Trichoderma: a multipurpose, plant-beneficial microorganism for eco-sustainable agriculture

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Trichoderma: a multipurpose, plant-beneficial microorganism for eco-sustainable agriculture"


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ABSTRACT _Trichoderma_ is a cosmopolitan and opportunistic ascomycete fungal genus including species that are of interest to agriculture as direct biological control agents of


phytopathogens. _Trichoderma_ utilizes direct antagonism and competition, particularly in the rhizosphere, where it modulates the composition of and interactions with other microorganisms.


In its colonization of plants, on the roots or as an endophyte, _Trichoderma_ has evolved the capacity to communicate with the plant and produce numerous multifaceted benefits to its host.


The intricacy of this plant–microorganism association has stimulated a marked interest in research on _Trichoderma_, ranging from its capacity as a plant growth promoter to its ability to


prime local and systemic defence responses against biotic and abiotic stresses and to activate transcriptional memory affecting plant responses to future stresses. This Review discusses the


ecophysiology and diversity of _Trichoderma_ and the complexity of its relationships in the agroecosystem, highlighting its potential as a direct and indirect biological control agent,


biostimulant and biofertilizer, which are useful multipurpose properties for agricultural applications. We also highlight how the present legislative framework might accommodate the


demonstrated evidence of _Trichoderma_ proficiency as a plant-beneficial microorganism contributing towards eco-sustainable agriculture. Access through your institution Buy or subscribe This


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ACCESS OPTIONS: * Log in * Learn about institutional subscriptions * Read our FAQs * Contact customer support SIMILAR CONTENT BEING VIEWED BY OTHERS EXPLORING EXTREMOPHILIC FUNGI IN SOIL


MYCOBIOME FOR SUSTAINABLE AGRICULTURE AMID GLOBAL CHANGE Article Open access 13 August 2024 HARNESSING THE PLANT MICROBIOME FOR SUSTAINABLE CROP PRODUCTION Article 15 August 2024 PLANT


PATHOGEN RESISTANCE IS MEDIATED BY RECRUITMENT OF SPECIFIC RHIZOSPHERE FUNGI Article 10 April 2023 REFERENCES * 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). Article  PubMed  Google Scholar  * 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). Article  CAS  PubMed  Google Scholar  * 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. Article  CAS  PubMed


  Google Scholar  * Kubicek, C. P. et al. Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of _Trichoderma_. _Genome Biol._ 12, R40 (2011). Article


  CAS  PubMed  PubMed Central  Google Scholar  * Druzhinina, I. S. et al. _Trichoderma_: the genomics of opportunistic success. _Nat. Rev. Microbiol._ 9, 749–759 (2011). Article  CAS  PubMed


  Google Scholar  * 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. Article  CAS  PubMed  Google Scholar  * 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_. Article  Google Scholar  * 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. Article  CAS  Google Scholar  * 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). PubMed  Google Scholar  * 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). Article 


PubMed  PubMed Central  Google Scholar  * Kubicek, C. P. et al. Evolution and comparative genomics of the most common _Trichoderma_ species. _BMC Genomics_ 20, 485 (2019). Article  PubMed 


PubMed Central  Google Scholar  * Vajda, V. & McLoughlin, S. Fungal proliferation at the cretaceous-tertiary boundary. _Science_ 303, 1489 (2004). Article  CAS  PubMed  Google Scholar  *


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). Article  PubMed  PubMed Central  Google Scholar  * 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. Article  PubMed  PubMed Central  Google Scholar  * Vargas, W. A. et al. Role of gliotoxin in the symbiotic and pathogenic


interactions of _Trichoderma virens_. _Microbiology_ 160, 2319–2330 (2014). Article  CAS  PubMed  Google Scholar  * 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). Article  CAS  PubMed  PubMed Central  Google Scholar  * 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). Article  CAS  PubMed  Google Scholar  * Lombardi, N. et al. Root exudates


of stressed plants stimulate and attract _Trichoderma_ soil fungi. _Mol. Plant Microbe Interact._ 31, 982–994 (2018). Article  CAS  PubMed  Google Scholar  * 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). Article  CAS 


PubMed  Google Scholar  * 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). Article  Google Scholar  * 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). Article 


PubMed  PubMed Central  Google Scholar  * 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). Article  PubMed  PubMed Central  Google Scholar  * 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). Article  CAS  PubMed  Google


