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Colonization of the Arabidopsis rhizosphere by fluorescent Pseudomonas spp. activates a root-specific, ethylene-responsive PR-5 gene in the vascular bundle

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Abstract

Plants of which the roots are colonized by selected strains of non-pathogenic, fluorescent Pseudomonas spp. develop an enhanced defensive capacity against a broad spectrum of foliar pathogens. In Arabidopsis thaliana, this rhizobacteria-induced systemic resistance (ISR) functions independently of salicylic acid but requires responsiveness to jasmonic acid and ethylene. In contrast to pathogen-induced systemic acquired resistance (SAR), ISR is not associated with systemic changes in the expression of genes encoding pathogenesis-related (PR) proteins. To identify genes that are specifically expressed in response to colonization of the roots by ISR-inducing Pseudomonas fluorescens WCS417r bacteria, we screened a collection of Arabidopsis enhancer trap and gene trap lines containing a transposable element of the Ac/Ds system and the GUS reporter gene. We identified an enhancer trap line (WET121) that specifically showed GUS activity in the root vascular bundle upon colonization of the roots by WCS417r. Fluorescent Pseudomonas spp. strains P. fluorescens WCS374r and P. putida WCS358r triggered a similar expression pattern, whereas ISR-non-inducing Escherichia coli bacteria did not. Exogenous application of the ethylene precursor 1-aminocyclopropane-1-carboxylate (ACC) mimicked the rhizobacteria-induced GUS expression pattern in the root vascular bundle, whereas methyl jasmonic acid and salicylic acid did not, indicating that the Ds element in WET121 is inserted in the vicinity of an ethylene-responsive gene. Analysis of the expression of the genes in the close vicinity of the Ds element revealed AtTLP1 as the gene responsible for the in cis activation of the GUS reporter gene in the root vascular bundle. AtTLP1 encodes a thaumatin-like protein that belongs to the PR-5 family of PR proteins, some of which possess antimicrobial properties. AtTLP1 knockout mutant plants showed normal levels of WCS417r-mediated ISR against the bacterial leaf pathogen Pseudomonas syringae pv. tomato DC3000, suggesting that expression of AtTLP1 in the roots is not required for systemic expression of ISR in the leaves. Together, these results indicate that induction of AtTLP1 is a local response of Arabidopsis roots to colonization by non-pathogenic fluorescent Pseudomonas spp. and is unlikely to play a role in systemic resistance.

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Authors and Affiliations

  1. Faculty of Biology, Graduate School Experimental Plant Sciences, Section Phytopathology, Utrecht University, P.O. Box 800.84, 3508, TB Utrecht, The Netherlands

    Karen M. Léon-Kloosterziel, Bas W. M. Verhagen, Joost J. B. Keurentjes, Johan A. Van Pelt, L. C. Van Loon & Corné M.J. Pieterse

  2. Faculty of Science, Plant Pathology, Swammerdam Institute for Life Sciences, University of Amsterdam, P.O. Box 94062, 1090, GB Amsterdam, The Netherlands

    Martijn Rep

  3. Department of Cell Biology and Immunology, Wageningen University, P.O. Box 338, 6700, AH Wageningen, the Netherlands

    Karen M. Léon-Kloosterziel

  4. Laboratoire d’Eco-Toxicologie, UFR Science Exactes et Naturelles, Université de Reims, Moulin de la Housse, BP1039 – 51687, Reims, France

    Bas W. M. Verhagen

  5. Laboratory of Genetics, Wageningen University, Arboretumlaan 4, 6703 BD, Wageningen, the Netherlands

    Joost J. B. Keurentjes

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  1. Karen M. Léon-Kloosterziel
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  2. Bas W. M. Verhagen
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  3. Joost J. B. Keurentjes
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  4. Johan A. Van Pelt
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  5. Martijn Rep
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  6. L. C. Van Loon
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  7. Corné M.J. Pieterse
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Correspondence to Corné M.J. Pieterse.

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Léon-Kloosterziel, K.M., Verhagen, B.W.M., Keurentjes, J.J.B. et al. Colonization of the Arabidopsis rhizosphere by fluorescent Pseudomonas spp. activates a root-specific, ethylene-responsive PR-5 gene in the vascular bundle. Plant Mol Biol 57, 731–748 (2005). https://doi.org/10.1007/s11103-005-3097-y

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  • DOI: https://doi.org/10.1007/s11103-005-3097-y

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