Chaverri, P., Castlebury, L. A., Overton, B. E. & Samuels, G. J. Hypocrea/Trichoderma: species with conidiophore elongations and green conidia. Mycologia 95, 1100–1140 (2003).
Harman, G. E., Howell, C. R., Viterbo, A., Chet, I. & Lorito, M. Trichoderma species-opportunistic, avirulent plant symbionts. Nat. Rev. Microbiol. 2, 43–56 (2004).
Lorito, M., Woo, S. L., Harman, G. E. & Monte, E. Translational research on Trichoderma: from ‘omics to the field. Annu. Rev. Phytopathol. 48, 395–417 (2010). Review of early Trichoderma expressomes that have led to a better understanding of their complex interactions with other living organisms and their potential importance in agriculture and industry.
Kubicek, C. P. et al. Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma. Genome Biol. 12, R40 (2011).
Druzhinina, I. S. et al. Trichoderma: the genomics of opportunistic success. Nat. Rev. Microbiol. 9, 749–759 (2011).
Hermosa, R., Viterbo, A., Chet, I. & Monte, E. Plant-beneficial effects of Trichoderma and of its genes. Microbiology 158, 17–25 (2012). Trichoderma–plant cross-talk model showing phytohormone homeostasis in the control of plant development and immune responses.
Morán-Diez, M. E., Martínez de Alba, Á. E., Rubio, M. B., Hermosa, R. & Monte, E. Trichoderma and the plant heritable priming responses. J. Fungi 7, 318 (2021). Description of Trichoderma-induced priming stages in plants and summary of the main regulatory nodes in the transcriptional network of systemic defence and growth promotion triggered by Trichoderma.
Cai, F. & Druzhinina, I. S. In honor of John Bissett: authoritative guidelines on molecular identification of Trichoderma. Fungal Divers. 107, 1–69 (2021). Unified criteria for molecular identification and systematics of Trichoderma species.
Chaverri, P. & Samuels, G. J. Evolution of habitat preference and nutrition mode in a cosmopolitan fungal genus with evidence of interkingdom host jumps and major shifts in ecology. Evolution 67, 2823–2837 (2013).
Druzhinina, I. S. et al. Massive lateral transfer of genes encoding plant cell wall-degrading enzymes to the mycoparasitic fungus Trichoderma from its plant-associated hosts. PLoS Genet. 14, e1007322 (2018).
Kubicek, C. P. et al. Evolution and comparative genomics of the most common Trichoderma species. BMC Genomics 20, 485 (2019).
Vajda, V. & McLoughlin, S. Fungal proliferation at the cretaceous-tertiary boundary. Science 303, 1489 (2004).
Wen, C., Xiong, H., Wen, J., Wen, X. & Wang, C. Trichoderma species attract Coptotermes formosanus and antagonize termite pathogen Metarhizium anisopliae. Front. Microbiol. 11, 653 (2020).
Rubio, M. B. et al. Identifying beneficial qualities of Trichoderma parareesei for plants. Appl. Environ. Microbiol. 80, 1864–1873 (2014). The beneficial effects of Trichoderma are more apparent in plants subjected to some type of stress; Trichoderma-induced plant phytohormone signalling follows an undulating dynamic, which decreases in amplitude with time.
Vargas, W. A. et al. Role of gliotoxin in the symbiotic and pathogenic interactions of Trichoderma virens. Microbiology 160, 2319–2330 (2014).
Montero-Barrientos, M., Hermosa, R., Cardoza, R. E., Gutiérrez, S. & Monte, E. Functional analysis of the Trichoderma harzianum nox1 gene, encoding an NADPH oxidase, relates production of reactive oxygen species to specific biocontrol activity against Pythium ultimum. Appl. Environ. Microbiol. 77, 3009–3016 (2011).
Villalobos-Escobedo, J. M. et al. The fungal NADPH oxidase is an essential element for the molecular dialog between Trichoderma and Arabidopsis. Plant J. 103, 2178–2192 (2020).
Lombardi, N. et al. Root exudates of stressed plants stimulate and attract Trichoderma soil fungi. Mol. Plant Microbe Interact. 31, 982–994 (2018).
Mastouri, F., Björkman, T. & Harman, G. E. Trichoderma harzianum enhances antioxidant defense of tomato seedlings and resistance to water deficit. Mol. Plant Microbe Interact. 25, 1264–1271 (2012).
Pedrero-Méndez, A. et al. Why is the correct selection of Trichoderma strains important? The case of wheat endophytic strains of T. harzianum and T. simmonsii. J. Fungi 7, 1087 (2021).
