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 (H2O2), act as key signaling molecules in response to environmental stimuli such as osmotic stress. However, how extracellular H2O2
affects intracellular signaling has remained unknown. Here, we show
that osmotic stimulation induces the formation of localized, H2O2-rich nanoenvironments at the cytoplasmic face of the plasma membrane (PM) in Arabidopsis root cells. Using a PM-tethered H2O2
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 H2O2
transport via the PLASMA MEMBRANE INTRINSIC PROTEIN2;7 (PIP2;7). These
local redox hotspots at the PM create a feedforward loop in which H2O2 enhances ROP6 nanoclustering, thereby amplifying ROS signaling. Disruption of H2O2
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.
FörderungenDAAD, Germany European Molecular Biology Organization (EMBO) EC | European Research Council (ERC) Agence Nationale de la Recherche (ANR) Marie Curie Sklodowska Action Deutsche Forschungsgemeinschaft (DFG)