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Unveiling the biocontrol potential of Trichoderma

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Abstract   

Trichoderma, a well-known fungal genus and opportunistic plant symbiont, is a quintessential alternative to chemicals with great potential to minimize disease incidence. The mycoparasitic ability along with antibiosis and induction of host immunity are the main mechanisms of biocontrol by this fungus. Fungi belonging to genus Trichoderma have been identified as potential biocontrol agents due to majority of isolated antifungal bioactive compounds. This review summarizes the biological control activity exerted by Trichoderma spp. against plant pathogenic fungi, bacteria, viruses, nematodes and insect pests. In addition, the research on formulations advocates that encapsulation could be a promising tool for increasing efficacy and durability of these fungi under field conditions. Further, advances in different areas of science and technology would strengthen the future research on Trichoderma-based products for its efficient use in agriculture.

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References

  • Ab Rahman, S. S., Singh, E., Pieterse, C. M., & Schenk, P. M. (2018). Emerging microbial biocontrol strategies for plant pathogens. Plant Science, 267, 102–111.

    Google Scholar 

  • Abbasi, K., Zafari, D., Wick, R., & Hamedan, I. (2017). Evaluation of chitinase enzyme in fungal isolates obtained from golden potato cyst nematode (Globoderarostochiensis). Žemdirbystė (agriculture), 104(2), 179–184.

    Google Scholar 

  • Abd-El-Khair, H., Abdel-Gaied, T. G., Mikhail, M. S., Abdel-Alim, A. I., & El-Nasr, H. I. S. (2021). Biological control of Pectobacterium carotovorum subsp. carotovorum, the causal agent of bacterial soft rot in vegetables, in vitro and in vivo tests. Bulletin of the National Research Centre, 45(1), 1–9.

    Google Scholar 

  • Abdelkhalek, A., Al-Askar, A. A., Arishi, A. A., & Behiry, S. I. (2022). Trichoderma hamatum strain Th23 promotes tomato growth and induces systemic resistance against Tobacco Mosaic Virus. Journal of Fungi, 8(3), 228.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Abdel-Shafi, S., Abdel-Gawd, S., & Sleem, E. (2013). Induction of systemic resistance and enhanced enzyme activity by Trichoderma sp. Shmosa Tri (FJ 937359) in Squash against Zucchini Yellow Mosaic Virus (ZYMV). Egyptian Journal of Botany, 3rd International Con 17-18 April (pp. 539–558) Helwan University.

  • Abdenaceur, R., Farida, B. T., Mourad, D., Rima, H., Zahia, O., & Fatma, S. H. (2022). Effective biofertilizer Trichoderma spp. isolates with enzymatic activity and metabolites enhancing plant growth. International Microbiology, 25(4), 817–829.

    CAS  PubMed  Google Scholar 

  • Abelyousr, K. A. M., & Almasaudi, N. (2022). Application of Trichoderma harzianum Strain KABOFT4 for management of tomato bacterial wilt under greenhouse conditions. Gesunde Pflanzen, 74(2), 413–421.

    Google Scholar 

  • Agrios, G. N. (2005). Plant Pathology. Elsevier Academic Press.

    Google Scholar 

  • AL-Abedy, A. N., Al-Shujairi, K. A., Al-Salami, I., Ashfaq, M., & AL-Musawi, B. H. (2021). Genetic variation among some isolates of tomato yellow leaf curl virus and its control using some biological control fungi and nanoparticles. International Journal of Agricultural and Statistical Sciences, 17(1), 229–236.

    Google Scholar 

  • Al-Askar, A. A., Saber, W. I., Ghoneem, K. M., Hafez, E. E., & Ibrahim, A. A. (2021). Crude citric acid of Trichoderma asperellum: tomato growth promotor and suppressor of Fusarium oxysporum f. sp. lycopersici. Plants, 10(2), 222.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Almeida, N. O., de Oliveira, C. M., Ulhoa, C. J., Cortes, M. V. D. C. B., Júnior, M. L., & da Rocha, M. R. (2022). Trichoderma harzianum and Trichoderma asperellum are potential biocontrol agents of Meloidogyne javanica in banana cv. Grande Naine. Biological Control, 175, 105054.

    Google Scholar 

  • Anwar, J., & Iqbal, Z. (2017). Effect of growth conditions on antibacterial activity of Trichoderma harzianum against selected pathogenic bacteria. Sarhad Journal of Agriculture, 33(4), 501–510.

    Google Scholar 

  • Anwar, W., Subhani, M. N., Haider, M. S., Shahid, A. A., Mushatq, H., Rehman, M. Z., & Javed, S. (2016). First record of Trichoderma longibrachiatum as entomopathogenic fungi against Bemisia tabaci in Pakistan. Pakistan Journal of Phytopathology, 28(2), 287–294.

    Google Scholar 

  • Atanasova, L., Druzhinina, I. S., Jaklitsch, W. M., Mukherjee, P., Horwitz, B., & Singh, U. (2013). Two hundred Trichoderma species recognized on the basis of molecular phylogeny. In P. Mukherjee, B. A. Horwitz, U. S. Singh, M. Mukherjee, & M. Schmoll (Eds.), Trichoderma: biology and applications (pp. 10–42). CABI.

    Google Scholar 

  • Babu, B. V., Kamra, A., Paul, S., & Devi, T. P. (2019). Antibiosis and egg parasitization in root-knot nematode., Meloidogyne incognita by indigenous isolates of Trichoderma harzianum rifai, 1969 in relation to chitinase and protease levels. Indian Journal of Nematology, 49(2), 187–192.

    Google Scholar 

  • Baiyee, B., Ito, S. I., & Sunpapao, A. (2019). Trichoderma asperellum T1 mediated antifungal activity and induced defense response against leaf spot fungi in lettuce (Lactuca sativa L.). Physiological and Molecular Plant Pathology, 106, 96–101.

    CAS  Google Scholar 

  • Barakat, F. M., Abada, K. A., Abou-Zeid, N. M., & El-Gammal, Y. H. E. (2014). Effect of volatile and non-volatile compounds of Trichoderma spp. on Botrytis fabae the causative agent of faba bean chocolate spot. American Journal of Life Sciences, 2, 11–18.

    Google Scholar 

  • Battaglia, D., Bossi, S., Cascone, P., Digilio, M. C., Prieto, J. D., Fanti, P., ... & Trotta, V. (2013). Tomato below ground–above ground interactions: Trichoderma longibrachiatum affects the performance of Macrosiphum euphorbiae and its natural antagonists. Molecular plant-microbe interactions, 26(10), 1249-1256.

  • Berbert, P. S., Vieira, P. M., Cabral, G. B., Martins, E. C., Wulff, N. A., Ulhoa, C. J., & Aragão, F. J. (2022). Expression of a sphingomyelinase-coding gene from Trichoderma harzianum conferred bacterial tolerance in tobacco. Plant Pathology, 71(5), 1048–1055.

    CAS  Google Scholar 

  • Berini, F., Caccia, S., Franzetti, E., Congiu, T., Marinelli, F., Casartelli, M., & Tettamanti, G. (2016). Effects of Trichoderma viride chitinases on the peritrophic matrix of Lepidoptera. Pest Management Science, 72(5), 980–989.

    CAS  PubMed  Google Scholar 

  • Bernard, G. C., Egnin, M., & Bonsi, C. (2017). The impact of plant-parasitic nematodes on agriculture and methods of control. Nematology Concepts, Diagnosis and Control, 10, 121–151.

    Google Scholar 

  • Bisen, K., Keswani, C., Patel, J. S., Sarma, B. K., & Singh, H. B. (2016). Trichoderma spp efficient inducers of systemic resistance in plants. In D. K. Chaudhary & A. Verma (Eds.), Microbial-mediated induced systemic resistance in plants (pp. 185–195). Singapore: Springer.

    Google Scholar 

  • Bissett, J., Szakacs, G., Nolan, C. A., Druzhinina, I., Gradinger, C., & Kubicek, C. P. (2003). New species of Trichoderma from Asia. Canadian Journal of Botany, 81(6), 570–586.

    Google Scholar 

  • Bissett, J., Gams, W., Jaklitsch, W., & Samuels, G. J. (2015). Trichoderma names in the year 2015. IMA Fungus, 6, 263–295.

    PubMed  PubMed Central  Google Scholar 

  • Bononi, L., Chiaramonte, J. B., Pansa, C. C., Moitinho, M. A., & Melo, I. S. (2020). Phosphorus-solubilizing Trichoderma spp. from Amazon soils improves soybean plant growth. Scientific Reports, 10(1), 2858.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Braithwaite, M., Clouston, A., Minchin, R., Yardley, J., Nieto-Jacobo, M. F., Mendoza-Mendoza, A., Steyaert, J., Hill, R., Marshall, J., & Stewart, A. (2016). The density-dependent effect of initial nematode population levels on the efficacy of Trichoderma as a bio-nematicide against Meloidogyne hapla on tomato. Australasian Plant Pathology, 45, 473–479.

