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The role of phytohormones in basal resistance and Trichoderma-induced systemic resistance to Botrytis cinerea in Arabidopsis thaliana

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Abstract

Thirty-six phytohormone-affected mutants of Arabidopsis thaliana (L.) Heynh. and their parental ecotypes were tested for resistance/susceptibility to Botrytis cinerea Pers.; Fr. and ability to develop Trichoderma-mediated induced systemic resistance (ISR). Ecotype Colombia-0 (Col-0) was relatively resistant to B. cinerea, and Trichoderma harzianum Rifai T39 application at sites spatially separated (roots) from the B. cinerea inoculation (leaves) resulted in reduction of grey mold symptoms. Ecotypes Wassilewskija-4, Nossen-0 and Landsberg-0 had low levels of basal resistance to B. cinerea and were unable to express ISR. Mutants derived from ISR-non-inducible ecotypes displayed ISR-non-inducible phenotypes, whereas the ISR inducibility of mutants derived from the ISR-inducible genotype Col-0 varied according to the type of mutant. Thus, salicylic acid (SA)-impaired mutants derived from Col-0 were ISR-inducible, while ethylene/jasmonic acid (ethylene/JA)-impaired mutants of the same origin were ISR-non-inducible. SA-impaired mutants retained basal level of resistance to B. cinerea, while most ethylene/JA-impaired mutants were highly susceptible. Abscisic acid- and gibberellin-impaired mutants were highly susceptible to B. cinerea and showed ISR-non-inducible phenotypes irrespective of their lines of origin. Auxin-resistant mutants derived from Col-0 were ISR-inducible; mutant originating from Landsberg-0 and mutants which were resistant to both auxin and ethylene were ISR-non-inducible. Most of the arabidopsis genotypes which were unable to express Trichoderma-mediated ISR against B. cinerea exhibited enhanced susceptibility to this pathogen. T. harzianum treatments enhanced the growth of arabidopsis plants regardless of genotype or ISR inducibility.

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Abbreviations

ABA:

Abscisic acid

GA:

Gibberellic acid

HR:

Hypersensitive response

IAA:

Indole-3-acetic acid

ISR:

Induced systemic resistance

JA:

Jasmonic acid

SA:

Salicylic acid

SAR:

Systemic acquired resistance

PR:

Pathogenesis-related

PGPR:

Plant growth promoting rhizobacteria

References

  • Anderson JP, Badruzsaufari E, Schenk PM, Manners JM, Desmond OJ, Ehlert C, Macleon DJ, Ebert PR, Kazan K (2004) Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell 16:3460–3479

    Article  PubMed  CAS  Google Scholar 

  • Denby KJ, Kumar P, Kliebenstein DJ (2004) Identification of Botrytis cinerea susceptibility loci in Arabidopsis thaliana. Plant J 38:473–486

    Article  PubMed  CAS  Google Scholar 

  • Dik JA, Elad Y (1999) Comparison of antagonists of Botrytis cinerea in greenhouse-grown cucumber and tomato under different climatic conditions. Eur J Plant Pathol 105:123–137

    Article  Google Scholar 

  • Dissevelt M, Ravensberg WJ (2002) The effect of cultural and environmental conditions on the performance of Trichoderma harzianum strain T-22. IOBC WPRS Bull 25(10):49–52

    Google Scholar 

  • Elad Y (2000) Biological control of foliar pathogens by means of Trichoderma harzianum and potential modes of action. Crop Prot 19:709–714

    Article  Google Scholar 

  • Ferrari S, Plotnikova JM, De Lorenzo G, Ausubel FM (2003) Arabidopsis local resistance to Botrytis cinerea involves salicylic acid and camalexin and requires EDS4 and PAD2, but not SID2, EDS5 or PAD4. Plant J 35:193–205

    Article  PubMed  CAS  Google Scholar 

  • Govrin EM, Levine A (2000) The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr Biol 10:751–757

