European Journal of Plant Pathology

, Volume 131, Issue 1, pp 15–26 | Cite as

Colonization of Arabidopsis roots by Trichoderma atroviride promotes growth and enhances systemic disease resistance through jasmonic acid/ethylene and salicylic acid pathways

  • Miguel Angel Salas-Marina
  • Miguel Angel Silva-Flores
  • Edith Elena Uresti-Rivera
  • Ernestina Castro-Longoria
  • Alfredo Herrera-Estrella
  • Sergio Casas-FloresEmail author


Trichoderma spp. are common soil fungi used as biocontrol agents due to their capacity to produce antibiotics, induce systemic resistance in plants and parasitize phytopathogenic fungi of major agricultural importance. The present study investigated whether colonization of Arabidopsis thaliana seedlings by Trichoderma atroviride affected plant growth and development. Here it is shown that T. atroviride promotes growth in Arabidopsis. Moreover, T. atroviride produced indole compounds in liquid cultures. These results suggest that indoleacetic acid-related indoles (IAA-related indoles) produced by T. atroviride may have a stimulatory effect on plant growth. In addition, whether colonization of Arabidopsis roots by T. atroviride can induce systemic protection against foliar pathogens was tested. Arabidopsis roots inoculation with T. atroviride provided systemic protection to the leaves inoculated with bacterial and fungal pathogens. To investigate the possible pathway involved in the systemic resistance induced by T. atroviride, the expression profile of salicylic acid, jasmonic acid/ethylene, oxidative burst and camalexin related genes was assessed in Arabidopsis. T. atroviride induced an overlapped expression of defence-related genes of SA and JA/ET pathways, and of the gene involved in the synthesis of the antimicrobial phytoalexin, camalexin, both locally and systemically. This is the first report where colonization of Arabidopsis roots by T. atroviride induces the expression of SA and JA/ET pathways simultaneously to confer resistance against hemibiotrophic and necrotrophic phytopathogens. The beneficial effects induced by the inoculation of Arabidopsis roots with T. atroviride and the induction of the plant defence system suggest a molecular dialogue between these organisms.


Plant–fungus interaction Systemic resistance Camalexin PR proteins 



Arabidopsis thaliana Peroxidase A


Indole Acetic Acid


Induced Systemic Resistance


Lipoxygenase 1


Non-Expressor of PR genes 1


Phytoalexin Deficient 3


Plant Defensin 1.2


Pathogenesis Related Protein


Salicylic Acid


Systemic Acquired Resistance


Jasmonic Acid



This work was supported in part by grants from CONACYT (SEP-103733) and IPICYT to S.C-F, and from FOMIX-GTO (GTO-2008-C03-91748) to A.H-E. M.A.S-M, M.A.S-F, and E.E.U-R are indebted to CONACYT for doctoral fellowships. We would like to thank Barbara Reithner for initial experiments on real time PCR.


