ROS burst prolongs transcriptional condensation to slow shoot apical meristem maturation and achieve heat-stress resilience in tomato

The transition of the shoot apical meristem (SAM) from vegetative growth to flowering, a key step of angiosperm reproductive success, is highly vulnerable to heat stress. Overproduction of reactive oxygen species (ROS) is a hallmark of such environmental stresses, but how SAM exploits the extra ROS to achieve heat-stress resilience is largely unknown. Here, we report that tomato plants respond to heat-induced ROS burst by slowing down SAM maturation and lengthening the vegetative state to achieve heat resilience. Heat-induced extra ROS prolonged the transcriptional condensation status of TERMINATING FLOWER (TMF), a prion-like transcription repressor that undergoes phase separation by sensing hydrogen peroxide (H2O2), therefore temporarily delaying activation of flowering transition and extending vegetative growth. Loss-of-function of TMF, or base editing of a single cysteine residue that senses H2O2, abolishes heat resilience. Our findings demonstrate that transcriptional reprogramming triggered by ROS might be a molecular basis of plant developmental plasticity underlying heat-stress resilience.