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...
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eLife Sciences Publications Ltd
2025-05-01
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| Online Access: | https://elifesciences.org/articles/90309 |
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| author | Marie-Dominique Jolivet Anne Flore Deroubaix Marie Boudsocq Nikolaj B Abel Marion Rocher Terezinha Robbe Valérie Wattelet-Boyer Jennifer Huard Dorian Lefebvre Yi-Ju Lu Brad Day Grégoire Saias Jahed Ahmed Valérie Cotelle Nathalie Giovinazzo Jean-Luc Gallois Yasuyuki Yamaji Sylvie German-Retana Julien Gronnier Thomas Ott Sébastien Mongrand Véronique Germain |
| author_facet | Marie-Dominique Jolivet Anne Flore Deroubaix Marie Boudsocq Nikolaj B Abel Marion Rocher Terezinha Robbe Valérie Wattelet-Boyer Jennifer Huard Dorian Lefebvre Yi-Ju Lu Brad Day Grégoire Saias Jahed Ahmed Valérie Cotelle Nathalie Giovinazzo Jean-Luc Gallois Yasuyuki Yamaji Sylvie German-Retana Julien Gronnier Thomas Ott Sébastien Mongrand Véronique Germain |
| author_sort | Marie-Dominique Jolivet |
| collection | DOAJ |
| description | 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. |
| format | Article |
| id | doaj-art-64ac1fa838fa4e338f31d1abd0ac22f2 |
| institution | Kabale University |
| issn | 2050-084X |
| language | English |
| publishDate | 2025-05-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj-art-64ac1fa838fa4e338f31d1abd0ac22f22025-08-20T03:52:07ZengeLife Sciences Publications LtdeLife2050-084X2025-05-011210.7554/eLife.90309Interdependence of plasma membrane nanoscale dynamics of a kinase and its cognate substrate underlies Arabidopsis response to viral infectionMarie-Dominique Jolivet0Anne Flore Deroubaix1Marie Boudsocq2Nikolaj B Abel3Marion Rocher4Terezinha Robbe5Valérie Wattelet-Boyer6Jennifer Huard7Dorian Lefebvre8Yi-Ju Lu9Brad Day10Grégoire Saias11Jahed Ahmed12Valérie Cotelle13Nathalie Giovinazzo14Jean-Luc Gallois15Yasuyuki Yamaji16Sylvie German-Retana17Julien Gronnier18https://orcid.org/0000-0002-1429-0542Thomas Ott19https://orcid.org/0000-0002-4494-9811Sébastien Mongrand20https://orcid.org/0000-0002-9198-015XVéronique Germain21https://orcid.org/0000-0001-6322-1204Univ. Bordeaux, CNRS, Laboratoire de Biogenèse Membranaire (LBM), Villenave d'Ornon, FranceUniv. Bordeaux, CNRS, Laboratoire de Biogenèse Membranaire (LBM), Villenave d'Ornon, FranceUniversité Paris-Saclay, CNRS, INRAE, Univ Evry, Université Paris Cité, Institute of Plant Sciences Paris-Saclay (IPS2), Saclay, FranceFaculty of Biology, University of Freiburg, Freiburg, Germany; Faculty of Biology, University of Munich (LMU), Munich, GermanyUniv. Bordeaux, CNRS, Laboratoire de Biogenèse Membranaire (LBM), Villenave d'Ornon, FranceUniv. Bordeaux, CNRS, Laboratoire de Biogenèse Membranaire (LBM), Villenave d'Ornon, FranceUniv. Bordeaux, CNRS, Laboratoire de Biogenèse Membranaire (LBM), Villenave d'Ornon, FranceUniv. Bordeaux, CNRS, Laboratoire de Biogenèse Membranaire (LBM), Villenave d'Ornon, FranceUniversité Paris-Saclay, CNRS, INRAE, Univ Evry, Université Paris Cité, Institute of Plant Sciences Paris-Saclay (IPS2), Saclay, FranceDepartment of Plant, Soil and Microbial Sciences, Michigan State University, East Lansing, United StatesDepartment of Plant, Soil and Microbial Sciences, Michigan State University, East Lansing, United StatesUniv. Bordeaux, CNRS, Laboratoire de Biogenèse Membranaire (LBM), Villenave d'Ornon, FranceUniv. Bordeaux, CNRS, Laboratoire de Biogenèse Membranaire (LBM), Villenave d'Ornon, FranceLaboratoire de Recherche en Sciences Végétales (LRSV), Université de Toulouse, CNRS, UPS, Toulouse INP, Toulouse, FranceINRAE, GAFL, Montfavet, FranceINRAE, GAFL, Montfavet, FranceGraduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo, JapanUMR 1332 BFP, INRAE Univ. Bordeaux, Bordeaux, FranceUniv. Bordeaux, CNRS, Laboratoire de Biogenèse Membranaire (LBM), Villenave d'Ornon, France; Center of Plant Molecular Biology (ZMBP), University of Tübingen, Tübingen, GermanyFaculty of Biology, University of Freiburg, Freiburg, Germany; Faculty of Biology, University of Munich (LMU), Munich, Germany; CIBSS – Centre for Integrative Biological Signalling Studies, University of Freiburg, Freiburg, GermanyUniv. Bordeaux, CNRS, Laboratoire de Biogenèse Membranaire (LBM), Villenave d'Ornon, FranceUniv. Bordeaux, CNRS, Laboratoire de Biogenèse Membranaire (LBM), Villenave d'Ornon, FrancePlant 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.https://elifesciences.org/articles/90309lipidmembraneskinasesnanodomainsvirusremorin |
| spellingShingle | Marie-Dominique Jolivet Anne Flore Deroubaix Marie Boudsocq Nikolaj B Abel Marion Rocher Terezinha Robbe Valérie Wattelet-Boyer Jennifer Huard Dorian Lefebvre Yi-Ju Lu Brad Day Grégoire Saias Jahed Ahmed Valérie Cotelle Nathalie Giovinazzo Jean-Luc Gallois Yasuyuki Yamaji Sylvie German-Retana Julien Gronnier Thomas Ott Sébastien Mongrand Véronique Germain Interdependence of plasma membrane nanoscale dynamics of a kinase and its cognate substrate underlies Arabidopsis response to viral infection eLife lipid membranes kinases nanodomains virus remorin |
| title | Interdependence of plasma membrane nanoscale dynamics of a kinase and its cognate substrate underlies Arabidopsis response to viral infection |
| title_full | Interdependence of plasma membrane nanoscale dynamics of a kinase and its cognate substrate underlies Arabidopsis response to viral infection |
| title_fullStr | Interdependence of plasma membrane nanoscale dynamics of a kinase and its cognate substrate underlies Arabidopsis response to viral infection |
| title_full_unstemmed | Interdependence of plasma membrane nanoscale dynamics of a kinase and its cognate substrate underlies Arabidopsis response to viral infection |
| title_short | Interdependence of plasma membrane nanoscale dynamics of a kinase and its cognate substrate underlies Arabidopsis response to viral infection |
| title_sort | interdependence of plasma membrane nanoscale dynamics of a kinase and its cognate substrate underlies arabidopsis response to viral infection |
| topic | lipid membranes kinases nanodomains virus remorin |
| url | https://elifesciences.org/articles/90309 |
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