Trichoderma e seus mecanismos de ação para o biocontrole de doenças de plantas

  1. Monte, E. 1
  2. Bettiol, W
  3. Hermosa, R. 1
  1. 1 Spanish-Portuguese Institute for Agricultural Research (CIALE), Department of Microbiology and Genetics, University of Salamanca
Libro:
Trichoderma uso na agricultura

Editorial: Embrapa: Brasilia DF (Brasil)

ISBN: 978-85-7035-943-8

Año de publicación: 2019

Páginas: 181-199

Tipo: Capítulo de Libro

Resumen

Neste capítulo serão abordados os conhecimentos detalhados das espécies de Trichoderma e seus mecanismos de ação, não somente como agentes de controle biológico, mas também como microrganismos simbiontes com plantas, constituindo em um modelo de estudo para aproximações moleculares mutualistas entre fungos e plantas, que permitem aos fungos se alimentarem e crescerem e às plantas se desenvolverem e se defenderem frente ao ataque de patógenos e situações de estresses abióticos e bióticos.

Referencias bibliográficas

  • ALONSO-RAMÍREZ, A.; POVEDA, J.; MARTÍN, I.; HERMOSA, R.; MONTE, E.; NICOLÁS, C. Salicylic acid prevents Trichoderma harzianum from entering the vascular system of roots. Molecular Plant Pathology, v. 15, n. 8, p. 823-831, 2014.
  • ATANASOVA, L. Ecophysiology of Trichoderma and Gliocladium in genome perspective. In: GUPTA, V. S.; SCHMOLL, M.; HERRERA-ESTRELLA, A.; UPADHYAY, R. S.; DRUZHININA, I., TUOHY, M. (Ed.). Biotechnology and biology of Trichoderma. Boston: Elsevier, 2014. p. 25-40.
  • ATANASOVA, L.; LE CROM, S.; GRUBER, S.; COULPIER, F.; SEIDL-SEIBOTH, V.; KUBICEK, C. P.; DRUZHININA, I. S. Comparative transcriptomics reveals different strategies of Trichoderma mycoparasitism. BMC Genomics, v. 14, p. 121, 2013.
  • BAE, H.; SICHER, R. C.; KIM, M. S.; KIM, S-H.; STREM, M. D.; MELNICK, R. L.; BAILEY, B. A. The beneficial endophyte Trichoderma hamatum isolate DIS 219b promotes growth and delays the onset of the drought response in Theobroma cacao. Journal of Experimental Botany, v. 60, n. 11, p. 3279-3295, 2009.
  • BAKER, R.; ELAD, Y.; CHET, I. The controlled experiment in the scientific method with special emphasis on biological control. Phytopathology, v. 74, n. 9, p. 1019-1021, 1984.
  • BOARI, A.; CIASCA, B.; PINEDA-MARTOS, R.; LATTANZIO, V. M.; YONEYAMA, K.; VURRO, M. Parasitic weed management by using strigolactones-degrading fungi. Pest Management Science, v. 72, n. 11, p. 2043-2047, 2016.
  • BROTMAN, Y.; LANDAU, U.; CUADROS-INOSTROZA, A.; TAKAYUKI, T.; FERNIE, A. R.; CHET, I.; VITERBO, A.; WILLMITZER, L. Trichoderma-plant root colonization: escaping early plant defense responses and activation of the antioxidant machinery for saline stress tolerance. PLoS Pathogens, v. 9, e1003221, 2013.
  • BUYSENS, C.; CÉSAR, V.; FERRAIS, F.; DE BOULOIS, H. D.; 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. Applied Soil Ecology, v. 105, p. 137-143, 2016.
  • CARRERO-CARRÓN, I.; RUBIO, M. B.; NIÑO-SÁNCHEZ, J.; NAVAS, J. A.; JIMÉNEZ-DÍAZ, R. M.; MONTE, E.; HERMOSA, R. Interactions between Trichoderma harzianum and defoliating Verticillium dahliae in resistant and susceptible wild olive clones. Plant Pathology, v. 67, n. 8, p. 1758-1767, 2018.