    Google Scholar 

  • Brondi, M., Florencio, C., Mattoso, L., Ribeiro, C., & Farinas, C. (2022). Encapsulation of Trichoderma harzianum with nanocellulose/carboxymethyl cellulose nanocomposite. Carbohydrate Polymers, 295, 119876.

    CAS  PubMed  Google Scholar 

  • Cai, F., Dou, K., Wang, P., Chenthamara, K., Chen, J., & Druzhinina, I. S. (2022). The current state of Trichoderma taxonomy and species identification. In N. Amaresan, A. Sankaranarayanan, M. K. Dwivedi, & I. S. Druzhinina (Eds.), Advances in Trichoderma Biology for Agricultural Applications. Fungal Biology (pp. 3–35). Cham: Springer.

    Google Scholar 

  • Caracciolo, R., Sella, L., De Zotti, M., Bolzonello, A., Armellin, M., Trainotti, L., ... & Tundo, S. (2023). Efficacy of Trichoderma longibrachiatum Trichogin GA IV peptaibol analogs against the black rot pathogen Xanthomonas campestris pv. campestris and other phytopathogenic bacteria. Microorganisms11(2), 480.

  • Carillo, P., Woo, S. L., Comite, E., El-Nakhel, C., Rouphael, Y., Fusco, G. M., ... & Vinale, F. (2020). Application of Trichoderma harzianum, 6-pentyl-α-pyrone and plant biopolymer formulations modulate plant metabolism and fruit quality of plum tomatoes. Plants, 9(6), 771.

  • Chen, J., Li, Q. X., & Song, B. (2020). Chemical nematicides: Recent research progress and outlook. Journal of Agricultural and Food Chemistry, 68(44), 12175–12188.

    CAS  PubMed  Google Scholar 

  • Chin, J. M., Lim, Y. Y., & Ting, A. S. Y. (2022). Biopriming chilli seeds with Trichoderma asperellum: A study on biopolymer compatibility with seed and biocontrol agent for disease suppression. Biological Control, 165, 104819.

    CAS  Google Scholar 

  • Contreras-Cornejo, H. A., Macías-Rodríguez, L., del-Val, E., & Larsen, J. (2018). The root endophytic fungus Trichoderma atroviride induces foliar herbivory resistance in maize plants. Applied Soil Ecology, 124, 45–53.

    Google Scholar 

  • Contreras-Cornejo, H. A., Viveros-Bremauntz, F., del-Val, E., Macías-Rodríguez, L., López-Carmona, D. A., Alarcón, A., ... & Larsen, J. (2021). Alterations of foliar arthropod communities in a maize agroecosystem induced by the root-associated fungus Trichoderma harzianumJournal of Pest Science, 94(2), 363-374

  • Coppola, M., Diretto, G., Digilio, M. C., Woo, S. L., Giuliano, G., Molisso, D., ... & Rao, R. (2019). Transcriptome and metabolome reprogramming in tomato plants by Trichoderma harzianum strain T22 primes and enhances defense responses against aphids. Frontiers in Physiology, 10, 745.

  • Cotazo-Calambas, K. M., Niño-Castro, A., Valencia-Giraldo, S. M., Gómez-Díaz, J. S., & Montoya-Lerma, J. (2022). Behavioral Response of the Leaf-Cutting Ant Atta cephalotes (Hymenoptera: Formicidae) to Trichoderma sp. Journal of Insect Behavior, 35(4), 92–102.

    Google Scholar 

  • De la Cruz-Quiroz, R., Roussos, S., Rodríguez-Herrera, R., Hernandez-Castillo, D., & Aguilar, C. N. (2018). Growth inhibition of Colletotrichum gloeosporioides and Phytophthora capsici by native Mexican Trichoderma strains. Karbala International Journal of Modern Science, 4(2), 237–243.

    Google Scholar 

  • de Oliveira, C. M., Almeida, N. O., Côrtes, M. V. D. B., Júnior, M. L., da Rocha, M. R., & Ulhoa, C. J. (2021). Biological control of Pratylenchus brachyurus with isolates of Trichoderma spp. on soybean. Biological Control, 152, 104425.

    Google Scholar 

  • Decraemer, W., & Hunt, D. J. (2006). Structure and classification. In R. N. Perry & M. Moens (Eds.), Plant Nematology (pp. 3–32). Wallingford, Oxfordshire: CAB International.

    Google Scholar 

  • Degani, O., & Gordani, A. (2022). New Antifungal Compound., 6-Pentyl-α-Pyrone., against the Maize Late Wilt Pathogen. Magnaporthiopsis maydis. Agronomy, 12(10), 2339.

    CAS  Google Scholar 

  • del Carmen, H., Rodríguez, M., Evans, H. C., de Abreu, L. M., de Macedo, D. M., Ndacnou, M. K., Bekele, K. B., & Barreto, R. W. (2021). New species and records of Trichoderma isolated as mycoparasites and endophytes from cultivated and wild coffee in Africa. Scientific Reports, 11(1), 1–30.

    Google Scholar 

  • Doehlemann, G., Ökmen, B., Zhu, W., & Sharon, A. (2017).Plant pathogenic fungi. Microbiology Spectrum, 5(1), 5-1.

  • Dou, K., Lu, Z., Wu, Q., Ni, M., Yu, C., Wang, M., & Zhang, C. (2020). MIST: A multilocus identification system for Trichoderma. Applied and Environmental Microbiology, 86(18), e01532-e1620.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Druzhinina, I. S., Kopchinskiy, A. G., Komoń, M., Bissett, J., Szakacs, G., & Kubicek, C. P. (2005). An oligonucleotide barcode for species identification in Trichoderma and Hypocrea. Fungal Genetics and Biology, 42, 813–828.

    CAS  PubMed  Google Scholar 

  • Druzhinina, I. S., Kopchinskiy, A. G., & Kubicek, C. P. (2006). The first 100 Trichoderma species characterized by molecular data. Mycoscience, 47(2), 55–64.

    CAS  Google Scholar 

  • Du, F. Y., Ju, G. L., Xiao, L., Zhou, Y. M., & Wu, X. (2020). Sesquiterpenes and cyclodepsipeptides from marine-derived fungus Trichoderma longibrachiatum and their antagonistic activities against soil-borne pathogens. Marine Drugs, 18(3), 165.

    PubMed  PubMed Central  Google Scholar 

  • Dubey, V. K., & Singh, V. P. (2010). Molecular characterization of cucumber mosaic virus infecting gladiolus, revealing its phylogeny distinct from the Indian isolate and alike the Fny strain of CMV. Virus Genes, 41(1), 126–134.

    CAS  PubMed  Google Scholar 

  • Ebrahimi, N., Amirmahani, F., Sadeghi, B., & Ghanaatian, M. (2021). Trichoderma longibrachiatum derived metabolite as a potential source of anti-breast-cancer agent. Biologia, 76, 1595–1601.

    CAS  Google Scholar 

  • Elgorban, A. M., Abdel-Wahab, M. A., Bahkali, A. H., & Al-Sum, B. A. (2014). Biocontrol of Meloidogyne javanica on tomato plants by Hypocrea lixii (the Teleomorph of Trichoderma harzianum). Clean-Soil Air Water, 42, 1464–1469.

    Google Scholar 

  • Elad, Y., Chet, I., Boyle, P., & Henis, Y. (1983). Parasitism of Trichoderma spp. on Rhizoctoniasolani and Sclerotiumrolfsii-scanning electron microscopy and fluorescence microscopy. Phytopathology, 73(1), 85–88.

    Google Scholar 

  • El-Hasan, A., Walker, F., Klaiber, I., Schöne, J., Pfannstiel, J., & Voegele, R. T. (2022). New approaches to manage Asian soybean rust (Phakopsora pachyrhizi) using Trichoderma spp. or their antifungal secondary metabolites. Metabolites, 12(6), 507.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Elsharkawy, M. M., Shimizu, M., Takahashi, H., Ozaki, K., & Hyakumachi, M. (2013). Induction of systemic resistance against cucumber mosaic virus in Arabidopsis thaliana by Trichoderma asperellum SKT-1. The Plant Pathology Journal, 29(2), 193.

    PubMed  PubMed Central  Google Scholar 

  • Esmail, S. M., Omar, G. E., & Mourad, A. M. (2023). In-depth understanding of the genetic control of stripe rust resistance (Puccinia striiformis f. sp. tritici) induced in wheat (Triticum aestivum L.) by Trichoderma asperellum T34. Plant Disease, 107(2), 457–472.