Scholar  * 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). Article  CAS  PubMed  Google Scholar  * Vinale, F. et al. Harzianic acid: a novel siderophore from _Trichoderma


harzianum_. _FEMS Microbiol. Lett._ 347, 123–129 (2013). CAS  PubMed  Google Scholar  * 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). Article  CAS  Google Scholar  * 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). Article  PubMed  PubMed Central  Google Scholar  *


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). Article  CAS  PubMed  PubMed Central  Google Scholar  * 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. Article  CAS  Google Scholar  * 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). Article  CAS  Google Scholar  * Guzmán-Guzmán, P., Porras-Troncoso, M. D.,


Olmedo-Monfil, V. & Herrera-Estrella, A. _Trichoderma_ species: versatile plant symbionts. _Phytopathology_ 109, 6–16 (2019). Article  PubMed  Google Scholar  * 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). Article  CAS  PubMed  PubMed Central  Google Scholar  * 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_. Article  CAS  PubMed  PubMed Central  Google Scholar  * 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). Article  PubMed  PubMed Central  Google Scholar  * 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). Article  CAS  PubMed  Google Scholar  *


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). Article  CAS  PubMed  Google Scholar  * 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). Article  CAS  PubMed  PubMed Central  Google Scholar


  * Harman, G. E. & Uphoff, N. Symbiotic root-endophytic soil microbes improve crop productivity and provide environmental benefits. _Scientifica_ 2019, 9106395 (2019). Article  PubMed 


PubMed Central  Google Scholar  * 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). Article  PubMed  PubMed Central  Google Scholar  * 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). Article  Google Scholar  * 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). Article  CAS  PubMed  Google Scholar  * 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). Article  CAS 


PubMed  Google Scholar  * Zhang, F. et al. _Trichoderma_ biofertilizer links to altered soil chemistry, altered microbial communities, and improved grassland biomass. _Front. Microbiol._ 9,


848 (2018). Article  PubMed  PubMed Central  Google Scholar  * 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). Article  PubMed  PubMed Central  Google Scholar  * 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). Article  PubMed  PubMed Central  Google Scholar  * 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). Article  PubMed  PubMed Central  Google


Scholar  * 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).


Article  Google Scholar  * 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). Article  CAS  PubMed  Google Scholar  * 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). Article  CAS  PubMed  PubMed Central  Google


Scholar  * Rousseau, A., Benhamou, N., Chet, I. & Piche, Y. Mycoparasitism of the extramatrical phase of _Glomus intraradices_ by _Trichoderma harzianum_. _Phytopathology_ 86, 434–443


(1996). Article  Google Scholar  * Guo, Y. et al. _Trichoderma_ species differ in their volatile profiles and in antagonism toward ectomycorrhiza _Laccaria bicolor_. _Front. Microbiol._ 10,


891 (2019). Article  PubMed  PubMed Central  Google Scholar  * 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. Article  CAS  PubMed  PubMed Central  Google Scholar  * 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). Article  Google Scholar  * 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). Article  PubMed  Google Scholar  * 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). Article  PubMed  PubMed Central  Google Scholar  * 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). Article  PubMed  PubMed Central  Google Scholar  * 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). Article  PubMed  Google Scholar  * 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). Article  CAS  PubMed  PubMed Central  Google


Scholar  * Kredics, L. et al. Clinical importance of the genus _Trichoderma_. A review. _Acta Microbiol. Immunol. Hung._ 50, 105–117 (2003). Article  CAS  PubMed  Google Scholar  * 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). Article 


PubMed  PubMed Central  Google Scholar  * 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). Article  CAS  PubMed  Google Scholar  * 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). Article  CAS  PubMed  PubMed Central  Google Scholar  * 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. Article 


CAS  PubMed  PubMed Central  Google Scholar  * 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). Article  PubMed  Google Scholar  * Vinale, F. et al. Major secondary metabolites produced by two commercial _Trichoderma_ strains active


against different phytopathogens. _Lett. Appl. Microbiol._ 43, 143–148 (2006). Article  CAS  PubMed  Google Scholar  * 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). Article  PubMed  Google Scholar  * 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). Article  CAS  PubMed  Google Scholar  * 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). Article  PubMed  PubMed Central  Google Scholar  * Li, N., Islam, M. T. & Kang, S. Secreted metabolite-mediated


interactions between rhizosphere bacteria and _Trichoderma_ biocontrol agents. _PLoS ONE _14, e0227228 (2019). Article  CAS  PubMed  PubMed Central  Google Scholar  * 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). Article  PubMed  Google Scholar  * 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). Article  Google Scholar  * 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. Article  Google Scholar  * 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). Article  CAS  Google Scholar  * 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).


