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

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Abstract

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.

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Abbreviations

ATPCA:

Arabidopsis thaliana Peroxidase A

IAA:

Indole Acetic Acid

ISR:

Induced Systemic Resistance

LOX-1 :

Lipoxygenase 1

NPR1 :

Non-Expressor of PR genes 1

PAD3 :

Phytoalexin Deficient 3

PDF1.2 :

Plant Defensin 1.2

PR:

Pathogenesis Related Protein

SA:

Salicylic Acid

SAR:

Systemic Acquired Resistance

JA:

Jasmonic Acid

References

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Bari, R., & Jones, J. D. G. (2009). Role of plant hormones in plant defence responses. Plant Molecular Biology, 69, 473–488.

    Article  PubMed  CAS  Google Scholar 

  • Beckers, G. J., & Spoel, S. H. (2006). Fine-tuning plant defence signaling: salicylate versus jasmonate. Plant Biology, 8, 1–10.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Chet, I., & Inbar, J. (1994). Biological control of fungal pathogens. Applied Biochemistry and Biotechnology, 48, 37–43.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Kleifeld, O., & Chet, I. (1992). Trichoderma harzianum - interaction with plants and effect on growth response. Plant and Soil, 144, 267–272.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Murashige, T., & Skoog, F. (1962). A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiologia Plantarum, 15, 473–497.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Van Loon, L. C. (2007). Plant responses to plant growth-promoting rhizobacteria. European Journal of Plant Patholology, 119, 243–254.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

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.

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Authors and Affiliations

  1. División de Biología Molecular, Instituto Potosino de Investigación Científica y Tecnológica, Camino a la Presa San Jose No. 2055, Col., Lomas 4a Sección, San Luis Potosí, SLP, 78216, Mexico

    Miguel Angel Salas-Marina, Miguel Angel Silva-Flores, Edith Elena Uresti-Rivera & Sergio Casas-Flores

  2. Departamento de Microbiología, Centro de Investigación Científica y de Educación Superior de Ensenada, Ensenada, Baja California, Mexico

    Ernestina Castro-Longoria

  3. Laboratorio Nacional de Genómica para la Biodiversidad, Km. 9.6 Libramiento Norte Carr. Irapuato-León 36821, Irapuato, Gto, Mexico

    Alfredo Herrera-Estrella

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  1. Miguel Angel Salas-Marina
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  2. Miguel Angel Silva-Flores
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  3. Edith Elena Uresti-Rivera
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  4. Ernestina Castro-Longoria
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  5. Alfredo Herrera-Estrella
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  6. Sergio Casas-Flores
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Corresponding author

Correspondence to Sergio Casas-Flores.

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Miguel Angel Salas-Marina and Miguel Angel Silva-Flores contributed equally to this work.

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Salas-Marina, M.A., Silva-Flores, M.A., Uresti-Rivera, E.E. 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). https://doi.org/10.1007/s10658-011-9782-6

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