Exploration and characterization of indigenous Trichoderma spp. as antagonist of Rhizoctonia solani and plant growth promoter of maize




Abstract. Iswati R, Aini LQ, Soemarno, Abadi AL. 2024. Exploration and characterization of indigenous Trichoderma spp. as antagonist of Rhizoctonia solani and plant growth promoter of maize. Biodiversitas 25: 1375-1385. Maize sheath blight disease, caused by Rhizoctonia solani, is the main maize disease in Gorontalo and is widespread from the lowlands to the highlands. The indigenous Trichoderma spp. is known to function as a biocontrol agent while producing secondary metabolites that promote plant growth. The objective of this study was to isolate, select, and identify indigenous Trichoderma strains that act as antagonistic agents and promote maize plants growth. The bulk of the soil samples were collected from the rhizosphere of maize plantations in the lowland (0-300 masl), medium (300-500 masl), and highland (500-1000 masl) regions at several sites in Gorontalo. Trichoderma spp. isolation was carried out using the serial dilution method on Rose Bengal chloramphenicol medium, and the strains were further purified in PDA medium, followed by morphological and molecular identification. The antagonistic effect was assessed using dual culture method. In addition, the plant growth-promoting traits examined were qualitative IAA production, potassium solubilization, phosphate solubilization, and in vivo for maize plant growth promotion. Molecular identification revealed that the indigenous fungal strains were dominated by three species, namely, Trichoderma asperellum, T. virens, and T. brevicompactum. Other strains identified were T. ghanense, T. reesei, and T. dorothopsis. Of the 30 Trichoderma spp. strains, 25 inhibited R. solani more than 50%. All Trichoderma spp. strains can produce IAA qualitatively and dissolve phosphate at different intensities; only one fungal strain namely T. dorothopsis-TZ31LU1, can solubilize potassium. In addition, several indigenous Trichoderma spp. strains were able to increase the growth of maize plants in vivo. Thus, 25 Trichoderma spp. strains had the potential to be developed as biological control agents for maize sheath blight disease as well as plant growth promoters in maize.


Asad, S.A., Tabassum, A., Hameed, A., Ul Hassan, F., Afzal, A., Khan, S.A., Ahmed, R., Shahzad, M., 2015. Determination of lytic enzyme activities of indigenous trichoderma isolates from Pakistan. Brazilian J. Microbiol. 46, 1053–1064. https://doi.org/10.1590/S1517-838246420140787
Badan Karantina Pertanian, 2018. Eksport Jagung Gorontalo 2018 [WWW Document]. URL https://www.google.com/search iqfast.karantina.pertanian.go.id iqfast.karantina.pertanian.go.id
Bader, A.N., Salerno, G.L., Covacevich, F., Consolo, V.F., 2020. Native Trichoderma harzianum strains from Argentina produce indole-3 acetic acid and phosphorus solubilization, promote growth and control wilt disease on tomato (Solanum lycopersicum L.). J. King Saud Univ. - Sci. 32, 867–873. https://doi.org/10.1016/j.jksus.2019.04.002
Bayoumi, Y., Taha, N., Shalaby, T., Alshaal, T., El-Ramady, H., 2019. Sulfur promotes biocontrol of purple blotch disease via Trichoderma spp. and enhances the growth, yield and quality of onion. Appl. Soil Ecol. 134, 15–24. https://doi.org/10.1016/j.apsoil.2018.10.011
BPS, 2022. Statistik Indonesia 2022 statistical yearbook of Indonesia 2022. Jakarta : BPS.
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 Physiol. 149, 1579–1592. https://doi.org/10.1104/pp.108.130369
Damalas, C.A., Eleftherohorinos, I.G., 2011. Pesticide exposure, safety issues, and risk assessment indicators. Int. J. Environ. Res. Public Health 8, 1402–1419. https://doi.org/10.3390/ijerph8051402
Dinas Pertanian Gorontalo, 2018. Laporan Tahunan?: Laporan tahun 2017. Pemerintah Daerah Provinsi Gorontalo.