Hernández-Oñate, M. A., Esquivel-Naranjo, E. U., Mendoza-Mendoza, A., Stewart, A. & Herrera-Estrella, A. H. An injury-response mechanism conserved across kingdoms determines entry of the fungus Trichoderma atroviride into development. Proc. Natl Acad. Sci. USA 109, 14918–14923 (2012).
Pola-Sánchez, E. et al. A global analysis of photoreceptor-mediated transcriptional changes reveals the intricate relationship between central metabolism and DNA repair in the filamentous fungus Trichoderma atroviride. Front. Microbiol. 12, 724676 (2021).
Montero-Barrientos, M. et al. Overexpression of a Trichoderma HSP70 gene increases fungal resistance to heat and other abiotic stresses. Fungal Genet. Biol. 45, 1506–1513 (2008).
Ruocco, M. et al. Identification of a new biocontrol gene in Trichoderma atroviride: the role of an ABC transporter membrane pump in the interaction with different plant-pathogenic fungi. Mol. Plant Microbe Interact. 22, 291–301 (2009).
Vinale, F. et al. Harzianic acid: a novel siderophore from Trichoderma harzianum. FEMS Microbiol. Lett. 347, 123–129 (2013).
Sarkar, D. & Rakshit, A. Bio-priming in combination with mineral fertilizer improves nutritional quality and yield of red cabbage under Middle Gangetic Plains, India. Sci. Hortic. 283, 110075 (2021).
Li, R. X. et al. Solubilisation of phosphate and micronutrients by Trichoderma harzianum and its relationship with the promotion of tomato plant growth. PLoS ONE 10, e0130081 (2015).
Bononi, L., Chiaramonte, J. B., Pansa, C. C., Moitinho, M. A. & Melo, I. S. Phosphorus-solubilizing Trichoderma spp. from Amazon soils improve soybean plant growth. Sci. Rep. 10, 2858 (2020).
Vinale, F. et al. A novel role for Trichoderma secondary metabolites in the interactions with plants. Physiol. Mol. Plant Pathol. 72, 80–86 (2008). Demonstration of the role of Trichoderma-produced secondary metabolites on the plant for biological control of pathogens, induced plant resistance and plant growth promotion.
Garnica-Vergara, A. et al. The volatile 6-pentyl-2H-pyran-2-one from Trichoderma atroviride regulates Arabidopsis thaliana root morphogenesis via auxin signaling and ETHYLENE INSENSITIVE 2 functioning. N. Phytol. 209, 1496–1512 (2016).
Guzmán-Guzmán, P., Porras-Troncoso, M. D., Olmedo-Monfil, V. & Herrera-Estrella, A. Trichoderma species: versatile plant symbionts. Phytopathology 109, 6–16 (2019).
Illescas, M., Pedrero-Méndez, A., Pitorini-Bovolini, M., Hermosa, R. & Monte, E. Phytohormone production profiles in Trichoderma species and their relationship to wheat plant responses to water stress. Pathogens 10, 991 (2021).
Contreras-Cornejo, H. A., Macías-Rodríguez, L., Cortés-Penagos, C. & López-Bucio, J. 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 (2009). Demonstration of the important role of auxin signalling in plant growth promotion by Trichoderma.
Pelagio-Flores, R., Esparza-Reynoso, S., Garnica-Vergara, A., López-Bucio, J. & Herrera-Estrella, A. Trichoderma-induced acidification is an early trigger for changes in Arabidopsis root growth and determines fungal phytostimulation. Front. Plant Sci. 8, 822 (2017).
Samolski, I., Rincón, A. M., Pinzón, L. M., Viterbo, A. & Monte, E. The qid74 gene from Trichoderma harzianum has a role in root architecture and plant biofertilization. Microbiology 158, 129–138 (2012).
Malmierca, M. G. et al. Trichodiene production in a Trichoderma harzianum erg1-silenced strain provides evidence of the importance of the sterol biosynthetic pathway in inducing plant defense-related gene expression. Mol. Plant Microbe Interact. 28, 1181–1197 (2015).
Bae, H. et al. The beneficial endophyte Trichoderma hamatum isolate DIS 219b promotes growth and delays the onset of the drought response in Theobroma cacao. J. Exp. Bot. 60, 3279–3295 (2009).
Harman, G. E. & Uphoff, N. Symbiotic root-endophytic soil microbes improve crop productivity and provide environmental benefits. Scientifica 2019, 9106395 (2019).
Tseng, Y. H. et al. An endophytic Trichoderma strain promotes growth of its hosts and defends against pathogen attack. Front. Plant Sci. 11, 573670 (2020).
Carrero-Carrón, I. et al. Interactions between Trichoderma harzianum and defoliating Verticillium dahliae in resistant and susceptible wild olive clones. Plant Pathol. 67, 1758–1767 (2018).
