Phase separation of the redox sensor RCD1 mediates differential ROS signals to regulate plant growth and stress...

Reactive oxygen species (ROS) function as essential signaling molecules regulating diverse processes in plants. However, the mechanisms by which plants accurately perceive and distinguish between physiological and stress-induced ROS signals to coordinate growth and stress responses remain largely unclear. Here, we show that Radical-induced Cell Death1 (RCD1) functions as a redox sensor that undergoes a ROS-triggered phase separation transition. Three cysteine residues within RCD1 regulate the formation of phase-separated condensates, and the transition between condensate and non-condensate states determines the spatiotemporal interactions of RCD1 with the leaf morphogenesis-related transcription factor ASYMMETRIC LEAVES1 (AS1) or the stress-responsive zinc-finger transcription factor ZAT12. Through this mechanism, RCD1 phase separation differentiates growth- and stress-related ROS signals to orchestrate downstream gene regulation. The dynamic formation of transcriptional condensates and ROS-induced phase separation transition allow plants to rapidly distinguish and respond to developmental and environmental cues, potentially representing a conserved mechanism in eukaryotes.