  • CHANDANIE, W. A.; KUBOTA, M.; HYAKUMACHI, M. Interactions between the arbuscular mycorrhizal fungus Glomus mosseae and plant growth-promoting fungi and their significance for enhancing plant growth and suppressing damping-off of cucumber (Cucumis sativus L.). Applied Soil Ecology, v. 41, n. 3, p. 336-341, 2009.
  • CHANG, Y.; CHANG, Y.; BAKER, R.; KLEIFELD, O.; CHET, I. Increased growth of plants in the presence of the biological control agent Trichoderma harzianum. Plant Disease, v. 70, n. 2, p. 145-148, 1986.
  • CHEN, L.; YANG, X.; RAZA, W.; LI, J.; LIU, Y.; QIU, M.; ZHANG, F.; SHEN, Q. Trichoderma harzianum SQR-T037 rapidly degrades allelochemicals in rhizospheres of continuously cropped cucumbers. Applied Microbiology and Biotechnology, v. 89, n. 5, p. 1653- 1663, 2011.
  • CONTRERAS-CORNEJO, H. A.; DEL-VAL, E.; MACÍAS-RODRÍGUEZ, L.; ALARCÓN, A.; GONZÁLEZ-ESQUIVEL, C. E.; LARSEN, J. 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 Biochemistry, v. 122, p. 196-202, 2018.
  • CONTRERAS-CORNEJO, H. A.; MACÍAS-RODRÍGUEZ, L.; CORTÉS-PANGO, 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 Physiology, v. 149, n. 3, p. 1579-1592, 2009.
  • COPPOLA, M.; CASCONE, P.; CHIUSANO, M. L.; COLANTUONO, C.; LORITO, M.; PENNACCHIO, F.; RAO, R.; WOO, S. L.; GUERRIERI, E.; DIGILIO, M. C. Trichoderma harzianum enhances tomato indirect defense against aphids. Insect Science, v. 24, n. 6, p. 1025-1033, 2017.
  • DE JAEGER, N.; DECLERCK, S.; DE LA PROVIDENCIA I. E. Mycoparasitism of arbuscular mycorrhizal fungi: a pathway for the entry of saprotrophic fungi into roots. FEMS Microbiology Ecology, v. 73, n. 2, p. 312-322, 2010.
  • DOMÍNGUEZ, S.; RUBIO, M. B.; CARDOZA, R. E.; GUTIÉRREZ, S.; NICOLÁS, C.; BETTIOL, W.; HERMOSA, R.; MONTE, E. Nitrogen metabolism and growth enhancement in tomato plants challenged with Trichoderma harzianum expressing the Aspergillus nidulans acetamidase amdS gene. Frontiers in Microbiology, v. 7, p. 1182, 2016.
  • DRUZHININA, I. S.; CHENTHAMARA, K.; ZHANG, J.; ATANASOVA, L.; YANG, D.; MIAO, Y.; RAHIMI, M. J., GRUJIC, M.; CAI, F.; POURMEHDI, S.; SALIM, K. A.; PRETZER, C.; KOPCHINSKLY, A. G.; HENRISSAT, B.; KUO, A.; HUNDLEY, H.; WANG, M.; AERTS, A.; SALAMOV, A.; LIPZEN, A.; LaBUTTI, K.; BARRY, K.; GRIGORIEV, I. V.; SHENG, Q.; KUBICEK, C. P. Massive lateral transfer of genes encoding plant cell wall-degrading enzymes to the mycoparasitic fungus Trichoderma from its plant-associated hosts. PLoS Genetics, v. 14, n. 4, e1007322, 2018.
  • DRUZHININA, I. S.; SEIDL-SEIBOTH, V.; HERRERA-ESTRELLA, A.; HORWITZ, B. A.; KENERLEY, C. M.; MONTE, E.; MUKHERJEE, P. K.; ZEILINGER, S.; GRIGORIEV, I. V.; KUBICEK, C. P. Trichoderma: the genomics of opportunistic success. Natural Reviews. Microbiology, v. 9, n. 10, p. 749-759, 2011.
  • ELSHARKAWY, M. M.; SHIMIZU, M.; TAKAHASHI, H.; OZAKI, K.; HYAKUMACHI, M. Induction of systemic resistance against cucumber mosaic virus in Arabidopsis thaliana by Trichoderma asperellum SKT-1. Plant Pathology Journal, v. 29, n. 2, p. 193-200, 2013.
