Separation of early and late responses to herbivory in Arabidopsis by changing plasmodesmal function

Authors

  • Irene Bricchi,

    1. Plant Physiology Unit, Department of Life Sciences and Systems Biology, University of Turin, Innovation Centre, Via Quarello 11/A, 10135 Turin, Italy
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    • These two authors contributed equally to the work.

  • Andrea Occhipinti,

    1. Plant Physiology Unit, Department of Life Sciences and Systems Biology, University of Turin, Innovation Centre, Via Quarello 11/A, 10135 Turin, Italy
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    • These two authors contributed equally to the work.

  • Cinzia M. Bertea,

    1. Plant Physiology Unit, Department of Life Sciences and Systems Biology, University of Turin, Innovation Centre, Via Quarello 11/A, 10135 Turin, Italy
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  • Simon A. Zebelo,

    1. Plant Physiology Unit, Department of Life Sciences and Systems Biology, University of Turin, Innovation Centre, Via Quarello 11/A, 10135 Turin, Italy
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  • Carla Brillada,

    1. Plant Physiology Unit, Department of Life Sciences and Systems Biology, University of Turin, Innovation Centre, Via Quarello 11/A, 10135 Turin, Italy
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  • Francesca Verrillo,

    1. Plant Physiology Unit, Department of Life Sciences and Systems Biology, University of Turin, Innovation Centre, Via Quarello 11/A, 10135 Turin, Italy
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  • Cristina De Castro,

    1. Department of Organic Chemistry and Biochemistry, University of Naples Federico II, 80126 Naples, Italy
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  • Antonio Molinaro,

    1. Department of Organic Chemistry and Biochemistry, University of Naples Federico II, 80126 Naples, Italy
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  • Christine Faulkner,

    1. John Innes Centre, Norwich Research Park, Colney, Norwich NR4 7UH, UK
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  • Andrew J. Maule,

    1. John Innes Centre, Norwich Research Park, Colney, Norwich NR4 7UH, UK
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  • Massimo E. Maffei

    Corresponding author
    1. Plant Physiology Unit, Department of Life Sciences and Systems Biology, University of Turin, Innovation Centre, Via Quarello 11/A, 10135 Turin, Italy
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(e-mail massimo.maffei@unito.it).

Summary

Herbivory results in an array of physiological changes in the host that are separable from the associated physical damage. We have made the surprising observation that an Arabidopsis line (pdko3) mutated in genes encoding plasmodesmal proteins is defective in some, but not all, of the typical plant responses to herbivory. We tested the responses of plasma transmembrane potential (Vm) depolarization, voltage gated K+ channel activity, cytosolic calcium [Ca2+]cyt and reactive oxygen species (ROS) (H2O2 and NO) release, shoot-to-root signaling, biosynthesis of the phytohormone jasmonic acid (JA) and the elicitation of volatile organic compounds (VOCs). Following herbivory and the release of factors present in insect oral secretions (including a putative β-galactofuranose polysaccharide), both the pdko3 and wild type (WT) plants showed a increased accumulation of [Ca2+]cyt, NO and H2O2. In contrast, unlike WT plants, the mutant line showed an almost complete loss of voltage gated K+ channel activity and Vm depolarization, a loss of shoot-induced root-Vm depolarization, a loss of activation and regulation of gene expression of the JA defense pathway, and a much diminished release and altered profile of VOCs. The mutations in genes for plasmodesmal proteins have provided valuable genetic tools for the dissection of the complex spectrum of responses to herbivory and shown us that the responses to herbivory can be separated into a calcium-activated oxidative response and a K+-dependent Vm-activated jasmonate response associated with the release of VOCs.

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