Article  PubMed  PubMed Central  Google Scholar  * 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). Article  CAS  Google Scholar  * Zeilinger, S. et al. Chitinase gene expression during mycoparasitic interaction of


_Trichoderma harzianum_ with its host. _Fungal Genet. Biol._ 26, 131–140 (1999). Article  CAS  PubMed  Google Scholar  * 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). Article  PubMed 


PubMed Central  Google Scholar  * 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). Article  CAS  PubMed  Google Scholar  * 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). Article  CAS  PubMed  PubMed Central  Google


Scholar  * 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). Article  CAS  PubMed  PubMed Central  Google Scholar  * 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). Article  CAS  Google Scholar  * 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). Article  CAS  PubMed  Google Scholar  * 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). Article  CAS  PubMed  Google Scholar  * 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). Article  CAS  Google Scholar  * Bae, S.-J. et al. _Trichoderma_ metabolites as biological control agents


against _Phytophthora_ pathogens. _Biol. Control._ 92, 128–138 (2016). Article  CAS  Google Scholar  * 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). Article  PubMed  PubMed Central  Google Scholar  * 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). Article  Google Scholar  * 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). Article  CAS  PubMed  Google Scholar  * 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). CAS  PubMed  PubMed Central  Google Scholar  * Sharon, E. et al. Parasitism of _Trichoderma_ on


_Meloidogyne javanica_ and role of the gelatinous matrix. _Eur. J. Plant Pathol._ 118, 247–258 (2007). Article  Google Scholar  * 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). Article  PubMed  Google Scholar  * Sahebani, N. & Hadavi, N. Biological control of the root-knot nematode _Meloidogyne javanica_ by _Trichoderma harzianum_. _Soil.


Biol. Biochem._ 40, 2016–2020 (2008). Article  CAS  Google Scholar  * Berini, F. et al. Effects of _Trichoderma viride_ chitinases on the peritrophic matrix of Lepidoptera. _Pest Manag.


Sci._ 72, 980–989 (2016). Article  CAS  PubMed  Google Scholar  * 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). Article  PubMed  Google Scholar  * 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). Article  PubMed  PubMed Central  Google Scholar  * 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). Article  Google


Scholar  * 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). Article  CAS  PubMed  Google Scholar  * 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). Article  CAS  Google Scholar  * Conrath,


U., Beckers, G. J., Langenbach, C. J. & Jaskiewicz, M. R. Priming for enhanced defense. _Annu. Rev. Phytopathol._ 53, 97–119 (2015). Article  CAS  PubMed  Google Scholar  *


Mendoza-Mendoza, A. et al. Molecular dialogues between _Trichoderma_ and roots: role of the fungal secretome. _Fungal Biol. Rev._ 32, 62–85 (2018). Article  Google Scholar  * 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). Article 


PubMed  PubMed Central  Google Scholar  * 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). Article  CAS  PubMed  PubMed Central  Google Scholar  * 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). Article  CAS  PubMed  Google Scholar  * Hermosa, R. et al. The contribution of


_Trichoderma_ to balancing the costs of plant growth and defense. _Int. Microbiol._ 16, 69–80 (2013). CAS  PubMed  Google Scholar  * 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. Article  PubMed  PubMed Central  Google


Scholar  * 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). Article  CAS  PubMed  Google Scholar  * 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). Article  PubMed  PubMed Central  Google Scholar  * 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). Article  CAS  PubMed  Google Scholar  * 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). Article  CAS  PubMed  PubMed Central  Google Scholar  * 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). Article  CAS  PubMed 


Google Scholar  * 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). Article  CAS  PubMed  PubMed Central  Google Scholar  * Ramírez-Valdespino, C. A., Casas-Flores, S. & Olmedo-Monfil, V. _Trichoderma_ as a model to study effector-like


molecules. _Front. Microbiol._ 10, 1030 (2019). Article  PubMed  PubMed Central  Google Scholar  * 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). Article  CAS  Google Scholar  * 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). Article  CAS  PubMed


  Google Scholar  * 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). Article  CAS  PubMed  PubMed Central  Google Scholar  * Pieterse, C. M. et al. Induced systemic resistance by beneficial microbes. _Annu. Rev.


