Abiotic plant stress mitigation by Trichoderma species

Hexon Angel Contreras-Cornejo, Monika Schmoll, Blanca Alicia Esquivel-Ayala, Carlos E. González-Esquivel, Victor Rocha-Ramírez, John Larsen

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Soil Ecology Letters ›› 2024, Vol. 6 ›› Issue (4) : 240240. DOI: 10.1007/s42832-024-0240-8
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Abiotic plant stress mitigation by Trichoderma species

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Highlights

● Ascomycetes of the genus Trichoderma are beneficial fungi that promote plant growth.

● Several fungal species can mitigate abiotic stress in plants.

Trichoderma spp. induce salt stress tolerance and drought protection in plants.

● Soil contamination by heavy metals can be bioremediated by Trichoderma .

Trichoderma can detoxify pesticides and other pollutants in soils.

Abstract

Plants drive both carbon and nitrogen cycling and mediate complex biotic interactions with soil microorganisms. Climate change and the resulting temperature variations, altered precipitation, and water shortages in soils, affect the performance of plants. Negative effects of abiotic stress are reflected in changes of plant morphology associated with biochemical alterations and inadequate adaptation to rapid ecological change. Accumulation of chemical agents, derived from pesticides, salinity due to chemical fertilization, and accumulation of heavy metals, are recurrent problems in agricultural soils. Trichoderma spp. are soil fungi interacting with roots and in this way helping plants to cope with abiotic stresses by increasing root branching, shoot growth and productivity. In part, such fungal effects on the host plant are consequences of the activation of fine-tuned molecular mechanisms mediated by phytohormones, by profound biochemical changes that include production of osmolytes, by the activity of the redox-enzymatic machinery, as well by as complex processes of detoxification. Here, we summarize the most recent advances regarding the beneficial effects of Trichoderma in mitigating the negative effects on plant performance caused by different environmental and chemical factors associated with global change and agricultural practices that provoke abiotic stress. Additionally, we present new perspectives and propose further research directions in the field of Trichoderma-plant interactions when the two types of organism cooperate.

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Keywords

Trichoderma / abiotic stress tolerance / salinity / drought / pollution / beneficial fungi

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Hexon Angel Contreras-Cornejo, Monika Schmoll, Blanca Alicia Esquivel-Ayala, Carlos E. González-Esquivel, Victor Rocha-Ramírez, John Larsen. Abiotic plant stress mitigation by Trichoderma species. Soil Ecology Letters, 2024, 6(4): 240240 https://doi.org/10.1007/s42832-024-0240-8