  1. Baek, J. M., & Kenerley, C. M. (1998). The arg2 gene of Trichoderma virens: cloning and development of a homologous transformation system. Fungal Genetics and Biology, 23, 34–44.PubMedCrossRefGoogle Scholar
  2. Bailey, B. A., Bae, H., Strem, M. D., Roberts, D. P., Thomas, S. E., Crozier, J., et al. (2006). Fungal and plant gene expression during the colonization of cacao seedlings by endophytic isolates of four Trichoderma species. Planta, 224, 1449–1464.PubMedCrossRefGoogle Scholar
  3. Bakker, P. A. H. M., Ran, L. X., Pieterse, C. M. J., & Van Loon, L. C. (2003). Understanding the involvement of rhizobacteria mediated induction of systemic resistance in biocontrol of plant diseases. Canadian Journal of Plant Pathology, 25, 5–9.CrossRefGoogle Scholar
  4. Bari, R., & Jones, J. D. G. (2009). Role of plant hormones in plant defence responses. Plant Molecular Biology, 69, 473–488.PubMedCrossRefGoogle Scholar
  5. Beckers, G. J., & Spoel, S. H. (2006). Fine-tuning plant defence signaling: salicylate versus jasmonate. Plant Biology, 8, 1–10.PubMedCrossRefGoogle Scholar
  6. Chacón, M. R., Rodríguez-Galán, O., Benítez, T., Sousa, S., Rey, M., Llobell, A., et al. (2007). Microscopic and transcriptome analyses of early colonization of tomato roots by Trichoderma harzianum. International Microbiology, 10, 19–27.PubMedGoogle Scholar
  7. Chet, I., & Inbar, J. (1994). Biological control of fungal pathogens. Applied Biochemistry and Biotechnology, 48, 37–43.PubMedCrossRefGoogle Scholar
  8. Contreras-Cornejo, H. A., Macias-Rodríguez, L., Cortés-Penagos, C., & López-Bucio, J. (2009). Trichoderma virens, a plant beneficial fungus, enhances biomass production and promotes lateral root growth through an auxin-dependent mechanism in Arabidopsis. Plant Physiology, 149, 1579–1592.PubMedCrossRefGoogle Scholar
  9. De Meyer, G., Bigirimana, J., Elad, Y., & Höfte, M. (1998). Induced systemic resistance in Trichoderma harzianum T39 biocontrol of Botrytis cinerea. European Journal of Plant Pathology, 104, 279–286.CrossRefGoogle Scholar
  10. Glazebrook, J., & Ausubel, F. M. (1994). Isolation of phytoalexin-deficient mutants of Arabidopsis thaliana and characterization of their interactions with bacterial pathogens. Proceedings of the National Academy of Sciences, 91, 8955–8959.CrossRefGoogle Scholar
  11. Glickmann, E., & Dessaux, Y. (1995). A critical examination of the specificity of the Salkowski reagent for indolic compounds produce by phytopathogenic bacteria. Applied and Environmental Microbiology, 61, 763–796.Google Scholar
  12. Harman, G. E., Howell, C. R., Viterbo, A., Chet, I., & Lorito, M. (2004). Trichoderma species-opportunistic, avirulent plant symbionts. Nature Reviews. Microbiology, 2, 43–56.PubMedCrossRefGoogle Scholar
  13. Howell, C. R., Hanson, L. E., Stipanovic, R. D., & Puckhaber, L. S. (2000). Induction of terpenoid synthesis in cotton roots and control of Rhizoctonia solani by seed treatment with Trichoderma virens. Phytopathology, 90, 248–252.PubMedCrossRefGoogle Scholar
  14. King, E. O., Ward, M. K., & Raney, D. E. (1954). Two simple media for the demonstration of pyocyanin and fluorescin. The Journal of Laboratory and Clinical Medicine, 44, 301–307.PubMedGoogle Scholar
  15. Kleifeld, O., & Chet, I. (1992). Trichoderma harzianum - interaction with plants and effect on growth response. Plant and Soil, 144, 267–272.CrossRefGoogle Scholar
  16. Korolev, N., Rav David, D., & Elad, Y. (2008). The role of phytohormones in basal resistance and Trichoderma-induced systemic resistance to Botrytis cinerea in Arabidopsis thaliana. Biocontrol, 53, 667–683.CrossRefGoogle Scholar
  17. Martinez, C., Blanc, F., Le Claire, E., Besnard, O., Nicole, M., & Baccou, J. C. (2001). Salicylic acid and ethylene pathways are differentially activated in melon cotyledons by active or heat-denatured cellulase from Trichoderma longibrachiatum. Plant Physiology, 127, 334–344.PubMedCrossRefGoogle Scholar
  18. Mur, L. A. J., Kenton, P., Atzorn, R., Miersch, O., & Wasternack, C. (2006). The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiology, 140, 249–262.PubMedCrossRefGoogle Scholar
  19. Murashige, T., & Skoog, F. (1962). A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiologia Plantarum, 15, 473–497.CrossRefGoogle Scholar