Phytopathol._ 52, 347–375 (2014). Article  CAS  PubMed  Google Scholar  * 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). Article  CAS  PubMed  Google Scholar  * 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). Article  CAS  PubMed  Google Scholar  * 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). Article  CAS  Google Scholar  * 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). Article  CAS  PubMed  Google Scholar  * 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. Article  CAS  PubMed  PubMed Central  Google Scholar  * 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). Article  Google Scholar  * 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). Article  CAS  PubMed  Google Scholar  * 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). Article  PubMed  PubMed Central  Google Scholar  * 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. Article  PubMed  PubMed Central  Google Scholar  * 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). Article  CAS  PubMed  Google Scholar  * 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). Article  Google Scholar  * Kaushik, N. et al. Chemical composition of an aphid antifeedant extract from an endophytic fungus, _Trichoderma_


sp. EFI671. _Microorganisms_ 8, 420 (2020). Article  CAS  PubMed  PubMed Central  Google Scholar  * 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). Article  CAS  Google Scholar  *


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). CAS  Google Scholar  * 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). Article  Google Scholar  * Saijo, Y. & Loo, E. P. Plant immunity in signal integration between


biotic and abiotic stress responses. _N. Phytol._ 225, 87–104 (2020). Article  Google Scholar  * 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). Article  PubMed  PubMed Central  Google Scholar  * 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). Article  CAS 


PubMed  Google Scholar  * 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. Article  PubMed  Google Scholar  * 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). Article  Google Scholar  * 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). Article  CAS  PubMed  PubMed Central  Google Scholar  * 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). Article  PubMed  PubMed Central  Google Scholar


  * 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). Article  Google Scholar  * 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. Article  CAS  PubMed  PubMed Central  Google Scholar  *


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). Article  Google Scholar  * 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). Article  PubMed  PubMed Central  Google


Scholar  * 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).


Article  PubMed  PubMed Central  Google Scholar  * Slaughter, A. et al. Descendants of primed Arabidopsis plants exhibit resistance to biotic stress. _Plant Physiol._ 158, 835–843 (2012).


Article  CAS  PubMed  Google Scholar  * 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). Article  PubMed 


PubMed Central  Google Scholar  * 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). Article  CAS  PubMed  PubMed Central  Google Scholar  * 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). Article  CAS  PubMed  PubMed Central  Google Scholar  *


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). Article  CAS  Google Scholar  * 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). Article  CAS  PubMed  PubMed Central  Google Scholar  * Vinale, F. et al. Co-culture of plant beneficial microbes as source of


bioactive metabolites. _Sci. Rep._ 7, 14330 (2017). Article  CAS  PubMed  PubMed Central  Google Scholar  * 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). Article  Google Scholar  * 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). Article  CAS  Google Scholar  * 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). Article  CAS  PubMed  PubMed Central  Google Scholar  * 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). Article  CAS  PubMed  Google Scholar  * Kashyap, P. L.,


Rai, P., Srivastava, A. K. & Kumar, S. _Trichoderma_ for climate resilient agriculture. _World J. Microbiol. Biotechnol._ 33, 155 (2017). Article  PubMed  Google Scholar  * 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). Article  CAS  Google Scholar  * 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). Article  Google Scholar  * Rossman, A. Y. et al. Genera in bionectriaceae, hypocreaceae,


and nectriaceae (Hypocreales) proposed for acceptance or rejection. _IMA Fungus_ 4, 41–51 (2013). Article  PubMed  PubMed Central  Google Scholar  * Jones, J. D. G. & Dangl, J. L. The


plant immune system. _Nature_ 444, 323–329 (2006). Article  CAS  PubMed  Google Scholar  Download references ACKNOWLEDGEMENTS The authors would like to recognize the pioneering work on


_Trichoderma_ in agriculture by I. Chet and G. E. Harman that has served as the basis for our understanding of _Trichoderma_ today. S.L.W. and M.L. gratefully acknowledge research funding


from the European Union Horizon 2020 Research and Innovation Program — ECOSTACK (grant agreement no. 773554), the Ministry of University and Research Projects of National Relevance — PRIN


2017 PROSPECT (grant number 2017JLN833), and involvement in the Ministry of University and Research for National Recovery and Resilience Plan (PNRR), National Research Center for


Agricultural Technologies (AGRITECH — D.D. n.1032, 17/06/2022) and National Biodiversity Future Center (NBFC — D.D. n.1034, 17/06/2022). S.L.W. wishes to recognize her association with the


National Research Council, Institute for Sustainable Plant Protection, Portici, Italy, the Task Force on Microbiome Studies, and the BAT Center-Interuniversity Center for Studies on


