Nanoscale regulation of ROS signaling at the plasma membrane tunes the plant response to osmotic stress
Abstract
The spatiotemporal organization of proteins and lipids within membranes is crucial for ensuring proper cellular signaling. While the segregation of proteins and lipids into membrane nanodomains is well established, it remains unclear whether nanodomains can generate gradients of small diffusible molecules. In plants, reactive oxygen species (ROS), especially hydrogen peroxide (H 2 O 2 ), act as key signaling molecules in response to environmental stimuli such as osmotic stress. However, how extracellular H 2 O 2 affects intracellular signaling has remained unknown. Here, we show that osmotic stimulation induces the formation of localized, H 2 O 2 -rich nanoenvironments at the cytoplasmic face of the plasma membrane (PM) in Arabidopsis root cells. Using a PM-tethered H 2 O 2 biosensor, we found that these oxidized nanodomains arise from the clustering of RESPIRATORY BURST OXIDASE HOMOLOGs (RBOHs) and RHO OF PLANTS 6 (ROP6), in coordination with aquaporin-mediated H 2 O 2 transport via the PLASMA MEMBRANE INTRINSIC PROTEIN2;7 (PIP2;7). These local redox hotspots at the PM create a feedforward loop in which H 2 O 2 enhances ROP6 nanoclustering, thereby amplifying ROS signaling. Disruption of H 2 O 2 production or transport dampens both ROP6 clustering and anisotropic cell expansion, indicating a crucial role for spatially confined redox signaling in regulating plant growth under osmotic stress. Our findings propose a model in which ROP6/RBOHD-F/PIP2;7 nanodomains function as discrete redox signaling units, redefining ROS signaling at the PM as a structured, signal-specific, and compartmentalized process.
Article Details
Journal Info
Proceedings of the National Academy of Sciences
National Academy of Sciences
Authors (16)
Arthur Poitout
Institute for Plant Sciences of Montpellier, Univ Montpellier, CNRS, Institut national de recherche pour l‘agriculture, l‘alimentation et l‘environnement, Institut Agro
José M. Ugalde
Institut für Nutzpflanzenwissenschaften und Ressourcenschutz-Chemical Signalling, University of Bonn
Lucille Gorgues
Institute for Plant Sciences of Montpellier, Univ Montpellier, CNRS, Institut national de recherche pour l‘agriculture, l‘alimentation et l‘environnement, Institut Agro
Armelle Dongois
Institute for Plant Sciences of Montpellier, Univ Montpellier, CNRS, Institut national de recherche pour l‘agriculture, l‘alimentation et l‘environnement, Institut Agro
Patricia Scholz
Philippe Nacry
Institute for Plant Sciences of Montpellier, Univ Montpellier, CNRS, Institut national de recherche pour l‘agriculture, l‘alimentation et l‘environnement, Institut Agro
Carine Alcon
Institute for Plant Sciences of Montpellier, Univ Montpellier, CNRS, Institut national de recherche pour l‘agriculture, l‘alimentation et l‘environnement, Institut Agro
Jean-Bernard Fiche
Centre de Biochimie Structurale, CNRS Unité Mixte de Recherche 5048, Institut National de la Santé et de la Recherche Médicale U1054, Université de Montpellier
Xavier Dumont
Institute for Plant Sciences of Montpellier, Univ Montpellier, CNRS, Institut national de recherche pour l‘agriculture, l‘alimentation et l‘environnement, Institut Agro
Marcelo Nollman
Centre de Biochimie Structurale, CNRS Unité Mixte de Recherche 5048, Institut National de la Santé et de la Recherche Médicale U1054, Université de Montpellier
Komal Jhala
Department of Environmental Sciences, Institute of Biochemical Plant Pathology, Helmholtz Zentrum München
Anton R. Schäffner
Department of Environmental Sciences, Institute of Biochemical Plant Pathology, Helmholtz Zentrum München
Yvon Jaillais
Lionel Verdoucq
Institute for Plant Sciences of Montpellier, Univ Montpellier, CNRS, Institut national de recherche pour l‘agriculture, l‘alimentation et l‘environnement, Institut Agro
Andreas J. Meyer
Institut für Nutzpflanzenwissenschaften und Ressourcenschutz-Chemical Signalling, University of Bonn
Alexandre Martinière
Institute for Plant Sciences of Montpellier, Univ Montpellier, CNRS, Institut national de recherche pour l‘agriculture, l‘alimentation et l‘environnement, Institut Agro