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Vitis vinifera VvNPR1.1 is the functional ortholog of AtNPR1 and its overexpression in grapevine triggers constitutive activation of PR genes and enhanced resistance to powdery mildew

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Abstract

Studying grapevine (Vitis vinifera) innate defense mechanisms is a prerequisite to the development of new protection strategies, based on the stimulation of plant signaling pathways to trigger pathogen resistance. Two transcriptional coactivators (VvNPR1.1 and VvNPR1.2) with similarity to Arabidopsis thaliana NPR1 (Non-Expressor of PR genes 1), a well-characterized and key signaling element of the salicylic acid (SA) pathway, were recently isolated in Vitis vinifera. In this study, functional characterization of VvNPR1.1 and VvNPR1.2, including complementation of the Arabidopsis npr1 mutant, revealed that VvNPR1.1 is a functional ortholog of AtNPR1, whereas VvNPR1.2 likely has a different function. Ectopic overexpression of VvNPR1.1 in the Arabidopsis npr1-2 mutant restored plant growth at a high SA concentration, Pathogenesis Related 1 (PR1) gene expression after treatment with SA or bacterial inoculation, and resistance to virulent Pseudomonas syringae pv. maculicola bacteria. Moreover, stable overexpression of VvNPR1.1-GFP in V. vinifera resulted in constitutive nuclear localization of the fusion protein and enhanced PR gene expression in uninfected plants. Furthermore, grapevine plants overexpressing VvNPR1.1-GFP exhibited an enhanced resistance to powdery mildew infection. This work highlights the importance of the conserved SA/NPR1 signaling pathway for resistance to biotrophic pathogens in V. vinifera.

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Abbreviations

BTH:

Benzothiadiazole

EDS1:

Enhanced disease susceptibility

ET:

Ethylene

INA:

2.6-dichloroisonicotinic acid

JA:

Jasmonic acid

MeJA:

Methyljasmonate

NPR1:

Non-expressor of PR genes 1

PR:

Pathogenesis related

SA:

Salicylic acid

SAR:

Systemic acquired resistance

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Acknowledgments

We are grateful to J. Mutterer (IBMP-CNRS, Strasbourg, France) for help with confocal microscopy observations, to J. Glazebrook (University of Minnesota, St Paul, USA) for npr1-2 mutant seeds and to J. Dewdney and S. Gopalan (Massachusets General Hospital, Boston, USA) for the PsmES4326 strain. Special thanks to R. Wagner, S. Staerck, M. Kerneis and P. Geoffroy (IBMP-CNRS, Strasbourg, France) for taking care of Arabidopsis plants. This work was supported by the Université de Haute Alsace and by a doctoral fellowship from the French Ministry of Research to G. Le Henanff.

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  1. Anne-Sophie Miclot

    Present address: UMR Génétique et Horticulture (GenHort), IFR149 QUASAV, Centre INRA Angers-Nantes, BP 60057, 49071, Beaucouzé, France

Authors and Affiliations

  1. Université de Haute Alsace, Laboratoire Vigne, Biotechnologies et Environnement (EA3991), 33 rue de Herrlisheim, 68000, Colmar, France

    Gaëlle Le Henanff, Sibylle Farine, Flore Kieffer-Mazet, Christophe Bertsch & Julie Chong

  2. INRA, UMR1131 Santé de la Vigne et Qualité du Vin, 68000, Colmar, France

    Anne-Sophie Miclot & Pere Mestre

  3. Université de Strasbourg, UMR 1131 Santé de la Vigne et Qualité du Vin, 68000, Colmar, France

    Anne-Sophie Miclot & Pere Mestre

  4. IBMP du CNRS (UPR2357), Département Réseaux Métaboliques chez les Végétaux, 12 rue du général Zimmer, 67000, Strasbourg, France

    Thierry Heitz

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  1. Gaëlle Le Henanff
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Le Henanff, G., Farine, S., Kieffer-Mazet, F. et al. Vitis vinifera VvNPR1.1 is the functional ortholog of AtNPR1 and its overexpression in grapevine triggers constitutive activation of PR genes and enhanced resistance to powdery mildew. Planta 234, 405–417 (2011). https://doi.org/10.1007/s00425-011-1412-1

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