Volume 70, Issues 13–14, September 2009, Pages 1581–1588

Jasmonates in Stress Responses and Development

Review

Jasmonate signaling in plant interactions with resistance-inducing beneficial microbes

·         Sjoerd Van der Enta, b [Author Vitae],

·         Saskia C.M. Van Weesa [Author Vitae],

·         Corné M.J. Pietersea, b, ,  [Author Vitae]

·         a Plant–Microbe Interactions, Institute of Environmental Biology, Faculty of Science, Utrecht University, P.O. Box 800.56, 3508 TB Utrecht, The Netherlands

·         b Centre for Biosystems Genomics, P.O. Box 98, 6700 AB Wageningen, The Netherlands

·         Received 27 March 2009. Revised 5 June 2009. Accepted 11 June 2009. Available online 25 August 2009.

·         http://dx.doi.org/10.1016/j.phytochem.2009.06.009, How to Cite or Link Using DOI

·         Cited by in Scopus (14)

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1. Introduction

2. Systemically induced disease resistance

3. ISR signal transduction

4. Beneficial microbe-associated molecular patterns

5. Local responses to beneficial microbes

6. Systemic responses to beneficial microbes

7. Conclusions

Acknowledgements

References


Abstract

Beneficial soil-borne microorganisms can induce an enhanced defensive capacity in above-ground plant parts that provides protection against a broad spectrum of microbial pathogens and even insect herbivores. The phytohormones jasmonic acid (JA) and ethylene emerged as important regulators of this induced systemic resistance (ISR). ISR triggered by plant growth-promoting rhizobacteria and fungi is often not associated with enhanced biosynthesis of these hormones, nor with massive changes in defense-related gene expression. Instead, ISR-expressing plants are primed for enhanced defense. Priming is characterized by a faster and stronger expression of cellular defense responses that become activated only upon pathogen or insect attack, resulting in an enhanced level of resistance to the invader encountered. Recent advances in induced defense signaling research revealed regulators of ISR and suggest a model in which (JA)-related transcription factors play a central role in establishing the primed state.


Graphical abstract

Jasmonates are important regulators of plant immune responses that are triggered by beneficial soil-borne microorganisms. In many cases ISR is associated with potentiated expression of jasmonate-responsive genes. Recent advances in research on induced systemic resistance (ISR) signaling suggests a model in which jasmonate-related transcription factors play a central role in establishing the primed state that is characteristic for ISR.

Abbreviations

·    BTH, benzothiadiazole;

·    ET, ethylene;

·    ETI, effector triggered immunity;

·    ISR, induced systemic resistance;

·    JA, jasmonic acid;

·    LPS, lipopolysaccharides;

·    MAMPs, microbe-associated molecular patterns;

·    MAPKs, mitogen activated protein kinases;

·    PAMPs, pathogen associated molecular patterns;

·    PGPR, plant growth-promoting rhizobacteria;

·    PGPF, plant growth-promoting fungi;

·    PR, pathogenesis related;

·    PTI, PAMP-triggered immunity;

·    RT-PCR, real-time reverse transcriptase polymerase chain reaction;

·    SA, salicylic acid;

·    SAR, systemic acquired resistance;

·    VOCs, volatile organic compounds

Keywords

·    Beneficial microorganisms;

·    Plant growth-promoting rhizobacteria (PGPR) and fungi (PGPF);

·    Induced systemic resistance (ISR);

·    Defense signaling;

·    Ethylene;

·    Jasmonic acid;

·    Microbe-associated molecular patterns (MAMPs);

·    Priming;

·    Transcription factors


Figures and tables from this article:

Fig. 1. WCS417r-ISR in Arabidopsis is associated with priming for enhanced JA-regulated defenses. (A) Colonization of the roots of Arabidopsis by the PGPR Pseudomonas fluorescens WCS417r triggers an ISR response that is effective against a broad range of pathogens and against specific insects ( [71] and [81]). Systemic activation of ISR requires activation of the transcription factor gene MYB72 in the roots (Van der Ent et al., 2008) and an intact response to the plant hormones JA and ET (Pieterse et al., 1998). (B) WCS417r does not trigger direct changes in defense-related gene-expression in above-ground plant parts, but primes the leaf tissue for a faster and stronger response to pathogen and insect attack ( [81], [83] and [87]). The set of WCS417r-primed genes, represented by the dark parts of the ISR bars, is enriched for JA- and/or ET-responsive genes (Verhagen et al., 2004).