Zachow, C. et al. Fungal diversity in the rhizosphere of endemic plant species of Tenerife (Canary Islands): relationship to vegetation zones and environmental factors. ISME J. 3, 79–92 (2009).
Zachow, C., Berg, C., Müller, H., Monk, J. & Berg, G. Endemic plants harbour specific Trichoderma communities with an exceptional potential for biocontrol of phytopathogens. J. Biotechnol. 235, 162–170 (2016).
Zhang, F. et al. Trichoderma biofertilizer links to altered soil chemistry, altered microbial communities, and improved grassland biomass. Front. Microbiol. 9, 848 (2018).
Fiorentino, N. et al. Trichoderma-based biostimulants modulate rhizosphere microbial populations and improve N uptake efficiency, yield, and nutritional quality of leafy vegetables. Front. Plant Sci. 9, 743 (2018).
Illescas, M. et al. Effect of inorganic N top dressing and Trichoderma harzianum seed-inoculation on crop yield and the shaping of root microbial communities of wheat plants cultivated under high basal N fertilization. Front. Plant Sci. 11, 575861 (2020).
Ros, M., Raut, I., Santisima-Trinidad, A. B. & Pascual, J. A. Relationship of microbial communities and suppressiveness of Trichoderma fortified composts for pepper seedlings infected by Phytophthora nicotianae. PLoS ONE 12, e0174069 (2017).
Qiao, C. et al. Reshaping the rhizosphere microbiome by bio-organic amendment to enhance crop yield in a maize-cabbage rotation system. Appl. Soil Ecol. 142, 136–146 (2019).
Bonanomi, G., Lorito, M., Vinale, F. & Woo, S. L. Organic amendments, beneficial microbes, and soil microbiota: toward a unified framework for disease suppression. Annu. Rev. Phytopathol. 56, 1–20 (2018).
He, C. et al. Dual inoculation of dark septate endophytes and Trichoderma viride drives plant performance and rhizosphere microbiome adaptations of Astragalus mongholicus to drought. Environ. Microbiol. 24, 324–340 (2022).
Rousseau, A., Benhamou, N., Chet, I. & Piche, Y. Mycoparasitism of the extramatrical phase of Glomus intraradices by Trichoderma harzianum. Phytopathology 86, 434–443 (1996).
Guo, Y. et al. Trichoderma species differ in their volatile profiles and in antagonism toward ectomycorrhiza Laccaria bicolor. Front. Microbiol. 10, 891 (2019).
Cameron, D. D., Neal, A. L., van Wees, S. C. & Ton, J. Mycorrhiza-induced resistance: more than the sum of its parts? Trends Plant Sci. 18, 539–545 (2013). This article reflects that mycorrhizae are not only microbial plant biostimulants but also induce plant systemic defences and might be considered indirect biological control agents.
Buysens, C., César, V., Ferrais, F., Dupré de Boulois, H. & Declerck, S. Inoculation of Medicago sativa cover crop with Rhizophagus irregularis and Trichoderma harzianum increases the yield of subsequently-grown potato under low nutrient conditions. Appl. Soil Ecol. 105, 137–143 (2016).
Martínez-Medina, A., Roldán, A., Albacete, A. & Pascual, J. A. The interaction with arbuscular mycorrhizal fungi or Trichoderma harzianum alters the shoot hormonal profile in melon plants. Phytochemistry 72, 223–229 (2011).
Minchev, Z., Kostenko, O., Soler, R. & Pozo, M. J. Microbial consortia for effective biocontrol of root and foliar diseases in tomato. Front. Plant Sci. 12, 756368 (2021).
Poveda, J., Hermosa, R., Monte, E. & Nicolás, C. Trichoderma harzianum favours the access of arbuscular mycorrhizal fungi to non-host Brassicaceae roots and increases plant productivity. Sci. Rep. 9, 11650 (2019).
Samuels, G., Dodd, S. L., Gams, W., Castlebury, L. A. & Petrini, O. Trichoderma species associated with the green mold epidemic of commercially grown Agaricus bisporus. Mycologia 94, 146–170 (2002).
Tijerino, A. et al. Overexpression of the Trichoderma brevicompactum tri5 gene: effect on the expression of the trichodermin biosynthetic genes and on tomato seedlings. Toxins 3, 1220–1232 (2011).
Kredics, L. et al. Clinical importance of the genus Trichoderma. A review. Acta Microbiol. Immunol. Hung. 50, 105–117 (2003).
Rocha, S. L. et al. Recognition of endophytic Trichoderma species by leaf-cutting ants and their potential in a Trojan-horse management strategy. R. Soc. Open Sci. 4, 160628 (2017).