  20. Park, S. W., Kaimoyo, E., Kumar, D., Mosher, S., & Klessig, D. F. (2007). Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science, 318, 113–116.PubMedCrossRefGoogle Scholar
  21. Pieterse, C. M. J., Leon-Reyes, A., Van der Ent, S., & Van Wees, S. C. M. (2009). Networking by small-molecule hormones in plant immunity. Nature Chemical Biology, 5, 308–316.PubMedCrossRefGoogle Scholar
  22. Segarra, G., Van der Ent, S., Trillas, I., & Pieterse, C. M. J. (2009). MYB72, a node of convergence in induced systemic resistance triggered by a fungal and a bacterial beneficial microbe. Plant Biology, 11, 90–96.PubMedCrossRefGoogle Scholar
  23. Shoresh, M., Yedidia, I., & Chet, I. (2005). Involvement of jasmonic acid/ethylene signaling pathway in the systemic resistance induced in cucumber by Trichoderma asperellum T203. Phytopathology, 95, 76–84.PubMedCrossRefGoogle Scholar
  24. Shoresh, M., Harman, G. E., & Mastoury, F. (2010). Induced systemic resistance and plant responses to fungal biocontrol agents. Annual Review of Phytopathology, 48, 21–43.PubMedCrossRefGoogle Scholar
  25. Ton, J., Van Pelt, J. A., Van Loon, L. C., & Pieterse, C. M. J. (2002). Differential effectiveness of salicylate-dependent and jasmonate/ethylene-dependent induced resistance in Arabidopsis. Molecular Plant-Microbe Interactions, 15, 27–34.PubMedCrossRefGoogle Scholar
  26. Van Loon, L. C. (2007). Plant responses to plant growth-promoting rhizobacteria. European Journal of Plant Patholology, 119, 243–254.CrossRefGoogle Scholar
  27. Van Loon, L. C., Rep, M., & Pieterse, C. M. J. (2006). Significance of inducible defense-related proteins in infected plants. Annual Review of Phytopathology, 44, 135–162.PubMedCrossRefGoogle Scholar
  28. Van Wees, S. C. M., de Swart, E. A. M., van Pelt, J. A., van Loon, L. C., & Pieterse, C. M. J. (2000). Enhancement of induced disease resistence by simultaneous activation of salicylate- and jasmonate-dependent defense pathways in Arabidopsis thaliana. Proceeding of the National Academy of Sciencies, 97, 8711–8716.CrossRefGoogle Scholar
  29. White, T. J., Brunts, T., Lee, S., & Taylor, J. W. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M. A. Innis, D. H. Gelfand, J. J. Sninsky, & T. J. White (Eds.), PCR protocols: a guide to methods and applications (pp. 315–322). New York: Academic Press, Inc.Google Scholar
  30. Yedidia, I., Benhamou, N., & Chet, I. (1999). Induction of defense responses in cucumber plants (Cucumis sativus L.) by the biocontrol agent Trichoderma harzianum. Applied and Environmental Microbiology, 65, 1061–1070.PubMedGoogle Scholar
  31. Yedidia, I., Srivastva, A. K., Kapulnik, Y., & Chet, I. (2001). Effect of Trichoderma harzianum on microelement concentrations and increased growth of cucumber plants. Plant and Soil, 235, 235–242.CrossRefGoogle Scholar
  32. Yedidia, I., Shoresh, M., Kerem, Z., Benhamou, N., Kapulnik, Y., & Chet, I. (2003). Concomitant induction of systemic resistance to Pseudomonas syringae pv. lachrymans in cucumber by Trichoderma asperellum (T-203) and the accumulation of phytoalexins. Applied and Environmental Microbiology, 69, 7343–7353.PubMedCrossRefGoogle Scholar
  33. Zeilinger, S., Galhaup, C., Payer, K., Woo, S. L., Mach, R. L., Fekete, C., et al. (1999). Chitinase gene expression during mycoparasitic interaction of Trichoderma harzianum with its host. Fungal Genetetic and Biology, 26, 131–140.CrossRefGoogle Scholar
  34. Zhou, N., Tootle, T. L., & Glazebrook, J. (1999). Arabidopsis PAD3, a gene required for camalexin biosynthesis, encodes a putative cytochrome P450 monooxygenase. The Plant Cell, 11, 2419–2428.PubMedCrossRefGoogle Scholar

Copyright information

© KNPV 2011

Authors and Affiliations

  • Miguel Angel Salas-Marina
    • 1
  • Miguel Angel Silva-Flores
    • 1
  • Edith Elena Uresti-Rivera
    • 1
  • Ernestina Castro-Longoria
    • 2
  • Alfredo Herrera-Estrella
    • 3
  • Sergio Casas-Flores
    • 1
    Email author
  1. 1.División de Biología MolecularInstituto Potosino de Investigación Científica y TecnológicaSan Luis PotosíMexico
  2. 2.Departamento de MicrobiologíaCentro de Investigación Científica y de Educación Superior de EnsenadaEnsenadaMexico
  3. 3.Laboratorio Nacional de Genómica para la BiodiversidadIrapuatoMexico

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