Arabidopsis wat1 (walls are thin1)-mediated resistance to the bacterial vascular pathogen, Ralstonia solanacearum, is accompanied by cross-regulation of salicylic acid and tryptophan metabolism

Authors

  • Nicolas Denancé,

    1. Université de Toulouse, UPS, Unité Mixte de Recherche 5546, Laboratoire de Recherche en Sciences Végétales, Castanet-Tolosan, France
    2. Centre National de la Recherche Scientifique, CNRS, Unité Mixte de Recherche 5546, Laboratoire de Recherche en Sciences Végétales, Castanet-Tolosan, France
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    • These authors contributed equally to this work.
  • Philippe Ranocha,

    1. Université de Toulouse, UPS, Unité Mixte de Recherche 5546, Laboratoire de Recherche en Sciences Végétales, Castanet-Tolosan, France
    2. Centre National de la Recherche Scientifique, CNRS, Unité Mixte de Recherche 5546, Laboratoire de Recherche en Sciences Végétales, Castanet-Tolosan, France
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    • These authors contributed equally to this work.
  • Nicolas Oria,

    1. Institut National de la Recherche Agronomique, INRA, AgroParisTech, Unité Mixte de Recherche 1318, Institut Jean-Pierre Bourgin, Centre de Versailles-Grignon, Versailles, France
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  • Xavier Barlet,

    1. Institut National de la Recherche Agronomique, INRA, Unité Mixte de Recherche 441, Laboratoire des Interactions Plantes Microorganismes, Castanet-Tolosan, France
    2. Centre National de la Recherche Scientifique, CNRS, Unité Mixte de Recherche 2594, Laboratoire des Interactions Plantes Microorganismes, Castanet-Tolosan, France
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  • Marie-Pierre Rivière,

    1. Centro de Biotecnología y Genómica de Plantas, Universidad Politécnica de Madrid, Pozuelo de Alarcón, Spain
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  • Koste A. Yadeta,

    1. Laboratory of Phytopathology, Wageningen University, PB Wageningen, The Netherlands
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  • Laurent Hoffmann,

    1. Université de Toulouse, UPS, Unité Mixte de Recherche 5546, Laboratoire de Recherche en Sciences Végétales, Castanet-Tolosan, France
    2. Centre National de la Recherche Scientifique, CNRS, Unité Mixte de Recherche 5546, Laboratoire de Recherche en Sciences Végétales, Castanet-Tolosan, France
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  • François Perreau,

    1. Institut National de la Recherche Agronomique, INRA, AgroParisTech, Unité Mixte de Recherche 1318, Institut Jean-Pierre Bourgin, Centre de Versailles-Grignon, Versailles, France
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  • Gilles Clément,

    1. Institut National de la Recherche Agronomique, INRA, AgroParisTech, Unité Mixte de Recherche 1318, Institut Jean-Pierre Bourgin, Centre de Versailles-Grignon, Versailles, France
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  • Alessandra Maia-Grondard,

    1. Institut National de la Recherche Agronomique, INRA, AgroParisTech, Unité Mixte de Recherche 1318, Institut Jean-Pierre Bourgin, Centre de Versailles-Grignon, Versailles, France
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  • Grardy C.M. van den Berg,

    1. Laboratory of Phytopathology, Wageningen University, PB Wageningen, The Netherlands
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  • Bruno Savelli,

    1. Université de Toulouse, UPS, Unité Mixte de Recherche 5546, Laboratoire de Recherche en Sciences Végétales, Castanet-Tolosan, France
    2. Centre National de la Recherche Scientifique, CNRS, Unité Mixte de Recherche 5546, Laboratoire de Recherche en Sciences Végétales, Castanet-Tolosan, France
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  • Sylvie Fournier,

    1. Université de Toulouse, UPS, Unité Mixte de Recherche 5546, Laboratoire de Recherche en Sciences Végétales, Castanet-Tolosan, France
    2. Centre National de la Recherche Scientifique, CNRS, Unité Mixte de Recherche 5546, Laboratoire de Recherche en Sciences Végétales, Castanet-Tolosan, France
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  • Yann Aubert,

    1. Université de Toulouse, UPS, Unité Mixte de Recherche 5546, Laboratoire de Recherche en Sciences Végétales, Castanet-Tolosan, France
    2. Centre National de la Recherche Scientifique, CNRS, Unité Mixte de Recherche 5546, Laboratoire de Recherche en Sciences Végétales, Castanet-Tolosan, France
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  • Sandra Pelletier,

    1. Unité de Recherche en Génomique Végétale, Institut National de la Recherche Agronomique (INRA)/ Centre National de la Recherche Scientifique (CNRS), Evry, France
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  • Bart P.H.J. Thomma,

    1. Laboratory of Phytopathology, Wageningen University, PB Wageningen, The Netherlands
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  • Antonio Molina,

    1. Centro de Biotecnología y Genómica de Plantas, Universidad Politécnica de Madrid, Pozuelo de Alarcón, Spain
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  • Lise Jouanin,

    1. Institut National de la Recherche Agronomique, INRA, AgroParisTech, Unité Mixte de Recherche 1318, Institut Jean-Pierre Bourgin, Centre de Versailles-Grignon, Versailles, France
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  • Yves Marco,

    1. Institut National de la Recherche Agronomique, INRA, Unité Mixte de Recherche 441, Laboratoire des Interactions Plantes Microorganismes, Castanet-Tolosan, France
    2. Centre National de la Recherche Scientifique, CNRS, Unité Mixte de Recherche 2594, Laboratoire des Interactions Plantes Microorganismes, Castanet-Tolosan, France
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  • Deborah Goffner

    Corresponding author
    1. Centre National de la Recherche Scientifique, CNRS, Unité Mixte de Recherche 5546, Laboratoire de Recherche en Sciences Végétales, Castanet-Tolosan, France
    • Université de Toulouse, UPS, Unité Mixte de Recherche 5546, Laboratoire de Recherche en Sciences Végétales, Castanet-Tolosan, France
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For correspondence (email goffner@lrsv.ups-tlse.fr).

Summary

Inactivation of Arabidopsis WAT1 (Walls Are Thin1), a gene required for secondary cell-wall deposition, conferred broad-spectrum resistance to vascular pathogens, including the bacteria Ralstonia solanacearum and Xanthomonas campestris pv. campestris, and the fungi Verticillium dahliae and Verticillium albo-atrum. Introduction of NahG, the bacterial salicylic acid (SA)-degrading salicylate hydroxylase gene, into the wat1 mutant restored full susceptibility to both R. solanacearum and X. campestris pv. campestris. Moreover, SA content was constitutively higher in wat1 roots, further supporting a role for SA in wat1-mediated resistance to vascular pathogens. By combining transcriptomic and metabolomic data, we demonstrated a general repression of indole metabolism in wat1-1 roots as shown by constitutive down-regulation of several genes encoding proteins of the indole glucosinolate biosynthetic pathway and reduced amounts of tryptophan (Trp), indole-3-acetic acid and neoglucobrassicin, the major form of indole glucosinolate in roots. Furthermore, the susceptibility of the wat1 mutant to R. solanacearum was partially restored when crossed with either the trp5 mutant, an over-accumulator of Trp, or Pro35S:AFB1-myc, in which indole-3-acetic acid signaling is constitutively activated. Our original hypothesis placed cell-wall modifications at the heart of the wat1 resistance phenotype. However, the results presented here suggest a mechanism involving root-localized metabolic channeling away from indole metabolites to SA as a central feature of wat1 resistance to R. solanacearum.

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