Tucci, M., Ruocco, M., de Masi, L., de Palma, M. & Lorito, M. The beneficial effect of Trichoderma spp. on tomato is modulated by the plant genotype. Mol. Plant Pathol. 12, 341–354 (2011).
Bazghaleh, N., Prashar, P., Woo, S. & Vanderberg, A. Effects of lentil genotype on the colonization of beneficial Trichoderma species and biocontrol of Aphanomyces root rot. Microorganisms 8, 1290 (2020).
Chaverri, P. et al. Systematics of the Trichoderma harzianum species complex and the re-identification of commercial biocontrol strains. Mycologia 107, 558–590 (2015). Identification of Trichoderma strains used as active matter in commercial products, highlighting the need for re-identification of those included in patents and registrations present and future.
Vos, C. M., De Cremer, K., Cammue, B. P. & De Coninck, B. The toolbox of Trichoderma spp. in the biocontrol of Botrytis cinerea disease. Mol. Plant Pathol. 16, 400–412 (2015).
Vinale, F. et al. Major secondary metabolites produced by two commercial Trichoderma strains active against different phytopathogens. Lett. Appl. Microbiol. 43, 143–148 (2006).
Xiao-Yan, S. et al. Broad-spectrum antimicrobial activity and high stability of trichokonins from Trichoderma koningii SMF2 against plant pathogens. FEMS Microbiol. Lett. 260, 119–125 (2006).
Stoppacher, N., Kluger, B., Zeilinger, S., Krska, R. & Schuhmacher, R. Identification and profiling of volatile metabolites of the biocontrol fungus Trichoderma atroviride by HS-SPME-GC-MS. J. Microbiol. Methods 81, 187–193 (2010).
Lee, S., Yap, M., Behringer, G., Hung, R. & Bennett, J. W. Volatile organic compounds emitted by Trichoderma species mediate plant growth. Fungal Biol. Biotechnol. 3, 7 (2016).
Li, N., Islam, M. T. & Kang, S. Secreted metabolite-mediated interactions between rhizosphere bacteria and Trichoderma biocontrol agents. PLoS ONE 14, e0227228 (2019).
Martínez-Medina, A., Van Wees, S. C. M. & Pieterse, C. M. J. Airborne signals from Trichoderma harzianum stimulate iron uptake responses in roots resulting in priming of jasmonic acid-dependent defences in shoots of Arabidopsis thaliana and Solanum lycopersicum. Plant Cell Environ. 40, 2691–21705 (2017).
Collinge, D. B. et al. Biological control of plant diseases — what has been achieved and what is the direction? Plant Pathol. 71, 1024–1047 (2022).
Woo, S. L. et al. Trichoderma-based products and their widespread use in agriculture. Open Mycol. J. 8, 71–126 (2014). An overview of Trichoderma-based products on the global commercial market, species utilized as active substances, companies, product claims, formulations, countries where used, and registrations.
Baazeem, A. et al. In vitro antibacterial, antifungal, nematocidal and growth promoting activities of Trichoderma hamatum FB10 and its secondary metabolites. J. Fungi 7, 331 (2021).
Morán-Diez, M. E. et al. Transcriptomic analysis of Trichoderma atroviride overgrowing plant-wilting Verticillium dahliae reveals the role of a new M14 metallocarboxypeptidase CPA1 in biocontrol. Front. Microbiol. 10, 1120 (2019).
Mukherjee, P. K., Mendoza-Mendoza, A., Zeilinger, S. & Horwitz, B. A. Mycoparasitism as a mechanism of Trichoderma-mediated suppression of plant diseases. Fungal Biol. Rev. 39, 15–33 (2022).
Zeilinger, S. et al. Chitinase gene expression during mycoparasitic interaction of Trichoderma harzianum with its host. Fungal Genet. Biol. 26, 131–140 (1999).
de la Cruz, J., Pintor-Toro, J. A., Benítez, T. & Llobell, A. Purification and characterization of an endo-β-1,6-glucanase from Trichoderma harzianum that is related to its mycoparasitism. J. Bacteriol. 177, 1864–1871 (1995).
Migheli, Q., González-Candelas, L., Dealessi, L., Camponogara, A. & Ramón-Vidal, D. Transformants of Trichoderma longibrachiatum overexpressing the β-1,4-endoglucanase gene egl1 show enhanced biocontrol of Pythium ultimum on cucumber. Phytopathology 88, 673–677 (1998).
Ait-Lahsen, H. et al. An antifungal exo-α-1,3-glucanase (AGN13.1) from the biocontrol fungus Trichoderma harzianum. Appl. Environ. Microbiol. 67, 5833–5839 (2001).
Djonovic, S., Pozo, M. J. & Kenerley, C. M. Tvbgn3, a β-1,6-glucanase from the biocontrol fungus Trichoderma virens, is involved in mycoparasitism and control of Pythium ultimum. Appl. Environ. Microbiol. 72, 7661–7670 (2006).