Ghasemi, S., Safaie, N., Shahbazi, S., Shams-Bakhsh, M., Askari, H., 2020. The role of cell wall degrading enzymes in antagonistic traits of trichoderma virens against rhizoctonia solani. Iran. J. Biotechnol. 18, 18–28. https://doi.org/10.30498/IJB.2020.2333
Haque, M.A., Marwaha, S., Deb, C.K., Nigam, S., Arora, A., Hooda, K.S., Soujanya, P.L., Aggarwal, S.K., Lall, B., Kumar, M., Islam, S., Panwar, M., Kumar, P., Agrawal, R.C., 2022. Deep learning-based approach for identification of diseases of maize crop. Sci. Rep. 12, 1–14. https://doi.org/10.1038/s41598-022-10140-z
He, A. le, Liu, J., Wang, X. hua, Zhang, Q. guo, Song, W., Chen, J., 2019. Soil application of Trichoderma asperellum GDFS1009 granules promotes growth and resistance to Fusarium graminearum in maize. J. Integr. Agric. 18, 599–606. https://doi.org/10.1016/S2095-3119(18)62089-1
Herrera, W., Valbuena, O., Pavone-Maniscalco, D., 2020. Formulation of Trichoderma asperellum TV190 for biological control of Rhizoctonia solani on corn seedlings. Egypt. J. Biol. Pest Control 30. https://doi.org/10.1186/s41938-020-00246-9
Hu, X., Chen, J., Guo, J., 2006. Two phosphate- and potassium-solubilizing bacteria isolated from Tianmu Mountain, Zhejiang, China. World J. Microbiol. Biotechnol. 22, 983–990. https://doi.org/10.1007/s11274-006-9144-2
Jayalakshmi, S.K., Raju, S., Usha Rani, S., Benagi, V.I., 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. Aust. J. Crop Sci. 3, 44–52.
Ji, S., Liu, Z., Liu, B., Wang, Y., Wang, J., 2020. The effect of Trichoderma biofertilizer on the quality of flowering Chinese cabbage and the soil environment. Sci. Hortic. (Amsterdam). 262. https://doi.org/10.1016/j.scienta.2019.109069
Jogaiah, S., Abdelrahman, M., Tran, L.S.P., Ito, S.I., 2018. Different mechanisms of Trichoderma virens-mediated resistance in tomato against Fusarium wilt involve the jasmonic and salicylic acid pathways. Mol. Plant Pathol. 19, 870–882. https://doi.org/10.1111/mpp.12571
Kamal, R.K., 2018. Trichoderma: a Most Common Biofertilizer with Multiple Roles in Agriculture. Biomed. J. Sci. Tech. Res. 4, 4136–4137. https://doi.org/10.26717/bjstr.2018.04.0001107
Kamaruzzaman, M., Islam, M.S., Mahmud, S., Polash, S.A., Sultana, R., Hasan, M.A., Wang, C., Jiang, C., 2021. In vitro and in silico approach of fungal growth inhibition by Trichoderma asperellum HbGT6-07 derived volatile organic compounds. Arab. J. Chem. 14, 103290. https://doi.org/10.1016/j.arabjc.2021.103290
Kementerian Pertanian Republik Indonesia, 2018. Data Lima Tahun Terakhir [WWW Document]. URL https://www.pertanian.go.id/home/?show=page&act=view&id=61 (accessed 8.20.23).
Khan, F., Siddique, A.B., Shabala, S., Zhou, M., Zhao, C., 2023. Phosphorus Plays Key Roles in Regulating Plants’ Physiological Responses to Abiotic Stresses. Plants 12. https://doi.org/10.3390/plants12152861
Khan, M.Y., Haque, M.M., Molla, A.H., Rahman, M.M., Alam, M.Z., 2017. Antioxidant compounds and minerals in tomatoes by Trichoderma-enriched biofertilizer and their relationship with the soil environments. J. Integr. Agric. 16, 691–703. https://doi.org/10.1016/S2095-3119(16)61350-3
Lesmana, A., Rianto, F., Sarbino, 2019. Exploration of Trichoderma spp From Rice Fields Area That Have the Potential as Biological Fertilizer. J. Sains Pertan. Equator 8.