    Article  PubMed  CAS  Google Scholar 

  • Govrin EM, Levine A (2002) Infection of Arabidopsis with a necrotrophic pathogen, Botrytis cinerea, elicits various responses but does not induce systemic acquired resistance (SAR). Plant Mol Biol 48:267–276

    Article  PubMed  CAS  Google Scholar 

  • Guimaraes RL, Stotz HU (2004) Oxalate production by Sclerotinia sclerotiorum deregulates guard cells during infection. Plant Physiol 136:3703–3711

    Article  PubMed  CAS  Google Scholar 

  • Hammerschmidt R (1999) Induced disease resistance: how do induced plants stop pathogens? Physiol Mol Plant Pathol 55:77–84

    Article  CAS  Google Scholar 

  • Harman GE, Howell CR, Vitebro A, Chet I, Lorito M (2004) Trichoderma species––opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56

    Article  PubMed  CAS  Google Scholar 

  • Iavicoli A, Boutet E, Buchalla A, Metraux JP (2003) Induced systemic resistance in Arabidopsis thaliana in response to root inoculation with Pseudomonas fluorescens CHAO. MPMI 16:851–858

    PubMed  CAS  Google Scholar 

  • Kloepper JW, Ruy CM, Zhang S (2004) Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94:1259–1266

    Article  CAS  Google Scholar 

  • Korolev N, Rav David D, Elad Y (2004) Involvement of plant hormones in the biocontrol achieved by Trichoderma harzianum. IOBC WPRS Bull 27(8):363–366

    Google Scholar 

  • Kunkel BN, Brooks DM (2002) Cross talk between signaling pathways in pathogen defense. Curr Opin Plant Biol 5:325–331

    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. Eur J Plant Pathol 104:279–286

    Article  Google Scholar 

  • Mohr PG, Gahill DM (2003) Abscisic acid influences the susceptibility of Arabidopsis thaliana to Pseudomonas syringae pv. tomato and Peronospora parasitica. Funct Plant Biol 30:461–469

    Article  CAS  Google Scholar 

  • Nickstadt A, Thomma BPHJ, Feussner I, Kangasjarvi J, Zeier J, Loeffler C, Scheel D, Berger A (2004) The jasmonate-insensitive mutant jin1 shows increased resistance to biotrophic as well as necrotrophic pathogens. Mol Plant Pathol 5:425–434

    Article  CAS  Google Scholar 

  • Okon Levy N, Elad Y, Korolev N, Katan J (2003) Resistance induced by soil biocontrol application and soil solarization for the control of foliar pathogens. IOBC WPRS Bulletin 27:171–176

    Google Scholar 

  • Ousley MA, Lynch JM, Whipps J (1994) Potential of Trichoderma spp. as consistent plant growth stimulators. Microbiol Fertil Soils 17:85–90

    Article  Google Scholar 

  • Pieters CMJ, Van Wees SCM, Van Pelt JA, Knoester M, Laan R, Gerrits H, Weisbeek PJ, Van Loon LC (1998) A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10:1571–1580

    Article  Google Scholar 

  • Pieterse CMJ, Van Pelt JA, Van Wees SCM, Ton J, Leon-Kloosterziel KM, Keurentjes JJB, Verhagen BWM, Knoester M, Van der Slius I, Bakker PAHM, Van Loon LC (2001) Rhizobacteria-mediated induced systemic resistance: triggering, signaling and expression. Eur J Plant Pathol 107:51–61

    Article  Google Scholar 

  • Ping L, Boland W (2004) Signals from the underground: bacterial volatiles promote growth in Arabidopsis. Trends in Plant Sci 9:263–266

    Article  CAS  Google Scholar 

  • Rusterucci C, Zhao Z, Haines K, Mellersh D, Neuman M, Cameron RK (2005) Age-related resistance to Pseudomonas syringae pv. tomato is associated with the transition to flowering in Arabidopsis and is effective against Peronospora parasitica. Physiol Mol Plant Pathol 66:222–231