    CAS  PubMed  Google Scholar 

  • Etim, D. O., & Onah, D. O. (2022). Trichoderma harzianum as biocontrol agent and molecular characterisation of papaya ringspot virus (PRSV) on Cucumeropsis mannii in Calabar., Cross River State., Nigeria. Asian Journal of Research in Botany, 7(4), 26–34.

    Google Scholar 

  • Evidente, A., Andolfi, A., Cimmino, A., Ganassi, S., Altomare, C., Favilla M., ...& Agnese Sabatini, M. (2009). Bisorbicillinoids produced by the fungus Trichoderma citrinoviride affect feeding preference of the aphid Schizaphis graminumJournal of Chemical Ecology, 35,533-541

  • Fan, H., Yao, M., Wang, H., Zhao, D., Zhu, X., Wang, Y., Liu, X., Duan, Y., & Chen, L. (2020). Isolation and effect of Trichoderma citrinoviride Snef 1910 for the biological control of root-knot nematode Meloidogyne incognita. BMC Microbiology, 20, 1–11.

    Google Scholar 

  • Ferreira, F. V., Herrmann-Andrade, A. M., Calabrese, C. D., Bello, F., Vázquez, D., & Musumeci, M. A. (2020). Effectiveness of Trichoderma strains isolated from the rhizosphere of citrus tree to control Alternaria alternata., Colletotrichum gloeosporioides and Penicillium digitatum A21 resistant to pyrimethanil in post-harvest oranges (Citrus sinensis L.(Osbeck)). Journal of applied microbiology, 129(3), 712–727.

    CAS  PubMed  Google Scholar 

  • Fontenelle, A. D. B., Guzzo, S. D., Lucon, C. M. M., & Harakava, R. (2011). Growth promotion and induction of resistance in tomato plant against Xanthomonas euvesicatoria and Alternariasolani by Trichoderma spp. Crop Protection, 30(11), 1492–1500.

    Google Scholar 

  • Gajera, H. P., Hirpara, D. G., Savaliya, D. D., & Golakiya, B. A. (2020). Extracellular metabolomics of Trichoderma biocontroller for antifungal action to restrain Rhizoctonia solani Kuhn. in cotton. Physiological and Molecular Plant Pathology, 112, 101547.

    CAS  Google Scholar 

  • Ganassi, S., Domenico, C. D., Altomare, C., Samuels, G. J., Grazioso, P., Cillo P., ... & De Cristofaro, A. (2022). Potential of fungi of the genus Trichoderma for biocontrol of Philaenus spumarius, the insect vector for the quarantine bacterium Xylella fastidosaPest Management Science, 79(2), 719–728.

  • Ge, Y. H., Liu, K. X., Zhang, J. X., Mu, S. Z., & Hao, X. J. (2012). The limonoids and their antitobacco mosaic virus (TMV) activities from Munronia unifoliolata Oliv. Journal of Agricultural and Food Chemistry, 60(17), 4289–4295.

    CAS  PubMed  Google Scholar 

  • Ghorbanpour, A., Salimi, A., Ghanbary, M. A. T., Pirdashti, H., & Dehestani, A. (2018). The effect of Trichoderma harzianum in mitigating low temperature stress in tomato (Solanum lycopersicum L.) plants. Scientia Horticulturae, 230, 134–141.

    Google Scholar 

  • Ghosh, S. K., & Pal, S. (2016). Entomopathogenic potential of Trichoderma longibrachiatum and its comparative evaluation with malathion against the insect pest Leucinodes orbonalis. Environmental Monitoring and Assessment, 188(1), 1–7.

    Google Scholar 

  • Górzyńska, K., Ślachetka, M., Ryszka, P., Turnau, K., Płachno, B. J., & Lembicz, M. (2018). Incidence, identification, and mycoparasitic activity of Clonostachys epichloë, a hyperparasite of the fungal endophyte Epichloë typhina. Plant Disease, 102(10), 1973–1980.

    PubMed  Google Scholar 

  • Goverse, A., & Smant, G. (2014). The activation and suppression of plant innate immunity by parasitic nematodes. Annual Review of Phytopathology, 52, 243–265.

    CAS  PubMed  Google Scholar 

  • Guigón López, C., Muñoz Castellanos, L. N., Flores Ortiz, N. A., & González González, J. A. (2019). Control of powdery mildew (Leveillula taurica) using Trichoderma asperellum and Metarhizium anisopliae in different pepper types. BioControl, 64(1), 77–89.

    Google Scholar 

  • Guler, N. S., Pehlivan, N., Karaoglu, S. A., Guzel, S., & Bozdeveci, A. (2016). Trichoderma atroviride ID20G inoculation ameliorates drought stress-induced damages by improving antioxidant defence in maize seedlings. Acta Physiologiae Plantarum, 38, 132.

    Google Scholar 

  • Guo, R., Ji, S., Wang, Z., Zhang, H., Wang, Y., & Liu, Z. (2021a). Trichoderma asperellum xylanases promote growth and induce resistance in poplar. Microbiological Research, 248, 12676.

    Google Scholar 

  • Guo, Y., Fan, Z., Yi, X., Zhang, Y., Khan, R. A. A., & Zhou, Z. (2021b). Sustainable management of soil-borne bacterium Ralstonia solanacearum in vitro and in vivo through fungal metabolites of different Trichoderma spp. Sustainability, 13(3), 1491.

    CAS  Google Scholar 

  • Hajji-Hedfi, L., Khaled, E. B., Arcos, S. C., Robertson, L, Ciordia, S, Gonzalez, M. R, ... & Navas A. (2021). Insights into nematode biocontrol potential through biological and proteomics analysis of the fungus Trichoderma viride. In Euro-Mediterranean Conference for Environmental Integration (pp.1327–1333) Springer Cham.

  • Halifu, S., Deng, X., Song, X., & Song, R. (2019). Effects of two Trichoderma strains on plant growth, rhizosphere soil nutrients and fungal community of Pinus sylvestris var. mongolica annual seedlings. Forests, 10, 758.

    Google Scholar 

  • Halifu, S., Deng, X., Song, X., Song, R., & Liang, X. (2020). Inhibitory mechanism of Trichoderma virens ZT05 on Rhizoctonia solani. Plants, 9(7), 912.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Harman, G. E., Howell, C. R., Viterbo, A., Chet, I., & Lorito, M. (2004). Trichoderma species—opportunistic, avirulent plant symbionts. Nature Reviews Microbiology, 2(1), 43–56.

    CAS  PubMed  Google Scholar 

  • Hebert, P. D. N., Cywinska, A., Ball, S. L., & de Waard, J. R. (2003). Biological identifications through DNA barcodes. Proceedings of the Royal Society of London. Series B: Biological Sciences, 270(1512), 313–321.

    CAS  PubMed Central  Google Scholar 

  • Heflish, A. A., Abdelkhalek, A., Al-Askar, A. A., & Behiry, S. I. (2021). Protective and curative effects of Trichoderma asperelloides Ta41 on tomato root rot caused by Rhizoctonia solani Rs33. Agronomy, 11(6), 1162.

    CAS  Google Scholar 

  • Hermosa, R., Viterbo, A., Chet, I., & Monte, E. (2012). Plant-beneficial effects of Trichoderma and of its genes. Microbiology, 158, 17–25.

    CAS  PubMed  Google Scholar 

  • Herrera, W., Valbuena, O., & Pavone-Maniscalco, D. (2020). Formulation of Trichoderma asperellum TV190 for biological control of Rhizoctonia solani on corn seedlings. Egyptian Journal of Biological Pest Control, 30, 1–8.

    Google Scholar 

  • Hewedy, O. A., Abdel, Lateif K. S., Seleiman, M. F., Shami, A., Albarakaty, F. M., & M El-Meihy, R. (2020). Phylogenetic diversity of Trichoderma strains and their antagonistic potential against soil-borne pathogens under stress conditions. Biology, 9(8), 189.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vijayakumar, N., & Alagar, S. (2017). Consequence of chitinase from Trichoderma viride integrated feed on digestive enzymes in Corcyra cephalonica (Stainton) and antimicrobial potential. Biosciences Biotechnology Research Asia, 14(2), 513–519.

    Google Scholar 

  • Inayati, A., Sulistyowati, L., Aini, L. Q., & Yusnawan, E. (2020). Mycoparasitic activity of indigenous Trichoderma virens strains against mungbean soil borne pathogen Rhizoctonia solani: Hyperparasite and hydrolytic enzyme production. AGRIVITA. Journal of Agricultural Science, 42(2), 229–242.

    Google Scholar 

  • Index Fungorum. Retrieved November 20, 2022 from http://www.indexfungorum.org/Names/Names.asp

  • Islam, M. R., Chowdhury, R., Roy, A. S., Islam, M. N., Mita, M. M., Bashar, S., ... & Latif, M. A. (2023). Native Trichoderma induced the defense-related enzymes and genes in rice against Xanthomonas oryzae pv. oryzae (Xoo). Plants12(9), 1864.