Li, M.F., Li, G.H., Zhang, K.Q., 2019. Non-volatile metabolites from Trichoderma spp. Metabolites 9. https://doi.org/10.3390/metabo9030058
Lim, J.A., Yaacob, J.S., Rasli, S.R.A.M., Eyahmalay, J.E., El Enshasy, H.A., Zakaria, M.R.S., 2023. Mitigating the repercussions of climate change on diseases affecting important crop commodities in Southeast Asia, for food security and environmental sustainability—A review. Front. Sustain. Food Syst. 6, 1–23. https://doi.org/10.3389/fsufs.2022.1030540
Manandhar, S., Pant, B., Manandhar, C., Baidya, S., 2019. In-vitro Evaluation of Bio-control agents against Soil Borne Plant Pathogens. J. Nepal Agric. Res. Counc. 5, 68–72. https://doi.org/10.3126/jnarc.v5i1.23810
Mirsam, H., Suriani, Kurniawati, S., Purwanto, O.D., Muis, A., Pakki, S., Tenrirawe, A., Nonci, N., Herawati, Muslimin, Azrai, M., 2023a. In vitro inhibition mechanism of Trichoderma asperellum isolates from corn against Rhizoctonia solani causing banded leaf and sheath blight disease and its role in improving the growth of corn seedlings. Egypt. J. Biol. Pest Control 33, 1–14. https://doi.org/10.1186/s41938-023-00729-5
Mirsam, H., Suriani, Kurniawati, S., Purwanto, O.D., Muis, A., Pakki, S., Tenrirawe, A., Nonci, N., Herawati, Muslimin, Azrai, M., 2023b. In vitro inhibition mechanism of Trichoderma asperellum isolates from corn against Rhizoctonia solani causing banded leaf and sheath blight disease and its role in improving the growth of corn seedlings. Egypt. J. Biol. Pest Control 33. https://doi.org/10.1186/s41938-023-00729-5
Muimba-Kankolongo, A., 2018. Cereal Production, in: Food Crop Production by Smallholder Farmers in Southern Africa. Elsevier, pp. 73–121. https://doi.org/10.1016/B978-0-12-814383-4.00008-6
Mukherjee, P.K., Mendoza-Mendoza, A., Zeilinger, S., Horwitz, B.A., 2022. Mycoparasitism as a mechanism of Trichoderma-mediated suppression of plant diseases. Fungal Biol. Rev. 39, 15–33. https://doi.org/10.1016/j.fbr.2021.11.004
Ngo, T., Van Nguyen, M., Han, J.W., Park, M.S., Kim, H., Choi, G.J., 2021. In vitro and in vivo antifungal activity of sorbicillinoids produced by trichoderma longibrachiatum men. J. Fungi 7. https://doi.org/10.3390/jof7060428
Nikmah, B.M., 2017. Uji Efektivitas Berbagai Media Selektif untuk Seleksi Trichoderma spp. dari Tanah pada Berbagai Lahan yang Berbeda. Universitas Brawijaya.
Ommati, F., Zaker, M., 2012. In vitro and greenhouse evaluations of Trichoderma isolates for biological control of potato wilt disease (Fusarium solani). Arch. Phytopathol. Plant Prot. 45, 1715–1723. https://doi.org/10.1080/03235408.2012.702467
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. Biotechnol. Lett. 35, 1461–1468. https://doi.org/10.1007/s10529-013-1225-3
Rai, D., Singh, S.K., 2018. Is Banded Leaf and Sheath Blight a Potential Threat to Maize Cultivation in Bihar? Int. J. Curr. Microbiol. Appl. Sci. 7, 671–683. https://doi.org/10.20546/ijcmas.2018.711.080
Saxena, A., Raghuwanshi, R., Singh, H.B. ahadu., 2015. Trichoderma species mediated differential tolerance against biotic stress of phytopathogens in Cicer arietinum L. J. Basic Microbiol. 55, 195–206. https://doi.org/10.1002/jobm.201400317
Setiawati, T.C., Mutmainnah, L., 2016. Solubilization of Potassium Containing Mineral by Microorganisms From Sugarcane Rhizosphere. Agric. Agric. Sci. Procedia 9, 108–117. https://doi.org/10.1016/j.aaspro.2016.02.134
Sharon, J.A., Hathwaik, L.T., Glenn, G.M., Imam, S.H., Lee, C.C., 2016. Isolation of efficient phosphate solubilizing bacteria capable of enhancing tomato plant growth. J. Soil Sci. Plant Nutr. 16, 525–536. https://doi.org/10.4067/S0718-95162016005000043
Shentu, X.P., Liu, W.P., Zhan, X.H., Yu, X.P., Zhang, C.X., 2013. The elicitation effect of pathogenic fungi on trichodermin production by trichoderma brevicompactum. Sci. World J. 2013. https://doi.org/10.1155/2013/607102
Silva, P.H.V., Souza, A.G.V., de Araujo, L.D., Frezarin, E.T., de Souza, G.V.L., da Silveira, C.M., Rigobelo, E.C., 2023. Trichoderma harzianum and Bacillus subtilis in Association with Rock Powder for the Initial Development of Maize Plants. Agronomy 13, 1–15. https://doi.org/10.3390/agronomy13030872
Skidmore, A.M., Dickinson, C.H., 1976. Colony interactions and hyphal interference between Septoria nodorum and phylloplane fungi. Trans. Br. Mycol. Soc. 66, 57–64. https://doi.org/10.1016/s0007-1536(76)80092-7
Soenartiningsih, Djaenuddin, N., Saenong, M.S., 2014. Efektivitas Trichoderma sp. dan Gliocladium sp. sebagai Agen Biokontrol Hayati Penyakit Busuk Pelepah Daun pada Jagung. Penelit. Pertan. Tanam. Pangan 33, 129–135.
