Phase separation transitions of the redox sensor RCD1 mediate differential ROS signals to regulate plant growth and stress responses

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 demonstrate that Radical-induced Cell Death1 (RCD1) functions as a redox sensor that undergoes a ROS-triggered phase separation transition. Three cysteine residues within RCD1 contribute to the formation of phase-separated condensates, and the transition from condensate to non-condensate determines the spatiotemporal interactions of RCD1 with the leaf morphogenesis-related transcription factor ASYMMETRIC LEAVES1 (AS1) or the stress-responsive transcription factor zinc-finger protein ZAT12. Therefore, the phase separation transition of RCD1 differentiates between 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 growth and stress cues, potentially representing a conserved mechanism in eukaryotes.