References

[1]
Abogadallah, G.M., 2010. Antioxidative defense under salt stress. Plant Signaling & Behavior5, 369–374.
[2]
Achard, P., Cheng, H., De Grauwe, L., Decat, J., Schoutteten, H., Moritz, T., Van Der Straeten, D., Peng, J.R., Harberd, N.P., 2006. Integration of plant responses to environmentally activated phytohormonal signals. Science311, 91–94.
CrossRef Google scholar
[3]
Adams, P., De-Leij, F.A.A.M., Lynch, J.M., 2007. Trichoderma harzianum Rifai 1295–22 mediates growth promotion of crack willow (Salix fragilis) saplings in both clean and metal-contaminated soil. Microbial Ecology54, 306–313.
CrossRef Google scholar
[4]
Allen, C.D., Macalady, A.K., Chenchouni, H., Bachelet, D., McDowell, N., Vennetier, M., Kitzberger, T., Rigling, A., Breshears, D.D., Hogg, E.H., Gonzalez, P., Fensham, R., Zhang, Z., Castro, J., Demidova, N., Lim, J.H., Allard, G., Running, S.W., Semerci, A., Cobb, N., 2010. A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. Forest Ecology and Management259, 660–684.
CrossRef Google scholar
[5]
Anshu, A., Agarwal, P., Mishra, K., Yadav, U., Verma, I., Chauhan, S., Srivastava, P.K., Singh, P.C., 2022. Synergistic action of Trichoderma koningiopsis and T. asperellum mitigates salt stress in paddy. Physiology and Molecular Biology of Plants28, 987–1004.
CrossRef Google scholar
[6]
Arroyo, A., Bossi, F., Finkelstein, R.R., León, P., 2003. Three genes that affect sugar sensing (abscisic acid insensitive 4, abscisic acid insensitive 5, and constitutive triple response 1) are differentially regulated by glucose in Arabidopsis. Plant Physiology133, 231–242.
CrossRef Google scholar
[7]
Averill, C., Anthony, M.A., Baldrian, P., Finkbeiner, F., van den Hoogen, J., Kiers, T., Kohout, P., Hirt, E., Smith, G.R., Crowther, T.W., 2022. Defending Earth's terrestrial microbiome. Nature Microbiology7, 1717–1725.
CrossRef Google scholar
[8]
Bae, H., Roberts, D.P., Lim, H.S., Strem, M.D., Park, S.C., Ryu, C.M., Melnick, R.L., Bailey, B.A., 2011. Endophytic Trichoderma isolates from tropical environments delay disease onset and induce resistance against Phytophthora capsici in hot pepper using multiple mechanisms. Molecular Plant-Microbe Interactions24, 336–351.
CrossRef Google scholar
[9]
Bae, H., Sicher, R.C., Kim, M.S., Kim, S.H., Strem, M.D., Melnick, R.L., Bailey, B.A., 2009. The beneficial endophyte Trichoderma hamatum isolate DIS 219b promotes growth and delays the onset of the drought response in Theobroma cacao. Journal of Experimental Botany60, 3279–3295.
CrossRef Google scholar
[10]
Bao, F., Li, J.Y., 2002. Evidence that the auxin signaling pathway interacts with plant stress response. Acta Botanica Sinica44, 532–536.
[11]
Bashyal, B.M., Parmar, P., Zaidi, N.W., Aggarwal, R., 2021. Molecular programming of drought-challenged Trichoderma harzianum-bioprimed rice (Oryza sativa L.). Frontiers in Microbiology12, 655165.
CrossRef Google scholar
[12]
Björkman, T., Blanchard, L.M., Harman, G.E., 1998. Growth enhancement of shrunken-2 (sh2) sweet corn by Trichoderma harzianum 1295-22: effect of environmental stress. Journal of the American Society for Horticultural Science123, 35–40.
CrossRef Google scholar
[13]
Boamah, S., Zhang, S.W., Xu, B.L., Li, T., Calderón-Urrea, A., 2021. Trichoderma longibrachiatum (TG1) enhances wheat seedlings tolerance to salt stress and resistance to Fusarium pseudograminearum. Frontiers in Plant Science12, 741231.
CrossRef Google scholar
[14]