Sood, M., Kapoor, D., Kumar, V., Sheteiwy, M.S., 2020. Trichoderma?: The “ Secrets ” of a Multitalented. Plants 9, 762.
Stracquadanio, C., Quiles, J.M., Meca, G., Cacciola, S.O., 2020. Antifungal activity of bioactive metabolites produced by trichoderma asperellum and trichoderma atroviride in liquid medium. J. Fungi 6, 1–18. https://doi.org/10.3390/jof6040263
Susiana, P., Achmadi, P., Retno, P.S., Rina, S.K., Kadarwati, B., 2018. The Resistance of Potatoes by Application of Trichoderma viride Antagonists Fungus. E3S Web Conf. 73. https://doi.org/10.1051/e3sconf/20187306014
Tabarestani, M.S., Rahnama, K., Jahanshahi, M., Nasrollahnejad, S., Fatemi, M.H., 2016. Identification of volatile organic compounds of Trichoderma spp. using static headspace gas chromatography-mass spectrometry. Mycol. Iran. 3, 47–55. https://doi.org/10.22043/mi.2017.41532.1072
Talib, H.A., 2017. Potensi Kehilangan Hasil akibat Penyakit pada Tanaman Jagung (Zea Mays) di Desa Tolite Jaya Kecamatan Tolingula Kabupaten Gorontalo Utara. Universitas Negeri Gorontalo. https://repository.ung.ac.id/skripsi/show/613412036/kehilangan-hasil-akibat-penyakit-pada-tanaman-jagung-zea-mays-l-di-desa-tolite-jaya-kecamatan-tolinggula-kabupaten-gorontalo-utara.html
Tenteyali, M.S., 2016. Potensi Kehilangan Hasil akibat Penyakit pada Tanaman Jagung (Zea Mays) di Desa Trirukun Kecamatan Wonosari Kabupaten Boalemo. Universitas Negeri Gorontalo. https://repository.ung.ac.id/en/skripsi/show/613412092/jenis-penyakit-dan-kehilangan-hasil-akibat-penyakit-pada-tanaman-jagung-zea-mays-di-desa-trirukun-kecamatan-wonosari-kabupaten-boalemo.html
Tzelepis, G., Dubey, M., Jensen, D.F., Karlsson, M., 2015. Identifying glycoside hydrolase family 18 genes in the mycoparasitic fungal species clonostachys rosea. Microbiol. (United Kingdom) 161, 1407–1419. https://doi.org/10.1099/mic.0.000096
Yadav, K., Damodaran, T., Kumari, N., Dutt, K., Gopal, R., Muthukumar, M., 2020. Characterization of Trichoderma isolates and assessment of antagonistic potential against Fusarium oxysporum f. sp. cumini. J. Appl. Hortic. 22, 38–44. https://doi.org/10.37855/jah.2020.v22i01.08
Yu, Z., Wang, Z., Zhang, Y., Wang, Y., Liu, Z., 2021. Biocontrol and growth-promoting effect of Trichoderma asperellum TaspHu1 isolate from Juglans mandshurica rhizosphere soil. Microbiol. Res. 242, 126596. https://doi.org/10.1016/j.micres.2020.126596
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. https://doi.org/10.13057/biodiv/d200735
Zamioudis, C., Mastranesti, P., Dhonukshe, P., Blilou, I., Pieterse, C.M.J., 2013. Unraveling root developmental programs initiated by beneficial Pseudomonas spp. Bacteria. Plant Physiol. 162, 304–318. https://doi.org/10.1104/pp.112.212597
Zhang, F., Yuan, J., Yang, X., Cui, Y., Chen, L., Ran, W., Shen, Q., 2013. Putative Trichoderma harzianum mutant promotes cucumber growth by enhanced production of indole acetic acid and plant colonization. Plant Soil 368, 433–444. https://doi.org/10.1007/s11104-012-1519-6
Zhao, L., Zhang, Y.Q., 2015. Effects of phosphate solubilization and phytohormone production of Trichoderma asperellum Q1 on promoting cucumber growth under salt stress. J. Integr. Agric. 14, 1588–1597. https://doi.org/10.1016/S2095-3119(14)60966-7

Most read articles by the same author(s)

1 2 > >>