  • EVIDENTE, A.; ANDOLFI, A.; CIMMINO, A.; GANASSI, S.; ALTOMARE, C.; FAVILLA, M.; DE CRISTOFARO, A.; VITAGLIANO, S.; SABATINI, M. A. Bisorbicillinoids produced by the fungus Trichoderma citrinoviride affect feeding preference of the aphid Schizaphis graminum. Journal of Chemical Ecology, v. 35, n. 5, p. 533-541, 2009.
  • FLORES, A.; CHET, I.; HERRERA-ESTRELLA, A. Improved biocontrol activity of Trichoderma harzianum by over-expression of the proteinase-encoding gene prb1. Current Genetics, v. 31, n. 1, p. 30-37, 1997.
  • FRANCESCHETTI, M.; MAQBOOL, A.; JIMENEZ-DALMARONI, M. J.; PENNINGTON, H. G.; KAMOUN, S.; BANFIELD, M. J. Effectors of filamentous plant pathogens: commonalities amid diversity. Microbiology and Molecular Biology Reviews, v. 81, n. 2, e00066-16, 2017.
  • GRAVEL, V.; ANTOUN, H.; TWEDDELL, R. J. 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 Biochemistry, v. 39, n. 8, p. 1968-1977, 2007.
  • HARMAN, G. E. Myths and dogmas of biocontrol: changes in perceptions derived from research on Trichoderma harzianum T-22. Plant Disease, v. 84, p. 377-393, 2000.
  • HARMAN, G. E.; HOWELL, C. R.; VITERBO, A.; CHET, I.; LORITO, M. Trichoderma species - opportunistic, avirulent plant symbionts. Nature Reviews. Microbiology, v. 2, n. 1, p. 43-56, 2004.
  • HERMOSA, R.; CARDOZA, R. E.; RUBIO, M. B.; GUTIÉRREZ, S.; MONTE, E. Secondary metabolism and antimicrobial metabolites of Trichoderma. In: GUPTA, V. K.; SCHMOLL, M.; HERRERA-ESTRELLA, A.; UPADHYAY, R. S.; DRUZHININA, I.; TUOHY, M. (Ed.). Biotechnology and biology of Trichoderma. Amsterdam: Elsevier, 2014. p. 125-137.
  • HERMOSA, R.; GRONDONA, I.; ITUARRIAGA, E.; DÍAZ-MÍNGUEZ, J.; CASTRO, C.; MONTE, E.; GARCÍA-ACHA, I. Molecular characterization and identification of biocontrol isolates of Trichoderma spp. Applied and Environmental Microbiology, v. 66, n. 5, p. 1890-1898, 2000.
  • HERMOSA, R.; RUBIO, M. B.; CARDOZA, R. E.; NICOLÁS, C.; MONTE, E.; GUTIÉRREZ, S. The contribution of Trichoderma to balancing the costs of plant growth and defense. International Microbiology, v. 16, n. 2, p. 69-80, 2013.
  • HERMOSA, R.; VITERBO, A.; CHET, I.; MONTE, E. Plant-beneficial effects of Trichoderma and of its genes. Microbiology, v. 158, p. 17-25, 2012.
  • KESWANI, C.; MISHRA, S.; SARMA, B. K.; SINGH, S. P.; SIGH, H. B. Unraveling the efficient applications of secondary metabolites of various Trichoderma spp. Applied and Environmental Microbiology, v. 98, p. 533-544, 2014.