Boamah, S., Zhang, S.W., Xu, B.L., Li, T., Calderón-Urrea, A., Tiika, R.J., 2022. Trichoderma longibrachiatum TG1 increases endogenous salicylic acid content and antioxidants activity in wheat seedlings under salinity stress. PeerJ10, e12923.
CrossRef Google scholar
[15]
Brotman, Y., Landau, U., Cuadros-Inostroza, Á., Takayuki, T., Fernie, A.R., Chet, I., Viterbo, A., Willmitzer, L., 2013. Trichoderma-plant root colonization: escaping early plant defense responses and activation of the antioxidant machinery for saline stress tolerance. PLoS Pathogens9, e1003221.
CrossRef Google scholar
[16]
Brotman, Y., Lisec, J., Méret, M., Chet, I., Willmitzer, L., Viterbo, A., 2012. Transcript and metabolite analysis of the Trichoderma-induced systemic resistance response to Pseudomonas syringae in Arabidopsis thaliana. Microbiology158, 139–146.
CrossRef Google scholar
[17]
Butterbach-Bahl, K., Dannenmann, M., 2011. Denitrification and associated soil N2O emissions due to agricultural activities in a changing climate. Current Opinion in Environmental Sustainability3, 389–395.
CrossRef Google scholar
[18]
Cabral-Miramontes, J.P., Olmedo-Mofil, V., Lara-Banda, M., Zúñiga-Romo, E.R., Aréchiga-Carvajal, E.T., 2022. Promotion of plant growth in arid zones by selected Trichoderma spp. strains with adaptation plasticity to alkaline pH. Biology11, 1206.
[19]
Cao, X., Sui, J.J., Li, H.Y., Yue, W.X., Liu, T., Hou, D., Liang, J.H., Wu, Z., 2023. Enhancing heat stress tolerance in Lanzhou lily (Lilium davidii var. unicolor) with Trichokonins isolated from Trichoderma longibrachiatum SMF2. Frontiers in Plant Science 14, 1182977
[20]
Carbone, M.J., Alaniz, S., Mondino, P., Gelabert, M., Eichmeier, A., Tekielska, D., Bujanda, R., Gramaje, D., 2021. Drought influences fungal community dynamics in the grapevine rhizosphere and root microbiome. Journal of Fungi7, 686.
CrossRef Google scholar
[21]
Cardarelli, M., Woo, S.L., Rouphael, Y., Colla, G., 2022. Seed treatments with microorganisms can have a biostimulant effect by influencing germination and seedling growth of crops. Plants11, 259.
CrossRef Google scholar
[22]
Cavicchioli, R., Ripple, W.J., Timmis, K.N., Azam, F., Bakken, L.R., Baylis, M., Behrenfeld, M.J., Boetius, A., Boyd, P.W., Classen, A.T., Crowther, T.W., Danovaro, R., Foreman, C.M., Huisman, J., Hutchins, D.A., Jansson, J.K., Karl, D.M., Koskella, B., Mark Welch, D.B., Martiny, J.B.H., Moran, M.A., Orphan, V.J., Reay, D.S., Remais, J.V., Rich, V.I., Singh, B.K., Stein, L.Y., Stewart, F.K., Sullivan, M.B., van Oppen, M.J.H., Weaver, S.C., Webb, E.A., Webster, N.S., 2019. Scientists’ warning to humanity: microorganisms and climate change. Nature Reviews Microbiology17, 569–586.
CrossRef Google scholar
[23]
Chaverri, P., Branco-Rocha, F., Jaklitsch, W., Gazis, R., Degenkolb, T., Samuels, G.J., 2015. Systematics of the Trichoderma harzianum species complex and the re-identification of commercial biocontrol strains. Mycologia107, 558–590.
CrossRef Google scholar
[24]
Chen, M.B., Liu, Q.K., Gao, S.S., Young, A.E., Jacobsen, S.E., Tang, Y., 2019. Genome mining and biosynthesis of a polyketide from a biofertilizer fungus that can facilitate reductive iron assimilation in plant. Proceedings of the National Academy of Sciences of the United States of America116, 5499–5504.
[25]
Chen, S.C., Yan, Y.R., Wang, Y.Q., Wu, M.J., Mao, Q., Chen, Y.F., Ren, J.J., Liu, A.R., Lin, X.M., Ahammed, G.J., 2020. Trichoderma asperellum reduces phoxim residue in roots by promoting plant detoxification potential in Solanum lycopersicum L. Environmental Pollution259, 113893.
CrossRef Google scholar
[26]