Thrane, C., Tronsmo, A. & Jensen, D. F. Endo-1,3-β-glucanase and cellulase from Trichoderma harzianum: purification and partial characterization, induction of and biological activity against plant pathogenic Pythium spp. Eur. J. Plant Pathol. 103, 331–344 (1997).
Almeida, F., Cerqueira, F. M., Silva, R. D. N., Ulhoa, C. J. & Lima, A. L. Mycoparasitism studies of Trichoderma harzianum strains against Rhizoctonia solani evaluation of coiling and hydrolytic enzyme production. Biotechnol. Lett. 29, 1189–1193 (2007).
Rubio, M. B., Hermosa, R., Reino, J. L., Collado, I. G. & Monte, E. The Thctf1 transcription factor of Trichoderma harzianum is involved in 6-pentyl-2H-pyran-2-one production and antifungal activity. Fungal Genet. Biol. 46, 17–27 (2009).
Howell, C. R. & Stipanovic, R. D. Gliovirin, a new antibiotic from Gliocladium virens, and its role in the biological control of Pythium ultimum. Can. J. Microbiol. 29, 321–324 (1983).
Bae, S.-J. et al. Trichoderma metabolites as biological control agents against Phytophthora pathogens. Biol. Control. 92, 128–138 (2016).
Manganiello, G. et al. Modulation of tomato response to Rhizoctonia solani by Trichoderma harzianum and its secondary metabolite harzianic acid. Front. Microbiol. 9, 1966 (2018).
Di Pietro, A., Lorito, M., Hayes, C. K., Broadway, R. M. & Harman, G. E. Endochitinase from Gliocladium virens: isolation, characterization, and synergistic antifungal activity in combination with gliotoxin. Phytopathology 83, 308–313 (1993).
Lace, B. et al. Gate crashing arbuscular mycorrhizas: in vivo imaging shows the extensive colonization of both symbionts by Trichoderma atroviride. Environ. Microbiol. Rep. 7, 64–77 (2015).
Yang, H., Powell, N. T. & Barker, K. R. The influence of Trichoderma harzianum on the root-knot Fusarium wilt complex in cotton. J. Nematol. 8, 81–86 (1976).
Sharon, E. et al. Parasitism of Trichoderma on Meloidogyne javanica and role of the gelatinous matrix. Eur. J. Plant Pathol. 118, 247–258 (2007).
Suárez, B., Rey, M., Castillo, P., Monte, E. & Llobell, A. Isolation and characterization of PRA1, a trypsin-like protease from the biocontrol agent Trichoderma harzianum CECT 2413 displaying nematicidal activity. Appl. Microbiol. Biotechnol. 65, 46–55 (2004).
Sahebani, N. & Hadavi, N. Biological control of the root-knot nematode Meloidogyne javanica by Trichoderma harzianum. Soil. Biol. Biochem. 40, 2016–2020 (2008).
Berini, F. et al. Effects of Trichoderma viride chitinases on the peritrophic matrix of Lepidoptera. Pest Manag. Sci. 72, 980–989 (2016).
da Silveira, A. A. et al. Larvicidal potential of cell wall degrading enzymes from Trichoderma asperellum against Aedes aegypti (Diptera: Culicidae). Biotechnol. Prog. 37, e3182 (2021).
Podder, D. & Ghosh, S. K. A new application of Trichoderma asperellum as an anopheline larvicide for eco friendly management in medical science. Sci. Rep. 9, 1108 (2019).
Kapat, A., Zimand, G. & Elad, Y. Effect of two isolates of Trichoderma harzianum on the activity of hydrolytic enzymes produced by Botrytis cinerea. Physiol. Mol. Plant Pathol. 52, 127–137 (1999).
Malmierca, M. G. et al. Trichothecenes and aspinolides produced by Trichoderma arundinaceum regulate expression of Botrytis cinerea genes involved in virulence and growth. Environ. Microbiol. 18, 3991–4004 (2016).
Contreras-Cornejo, H. A. et al. Trichoderma atroviride, a maize root associated fungus, increases the parasitism rate of the fall armyworm Spodoptera frugiperda by its natural enemy Campoletis sonorensis. Soil Biol. Biochem. 122, 196–202 (2018).
Conrath, U., Beckers, G. J., Langenbach, C. J. & Jaskiewicz, M. R. Priming for enhanced defense. Annu. Rev. Phytopathol. 53, 97–119 (2015).
Mendoza-Mendoza, A. et al. Molecular dialogues between Trichoderma and roots: role of the fungal secretome. Fungal Biol. Rev. 32, 62–85 (2018).