  • KUBICEK, C. P.; HERRERA-ESTRELLA, A.; SEIDL-SEIBOTH, V.; MARTINEZ, D. A.; DRUZHININA, I. S.; THON, M.; ZEILINGER, S.; CASAS-FLORES, S.; HORWITZ, B. A.; MUKHERJEE, P. K.; MUKHERJEE, M.; KREDICS, L.; ALCARAZ, L. D.; AERTS, A.; ANTAL, S.; ATANASOVA, L.; CERVANTES-BADILLO, M. G.; CHALLACOMBE, J.; CHERTKOV, O.; MCCLUSKEY, K.; COULPIER, F.; DESHPANDE, N.; HANS VON DÖHREN, H. von; EBBOLE, D. J.; ESQUIVEL-NARANJO, E. U.; FEKETE, E.; FLIPPHI, M.; GLASER, F.; GÓMEZ-RODRÍGUEZ, E. Y.; GRUBER, S.; HAN, C.; HENRISSAT, B.; HERMOSA, R.; HERNÁNDEZ-OÑATE, M.; KARAFFA, L.; KOSTI, I.; LE CROM, S.; LINDQUIST, E.; LUCAS, S.; LÜBECK, M.; LÜBECK, P. S.; MARGEOT, A.; METZ, B.; MISRA, M.; NEVALAINEN, E.; OMANN, M.; PACKER, N.; PERRONE, G.; URESTI-RIVERA, E. E.; SALAMOV, A.; SCHMOLL, S.; SEIBOTH, B.; SHAPIRO, H.; SUKNO, S.; TAMAYO-RAMOS, J. A.; TISCH, D.; WIEST, A.; WILKINSON, H. H.; ZHANG, M.; COUTINHO, P. M.; KENERLEY, C. M.; MONTE, E.; BAKER, S. E.; GRIGORIEV, I. V. Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma. Genome Biology, v. 12, n. 4, R40, 2011.
  • LI, R. X.; CAI, F.; PANG, G.; SHEN, Q. R.; LI, R.; CHEN, W. Solubilisation of phosphate and micronutrients by Trichoderma harzianum and its relationship with the promotion of tomato plant growth. PLoS One, v. 10, n. 6, e0130081, 2015.
  • LI, H. Y.; LUO, Y.; ZHANG, X. Z.; SHI, W. L.; GONG, Z. T.; SHI, M.; CHEN, L. L.; CHEN, X. L.; ZHANG, Y. Z.; SONG, X. Y. Trichokonins from Trichoderma pseudokoningii SMF2 induce resistance against gram-negative Pectobacterium carotovorum subsp. carotovoroum in Chinese cabbage. FEMS Microbiology Letters, v. 354, n. 1, p. 75-82, 2014.
  • LO PRESTI, L.; LANVER, D.; SCHWEIZER, G.; TANAKA, S.; LIANG, L.; TOLLOT, M.; ZUCCARO, A.; REISSMANN, S.; KAHMANN, R. Fungal effectors and plant susceptibility. Annual Review of Plant Biology, v. 66, p. 513-545, 2015.
  • MARRA, R.; AMBROSINO, P.; CARBONE, V.; VINALE, F.; WOO, S. L.; RUOCCO, M.; CILIENTO, R.; LANZUISE, S.; FERRAIOLI, S.; SORIENTE, I.; GIGANTE, S.; TURRA, D.; FOGLIANO, V.; SCALA, F.; LORITO, M. Study of the three-way interaction between Trichoderma atroviride, plant and fungal pathogens by using a proteomic approach. Current Genetics, v. 50, n. 5, p. 307-321, 2006.
  • MARRA, R.; LOMBARDI, N.; D’ERRICO, G.; TROISI, J.; SCALA, G.; VINALE, F.; WOO, S. L.; BONANOMI, G.; LORITO, M. Application of Trichoderma strains and metabolites enhances soybean productivity and nutrient content. Journal of Agricultural and Food Chemistry, v. 67, n. 7, p. 1814-1822, 2019.
  • MARTÍNEZ-MEDINA, A.; FERNÁNDEZ, I.; SÁNCHEZ-GUZMÁN, M. J.; JUNG, S. C.; PASCUAL, J. A.; POZO, M. J. Deciphering the hormonal signaling network behind the systemic resistance induced by Trichoderma harzianum in tomato. Frontiers in Plant Science, v. 4, article 206, 2013.
  • MASTOURI, F.; BJÖRKMAN, T.; HARMAN, G. E. Trichoderma harzianum enhances antioxidant defense of tomato seedlings and resistance to water deficit. Molecular Plant-Microbe Interactions, v. 25, n. 9, p. 1264-1271, 2012.
  • MASUNAKA, A.; HYAKUMACHI, M.; TAKENAKA, S. Plant growth-promoting fungus, Trichoderma koningii suppresses isoflavonoid phytoalexin vestitol production for colonization on/in the roots of Lotus japonicas. Microbes and Environments, v. 26, n. 2, p. 128-134, 2011.