Contreras-Cornejo, H.A., del-Val, E., Macías-Rodríguez, L., Alarcón, A., González-Esquivel, C.E., Larsen, J., 2018. Trichoderma atroviride, a maize root associated fungus, increases the parasitism rate of the fall armyworm Spodoptera frugiperda by its natural enemy Campoletis sonorensis. Soil Biology and Biochemistry122, 196–202.
CrossRef Google scholar
[27]
Contreras-Cornejo, H.A., Larsen, J., Fernández-Pavía, S.P., Oyama, K., 2023. Climate change, a booster of disease outbreaks by the plant pathogen Phytophthora in oak forests. Rhizosphere27, 100719.
CrossRef Google scholar
[28]
Contreras-Cornejo, H.A., Macías-Rodríguez, L., Alfaro-Cuevas, R., López-Bucio, J., 2014. Trichoderma spp. improve growth of Arabidopsis seedlings under salt stress through enhanced root development, osmolite production, and Na+ elimination through root exudates. Molecular Plant-Microbe Interactions 27, 503–514
[29]
Contreras-Cornejo, H.A., Macías-Rodríguez, L., del-Val, E., Larsen, J., 2020a. Interactions of Trichoderma with plants, insects, and plant pathogen microorganisms: chemical and molecular bases. In: Merillon, J.M., Ramawat, K.G., eds. Co-evolution of Secondary Metabolites. Cham: Springer, 1–28
[30]
Contreras-Cornejo, H.A., Macías-Rodríguez, L., del-Val, E., Larsen, J., 2016. Ecological functions of Trichoderma spp. and their secondary metabolites in the rhizosphere: interactions with plants. FEMS Microbiology Ecology92, fiw036.
[31]
Contreras-Cornejo, H.A., Macías-Rodríguez, L., Vergara, A.G., López-Bucio, J., 2015. Trichoderma modulates stomatal aperture and leaf transpiration through an abscisic acid-dependent mechanism in Arabidopsis. Journal of Plant Growth Regulation34, 425–432.
CrossRef Google scholar
[32]
Contreras-Cornejo, H.A., Orozco-Granados, O., Ramírez-Ordorica, A., García-Juárez, P., López-Bucio, J., Macías-Rodríguez, L., 2022. Light and mycelial injury influences the volatile and non-volatile metabolites and the biocontrol properties of Trichoderma atroviride. Rhizosphere22, 100511.
CrossRef Google scholar
[33]
Contreras-Cornejo, H.A., Viveros-Bremauntz, F., del-Val, E., Macías-Rodríguez, L., López-Carmona, D.A., Alarcón, A., González-Esquivel, C.E., Larsen, J., 2020b. Alterations of foliar arthropod communities in a maize agroecosystem induced by the root-associated fungus Trichoderma harzianum. Journal of Pest Science94, 363–374.
[34]
Cordier, C., Edel-Hermann, V., Martin-Laurent, F., Blal, B., Steinberg, C., Alabouvette, C., 2007. SCAR-based real time PCR to identify a biocontrol strain (T1) of Trichoderma atroviride and study its population dynamics in soils. Journal of Microbiological Methods68, 60–68.
CrossRef Google scholar
[35]
Cristaldi, A., Conti, G.O., Cosentino, S.L., Mauromicale, G., Copat, C., Grasso, A., Zuccarello, P., Fiore, M., Restuccia, C., Ferrante, M., 2020. Phytoremediation potential of Arundo donax (Giant Reed) in contaminated soil by heavy metals. Environmental Research185, 109427.
CrossRef Google scholar
[36]
de Almeida Silva, J.L., Nascimento Duarte, S., da Silva, D.D., de Oliveira Miranda, N., 2019. Reclamation of salinized soils due to excess of fertilizers: evaluation of leaching systems and equations. Dyna86, 115–124.
CrossRef Google scholar
[37]
Dixit, P., Mukherjee, P.K., Ramachandran, V., Eapen, S., 2011a. Glutathione transferase from Trichoderma virens enhances cadmium tolerance without enhancing its accumulation in transgenic Nicotiana tabacum. PLoS One6, e16360.
CrossRef Google scholar
[38]