  • Jafarbeigi, F., Samih, M. A., Alaei, H., & Shirani, H. (2020). Induced tomato resistance against Bemisia tabaci triggered by salicylic acid., β-aminobutyric acid., and Trichoderma. Neotropical Entomology, 49, 456–467.

    CAS  PubMed  Google Scholar 

  • Jaklitsch, W. M. (2009). European Species of Hypocrea Part I. The Green-Spored Species. Studies in Mycology, 63, 1–91.

    PubMed  PubMed Central  Google Scholar 

  • Jatav, P., Ahirwar, S. S., Gupta, A., Kushwaha, K., & Jatav, S. (2018). Antagonistic activity of cellulase enzyme produced by Trichoderma viride against Xanthomonas citri. Indian Journal of Agricultural Research, 52(5), 497–504.

    Google Scholar 

  • Jones, J. T., Haegeman, A., Danchin, E. G., Gaur, H. S., Helder, J., Jones, M. G., ... & Perry, R. N. (2013). Top 10 plant‐parasitic nematodes in molecular plant pathology. Molecular Plant Pathology, 14(9), 946–961.

  • Kamala, T., Devi, S. I., Sharma, K. C., & Kennedy, K. (2015). Phylogeny and taxonomical investigation of Trichoderma spp. from Indian region of Indo-Burma biodiversity hot spot region with special reference to Manipur. BioMed Research International, 2015, 1–21.

    Google Scholar 

  • Kaushik, N., Díaz, C. E., Chhipa, H., Julio, L. F., Andrés, M. F., & González-Coloma, A. (2020). Chemical composition of an aphid antifeedant extract from an endophytic fungus, Trichoderma sp. EFI671. Microorganisms, 8(3), 420.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Keswani, C., Mishra, S., Sarma, B. K., Singh, S. P., & Singh, H. B. (2014). Unraveling the efficient applications of secondary metabolites of various Trichoderma spp. Applied Microbiology and Biotechnology, 98, 533–544.

    CAS  PubMed  Google Scholar 

  • Khan, R. A. A., Najeeb, S., Hussain, S., Xie, B., & Li, Y. (2020). Bioactive secondary metabolites from Trichoderma spp. against phytopathogenic fungi. Microorganisms, 8(6), 817.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kiarie, S., Nyasani, J. O., Gohole, L. S., Maniania, N. K., & Subramanian, S. (2020). Impact of fungal endophyte colonization of maize (Zea mays L.) on induced resistance to thrips-and aphid-transmitted viruses. Plants, 9(4), 416.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kiriga, A. W., Haukeland, S., Kariuki, G. M., Coyne, D. L., & Beek, N. V. (2018). Effect of Trichoderma spp. and Purpureocillium lilacinum on Meloidogyne javanica in commercial pineapple production in Kenya. Biological Control, 119, 27–32.

    Google Scholar 

  • Klaram, R., Jantasorn, A., & Dethoup, T. (2022). Efficacy of marine antagonist Trichoderma spp. as halo-tolerant biofungicide in controlling rice diseases and yield improvement. Biological Control, 172, 104985.

    CAS  Google Scholar 

  • Konappa, N., Krishnamurthy, S., Siddaiah, C. N., Ramachandrappa, N. S., & Chowdappa, S. (2018). Evaluation of biological efficacy of Trichoderma asperellum against tomato bacterial wilt caused by Ralstonia solanacearum. Egyptian Journal of Biological Pest Control, 28(1), 1–11.

    Google Scholar 

  • Laib, D. E., Benzara, A., Akkal, S., & Bensouici, C. (2020). The anti-acetylcholinesterase, insecticidal and antifungal activities of the entophytic fungus Trichoderma sp. isolated from Ricinus communis L. against Locusta migratoria. Acta Scientifica Naturalis, 7(1), 112–125.

    CAS  Google Scholar 

  • Lang, B. Y., Li, J., Zhou, X. X., Chen, Y. H., Yang, Y. H., Li, X. N., Zeng, Y., & Zhao, P. J. (2015). Koninginins L and M, two polyketides from Trichoderma koningii 8662. Phytochemistry Letters, 11, 1–4.

    CAS  Google Scholar 

  • Latz, M. A., Jensen, B., Collinge, D. B., & Jørgensen, H. J. (2018). Endophytic fungi as biocontrol agents: Elucidating mechanisms in disease suppression. Plant Ecology and Diversity, 11(5–6), 555–567.

    Google Scholar 

  • Lazazzara, V., Vicelli, B., Bueschl, C., Parich, A., Pertot, I., Schuhmacher, R., & Perazzolli, M. (2021). Trichoderma spp. volatile organic compounds protect grapevine plants by activating defense-related processes against downy mildew. Physiologia plantarum, 172(4), 1950–1965.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lewis, J. A., & Lumsden, R. D. (2001). Biocontrol of damping-off of greenhouse-grown crops caused by Rhizoctonia solani with a formulation of Trichoderma spp. Crop Protection, 20(1), 49–56.

    Google Scholar 

  • Li, G., Zhang, K., Xu, J., Dong, J., & Liu, Y. (2007). Nematicidal substances from fungi. Recent Patents on Biotechnology, 1, 212–233.

    CAS  PubMed  Google Scholar 

  • Li, Y., Shao, J., Fu Y., Chen, Y., Wang, H., & Xu, Z, ... Zhang, R. (2022). The volatile cedrene from Trichoderma guizhouense modulates Arabidopsis root development through auxin transport and signalling. Plant, Cell and Environment, 45(3), 969–984.

  • Litwin, A., Nowak, M., & Różalska, S. (2020). Entomopathogenic fungi: unconventional applications. Reviews in Environmental Science and Bio/Technology, 19(1), 23–42.

    Google Scholar 

  • Locatelli, G. O., dos Santos, G. F., Botelho, P. S., Finkler, C. L. L., & Bueno, L. A. (2018). Development of Trichoderma sp. formulations in encapsulated granules (CG) and evaluation of conidia shelf-life. Biological Control, 117, 21–29.

    CAS  Google Scholar 

  • Locatelli, G. O., Pimentel, M. F., Bueno, L. A., Junior, M. L., Mascarin, G. M., & Finkler, C. L. L. (2022). Production of microsclerotia by Trichoderma asperellum through submerged liquid fermentation using low-cost nitrogen and carbon sources. Biocatalysis and Agricultural Biotechnology, 44, 102455.

    CAS  Google Scholar 

  • López-Bucio, J., Pelagio-Flores, R., & Herrera-Estrella, A. (2015). Trichoderma as biostimulant: Exploiting the multilevel properties of a plant beneficial fungus. Scientia Horticulturae, 196, 109–123.

    Google Scholar 

  • Mai, W. F., & Abawi, G. S. (1987). Interactions among root-knot nematodes and Fusarium wilt fungi on host plants. Annual Review Phytopathology, 25, 317–338.

    Google Scholar 

  • Manganyi, M. C., & Ateba, C. N. (2020). Untapped potentials of endophytic fungi: A review of novel bioactive compounds with biological applications. Microorganisms, 8(12), 1934.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Manivel, B. S., & Rajkumar, S. G. (2018). Mycopesticides: Fungal based pesticides for sustainable agriculture. In P. Gehlot & J. Singh (Eds.), Fungi and their Role in Sustainable Development: Current Perspectives (pp. 183–203). Singapore: Springer.

    Google Scholar 

  • Martínez, Y., Heeb, M., Kalač, T., Gholam, Z., Schwarze, F. W., Nyström, G., & De France K. (2023). Biopolymer-based emulsions for the stabilization of Trichoderma atrobrunneum conidia for biological control. Applied Microbiology and Biotechnology, 107(4), 1465–1476.

  • Martínez-Medina, A., Fernandez, I., Lok, G. B., Pozo, M. J., Pieterse, C. M., & Van Wees, S. C. (2017). Shifting from priming of salicylic acid-to jasmonic acid-regulated defences by Trichoderma protects tomato against the root knot nematode Meloidogyne incognita. New phytologist, 213(3), 1363–1377.

    PubMed  Google Scholar 

  • Maruyama, C. R., Bilesky-José, N., de Lima, R., & Fraceto, L. F. (2020). Encapsulation of Trichoderma harzianum preserves enzymatic activity and enhances the potential for biological control. Frontiers in Bioengineering and Biotechnology, 8, 225.

    PubMed  PubMed Central  Google Scholar 

  • Mastouri, F., Bjorkman, T., & Harman, G. E. (2012). Trichoderma harzianum enhances antioxidant defense of tomato seedlings and resistance to water deficit. Molecular Plant-Microbe Interactions, 25, 1264–1271.