  • MATHYS, J.; DE CREMER, K.; TIMMERMANS, P.; VAN KERCKHOVE, S.; LIEVENS, B.; VANHAECKE, M.; CAMMUE, B. P.; DE CONINCK, B. Genome-wide characterization of ISR induced in Arabidopsis thaliana by Trichoderma hamatum T382 against Botrytis cinerea infection. Frontiers in Plant Science, v. 3, p. 108, 2012.
  • MEDEIROS, H. A.; ARAUJO FILHO, J. V.; FREITAS, L. G.; CASTILLO, P.; RUBIO, M. B.; HERMOSA, R.; MONTE, E. Tomato progeny inherit resistance to the nematode Meloidogyne javanica linked to plant growth induced by the biocontrol fungus Trichoderma atroviride. Scientific Reports, v. 7, article 40216, 2017.
  • MENDOZA-MENDOZA, A.; ZAID, R.; LAWRY, R.; HERMOSA, R.; MONTE, E.; HORWITZ, B.; MUKHERJEE, P. K. Molecular dialogue between Trichoderma and roots. Role of the fungal secretome. Fungal Biology Reviews, v. 32, n. 2, p. 62-85, 2018.
  • MONTE, E. Understanding Trichoderma: between biotechnology and microbial ecology. International Microbiology, v. 4, n. 1, p. 1-4, 2001.
  • 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. Applied and Environmental Microbiology, v. 77, n. 9, p. 3009-3016, 2011.
  • MONTERO-BARRIENTOS, M.; HERMOSA, R.; NICOLÁS, C.; CARDOZA, R. E.; GUTIÉRREZ, S.; MONTE, E. Overexpression of a Trichoderma HSP70 gene increases fungal resistance to heat and other abiotic stresses. Fungal Genetics and Biology, v. 45, n. 11, p. 1506-1513, 2008.
  • MORÁN-DIEZ, E.; CARDOZA, R. E.; GUTIÉRREZ, S.; MONTE, E.; HERMOSA, R. TvDim1 of Trichoderma virens is involved in redox-processes and confers resistance to oxidative stresses. Current Genetics, v. 56, n. 1, p. 63-73, 2010.
  • MORÁN-DIEZ, E.; HERMOSA, M. R.; AMBROSIO, P.; CARDOZA, R. E.; GUTIÉRREZ, S.; LORITO, M.; MONTE, E. The ThPG1 endopolygalacturonase is required for the Trichoderma harzianum-plant beneficial interaction. Molecular Plant-Microbe Interactions, v. 22, n. 8, p. 1021-1031, 2009.
  • MORÁN-DIEZ, E.; RUBIO, B.; DOMÍNGUEZ, S.; HERMOSA, R.; MONTE, E.; NICOLÁS, C. Transcriptomic response of Arabidopsis thaliana after 24 h incubation with the biocontrol fungus Trichoderma harzianum. Journal of Plant Physiology, v. 169, n. 6, p. 614-620,2012.
  • MORÁN-DIEZ, M. E.; TRUSHINA, N.; LAMDAN, N. L.; ROSENFELDER, L.; MUKHERJEE, P. K.; KENERLEY, C. M.; HORWITZ, B. A. Hostspecific transcriptomic pattern of Trichoderma virens during interaction with maize or tomato roots. BMC Genomics, v. 16, n. 1, p. 8, 2015.
  • MUKHERJEE, P. K.; HORWITZ, B. A.; KENERLEY, C. M. Secondary metabolism in Trichoderma – a genomic perspective. Microbiology, v. 158, n. 1, p. 35-45, 2012.
  • PÉREZ, E.; RUBIO, M. B.; CARDOZA, R. E.; GUTIÉRREZ, S.; BETTIOL, W.; MONTE, E.; HERMOSA, R. The importance of chorismate mutase in the biocontrol potential of Trichoderma parareesei. Frontiers in Microbiology, v. 6, article 1181, 2015.
  • PIETERSE, C. M.; LEÓN-REYES, A.; ENT, S. V. D.; WEES, S. C. VAN. Networking by small-molecule hormones in plant immunity. Nature Chemical Biology, v. 5, p. 308-316, 2009.
  • PIETERSE, C. M.; ZAMIOUDIS, C.; BERENDSEN, R. L.; WELLER, D. M.; WEES, S. C. van; BAKKER, P. A. Induced systemic resistance by beneficial microbes. Annual Review of Phytopathology, v. 52, p. 347-375, 2014.