    Article  CAS  Google Scholar 

  • Ryu C-M, Farag MA, Hu C-H, Reddy MS, Kloepper JW, Pare PW (2004) Bacterial volatiles induced systemic resistance in Arabidopsis. Plant Physiol 234:1017–1026

    Article  Google Scholar 

  • Staswick PJ, Yuen GY, Lehman CC (1998) Jasmonate signaling mutants of Arabidopsis are susceptible to the soil fungus Pythium irregulare. Plant J 15:747–754

    Article  PubMed  CAS  Google Scholar 

  • Thaler JS, Owen B, Higgins VJ (2004) The role of the jasmonate response in plant susceptibility to diverse pathogens with a range of lifestyles. Plant Physiol 135:530–538

    Article  PubMed  CAS  Google Scholar 

  • Thomma BPHJ, Eggermont K, Penninckx IAMA, Mauch-Mani B, Vogelsang R, Cammue PA, Broekaert WF (1998) Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc Nat Acad Sci USA 95:15107–15111

    Article  PubMed  CAS  Google Scholar 

  • Tiryaki I, Staswick PE (2002) An Arabidopsis mutant defective in jasmonate response is allelic to the auxin-signaling mutant axr1. Plant Physiol 130:887–894

    Article  PubMed  CAS  Google Scholar 

  • Tjamos SE, Flemetakis E, Paplomatas EJ, Katinakis P (2005) Induction of resistance to Verticillium dahliae in Arabidopsis thaliana by the biocontrol agent K-165 and pathogenesis-related proteins gene expression. MPMI 18:555–561

    PubMed  CAS  Google Scholar 

  • Ton J, De Vos M, Robben C, Buchala A, Mètraux J-P, Van Lonn LC, Pieterse CMJ (2002) Characterization of Arabidopsis enchanced disease susceptibility mutants that are affected in systemically induced resistance. Plant J 29:11–21

    Article  PubMed  CAS  Google Scholar 

  • Ton J, Mauch-Mani B (2004) β-amino-butyric acid-induced resistance against necrotrophic pathogens is based on ABA-dependent priming for callose. Plant J 38:119–130

    Article  PubMed  CAS  Google Scholar 

  • Ton J, Davidson S, van Loon LS, Pieterse CMJ (2001) Heritability of rhizobacteria-mediated induced systemic resistance and basal resistance in Arabidopsis. Eur J Plant Pathol 107:63–68

    Article  Google Scholar 

  • Van Heuvel KHPT, Hulzink JNR, Barense GWM, Wullems GJ (2001) The expression of tgas118, encoding a defensin in Lycopersicon esculentum, is regulated by gibberellin. J Exp Bot 52:1427–1436

    Article  PubMed  Google Scholar 

  • Van Loon LC, Bakker PAHM, Pieterse CMJ (1998) Systemic resistance induced by Rhizosphere bacteria. Ann Rev Phytopathol 36:453–83

    Article  Google Scholar 

  • Weigel D, Glazenbook J (2002) Arabidopsis. A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

Download references

Acknowledgements

The study of the susceptibilities of arabidopsis mutants to B. cinerea was supported by grant No. TU 50/9-4 from the Deutsche Forschungsgemeinschaft (DFG). N. Korolev’s work was supported by a fellowship from the Israeli Ministry of Immigration. We thank the Nottingham Arabidopsis Stock Center and the Arabidopsis Biological Resource Center (Columbus, OH) for the arabidopsis seeds and the P. Tudzynski from the Institute Fuer Botanik, Muenster, Germany for fruitful discussions.

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Korolev, N., Rav David, D. & Elad, Y. The role of phytohormones in basal resistance and Trichoderma-induced systemic resistance to Botrytis cinerea in Arabidopsis thaliana . BioControl 53, 667–683 (2008). https://doi.org/10.1007/s10526-007-9103-3

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  • DOI: https://doi.org/10.1007/s10526-007-9103-3

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