Dixit, P., Mukherjee, P.K., Sherkhane, P.D., Kale, S.P., Eapen, S., 2011b. Enhanced tolerance and remediation of anthracene by transgenic tobacco plants expressing a fungal glutathione transferase gene. Journal of Hazardous Materials192, 270–276.
[39]
do Rêgo Meneses, F.J., de Oliveira Lopes, Á.L., Silva Setubal, I., da Costa Neto, V.P., Bonifácio, A., 2022. Inoculation of Trichoderma asperelloides ameliorates aluminum stress-induced damages by improving growth, photosynthetic pigments and organic solutes in maize. 3 Biotech 12, 246
[40]
Evans, H.C., Holmes, K.A., Thomas, S.E., 2003. Endophytes and mycoparasites associated with an indigenous forest tree, Theobroma gileri, in Ecuador and a preliminary assessment of their potential as biocontrol agents of cocoa diseases. Mycological Progress2, 149–160.
CrossRef Google scholar
[41]
Fu, J., Liu, Z.H., Li, Z.T., Wang, Y.F., Yang, K.J., 2017. Alleviation of the effects of saline-alkaline stress on maize seedlings by regulation of active oxygen metabolism by Trichoderma asperellum. PLoS One12, e0179617.
CrossRef Google scholar
[42]
Gadd, G.M., 2010. Metals, minerals and microbes: geomicrobiology and bioremediation. Microbiology156, 609–643.
CrossRef Google scholar
[43]
Gadd, G.M., Rhee, Y.J., Stephenson, K., Wei, Z., 2012. Geomycology: metals, actinides and biominerals. Environmental Microbiology Reports4, 270–296.
CrossRef Google scholar
[44]
Govarthanan, M., Lee, K.J., Cho, M., Kim, J.S., Kamala-Kannan, S., Oh, B.T., 2013. Significance of autochthonous Bacillus sp. KK1 on biomineralization of lead in mine tailings. Chemosphere 90, 2267–2272
[45]
Govarthanan, M., Mythili, R., Kamala-Kannan, S., Selvankumar, T., Srinivasan, P., Kim, H., 2019. In-vitro bio-mineralization of arsenic and lead from aqueous solution and soil by wood rot fungus, Trichoderma sp. Ecotoxicology and Environmental Safety174, 699–705.
CrossRef Google scholar
[46]
Gravel, V., Antoun, H., Tweddell ., R.J., 2007. Growth stimulation and fruit yield improvement of greenhouse tomato plants by inoculation with Pseudomonas putida or Trichoderma atroviride: possible role of indole acetic acid (IAA). Soil Biology and Biochemistry39, 1968–1977.
CrossRef Google scholar
[47]
Gupta, S., Smith, P.M.C., Boughton, B.A., Rupasinghe, T.W.T., Natera, S.H.A., Roessner, U., 2021. Inoculation of barley with Trichoderma harzianum T-22 modifies lipids and metabolites to improve salt tolerance. Journal of Experimental Botany72, 7229–7246.
CrossRef Google scholar
[48]
Harman, G.E., 2011. Multifunctional fungal plant symbionts: new tools to enhance plant growth and productivity. New Phytologist189, 647–649.
CrossRef Google scholar
[49]
Harman, G.E., Doni, F., Khadka, R.B., Uphoff, N., 2021. Endophytic strains of Trichoderma increase plants’ photosynthetic capability. Journal of Applied Microbiology130, 529–546.
CrossRef Google scholar
[50]
Harman, G.E., Howell, C.R., Viterbo, A., Chet, I., Lorito, M., 2004. Trichoderma species-opportunistic, avirulent plant symbionts. Nature Reviews Microbiology2, 43–56.
CrossRef Google scholar
[51]
Hoseini, A., Salehi, A., Sayyed, R.Z., Balouchi, H., Moradi, A., Piri, R., Fazeli-Nasab, B., Poczai, P., Ansari, M.J., Al Obaid, S., Datta, R., 2022. Efficacy of biological agents and fillers seed coating in improving drought stress in anise. Frontiers in Plant Science13, 955512.
CrossRef Google scholar
[52]
Illescas, M., Pedrero-Méndez, A., Pitorini-Bovolini, M., Hermosa, R., Monte, E., 2021. Phytohormone production profiles in Trichoderma species and their relationship to wheat plant responses to water stress. Pathogens10, 991.
CrossRef Google scholar
[53]