  • RIVAS, S.; GENIN, S. A plethora of virulence strategies hidden behind nuclear targeting of microbial effectors. Frontiers in Plant Science, v. 2, p. 104, 2011.
  • RUBIO, M. B.; HERMOSA, M. R.; KECK, E.; MONTE, E. Specific PCR assays for the detection and quantification of DNA from the biocontrol strain Trichoderma harzianum 2413 in soil. Microbial Ecology, v. 49, n. 1, p. 25-33, 2005.
  • RUBIO, M. B.; HERMOSA, R.; VICENTE, R.; GÓMEZ-ACOSTA, F. A.; MORCUENDE, R.; MONTE, E.; BETTIOL, W. 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. Frontiers in Plant Science, v. 8, p. 294, 2017.
  • RUBIO, M. B.; QUIJADA, N. M.; PÉREZ, E.; DOMÍNGUEZ, S.; MONTE, E.; HERMOSA, R. Identifying beneficial qualities of Trichoderma parareesei for plants. Applied and Environmental Microbiology, v. 80, n. 6, p. 1864-1873, 2014.
  • RUOCCO, M.; LANZUISE, S.; VINALE, F.; MARRA, R.; TURRÀ, D.; WOO, S. L.; LORITO, M. 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. Molecular Plant-Microbe Interactions, v. 22, n. 3, p. 291-301, 2009.
  • SABATINI, M. A.; GANASSI, S.; ALTOMARE, C.; FAVILLA, M.; EVIDENTE, A.; ANDOLFI, A. Phagodeterrent compounds of fungal origin. EP 2706846 A1, US 20140228448 A1, WO 2012153314 A1, 14 May 2012, 15 Nov. 2012.
  • SALAS-MARINA, M. A.; SILVA-FLORES, M. A.; URESTI-RIVERA, E. E.; CASTRO-LONGORIA, E.; HERRERA-ESTRELLA, A.; CASASFLORES, S. Colonization of Arabidopsis roots by Trichoderma atroviride promotes growth and enhances systemic disease resistance through jasmonic acid/ethylene and salicylic acid pathways. European Journal of Plant Pathology, v. 131, n. 1, p. 15-26, 2011.
  • 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, v. 158, n. 1, p. 129-138, 2012.
  • SANZ, L.; MONTERO, M.; GRONDONA, I.; VIZCAÍNO, J. A.; LLOBELL, A.; HERMOSA, R.; MONTE, E. Cell wall-degrading isoenzyme profiles of Trichoderma biocontrol strains show correlation with rDNA taxonomic species. Current Genetics, v. 46, n. 5, p. 277-286, 2004.
  • SEGARRA, G.; CASANOVA, E.; BELLIDO, D.; ODENA, M. A.; OLIVEIRA, E.; TRILLAS, I. Proteome, salicylic acid, and jasmonic acid changes in cucumber plants inoculated with Trichoderma asperellum strain T34. Proteomics, v. 7, n. 21, p. 3943-3952, 2007.
  • SEIDL, V.; SEIBEL, C.; KUBICEK, C. P.; SCHMOLL, M. Sexual development in the industrial workhorse Trichoderma reesei. Proceedings of the National Academy of Science of United States of America, v. 106, n. 33, p. 13909-13914, 2009.
  • SELIN, C.; DE KIEVIT, T. R.; BELMONTE, M. F.; FERNANDO, W. G. Elucidating the role of effectors in plantefungal interactions: progress and challenges. Frontiers in Microbiology, v. 7, p. 600, 2016.
  • SHAKERI, J.; FOSTER, H. A. PROTEOLYTIC ACTIVITY AND ANTIBIOTIC PRODUCTION BY TRICHODERMA HARZIANUM IN RELATION TO PATHOGENICITY TO INSECTS. ENZYME AND MICROBIAL TECHNOLOGY, v. 40, n. 4, p. 961-968, 2007.
  • SHORESH, M.; HARMAN, G. E.; MASTOURI, F. Induced systemic resistance and plant responses to fungal biocontrol agents. Annual Review of Phytopathology, v. 48, p. 21-43, 2010.
