promoting Activity on Melon Plants (Vol. 40).
Martínez-Medina, A., Fernández, I., Sánchez-Guzmán, M. J., Jung, S. C., Pascual, J. A., & Pozo, M. J. (2013). Deciphering the hormonal signalling network behind the systemic resistance induced by Trichoderma harzianum in tomato. J Frontiers in plant science, 4, 206.
Martínez-Medina, A., Roldán, A., Albacete, A., & Pascual, J. A. (2011). The interaction with arbuscular mycorrhizal fungi or Trichoderma harzianum alters the shoot hormonal profile in melon plants. Phytochemistry, 72(2-3), 223-229.
Mazzei, P., Vinale, F., Woo, S. L., Pascale, A., Lorito, M., & Piccolo, A. (2016). Metabolomics by H-HRMAS-NMR of tomato plants treated with two secondary metabolites isolated from Trichoderma. J. Agric. Food. Chem, 64, 1021-1055.
Moharana, S., & Dutta, S. (2016). Spatial variability of chlorophyll and nitrogen content of rice from hyperspectral imagery. J ISPRS journal of photogrammetry remote sensing, 122, 17-29.
Mukherjee, M., Mukherjee, P. K., Horwitz, B. A., Zachow, C., Berg, G., & Zeilinger, S. (2012). Trichoderma-plant-pathogen interactions: advances in genetics of biological control. Indian journal of microbiology, 52(4), 522-529. doi:10.1007/s12088-012-0308-5
Pérez-Bueno, M. L., Pineda, M., & Barón, M. (2019). Phenotyping Plant Responses to Biotic Stress by Chlorophyll Fluorescence Imaging. Front.Plant.Sci, 10(1135). doi:10.3389/fpls.2019.01135
Phelps, R. H., & Sequeira, L. (1967). Synthesis of indoleacetic acid via tryptamine by a cell-free system from tobacco terminal buds. Plant physiology, 42(8), 1161.
Pieterse, C. M. J., Zamioudis, C., Berendsen, R. L., Weller, D. M., Van Wees, S. C. M., & Bakker, P. A. H. M. (2014). Induced Systemic Resistance by Beneficial Microbes. Annual Review of Phytopathology, 52(1), 347-375. doi:10.1146/annurev-phyto-082712-102340
Shakeri, J., & Foster, H. A. (2007). Proteolytic activity and antibiotic production by Trichoderma harzianum in relation to pathogenicity to insects. Enzyme and Microbial Technology, 40(4), 961-968.
Shoresh, M., & Harman, G. E. (2008). The molecular basis of shoot responses of maize seedlings to Trichoderma harzianum T22 inoculation of the root: a proteomic approach. J Plant physiology, 147(4), 2147-2163.
Shoresh, M., & Harman, G. E. (2010). Differential expression of maize chitinases in the presence or absence of Trichoderma harzianum strain T22 and indications of a novel exo-endo-heterodimeric chitinase activity. BMC plant biology, 10(1), 136.
Shoresh, M., Yedidia, I., & Chet, I. (2005). Involvement of jasmonic acid/ethylene signaling pathway in the systemic resistance induced in cucumber by Trichoderma asperellum T203. J Phytopathology, 95(1), 76-84.
Singh, B., Singh, A., Singh, B., & Singh, H. (2014). T richoderma harzianum elicits induced resistance in sunflower challenged by Rhizoctonia solani. Journal of Applied Microbiology, 116(3), 654-666.
Surekha, C., Neelapu, N., Prasad, B. S., & Ganesh, P. S. (2014). Induction of defense enzymes and phenolic content by Trichoderma viride in Vigna mungo infested with Fusarium oxysporum and Alternaria alternata. J Int J Agr Sci Res, 4(4), 31-40.
Team, R. J. R., Inc., Boston, MA URL http://www. rstudio. com. (2015). RStudio: integrated development for R. 42, 14.
Thakker, J. N., Patel, S., & Dhandhukia, P. C. (2012). Induction of defense-related enzymes in banana plants: Effect of live and dead pathogenic strain of Fusarium oxysporum f. sp. cubense. J ISRN biotechnology, 2013.
Treutter, D. (2005). Significance of flavonoids in plant resistance and enhancement of their biosynthesis. Plant biology, 7(06), 581-591.
Tucci, M., Ruocco, M., De Masi, L., De Palma, M., & Lorito, M. (2011). The beneficial effect of Trichoderma spp. on tomato is modulated by the plant genotype. Molecular plant pathology, 12(4), 341-354.
Van der Ent, S., Van Wees, S. C., & Pieterse, C. M. (2009). Jasmonate signaling in plant interactions with resistance-inducing beneficial microbes. J Phytochemistry, 70(13-14), 1581-1588.
Whipps, J. M., & Lumsden, R. D. (2001). Commercial use of fungi as plant disease biological control agents: status and prospects. Fungal biocontrol agents: progress, problems and potential, 9-22.
Woo, S., Scala, F., Ruocco, M., & Lorito, M. (2006). The molecular biology of the interactions between Trichoderma spp., phytopathogenic fungi, and plants. J Phytopathology, 96(2), 181-185.
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. doi:10.1371/journal.pone.0179957
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