    CAS  PubMed  Google Scholar 

  • Medeiros, H. A. D., Araújo Filho, J. V. D., Freitas, L. G. D., Castillo, P., Rubio, M. B., Hermosa, R., & Monte, E. (2017). Tomato progeny inherit resistance to the nematode Meloidogyne javanica linked to plant growth induced by the biocontrol fungus Trichoderma atroviride. Scientific reports, 7(1), 1–13.

    Google Scholar 

  • Mejía, C., Ardila, H. D., Espinel, C., Brandão, P. F., & Villamizar, L. (2021). Use of Trichoderma koningiopsis chitinase to enhance the insecticidal activity of Beauveria bassiana against Diatraea saccharalis. Journal of Basic Microbiology, 61(9), 814–824.

    PubMed  Google Scholar 

  • Mohamed, B. F., Sallam, N., Alamri, S. A., Abo-Elyousr, K. A., Mostafa, Y. S., & Hashem, M. (2020). Approving the biocontrol method of potato wilt caused by Ralstonia solanacearum (Smith) using Enterobacter cloacae PS14 and Trichoderma asperellum T34. Egyptian Journal of Biological Pest Control, 30(1), 1–13.

    Google Scholar 

  • Moo-Koh, F. A., Cristóbal-Alejo, J., Andrés, M. F., Martín, J., Reyes, F., Tun-Suárez, J. M., & Gamboa-Angulo, M. (2022). In vitro assessment of organic and residual fractions of nematicidal culture filtrates from thirteen tropical Trichoderma strains and metabolic profiles of most-active. Journal of Fungi, 8(1), 82.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Moosavi, M. R., & Zare, R. (2020). Fungi as biological control agents of plant-parasitic nematodes. In J. M. Mérillon & K. G. Ramawat (Eds.), Plant defence: biological control (2nd ed., pp. 333–384). Springer.

    Google Scholar 

  • Moussa, Z., Alanazi, Y. F., Khateb, A. M., Eldadamony, N. M., Ismail, M. M., Saber, W. I., & Darwish, D. B. E. (2023). Domiciliation of Trichoderma asperellum suppresses Globiosporangium ultimum and promotes pea growth, ultrastructure, and metabolic features. Microorganisms, 11(1), 198.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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, 53, 522–529.

    Google Scholar 

  • Mukherjee, P. K., Horwitz, B. A., Herrera-Estrella, A., Schmoll, M., & Kenerley, C. M. (2013). Trichoderma research in the genome era. Annual Review of Phytopathology, 51(1), 105–129.

    CAS  PubMed  Google Scholar 

  • Mukhopadhyay, R., & Kumar, D. (2020). Trichoderma: A beneficial antifungal agent and insights into its mechanism of biocontrol potential. Egyptian Journal of Biological Pest Control, 30(1), 1–8.

    Google Scholar 

  • Muñoz-Celaya, A. L., Ortiz-García, M., Vernon-Carter, E. J., Jauregui-Rincón, J., Galindo, E., & Serrano-Carreón, L. (2012). Spray-drying microencapsulation of Trichoderma harzianum conidias in carbohydrate polymers matrices. Carbohydrate Polymers, 88(4), 1141–1148.

    Google Scholar 

  • Muvea, A. M., Meyhöfer, R., Subramanian, S., Poehling, H. M., Ekesi, S., & Maniania, N. K. (2014). Colonization of onions by endophytic fungi and their impacts on the biology of Thrips tabaci. PLoS ONE, 9(9), e108242.

    PubMed  PubMed Central  Google Scholar 

  • Naeimi, S., Okhovvat, S. M., Javan-Nikkhah, M., Vágvölgyi, C., Khosravi, V., & Kredics, L. (2010). Biological control of Rhizoctonia solani AG1–1A., the causal agent of rice sheath blight with Trichoderma strains. Phytopathologia Mediterranea, 49(3), 287–300.

    Google Scholar 

  • Nandini, B., Puttaswamy, H., Prakash, H. S., Adhikari, S., Jogaiah, S., & Nagaraja, G. (2019). Elicitation of novel trichogenic-lipid nanoemulsion signaling resistance against pearl millet downy mildew disease. Biomolecules, 10(1), 25.

    PubMed  PubMed Central  Google Scholar 

  • Nawaz, A., Gogi, M. D., Naveed, M., Arshad, M., Sufyan, M., Binyameen, M., ... & Ali, H. (2020). In vivo and in vitro assessment of Trichoderma species and Bacillus thuringiensis integration to mitigate insect pests of brinjal (Solanum melongena L.). Egyptian Journal of Biological Pest Control, 30(1), 1-7.

  • Neumann, N. K., Stoppacher, N., Zeilinger, S., Degenkolb, T., Bruckner, H., & Schuhmacher, R. (2015). The peptaibiotics database—A comprehensive online resource. Chemistry & Biodiversity, 12(5), 743–751.

    CAS  Google Scholar 

  • Nicol, J. M., Turner, S. J., Coyne, D. L., Nijs, L. D., Hockland, S., & Maafi, Z. T. (2011). Current nematode threats to world agriculture. In J. Jones, G. Gheysen, & C. Fenoll (Eds.), Genomics and molecular genetics of plant-nematode interactions (pp. 21–43). Springer.

    Google Scholar 

  • Nicolopoulos-Stamati, P., Maipas, S., Kotampasi, C., Stamatis, P., & Hens, L. (2016). Chemical pesticides and human health: The urgent need for a new concept in agriculture. Frontiers in Public Health, 4, 1–8.

    Google Scholar 

  • Nuangmek, W., Aiduang, W., Kumla, J., Lumyong, S., & Suwannarach, N. (2021). Evaluation of a newly identified endophytic fungus, Trichoderma phayaoense for plant growth promotion and biological control of gummy stem blight and wilt of muskmelon. Frontiers in Microbiology, 12, 634772.

    PubMed  PubMed Central  Google Scholar 

  • Ons, L., Bylemans, D., Thevissen, K., & Cammue, B. P. (2020). Combining biocontrol agents with chemical fungicides for integrated plant fungal disease control. Microorganisms, 8(12), 1930.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Padovani, L., Trevisan, M., & Capri, E. (2004). A calculation procedure to assess potential environmental risk of pesticides at the farm level. Ecological Indicators, 4(2), 111–123.

    CAS  Google Scholar 

  • Papaianni, M., Ricciardelli, A., Fulgione, A., d’Errico, G., Zoina, A., Lorito, M., ... & Capparelli, R. (2020). Antibiofilm Activity of a Trichoderma Metabolite against Xanthomonas campestris pv. campestris., Alone and in Association with a Phage. Microorganisms, 8(5), 620.

  • Peil, S., Beckers, S. J., Fischer, J., & Wurm, F. R. (2020). Biodegradable, lignin-based encapsulation enables delivery of Trichoderma reesei with programmed enzymatic release against grapevine trunk diseases. Materials Today Bio, 7, 100061.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Persoon, C. H. (1794). Disposita methodica fungorum. Römer’s Neues Mag. Bot, 1, 81–128.

    Google Scholar 

  • Pocurull, M., Fullana, A.M., Ferro, M., Valero, P., Escudero, N., Saus, E., ... & Sorribas, F. J. (2020). Commercial formulates of Trichoderma induce systemic plant resistance to Meloidogyne incognita in tomato and the effect is additive to that of the Mi-1.2 resistance gene. Frontiers in Microbiology, 10, 3042.

  • Pradhan, P. C., Mukhopadhyay, A., Kumar, R., Kundu, A., Patanjali, N., Dutta, A., ... & Singh, A. (2022). Performance appraisal of Trichoderma viride based novel tablet and powder formulations for management of Fusarium wilt disease in chickpea. Frontiers in Plant Science13, 990392.

  • Purwantisari, S., Priyatmojo, A., Sancayaningsih, R. P., Kasiamdari, R. S., & Budihardjo, K. (2018). Systemic inducing resistance against late blight by applying antagonist Trichoderma viride. Journal of Physics: Conference Series, 1025(1), 012053.

    Google Scholar 

  • Qi, Q., Fan, C., Wu, H., Sun, L., & Cao, C. (2023). Preparation of Trichoderma asperellum microcapsules and biocontrol of cucumber powdery mildew. Microbiology Spectrum, 11(3), e05084–22.

  • Qin, W. T., & Zhuang, W. Y. (2016). Seven wood-inhabiting new species of the genus Trichoderma (Fungi., Ascomycota) in Viride clade. Scientific Reports, 6(1), 1–15.

    Google Scholar 

  • Rahim, S., & Iqbal, M. (2019). Exploring enhanced insecticidal activity of mycelial extract of Trichoderma harzianum against Diuraphis noxia and Tribolium castaneum. Sarhad Journal of Agriculture, 35(3), 757–762.