Irshad, K., Shaheed Siddiqui, Z., Chen, J.J., Rao, Y.N., Hamna Ansari, H., Wajid, D., Nida, K., Wei, X.Y., 2023. Bio-priming with salt tolerant endophytes improved crop tolerance to salt stress via modulating photosystem II and antioxidant activities in a sub-optimal environment. Frontiers in Plant Science14, 1082480.
CrossRef Google scholar
[54]
Jan, R., Khan, M.A., Asaf, S., Lubna, Lee, I.J., Kim, K.M., 2021. Over-expression of chorismate mutase enhances the accumulation of salicylic acid, lignin, and antioxidants in response to the white-backed planthopper in rice plants. Antioxidants10, 1680.
CrossRef Google scholar
[55]
Jasińska, A., Różalska, S., Rusetskaya, V., Słaba, M., Bernat, P., 2022. Microplastic-induced oxidative stress in metolachlor-degrading filamentous fungus Trichoderma harzianum. International Journal of Molecular Sciences23, 12978.
CrossRef Google scholar
[56]
Karuppiah, V., Zhang, X.F., Lu, Z.X., Hao, D.Z., Chen, J., 2022. Role of the global fitness regulator genes on the osmotic tolerance ability and salinity hazard alleviation of Trichoderma asperellum GDFS 1009 for sustainable agriculture. Journal of Fungi8, 1176.
CrossRef Google scholar
[57]
Kolandasamy, M., Mandal, A.K.A., Balasubramanian, M.G., Ponnusamy, P., 2023. Multifaceted plant growth-promoting traits of indigenous rhizospheric microbes against Phomopsis theae, a causal agent of stem canker in tea plants. World Journal of Microbiology and Biotechnology39, 237.
CrossRef Google scholar
[58]
Lesk, C., Rowhani, P., Ramankutty, N., 2016. Influence of extreme weather disasters on global crop production. Nature529, 84–87.
CrossRef Google scholar
[59]
Li, X.X., Zhang, X., Wang, X.L., Yang, X.Y., Cui, Z.J., 2019. Bioaugmentation-assisted phytoremediation of lead and salinity co-contaminated soil by Suaeda salsa and Trichoderma asperellum. Chemosphere224, 716–725.
CrossRef Google scholar
[60]
Liu, Q.M., Tang, S.Y., Meng, X.H., Zhu, H., Zhu, Y.Y., Liu, D.Y., Shen, Q.R., 2021. Proteomic analysis demonstrates a molecular dialog between Trichoderma guizhouense NJAU 4742 and cucumber (Cucumis sativus L.) roots: role in promoting plant growth. Molecular Plant-Microbe Interactions34, 631–644.
[61]
Lombardi, N., Vitale, S., Turrà, D., Reverberi, M., Fanelli, C., Vinale, F., Marra, R., Ruocco, M., Pascale, A., d’Errico, G., Woo, S.L., Lorito, M., 2018. Root exudates of stressed plants stimulate and attract Trichoderma soil fungi. Molecular Plant-Microbe Interactions31, 982–994.
CrossRef Google scholar
[62]
Macías-Rodríguez, L., Contreras-Cornejo, H.A., Adame-Garnica, S.G., del-Val, E., Larsen, J., 2020. The interactions of Trichoderma at multiple trophic levels: inter-kingdom communication. Microbiological Research240, 126552.
CrossRef Google scholar
[63]
Macías-Rodríguez, L., Guzmán-Gómez, A., García-Juárez, P., Contreras-Cornejo, H.A., 2018. Trichoderma atroviride promotes tomato development and alters the root exudation of carbohydrates, which stimulates fungal growth and the biocontrol of the phytopathogen Phytophthora cinnamomi in a tripartite interaction system. FEMS Microbiology Ecology94, fiy137.
[64]
Martínez-Medina, A., Van Wees, S.C.M., Pieterse, C.M.J., 2017. Airborne signals from Trichoderma fungi stimulate iron uptake responses in roots resulting in priming of jasmonic acid-dependent defences in shoots of Arabidopsis thaliana and Solanum lycopersicum. Plant, Cell & Environment40, 2691–2705.
[65]
Mastouri, F., Björkman, T., Harman, G.E., 2010. Seed treatment with Trichoderma harzianum alleviates biotic, abiotic, and physiological stresses in germinating seeds and seedlings. Phytopathology100, 1213–1221.
