Interdependence of plasma membrane nanoscale dynamics of a kinase and its cognate substrate underlies Arabidopsis response to viral infection

Plant viruses represent a risk to agricultural production and as only a few treatments exist, it is urgent to identify resistance mechanisms and factors. In plant immunity, plasma membrane (PM)-localized proteins play an essential role in sensing the extracellular threat presented by bacteria, fungi, or herbivores. Viruses are intracellular pathogens and as such the role of the plant PM in detection and resistance against viruses is often overlooked. We investigated the role of the partially PM-bound Calcium-dependent protein kinase 3 (CPK3) in viral infection and we discovered that it displayed a specific ability to hamper viral propagation over CPK isoforms that are involved in immune response to extracellular pathogens. More and more evidence supports that the lateral organization of PM proteins and lipids underlies signal transduction in plants. We showed here that CPK3 diffusion in the PM is reduced upon activation as well as upon viral infection and that such immobilization depended on its substrate, Remorin (REM1.2), a scaffold protein. Furthermore, we discovered that the viral infection induced a CPK3-dependent increase of REM1.2 PM diffusion. Such interdependence was also observable regarding viral propagation. This study unveils a complex relationship between a kinase and its substrate that contrasts with the commonly described co-stabilisation upon activation while it proposes a PM-based mechanism involved in decreased sensitivity to viral infection in plants.

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Publication Details

Journal
eLife
Published
2025-04-03
DOI
https://doi.org/10.7554/elife.90309.3
Citations
1
Primary Topic
Plant Virus Research Studies
Type
article
Field-Weighted Citation Impact
1.75

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article

Interdependence of plasma membrane nanoscale dynamics of a kinase and its cognate substrate underlies Arabidopsis response to viral infection

Brad Day, Julien Gronnier, Sylvie German‐Retana, Véronique Germain et al.
1 citations
eLife
Plant Virus Research Studies
1.75
article

Interdependence of plasma membrane nanoscale dynamics of a kinase and its cognate substrate underlies Arabidopsis response to viral infection

Brad Day, Julien Gronnier, Sylvie German‐Retana, Véronique Germain, Marie-Dominique Jolivet, Jean‐Luc Gallois, Dorian Lefebvre, Anne-Flore Deroubaix, Marion Rocher, Thomas Ott, Valérie Wattelet‐Boyer, Jahed Ahmed, Valérie Cotelle, Yasuyuki Yamaji, Nathalie Giovinazzo, Marie Boudsocq, Sébastien Mongrand, Terezinha Robbe, Yi‐Ju Lu, Nikolaj B. Abel, Grégoire Saias, Jennifer Huard
article en
1 citations

Abstract

Plant viruses represent a risk to agricultural production and as only a few treatments exist, it is urgent to identify resistance mechanisms and factors. In plant immunity, plasma membrane (PM)-localized proteins play an essential role in sensing the extracellular threat presented by bacteria, fungi, or herbivores. Viruses are intracellular pathogens and as such the role of the plant PM in detection and resistance against viruses is often overlooked. We investigated the role of the partially PM-bound Calcium-dependent protein kinase 3 (CPK3) in viral infection and we discovered that it displayed a specific ability to hamper viral propagation over CPK isoforms that are involved in immune response to extracellular pathogens. More and more evidence supports that the lateral organization of PM proteins and lipids underlies signal transduction in plants. We showed here that CPK3 diffusion in the PM is reduced upon activation as well as upon viral infection and that such immobilization depended on its substrate, Remorin (REM1.2), a scaffold protein. Furthermore, we discovered that the viral infection induced a CPK3-dependent increase of REM1.2 PM diffusion. Such interdependence was also observable regarding viral propagation. This study unveils a complex relationship between a kinase and its substrate that contrasts with the commonly described co-stabilisation upon activation while it proposes a PM-based mechanism involved in decreased sensitivity to viral infection in plants.

eLifeVol. 12
Centre National de la Recherche Scientifique (FR), Université Toulouse III - Paul Sabatier (FR), Université de Bordeaux (FR), University of Freiburg (DE), Université Fédérale de Toulouse Midi-Pyrénées (FR), Université Paris Cité (FR), Université Paris-Saclay (FR), Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (FR), Biologie du Fruit et Pathologie (FR), Institute of Plant Molecular Biology (CZ), Laboratoire de Biogenèse Membranaire (FR), Génétique et amélioration des fruits et légumes (FR), Laboratoire de Recherche en Sciences Végétales (FR), The University of Tokyo (JP), University of Tübingen (DE), Ludwig-Maximilians-Universität München (DE), Michigan State University (US)
Deutsche Forschungsgemeinschaft, Agence Nationale de la Recherche
Openalex Percentile: Top 16%
Plant Virus Research Studies
1.75
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