    Google Scholar 

  • Raja, H. A., Miller, A. N., Pearce, C. J., & Oberlies, N. H. (2017). Fungal identification using molecular tools: A primer for the natural products research community. Journal of Natural Products, 80(3), 756–770.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rajani, P., Rajasekaran, C., Vasanthakumari, M. M., Olsson, S. B., Ravikanth, G., & Shaanker, R. U. (2021). Inhibition of plant pathogenic fungi by endophytic Trichoderma spp. through mycoparasitism and volatile organic compounds. Microbiological Research, 242, 126595.

    CAS  PubMed  Google Scholar 

  • Raymaekers, K., Ponet, L., Holtappels, D., Berckmans, B., & Cammue, B. P. (2020). Screening for novel biocontrol agents applicable in plant disease management–a review. Biological Control, 144, 104240.

    CAS  Google Scholar 

  • Redda, E. T., Ma, J., Mei, J., Li, M., Wu, B., & Jiang, X. (2018). Antagonistic potential of different isolates of Trichoderma against Fusarium oxysporum, Rhizoctonia solani and Botrytis cinerea. European Journal of Experimental Biology, 8(2), 1–8.

    Google Scholar 

  • Rochal, K.K. L., Pierre, E., Diane, Y.Y., Sahu, K. P., Vanessa, N. D., Herman, K. W.T., ... & Louise, N. W. (2021). Biological elicitor potential of endospheric Trichoderma and derived consortia against pepper (Capsicum annuum L.) leaf curl virus. Archives of Phytopathology and Plant Protection, 54(19–20), 1926–1952.

  • Rodríguez-González, Á., Mayo, S., González-López, Ó., Reinoso, B., Gutierrez, S., & Casquero, P. A. (2017). Inhibitory activity of Beauveria bassiana and Trichoderma spp. on the insect pests Xylotrechus arvicola (Coleoptera: Cerambycidae) and Acanthoscelides obtectus (Coleoptera: Chrisomelidae: Bruchinae). Environmental Monitoring and Assessment, 189(1), 1–8.

    Google Scholar 

  • Rodríguez-Hernández, A. A., Herrera-Alvarez, M., Zapata-Sarmiento, D. H., Becerra-Martínez, E., Rodríguez-Monroy, M., & Sepúlveda-Jiménez, G. (2023). Trichoderma asperellum promotes the development and antioxidant activity of white onion (Allium cepa L.) plants. Horticulture, Environment, and Biotechnology, 64(1), 25–39.

  • Ruiz-Gómez, F. J., & Miguel-Rojas, C. (2021). Antagonistic potential of native Trichoderma spp. against Phytophthora cinnamomi in the control of holm oak decline in Dehesas ecosystems. Forests, 12(7), 945.

    Google Scholar 

  • Rush, T. A., Shrestha, H. K., Gopalakrishnan, M. M., Spangler, M. K., Ellis, J. C., Labbé, J. L., & Abraham, P. E. (2021). Bioprospecting Trichoderma: A systematic roadmap to screen genomes and natural products for biocontrol applications. Frontiers in Fungal Biology, 2, 41.

    Google Scholar 

  • Ryu, S.M., Lee, H. M., Song, E. G., Seo, Y. H., Lee, J., Guo, Y., ... & Lee, D. (2017). Antiviral activities of trichothecenes isolated from Trichoderma albolutescens against pepper mottle virus. Journal of agricultural and food chemistry, 65(21), 4273–4279.

  • Safari Motlagh, M. R., Jahangiri, B., Kulus, D., Tymoszuk, A., & Kaviani, B. (2022). Endophytic fungi as potential biocontrol agents against Rhizoctonia solani JG Kühn, the causal agent of rice sheath blight disease. Biology, 11(9), 1282.

  • Sahebani, N., & Hadavi, N. (2008). Biological control of the root-knot nematode Meloidogyne javanica by Trichoderma harzianum. Soil Biology and Biochemistry, 40(8), 2016–2020.

    CAS  Google Scholar 

  • Saikia, R., Paswan, R. R., Farwaha, N., & Borah, B. K. (2022). Plant viruses: Factors involved in emergence and recent advances in their management. In S. Roy, P. Mathur, A. P. Chakraborty, & S. P. Saha (Eds.), Plant Stress: Challenges and Management in the New Decade (pp. 29–55). Bangalore: Springer.

    Google Scholar 

  • Sala, A., Barrena, R., Artola, A., & Sánchez, A. (2019). Current developments in the production of fungal biological control agents by solid-state fermentation using organic solid waste. Critical Reviews in Environmental Science and Technology, 49(8), 655–694.

    CAS  Google Scholar 

  • Salwan, R., Sharma, A., Kaur, R., Sharma, R., & Sharma, V. (2022). The riddles of Trichoderma induced plant immunity. Biological Control, 174, 105037.

  • Sanchez, A. D., Ousset, M. J., & Sosa, M. C. (2019). Biological control of Phytophthora collar rot of pear using regional Trichoderma strains with multiple mechanisms. Biological Control, 135, 124–134.

    Google Scholar 

  • Sanjeev, K., Manibhushan, T., & Archana, R. (2014). Trichoderma: Mass production, formulation, quality control, delivery and its scope in commercialization in India for the management of plant diseases. African Journal of Agricultural Research, 9(53), 3838–3852.

    Google Scholar 

  • Santos-Díaz, A., Uribe-Gutiérrez, L., & Cruz-Barrera, M. (2022). High-throughput assessments for storage stability, in vitro release, and particle size of encapsulated biocontrol fungi in hydrogel Beads. Current Protocols, 2(7), e486.

    PubMed  Google Scholar 

  • Sawant, I. S., Wadkar, P. N., Ghule, S. B., Rajguru, Y. R., Salunkhe, V. P., & Sawant, S. D. (2017). Enhanced biological control of powdery mildew in vineyards by integrating a strain of Trichoderma afroharzianum with sulphur. Biological Control, 114, 133–143.

    CAS  Google Scholar 

  • Sayed, M., Abdel-rahman, T., Ragab, A., & Abdellatif, A. (2019). Biocontrol of root-knot nematode Meloidogyne incognita by Chitinolytic Trichoderma spp. Egyptian Journal of Agronematology, 18(1), 30–47.

    Google Scholar 

  • Scharf, D. H., Brakhage, A. A., & Mukherjee, P. K. (2016). Gliotoxine bane or boon? Environmental Microbiology, 18, 1096–1109.

    CAS  PubMed  Google Scholar 

  • Scholthof, K. B. G., Adkins, S., Czosnek. H., Palukaitis, P., Jacquot, E., Hohn, T., ... & Foster G. D. (2011). Top 10 plant viruses in molecular plant pathology. Molecular plant pathology, 12(9), 938–954.

  • Seinhorst, J. W. (1970). Dynamics of plant parasitic nematodes. Rev. Phytopath., 8, 131–156.

    Google Scholar 

  • Shah, M. M., & Afiya, H. (2019). Introductory chapter: identification and isolation of Trichoderma spp.-Their significance in agriculture, human health, industrial and environmental application. In M. S. Mohammad, S. Umar, & R. B. Tijjani (Eds.), Trichoderma-The Most Widely Used Fungicide (pp. 1–12). IntechOpen.

    Google Scholar 

  • Sharma, A., Gupta, A. K., Khosla, K., Mahajan, R., & Mahajan, P. K. (2017). Antagonistic potential of native agrocin-producing non-pathogenic Agrobacterium tumefaciens strain UHFBA-218 to control crown gall in peach. Phytoprotection, 97(1), 1–1.

    Google Scholar 

  • Sharma, A., Kumar, V., Shahzad, B., Tanveer, M., Sidhu, G. P. S., Handa, N., & Thukral, A. K. (2019). Worldwide pesticide usage and its impacts on ecosystem. SN Applied Sciences, 1(11), 1–16.

    Google Scholar 

  • Sharma, A., Gupta, A. K., & Devi, B. (2023). Current trends in management of bacterial pathogens infecting plants. Antonie van Leeuwenhoek, 116(4), 303–326.

  • Sharon, E., Chet, I., & Spiegel, Y. (2011). Trichoderma as a biological control agent. In K. Davies & Y. Spiegel (Eds.), Biological Control of Plant-Parasitic Nematodes: Building Coherence between Microbial Ecology and Molecular Mechanisms (pp. 183–201). Springer.

    Google Scholar 

  • Shi, X. S., Li, H. L., Li, X. M., Wang, D. J., Li, X., Meng, L. H., Zhou, X. W., & Wang, B. G. (2020). Highly oxygenated polyketides produced by Trichoderma koningiopsis QA-3., an endophytic fungus obtained from the fresh roots of the medicinal plant. Artemisia argyi. Bioorganic Chemistry, 94, 103448.