CrossRef Google scholar
[66]
Mastouri, F., Björkman, T., Harman, G.E., 2012. Trichoderma harzianum enhances antioxidant defense of tomato seedlings and resistance to water deficit. Molecular Plant-Microbe Interactions25, 1264–1271.
CrossRef Google scholar
[67]
Menegat, S., Ledo, A., Tirado, R., 2022. Greenhouse gas emissions from global production and use of nitrogen synthetic fertilisers in agriculture. Scientific Reports12, 14490.
CrossRef Google scholar
[68]
Metwally, R.A., Soliman, S.A., 2023. Alleviation of the adverse effects of NaCl stress on tomato seedlings (Solanum lycopersicum L. ) by Trichoderma viride through the antioxidative defense system. Botanical Studies64, 4.
[69]
Moharana, P.C., Singh, R.S., Singh, S.K., Tailor, B.L., Jena, R.K., Meena, M.D., 2019. Development of secondary salinity and salt migration in the irrigated landscape of hot arid India. Environmental Earth Sciences78, 454.
CrossRef Google scholar
[70]
Nykiel-Szymańska, J., Bernat, P., Słaba, M., 2020. Biotransformation and detoxification of chloroacetanilide herbicides by Trichoderma spp. with plant growth-promoting activities. Pesticide Biochemistry and Physiology163, 216–226.
[71]
Ou, T., Zhang, M., Gao, H.Y., Wang, F., Xu, W.F., Liu, X.J., Wang, L., Wang, R.L., Xie, J., 2023. Study on the potential for stimulating mulberry growth and drought tolerance of plant growth-promoting fungi. International Journal of Molecular Sciences24, 4090.
CrossRef Google scholar
[72]
Poosapati, S., Ravulapalli, P.D., Viswanathaswamy, D.K., Kannan, M., 2021. Proteomics of two thermotolerant isolates of Trichoderma under high-temperature stress. Journal of Fungi7, 1002.
CrossRef Google scholar
[73]
Poveda, J., 2020. Trichoderma parareesei favors the tolerance of rapeseed (Brassica napus L.) to salinity and drought due to a chorismate mutase. Agronomy10, 118.
[74]
Poveda, J., Rodríguez, V.M., Abilleira, R., Velasco, P., 2023. Trichoderma hamatum can act as an inter-plant communicator of foliar pathogen infections by colonizing the roots of nearby plants: a new inter-plant “wired communication”. Plant Science330, 111664.
CrossRef Google scholar
[75]
Rawal, R., Scheerens, J.C., Fenstemaker, S.M., Francis, D.M., Miller, S.A., Benitez, M.S., 2022. Novel Trichoderma isolates alleviate water deficit stress in susceptible tomato genotypes. Frontiers in Plant Science13, 869090.
CrossRef Google scholar
[76]
Rosmana, A., Nasaruddin, N., Hendarto, H., Hakkar, A.A., Agriansyah, N., 2016. Endophytic association of Trichoderma asperellum within Theobroma cacao suppresses vascular streak dieback incidence and promotes side graft growth. Mycobiology44, 180–186.
CrossRef Google scholar
[77]
Russo, F., Ceci, A., Maggi, O., Siciliano, A., Guida, M., Petrangeli-Papini, M., Černík, M., Persiani, A.M., 2019. Understanding fungal potential in the mitigation of contaminated areas in the Czech Republic: tolerance, biotransformation of hexachlorocyclohexane (HCH) and oxidative stress analysis. Environmental Science and Pollution Research26, 24445–24461.
CrossRef Google scholar
[78]
Russo, F., Ceci, A., Pinzari, F., Siciliano, A., Guida, M., Malusà, E., Tartanus, M., Miszczak, A., Maggi, O., Persiani, A.M., 2019. Bioremediation of dichlorodiphenyltrichloroethane (DDT)-contaminated agricultural soils: potential of two autochthonous saprotrophic fungal strains. Applied and Environmental Microbiology85, e01720–19.
[79]