Mathys, J. et al. Genome-wide characterization of ISR induced in Arabidopsis thaliana by Trichoderma hamatum T382 against Botrytis cinerea infection. Front. Plant Sci. 3, 108 (2012).
Brotman, Y. et al. Trichoderma-plant root colonization: escaping early plant defense responses and activation of the antioxidant machinery for saline stress tolerance. PLoS Pathog. 9, e1003221 (2013).
Moran-Diez, E. et al. The ThPG1 endopolygalacturonase is required for the Trichoderma harzianum-plant beneficial interaction. Mol. Plant Microbe Interact. 22, 1021–1031 (2009).
Hermosa, R. et al. The contribution of Trichoderma to balancing the costs of plant growth and defense. Int. Microbiol. 16, 69–80 (2013).
Alonso-Ramírez, A. et al. Salicylic acid prevents Trichoderma harzianum from entering the vascular system of roots. Mol. Plant Pathol. 15, 823–831 (2014). Salicylic acid is key to controlling Trichoderma early root colonization as without the support of this phytohormone the plants cannot prevent the fungus from entering the vascular system and spreading to the aerial parts.
Rotblat, B., Enshell-Seijffers, D., Gershoni, J. M., Schuster, S. & Avni, A. Identification of an essential component of the elicitation active site of the EIX protein elicitor. Plant J. 32, 1049–1055 (2002).
Romero-Contreras, Y. J. et al. Tal6 from Trichoderma atroviride is a LysM effector involved in mycoparasitism and plant association. Front. Microbiol. 10, 2231 (2019).
Djonovic, S., Pozo, M. J., Dangott, L. J., Howell, C. R. & Kenerley, C. M. Sm1, a proteinaceous elicitor secreted by the biocontrol fungus Trichoderma virens induces plant defense responses and systemic resistance. Mol. Plant Microbe Interact. 19, 838–853 (2006).
Engelberth, J. et al. Ion channel-forming alamethicin is a potent elicitor of volatile biosynthesis and tendril coiling. Cross talk between jasmonate and salicylate signaling in lima bean. Plant Physiol. 125, 369–377 (2001).
Malmierca, M. G. et al. Production of trichodiene by Trichoderma harzianum alters the perception of this biocontrol strain by plants and antagonized fungi. Environ. Microbiol. 17, 2628–2646 (2015).
Malmierca, M. G. et al. Involvement of Trichoderma trichothecenes in the biocontrol activity and induction of plant defense-related genes. Appl. Environ. Microbiol. 78, 4856–4868 (2012).
Ramírez-Valdespino, C. A., Casas-Flores, S. & Olmedo-Monfil, V. Trichoderma as a model to study effector-like molecules. Front. Microbiol. 10, 1030 (2019).
Lamdan, N., Shalaby, S., Ziv, T., Kenerley, C. M. & Horwitz, B. A. Secretome of the biocontrol fungus Trichoderma virens co-cultured with maize roots: role in induced systemic resistance. Mol. Cell Proteom. 14, 1054–1063 (2015).
Marra, R. et al. Study of the three-way interaction between Trichoderma atroviride, plant and fungal pathogens by using a proteomic approach. Curr. Genet. 50, 307–321 (2006).
Shoresh, M. & Harman, G. E. The molecular basis of shoot responses of maize seedlings to Trichoderma harzianum T22 inoculation of the root: a proteomic approach. Plant Physiol. 147, 2147–2163 (2008).
Pieterse, C. M. et al. Induced systemic resistance by beneficial microbes. Annu. Rev. Phytopathol. 52, 347–375 (2014).
Shoresh, M., Yedidia, I. & Chet, I. Involvement of jasmonic acid/ethylene signaling pathway in the systemic resistance induced in cucumber by Trichoderma asperellum T203. Phytopathology 95, 76–84 (2005).
Luo, Y. et al. Antimicrobial peptaibols induce defense responses and systemic resistance in tobacco against tobacco mosaic virus. FEMS Microbiol. Lett. 313, 120–126 (2010).
Salas-Marina, M. A. et al. Colonization of Arabidopsis roots by Trichoderma atroviride promotes growth and enhances systemic disease resistance through jasmonic acid/ethylene and salicylic acid pathways. Eur. J. Plant Pathol. 131, 15–26 (2011).
TariqJaveed, M., Farooq, T., Al-Hazmi, A. S., Hussain, M. D. & Rehman, A. U. Role of Trichoderma as a biocontrol agent (BCA) of phytoparasitic nematodes and plant growth inducer. J. Invertebr. Pathol. 183, 107626 (2021).