    CAS  PubMed  Google Scholar 

  • Shoresh, M., Harman, G. E., & Mastoury, F. (2010). Induced systemic resistance and plant response to fungal biocontrol agents. Annual Review of Phytopathology, 48, 21–43.

    CAS  PubMed  Google Scholar 

  • Shyamli, S., Prem, D., Rs, T., & Atar, S. (2005). Production and antifungal activity of secondary metabolites of Trichoderma virens. Pesticide Research Journal, 17, 26–29.

    Google Scholar 

  • Siebatcheu, E. C., Wetadieu, D., Youassi, Y.O., Bedine, B. M. A., Bedane, K. G., Tchameni., N. S., &Sameza, M. L. (2023). Secondary metabolites from an endophytic fungus Trichoderma erinaceum with antimicrobial activity towards Pythium ultimum. Natural Product Research, 37(4), 657–662.

  • Silva, B. B., Banaay, C. G., & Salamanez, K. (2019). Trichoderma-induced systemic resistance against the scale insect (Unaspis mabilis Lit & Barbecho) in lanzones (Lansium domesticum Corr.). Agriculture & Forestry, 65(2), 59–78.

    Google Scholar 

  • Sindhu, S. S., Sehrawat, A., Sharma, R., & Khandelwal, A. (2017). Biological control of insect pests for sustainable agriculture. In T. Adhya, B. Mishra, K. Annapurna, D. Verma, & U. Kumar (Eds.), Advances in Soil Microbiology Recent Trends and Future Prospects (pp. 189–218). Singapore: Advances in Soil Microbiology: Recent Trends and Future Prospects. Microorganisms for Sustainability.

    Google Scholar 

  • Singh, U. B., Singh, S., Malviya, D., Chaurasia, R., & Imran, M. R. J. (2017). Harnessing biocontrol potential of Trichoderma harzianum for control of Meloidogyne incognita in tomato. Indian Phytopathology, 70, 331–335.

    Google Scholar 

  • Singh, B. N., Dwivedi, P., Sarma, B. K., & Singh, H. B. (2019). Trichoderma asperellum T42 induces local defense against Xanthomonas oryzae pv. oryzae under nitrate and ammonium nutrients in tobacco. RSC advances, 9(68), 39793–39810.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Singh, R. K., Jatav, H. S., Lakpale, R., Khan, M., Rajput, V. D., & Minkina, T. (2022). Hydrogel-based Trichoderma formulation effects on different varieties of rice under rainfed condition of Indo-Gangetic Plains. Environment Development and Sustainability, 24(5), 7035–7056.

    Google Scholar 

  • Siphathele, S., Lucy, N. M., Divine, Y. S., & Teresa, A. C. (2018). Quorum sensing in gram-negative plant pathogenic bacteria. In N. K. Josphert (Ed.), Advances in Plant Pathology (pp. 67–89). Intech Open. https://doi.org/10.5772/intechopen.78003

    Chapter  Google Scholar 

  • Smirnova, I. P., Karimova, E. V., & Shneider, Y. A. (2017). Antibacterial activity of L-lysine-α-oxidase from the Trichoderma. Bulletin of Experimental Biology and Medicine, 163(6), 777–779.

    CAS  PubMed  Google Scholar 

  • Solanki, M. K., Singh, N., Singh, R. K., Singh, P., Srivastava, A. K., et al. (2011). Plant defense activation and management of tomato root rot by a chitin-fortified Trichoderma/Hypocrea formulation. Phytoparasitica, 39, 471–481.

    CAS  Google Scholar 

  • 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, 762.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sreenivasaprasad, S., & Manibhushanrao, K. (1990). Antagonistic potential of Gliocladium virens and Trichoderma longibrachiatum to phytopathogenic fungi. Mycopathologia, 109(1), 19–26.

    CAS  PubMed  Google Scholar 

  • Sridharan, A. P., Sugitha, T., Karthikeyan, G., Nakkeeran, S., & Sivakumar, U. (2021). Metabolites of Trichoderma longibrachiatum EF5 inhibits soil borne pathogen Macrophomina phaseolina by triggering amino sugar metabolism. Microbial Pathogenesis, 150, 104714.

    CAS  PubMed  Google Scholar 

  • Sriram, S., Roopa, K. P., & Savitha, M. J. (2011). Extended shelf-life of liquid fermentation derived talc formulations of Trichoderma harzianum with the addition of glycerol in the production medium. Crop Protection, 30(10), 1334–1339.

    CAS  Google Scholar 

  • Srivastava, C., & Subramanian, S. (2016). Storage insect pests and their damage symptoms: An overview. Indian Journal of Entomology, 78, 53–58.

    Google Scholar 

  • Sulaiman, M. M., Yass, S. T. A., Aish, A. A., Basheer, L., Yasir, S. J. A., & Youssef, S. A. (2020). Activity of Trichoderma spp. against Erwinia carotovora causal agent of potato tuber soft rot. Plant Archives, 20, 115–118.

    Google Scholar 

  • Swain, H., Adak, T., Mukherjee, A. K., Sarangi, S., Samal, P., Khandual, A., ... & Zaidi, N. W. (2021). Seed biopriming with Trichoderma strains isolated from tree bark improves plant growth, antioxidative defense system in rice and enhance straw degradation capacity. Frontiers in Microbiology, 12, 633881.

  • Swaminathan, J., van Koten, C., Henderson, H. V., Jackson, T. A., & Wilson, M. J. (2016). Formulations for delivering Trichoderma atroviridae spores as seed coatings, effects of temperature and relative humidity on storage stability. Journal of Applied Microbiology, 120(2), 425–431.

    PubMed  Google Scholar 

  • Szabó, M., Csepregi, K., Gálber, M., Virányi, F., & Fekete, C. (2012). Control plant-parasitic nematodes with Trichoderma species and nematode-trapping fungi: The role of chi18-5 and chi18-12 genes in nematode egg-parasitism. Biological Control, 63(2), 121–128.

    Google Scholar 

  • Taha, M. A., Ismaiel, A. A., & Ahmed, R. M. (2021). 6-pentyl-α-pyrone from Trichoderma koningii induces systemic resistance in tobacco against tobacco mosaic virus. European Journal of Plant Pathology, 159(1), 81–93.

    CAS  Google Scholar 

  • Tamandegani, P. R., Sharifnabi, B., Massah, A., & Zahravi, M. (2021). Induced reprogramming of oxidative stress responses in cucumber by Trichoderma asperellum (Iran 3062C) enhances defense against cucumber mosaic virus. Biological Control, 164, 104779.

    Google Scholar 

  • Tamizi, A. A., Mat-Amin, N., Weaver, J. A., Olumakaiye, R. T., Akbar, M. A., Jin, S., ... &Alberti, F. (2022). Genome sequencing and analysis of Trichoderma (Hypocreaceae) isolates exhibiting antagonistic activity against the papaya dieback pathogen Erwinia mallotivoraJournal of Fungi, 8(3), 246.

  • Tang, G. T., Li, Y., Zhou, Y., Zhu, Y. H., Zheng, X. J., Chang, X. L., ... & Gong, G. S. (2022). Diversity of Trichoderma species associated with soil in the Zoige alpine wetland of Southwest China. Scientific Reports, 12(1), 21709.

  • Tariq-Javeed, M., Farooq, T., Al-Hazmi, A. S., Hussain, M. D., & Rehman, A. U. (2021). Role of Trichoderma as a biocontrol agent (BCA) of phytoparasitic nematodes and plant growth inducer. Journal of Invertebrate Pathology, 183, 107626.

    CAS  PubMed  Google Scholar 

  • Thambugala, K. M., Daranagama, D. A., Phillips, A. J., Kannangara, S. D., & Promputtha, I. (2020). Fungi vs. fungi in biocontrol: An overview of fungal antagonists applied against fungal plant pathogens. Frontiers in cellular and infection microbiology, 10, 604923.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tilman, D. (1998). The Greening of the Green Revolution. Nature, 396, 211–212.

    CAS  Google Scholar 

  • Tilman, D. (1999). Global Environmental Impacts of Agricultural Expansion: The Need for Sustainable and Efficient Practices. Proceedings of the National Academy of Sciences USA, 96, 5995–6000.

    CAS  Google Scholar 

  • Topping, C. J., Aldrich, A., & Berny, P. (2020). Overhaul environmental risk assessment for pesticides. Science, 367(6476), 360–363.

    CAS  PubMed  Google Scholar 

  • Tripathi, R., Keswani, C., & Tewari, R. (2021). Trichoderma koningii enhances tolerance against thermal stress by regulating ROS metabolism in tomato (Solanum lycopersicum L.) plants. Journal of Plant Interaction, 16, 116–126.

    CAS  Google Scholar 

  • Tulasne, L. R., & Tulasne, C. (1865). Selecta Fungorum Carpologia, 3. Paris.