Shukla, N., Awasthi, R.P., Rawat, L., Kumar, J., 2012. Biochemical and physiological responses of rice (Oryza sativa L.) as influenced by Trichoderma harzianum under drought stress. Plant Physiology and Biochemistry54, 78–88.
[80]
Stavi, I., Thevs, N., Priori, S., 2021. Soil salinity and sodicity in drylands: a review of causes, effects, monitoring, and restoration measures. Frontiers in Environmental Science9, 712831.
CrossRef Google scholar
[81]
Su, S.M., Zeng, X.B., Feng, Q.F., Bai, L.Y., Zhang, L.L., Jiang, S., Li, A.G., Duan, R., Wang, X.R., Wu, C.X., Wang, Y.N., 2015. Demethylation of arsenic limits its volatilization in fungi. Environmental Pollution204, 141–144.
CrossRef Google scholar
[82]
TariqJaveed, 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 Pathology183, 107626.
CrossRef Google scholar
[83]
Viterbo, A., Landau, U., Kim, S., Chernin, L., Chet, I., 2010. Characterization of ACC deaminase from the biocontrol and plant growth-promoting agent Trichoderma asperellum T203. FEMS Microbiology Letters305, 42–48.
CrossRef Google scholar
[84]
Waadt, R., Seller, C.A., Hsu, P.K., Takahashi, Y., Munemasa, S., Schroeder, J.I., 2022. Plant hormone regulation of abiotic stress responses. Nature Reviews Molecular Cell Biology23, 680–694.
CrossRef Google scholar
[85]
Woo, S.L., Hermosa, R., Lorito, M., Monte, E., 2023. Trichoderma: a multipurpose, plant-beneficial microorganism for eco-sustainable agriculture. Nature Reviews Microbiology21, 312–326.
CrossRef Google scholar
[86]
Yao, X., Guo, H.L., Zhang, K.X., Zhao, M.Y., Ruan, J.J., Chen, J., 2023. Trichoderma and its role in biological control of plant fungal and nematode disease. Frontiers in Microbiology14, 1160551.
CrossRef Google scholar
[87]
Zafra, G., Cortés-Espinosa, D.V., 2015. Biodegradation of polycyclic aromatic hydrocarbons by Trichoderma species: a mini review. Environmental Science and Pollution Research22, 19426–19433.
CrossRef Google scholar
[88]
Zhang, C.Y., Wang, W.W., Hu, Y.H., Peng, Z.P., Ren, S., Xue, M., Liu, Z., Hou, J.M., Xing, M.Y., Liu, T., 2022. A novel salt-tolerant strain Trichoderma atroviride HN082102.1 isolated from marine habitat alleviates salt stress and diminishes cucumber root rot caused by Fusarium oxysporum. BMC Microbiology 22, 67
[89]
Zhang, F.L., Wang, Y.H., Liu, C., Chen, F.J., Ge, H.L., Tian, F.S., Yang, T.W., Ma, K.S., Zhang, Y., 2019a. Trichoderma harzianum mitigates salt stress in cucumber via multiple responses. Ecotoxicology and Environmental Safety170, 436–445.
CrossRef Google scholar
[90]
Zhang, S.W., Gan, Y.T., Xu, B.L., 2019b. Mechanisms of the IAA and ACC-deaminase producing strain of Trichoderma longibrachiatum T6 in enhancing wheat seedling tolerance to NaCl stress. BMC Plant Biology19, 22.
CrossRef Google scholar
[91]
Zhao, L., Zhang, Y.Q., 2015. Effects of phosphate solubilization and phytohormone production of Trichoderma asperellum Q1 on promoting cucumber growth under salt stress. Journal of Integrative Agriculture14, 1588–1597.
CrossRef Google scholar
[92]
Zhu, T.T., Dittrich, M., 2016. Carbonate precipitation through microbial activities in natural environment, and their potential in biotechnology: a review. Frontiers in Bioengineering and Biotechnology4, 4.

Acknowledgements

This work was supported by the Consejo Nacional de Humanidades Ciencias y Tecnologías of Mexico, grant PRONACE-CONAHCYT 316049. The work of MS was supported by the Austrian Science Fund (FWF, grant P31464 to MS).

Conflict of interest

The authors have no conflicts of interest to declare.

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