Medeiros, H. A. et al. Tomato progeny inherit resistance to the nematode Meloidogyne javanica linked to plant growth induced by the biocontrol fungus Trichoderma atroviride. Sci. Rep. 7, 40216 (2017). Plant responses to Trichoderma are heritable in terms of both induction of defence and growth promotion, and the expression of these traits in the offspring depends on the treatment to which the parental plant was subjected.
Martínez-Medina, A. et al. Shifting from priming of salicylic acid- to jasmonic acid-regulated defences by Trichoderma protects tomato against the root knot nematode Meloidogyne incognita. N. Phytol. 213, 1363–1377 (2017).
Rebolledo-Prudencio, O. G. et al. The small RNA-mediated gene silencing machinery is required in Arabidopsis for stimulation of growth, systemic disease resistance, and suppression of the nitrile-specifier gene NSP4 by Trichoderma atroviride. Plant J. 109, 873–890 (2022).
Coppola, M. et al. Transcriptome and metabolome reprogramming in tomato plants by Trichoderma harzianum strain T22 primes and enhances defense responses against aphids. Front. Physiol. 10, 745 (2019).
Coppola, M. et al. Trichoderma atroviride P1 colonization of tomato plants enhances both direct and indirect defense barriers against insects. Front. Physiol. 10, 813 (2019). Demonstration of both direct and indirect biological control of sucking and chewing insects feeding on Trichoderma-treated plants.
Gupta, S. et al. Inoculation of barley with Trichoderma harzianum T-22 modifies lipids and metabolites to improve salt tolerance. J. Exp. Bot. 72, 7229–7246 (2021).
Arnold, A. E., Praprotnik, E. & Lončar, J. Testing virulence of different species of insect associated fungi against yellow mealworm (Coleoptera: Tenebrionidae) and their potential growth stimulation to maize. Plants 10, 2498 (2021).
Kaushik, N. et al. Chemical composition of an aphid antifeedant extract from an endophytic fungus, Trichoderma sp. EFI671. Microorganisms 8, 420 (2020).
Li, Y. et al. Impacts on silkworm larvae midgut proteomics by transgenic Trichoderma strain and analysis of glutathione S-transferase sigma 2 gene essential for anti-stress response of silkworm larvae. J. Proteom. 126, 218–227 (2015).
Battaglia, D. et al. Tomato below ground-above ground interactions: Trichoderma longibrachiatum affects the performance of Macrosiphum euphorbiae and its natural antagonists. Biomed. Res. Int. 26, 1249–1256 (2013).
Contreras-Cornejo, H. A., Macías-Rodríguez, L., del-Val, E. & Larsen, J. The root endophytic fungus Trichoderma atroviride induces foliar herbivory resistance in maize plants. Appl. Soil Ecol. 124, 45–53 (2018).
Saijo, Y. & Loo, E. P. Plant immunity in signal integration between biotic and abiotic stress responses. N. Phytol. 225, 87–104 (2020).
Moscatiello, R. et al. The hydrophobin HYTLO1 secreted by the biocontrol fungus Trichoderma longibrachiatum triggers a NAADP-mediated calcium signalling pathway in Lotus japonicus. Int. J. Mol. Sci. 19, 2596 (2018).
Bailey, B. A. et al. Fungal and plant gene expression during the colonization of cacao seedlings by endophytic isolates of four Trichoderma species. Planta 224, 1449–1464 (2006).
Mastouri, F., Björkman, T. & Harman, G. E. Seed treatment with Trichoderma harzianum alleviates biotic, abiotic, and physiological stresses in germinating seeds and seedlings. Phytopathology 100, 1213–1221 (2010). Pioneering work describing that Trichoderma reduces the damage caused by ROS in the plant, resulting in the alleviation of a range of biotic, abiotic and physiological stresses.
Ghorbanpour, A., Salimi, A., Ghanbary, M. A. T., Pirdashti, H. & Dehestani, A. The effect of Trichoderma harzianum in mitigating low temperature stress in tomato (Solanum lycopersicum L.) plants. Sci. Hortic. 230, 134–141 (2018).
Zhang, S., Xu, B. & Gan, Y. Seed treatment with Trichoderma longibrachiatum T6 promotes wheat seedling growth under NaCl stress through activating the enzymatic and nonenzymatic antioxidant defense systems. Int. J. Mol. Sci. 20, 3729 (2019).
Rauf, M. et al. Molecular mechanisms of the 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase producing Trichoderma asperellum MAP1 in enhancing wheat tolerance to waterlogging stress. Front. Plant Sci. 11, 614971 (2021).
Jalali, F., Zafari, D. & Salari, H. Volatile organic compounds of some Trichoderma spp. increase growth and induce salt tolerance in Arabidopsis thaliana. Fungal Ecol. 29, 67–75 (2017).