  • Tyśkiewicz, R., Nowak, A., Ozimek, E., & Jaroszuk-Ściseł, J. (2022). Trichoderma: The current status of its application in agriculture for the biocontrol of fungal phytopathogens and stimulation of plant growth. International Journal of Molecular Sciences, 23(4), 2329.

    PubMed  PubMed Central  Google Scholar 

  • Verma, M., Brar, S., Tyagi, R., Surampalli, R., & Valero, J. (2007). Antagonistic fungi, Trichoderma spp.: Panoply of biological control. Biochemical Engineering Journal, 37, 1–20.

    Google Scholar 

  • Vinale, F., Sivasithamparam, K., Ghisalberti, E. L., Marra, R., Woo, S. L., & Lorito, M. (2008). Trichoderma–plant–pathogen interactions. Soil Biology and Biochemistry, 40(1), 1–10.

    CAS  Google Scholar 

  • Vinale, F., Flematti, G., Sivasithamparam, K., Lorito, M., Marra, M., Skelton, B. W., & Ghisalberti, E. L. (2009). Harzianic acid, an antifungal and plant growth promoting metabolite from Trichoderma harzianum. Journal of Natural Products, 72, 2032–2035.

    CAS  PubMed  Google Scholar 

  • Vitti, A., Pellegrini, E., Nali, C., Lovelli, S., Sofo, A., Valerio, M., ... & Nuzzaci, M. (2016). Trichoderma harzianum T-22 induces systemic resistance in tomato infected by cucumber mosaic virus. Frontiers in plant science, 7, 1520.

  • Waghunde, R. R., Shelake, R. M., & Sabalpara, A. N. (2016). Trichoderma: A significant fungus for agriculture and environment. African Journal of Agricultural Research, 11, 1952–1965.

    Google Scholar 

  • Węgrzyn, E., & Górzyńska, K. (2019). Influence of the fungal hyperparasite Trichoderma harzianum on the growth of Epichloë typhina, an agent of choke disease in grasses. Journal of Plant Diseases and Protection, 126, 39–45.

    Google Scholar 

  • Weindling, R. (1932). Trichoderma lignorumas a parasite of other soil fungi. Phytopathology, 22, 837–45.

    Google Scholar 

  • Weindling, R. (1934). Studies on a lethal principle effective in the parasitic action of Trichoderma lignorumonRhizoctonia solani and other soil fungi. Phytopathology, 24, 1153–1179.

    Google Scholar 

  • Wells, H., Bell, D., & Jaworski, A. (1972). Efficacy of Trichoderma harzianumas a biological control for Sclerotium rolfsii. Phytopathology, 62, 442–447.

    Google Scholar 

  • Woo, S. L., Ruocco, M., Vinale, F., Nigro, M., Marra, R., Lombardi, N., & Lorito, M. (2014). Trichoderma-based products and their widespread use in agriculture. The Open Mycology Journal, 8(1), 71–126.

    Google Scholar 

  • Xie, X., Zhao, Z., Yang, H., Pan, H., Zhu, C., Hu, J., & Bai, Y. (2022). Nigirpexin E., a new azaphilone derivative with anti-tobacco mosaic virus activity from soil-derived fungus Trichoderma afroharzianum LTR-2. The Journal of Antibiotics, 75(2), 117–121.

    CAS  PubMed  Google Scholar 

  • Xiong, H., Xue, K., Qin, W., Chen, X., Wang, H., Shi, X., .. & Wang, C. (2018). Does soil treated with conidial formulations of Trichoderma spp. attract or repel subterranean termites? Journal of economic entomology 111(2), 808–816.

  • Xu, H., Yan, L., Zhang, M., Chang, X., Zhu, D., Wei, D., ... & Yang, W. (2022). Changes in the density and composition of rhizosphere pathogenic Fusarium and beneficial Trichoderma contributing to reduced root rot of intercropped soybean. Pathogens11(4), 478.

  • Yan, Y., Mao, Q., Wang, Y., Zhao, J., Fu, Y., Yang, Z., ...& Ahammed, G. J. (2021).Trichoderma harzianum induces resistance to root-knot nematodes by increasing secondary metabolite synthesis and defense-related enzyme activity in Solanum lycopersicum L. Biological Control, 158, 104609

  • Yan, L., & Khan, R. A. A. (2021). Biological control of bacterial wilt in tomato through the metabolites produced by the biocontrol fungus, Trichoderma harzianum. Egyptian Journal of Biological Pest Control, 31(1), 1–9.

    Google Scholar 

  • Yang, Z., Yu, Z., Lei, L., Xia, Z., Shao, L., Zhang, K., & Li, G. (2012). Nematicidal effect of volatiles produced by Trichoderma sp. Journal of Asia-Pacific Entomology, 15(4), 647–650.

    CAS  Google Scholar 

  • Yassin, M. T., Mostafa, A. A. F., Al-Askar, A. A., Sayed, S. R., & Rady, A. M. (2021). Antagonistic activity of Trichoderma harzianum and Trichoderma viride strains against some fusarial pathogens causing stalk rot disease of maize., in vitro. Journal of King Saud University-Science, 33(3), 101363.

    Google Scholar 

  • Yassin, M. T., Mostafa, A. A. F., & Al-Askar, A. A. (2022). In vitro antagonistic activity of Trichoderma spp. against fungal pathogens causing black point disease of wheat. Journal of Taibah University for Science, 16(1), 57–65.

    Google Scholar 

  • Yobo, K. S., Mngadi, Z. N. C., & Laing, M. D. (2019). Efficacy of two potassium silicate formulations and two Trichoderma strains on Fusarium head blight of wheat. Proceedings of the National Academy of Sciences., India Section B: Biological Sciences, 89(1), 185–190.

    CAS  Google Scholar 

  • You, J., Li, G., Li, C., Zhu, L., Yang, H., Song, R., & Gu, W. (2022). Biological control and plant growth promotion by volatile organic compounds of Trichoderma koningiopsis T-51. Journal of Fungi, 8(2), 131.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zahran, Z., Nor, N. M. I. M., Dieng, H., Satho, T., & Ab Majid, A. H. (2017). Laboratory efficacy of mycoparasitic fungi (Aspergillus tubingensis and Trichoderma harzianum) against tropical bed bugs (Cimex hemipterus)(Hemiptera: Cimicidae). Asian Pacific Journal of Tropical Biomedicine, 7(4), 288–293.

    Google Scholar 

  • Zehra, A., Aamir, M., Dubey, M. K., Ansari., W. A., Meena, M., Swapnil P., ... & Lee, J. (2023).Enhanced protection of tomato against Fusarium wilt through biopriming with Trichoderma harzianum. Journal of King Saud University-Science, 35(2), 102466

  • Zhang, Q., Zhang, J., Yang, L., Zhang, L., Jiang, D., Chen, W., & Li, G. (2014). Diversity and biocontrol potential of endophytic fungi in Brassica napus. Biological Control, 72, 98–108.

    Google Scholar 

  • Zhang, S., Gan, Y., Ji, W., Xu, B., Hou, B., & Liu, J. (2017). Mechanisms and characterization of Trichoderma longibrachiatum T6 in suppressing nematodes (Heterodera avenae) in wheat. Frontiers in Plant Science, 8, 1491.

    PubMed  PubMed Central  Google Scholar 

  • Zhang, Y. Q., Zhang, S., Sun, M. L., Su, H. N., Li, H. Y., Zhang, Y. Z., ... & Song, X. Y. (2022). Antibacterial activity of peptaibols from Trichoderma longibrachiatum SMF2 against gram-negative Xanthomonas oryzae pv. oryzae, the causal agent of bacterial leaf blight on rice. Frontiers in Microbiology13, 1034779.

  • Zhou, X. X., Li, J., Yang, Y. H., Zeng, Y., & Zhao, P. J. (2014). Three new koninginins from Trichoderma neokongii 8722. Phytochemisty Letters, 8, 137–140.

    CAS  Google Scholar 

  • Zhou, Y. M., Ju, G. L., Xiao, L., Zhang, X. F., & Du, F. Y. (2018). Cyclodepsipeptides and sesquiterpenes from marine-derived fungus Trichothecium roseum and their biological functions. Marine Drugs, 16, 519.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou, Y., Wang, Y., Chen, K., Wu, Y., Hu, J., Wei, Y., ... & Denton, M. D. (2020). Near-complete genomes of two Trichoderma species: A resource for biological control of plant pathogens. Molecular Plant-Microbe Interactions, 33(8), 1036–1039.

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The authors are grateful to the Department of Plant Pathology, Dr Y S Parmar University of Horticulture and Forestry Solan, for continuous support.

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Sharma, A., Gupta, B., Verma, S. et al. Unveiling the biocontrol potential of Trichoderma. Eur J Plant Pathol 167, 569–591 (2023). https://doi.org/10.1007/s10658-023-02745-5

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