Bioinspired Agro-Environmental Technology, University of Naples Federico II, Portici, Italy; and thank L. Gioia, G. Manganiello, E. Comite, A. Pironti, S. Lanzuise and M. Ranesi for the


technical assistance in the preparation of the manuscript. R.H. and E.M. acknowledge the support of grants co-financed by the European Regional Development Fund (FEDER) and the governments


of Spain (MCIN/AEI PDI-2021-126575OB-I00) and Castile and Leon (SA094P20, Escalera de Excelencia CLU-2018-04 and IR2020-1-USAL05). AUTHOR INFORMATION AUTHORS AND AFFILIATIONS * Department of


Pharmacy, University of Naples Federico II, Naples, Italy Sheridan L. Woo * Department of Microbiology and Genetics, Institute for Agribiotechnology Research (CIALE), University of


Salamanca, Salamanca, Spain Rosa Hermosa & Enrique Monte * Department of Agricultural Sciences, University of Naples Federico II, Portici, Italy Matteo Lorito Authors * Sheridan L. Woo


View author publications You can also search for this author inPubMed Google Scholar * Rosa Hermosa View author publications You can also search for this author inPubMed Google Scholar *


Matteo Lorito View author publications You can also search for this author inPubMed Google Scholar * Enrique Monte View author publications You can also search for this author inPubMed 


Google Scholar CONTRIBUTIONS S.L.W. and M.L. conceptualized the idea of this manuscript. S.L.W. and R.H. collected data, designed the content for the article, designed figures and drafted


the tables. S.L.W., R.H., M.L. and E.M. contributed substantially to the discussion of the content. S.L.W. and E.M. wrote the article. All authors reviewed and edited the final version of


the draft and agreed to the published version of the manuscript. CORRESPONDING AUTHOR Correspondence to Sheridan L. Woo. ETHICS DECLARATIONS COMPETING INTERESTS The authors declare no


competing interests. PEER REVIEW PEER REVIEW INFORMATION _Nature Reviews Microbiology_ thanks Alfredo Herrera-Estrella, Qirong Shen and the other, anonymous, reviewer(s) for their


contribution to the peer review of this work. ADDITIONAL INFORMATION PUBLISHER’S NOTE Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional


affiliations. RELATED LINKS INTERNATIONAL COMMISSION ON TRICHODERMA TAXONOMY: www.trichoderma.info SUPPLEMENTARY INFORMATION SUPPLEMENTARY INFORMATION GLOSSARY * Agroecosystem An ecosystem


subjected to anthropological activities that are finalized in agricultural production involving the continuous manipulation of biotic and abiotic components to obtain maximum yields and


quality of the produce such as food, textile and biofuel plant products, and animal goods. * Biofertilizers Products that contain living organisms that promote plant growth by increasing the


supply or availability of primary nutrients to the host plant. * Biological control agent (BCA). A natural enemy or antagonistic organism used in plant protection that can inhibit or


eliminate harmful organisms and their negative effects through direct or indirect mechanisms of parasitism, antibiosis, competition or induced plant defence. * Bioprotectants Biological


tools providing the protection of plants or the environment from biotic and/or abiotic stress by methods of biocontrol or bioremediation. * Biostimulant A biological product used to improve


plant nutrient use efficiency, tolerance to abiotic stress, quality traits or availability of confined nutrients in the soil by using components of microbial or non-microbial origins. *


Eco-sustainable agriculture A system that generates increasing prosperity by reducing chemical inputs and implementing alternative methods to minimize negative impacts to the environment,


biodiversity, and human and animal health, thus permitting the renewal of natural resources. * Plant protection products (PPPs). Products consisting of an approved active substance (chemical


or biological) with the capacity to protect plants or plant products against harmful organisms, that positively influence the life processes of plants, preserve plant products, destroy


undesired plants or parts of plants, or control or prevent undesired growth of plants. * Priming An adaptive strategy improving plant defence capacity whereby an initial stimulus activates


the physiological, transcriptional, metabolic and epigenetic mechanisms that enable the plant to respond more rapidly and/or efficiently to subsequent exposure to biotic or abiotic stress.


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rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law. Reprints and


permissions ABOUT THIS ARTICLE CITE THIS ARTICLE Woo, S.L., Hermosa, R., Lorito, M. _et al._ _Trichoderma_: a multipurpose, plant-beneficial microorganism for eco-sustainable agriculture.


_Nat Rev Microbiol_ 21, 312–326 (2023). https://doi.org/10.1038/s41579-022-00819-5 Download citation * Accepted: 11 October 2022 * Published: 22 November 2022 * Issue Date: May 2023 * DOI:


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