Rubio, M. B. et al. The combination of Trichoderma harzianum and chemical fertilization leads to the deregulation of phytohormone networking, preventing the adaptive responses of tomato plants to salt stress. Front. Plant Sci. 8, 294 (2017). Combined applications of Trichoderma and chemical fertilizer might have positive synergistic effects for plants but overstimulation leads to dysregulation of phytohormone networking if under stress conditions.
Rivera-Méndez, W., Obregón, M., Morán-Diez, M. E., Hermosa, R. & Monte, E. Trichoderma asperellum biocontrol activity and induction of systemic defenses against Sclerotium cepivorum in onion plants under tropical climate conditions. Biol. Control. 141, 104145 (2020).
Domínguez, S. et al. Nitrogen metabolism and growth enhancement in tomato plants challenged with Trichoderma harzianum expressing the Aspergillus nidulans acetamidase amdS gene. Front. Microbiol. 7, 1182 (2016).
Liu, N. & Avramova, Z. Molecular mechanism of the priming by jasmonic acid of specific dehydration stress response genes in Arabidopsis. Epigenetics Chromatin 9, 8 (2016).
Slaughter, A. et al. Descendants of primed Arabidopsis plants exhibit resistance to biotic stress. Plant Physiol. 158, 835–843 (2012).
FAO. The State of Food and Agriculture 2019. Moving Forward on Food Loss and Waste Reduction 1–182 (Food and Agriculture Organization of the United Nations, 2019).
DeClerck, F. A. J. et al. A whole earth approach to nature positive food: biodiversity and agriculture. United Nations Food Systems Summit 2021 – Scientific Group 1–26 (CGIAR, 2021).
Woo, S. L. & Pepe, O. Microbial consortia: promising probiotics as plant biostimulants for sustainable agriculture. Front. Plant Sci. 9, 1801 (2018).
Carillo, P. et al. Application of Trichoderma harzianum, 6-pentyl-α-pyrone and plant biopolymer formulations modulate plant metabolism and fruit quality of plum tomatoes. Plants 9, 771 (2020).
Comite, E. et al. Bioformulations with beneficial microbial consortia, a bioactive compound and plant biopolymers modulate sweet basil productivity, photosynthetic activity and metabolites. Pathogens 10, 870 (2021).
Lanzuise, S. et al. Combined biostimulant applications of Trichoderma spp. with fatty acid mixtures improve biocontrol activity, horticultural crop yield and nutritional quality. Agronomy 12, 275 (2022).
Ons, L., Bylemans, D., Thevissen, K. & Cammue, B. P. A. Combining biocontrol agents with chemical fungicides for integrated plant fungal disease control. Microorganisms 8, 1930 (2020).
Vinale, F. et al. Co-culture of plant beneficial microbes as source of bioactive metabolites. Sci. Rep. 7, 14330 (2017).
Karuppiah, V., Sun, J., Li, T., Vallikkannu, M. & Chen, J. Co-cultivation of Trichoderma asperellum GDFS1009 and Bacillus amyloliquefaciens 1841 causes differential gene expression and improvement in the wheat growth and biocontrol activity. Front. Microbiol. 10, 68 (2019).
Fraceto, L. F. et al. Trichoderma harzianum-based novel formulations: potential applications for management of next-gen agricultural challenges. J. Chem. Technol. Biotechnol. 93, 2056–2063 (2018).
Lorito, M. et al. Genes from mycoparasitic fungi as a source for improving plant resistance to fungal pathogens. Proc. Natl Acad. Sci. USA 95, 7860–7865 (1998).
Montero-Barrientos, M. et al. Transgenic expression of the Trichoderma harzianum hsp70 gene increases Arabidopsis resistance to heat and other abiotic stresses. J. Plant Physiol. 167, 659–665 (2010).
Kashyap, P. L., Rai, P., Srivastava, A. K. & Kumar, S. Trichoderma for climate resilient agriculture. World J. Microbiol. Biotechnol. 33, 155 (2017).
Zafra, G., Moreno-Montano, A., Absalon, A. E. & Cortés-Espinosa, D. V. Degradation of polycyclic aromatic hydrocarbons in soil by a tolerant strain of Trichoderma asperellum. Environ. Sci. Pollut. Res. 22, 1034–1042 (2015).
Robbertse, B. et al. Improving taxonomic accuracy for fungi in public sequence databases: applying ‘one name one species’ in well-defined genera with Trichoderma/Hypocrea as a test case. Database 2017, 1–14 (2017).
Rossman, A. Y. et al. Genera in bionectriaceae, hypocreaceae, and nectriaceae (Hypocreales) proposed for acceptance or rejection. IMA Fungus 4, 41–51 (2013).
Jones, J. D. G. & Dangl, J. L. The plant immune system. Nature 444, 323–329 (2006).