  • SHORESH, M.; YEDIDIA, I.; CHET, I. Involvement of the jasmonic acid/ethylene signaling pathway in the systemic resistance induced in cucumber by Trichoderma asperellum T203. Phytopathology, v. 95, n. 1, p. 76-84, 2005.
  • SIVAN, A.; CHET, I. The possible role of competition between Trichoderma harzianum and Fusarium oxysporum of rhizosphere colonization. Phytopathology, v. 79, n. 2, p. 198-203, 1989.
  • 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. Applied Microbiology and Biotechnology, v. 65, n. 1, p. 46-55, 2004.
  • SUÁREZ, M. B.; VIZCAÍNO, J. A.; LLOBELL, A.; MONTE, E. Characterization of genes encoding novel peptidases in the biocontrol fungus Trichoderma harzianum CECT 2413 using the TrichoEST functional genomics approach. Current Genetics, v. 51, n. 5, p. 331- 342, 2007.
  • TIJERINO, A.; HERMOSA, R.; CARDOZA, R. E.; MORAGA, J.; MALMIERCA, M. G.; ALEU, J.; COLLADO, I. G.; MONTE, E.; GUTIÉRREZ, S. Overexpression of the Trichoderma brevicompactum tri5 gene: effect on the expression of the trichodermin biosynthetic genes and on tomato seedlings. Toxins, v. 3, n. 9, p. 1220-1232, 2011.
  • VARGAS, W. A.; MANDAWE, J. C.; KENERLEY, C. M. Plant-derived sucrose is a key element in the symbiotic association between Trichoderma virens and maize plants. Plant Physiology, v. 151, n. 2, p. 792-808, 2009.
  • VARGAS, W. A.; MUKHERJEE, P. K.; LAUGHLIN, D.; WIEST, A.; MORÁN-DIEZ, M. E.; KENERLEY, C. M. Role of gliotoxin in the symbiotic and pathogenic interactions of Trichoderma virens. Microbiology, v. 160, p. 2319-2330, 2014.
  • VINALE, F.; SIVASITHAMPARAM, K.; GHISALBERTI, E. L.; MARRA, R.; BARBETTI, M. J.; LI, H.; WOO, S. L.; LORITO, M. A novel role for Trichoderma secondary metabolites in the interactions with plants. Physiological and Molecular Plant Pathology, v. 72, n. 1-3, p. 80-86, 2008.
  • VITERBO, A.; LANDAU, U.; KIM, S.; CHERNIN, L.; CHET, I. Characterization of ACC deaminase from the biocontrol and plant growth-promoting agent Trichoderma asperellum T203. FEMS Microbiology Letters, v. 305, n. 1, p. 42-48, 2010.
  • WEINDLING, R. Trichoderma lignorum as a parasite of other soil fungi. Phytopathology, v. 22, p. 837-845, 1932.
  • WEINDLING, R. Studies on a lethal principle effective in the parasitic action of Trichoderma lignorum on Rhizoctonia solani and other soil fungi. Phytopathology, v. 24, p. 1153-1179, 1934.
  • WIN, J.; CHAPARRO-GARCIA, A.; BELHAJ, K.; SAUNDERS, D. G.; YOSHIDA, K.; DONG, S.; SCHORNACK, S.; ZIPFEL, C.; ROBATZEK, S.; HOGENHOUT, S. A.; KAMOUN, S. Effector biology of plant associated organisms: concepts and perspectives. Cold Spring Harbor Symposia on Quantitative Biology, v. 77, p. 235-247, 2012.
  • WOO, S. L.; PEPE, O. Microbial consortia: promising probiotics as plant biostimulants for sustainable agriculture. Frontiers in Plant Science, v. 9, p. 1801, 2018.
  • YEDIDIA, I.; SRIVASTVA, A. K.; KAPULNIK, Y.; CHET, I. Effect of Trichoderma harzianum on microelement concentrations and increased growth of cucumber plants. Plant and Soil, v. 235, n. 2, p. 235-242, 2001.
  • YEDIDIA, I.; BENHAMOU, N.; CHET, I. Induction of defense responses in cucumber plants (Cucumis sativus L.) by the biocontrol agent Trichoderma harzianum. Applied and Environmental Microbiology, v. 65, n. 3, p. 1061-1070, 1999.