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Fig. 2. Potentiated expression of JA-responsive defense-related genes. LOX2 and PYK10 are examples of ISR-primed, MeJA-responsive genes that show a potentiated MeJA-induced expression pattern in WCS417r-ISR-expressing plants (Pozo et al., 2008).

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Fig. 3. ISR-primed JA-responsive genes are enriched for defense-related genes. The set of ISR-primed genes is enriched for JA-responsive genes that were previously identified as responsive to the JA-inducing pathogens Pseudomonas syringae pv. tomato DC3000 (Pst DC3000) and Alternaria brassicicola, and the insect herbivores Pieris rapae and Frankliniella occidentalis ( [15] and [54]), suggesting that JA-responsive genes that are activated by JA-inducing attackers are selectively primed during ISR.

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Fig. 4. The transcription factor MYC2 is required for WCS417r-mediated ISR. (A) In silico analysis of the promoter regions of MeJA-responsive genes demonstrated that the cis-acting G-box-like motif CACATG, which serves as a docking site for the transcription factor MYC2, was significantly overrepresented in ISR-primed, MeJA-responsive genes (grey dashed lines) when compared to unprimed, MeJA-responsive genes (black dashed lines), and randomly selected promoters from the Arabidopsis genome (solid black lines) (Pozo et al., 2008). (B) WCS417r-mediated protection against Pst DC3000, as observed in wildtype Arabidopsis Col-0 plants, is lost in MYC2-impaired mutants jin1-1 and jin1-2 (Pozo et al., 2008).

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Fig. 5. Model for the role of transcription factors in priming for enhanced defense. Whole-genome expression profiling of transcription factor genes revealed a large number of transcription factor genes that are activated upon colonization of the roots by WCS417r (Van der Ent et al., 2009). This may lead to the accumulation of a pool of inactive transcription factors (TFs) in the cytosol (left panel). In response to a secondary stress stimulus, such as infection by a pathogen, specific TFs are activated (middle panel). Since the primed cells of WCS417r-treated plants contain a larger pool of latent TFs, cellular defense responses can be activated faster and stronger, resulting in an enhanced level of resistance when compared to the non-primed plants (courtesy of Dr. Jurriaan Ton).

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Corresponding author. Address: Plant–Microbe Interactions, Institute of Environmental Biology, Faculty of Science, Utrecht University, P.O. Box 800.56, 3508 TB Utrecht, The Netherlands. Tel.: +31 30 253 6887; fax: +31 30 253 2837.

Copyright © 2009 Elsevier Ltd. All rights reserved.

Vitae

Sjoerd van der Ent performed his PhD research at the Utrecht University on the role of transcription factors in the regulation of rhizobacteria-mediated induced systemic resistance (ISR) in Arabidopsis thaliana. He was able to gain novel insights into the molecular mechanisms underlying the phenomenon of priming for enhanced defense, which emerged as an important mechanism associated with induced resistance that is triggered by beneficial microbes. After his graduation in 2008, he continued his research as a postdoctoral fellow in the Plant–Microbe Interactions group at the Department of Biology, Utrecht University.

 

Saskia van Wees obtained her PhD degree in 1999 at the Utrecht University where she performed pioneering work on signaling during rhizobacteria-mediated induced systemic resistance (ISR) in Arabidopsis thaliana. After her graduation she moved to the Torrey Mesa Research Institute, San Diego, USA where she worked as a postdoctoral fellow in the laboratory of Jane Glazebrook on mechanisms of disease resistance against necrotrophic fungi. In 2004, she received a VENI fellowship from the Netherlands Science Foundation to study the role of phospholipids in plant defense at the University of Amsterdam in the laboratory of Teun Munnik. In 2007, she moved back to her roots at the Utrecht University where she now works as a senior scientist in the Plant–Microbe Interactions laboratory.

 

Corné Pieterse was educated at the Wageningen University where he studied Plant Breeding and perfomed his PhD research at the laboratory of Phytopathology on differential gene expression in Phytophthora infestans during pathogenesis on potato. After receiving his PhD degree in 1993, he moved to the Phytopathology laboratory at the