SlWRKY2 orchestrates cold tolerance via phytochromes interaction and SlPIF4 stabilization in tomato

Plants orchestrate stress responses through the integration of light and temperature signals, yet the molecular mechanisms involved in this crosstalk are incompletely elucidated. Here, we identify the transcription factor SlWRKY2 as a critical hub linking phytochrome-mediated light perception with cold stress adaptation in tomato (Solanum lycopersicum). Under cold stress, low red/far-red light ratios significantly induce SlWRKY2 expression and protein accumulation, with phytochrome B (SlphyB) repressing and SlphyA promoting this process. Genetic analyses confirm that SlWRKY2 functions downstream of SlphyB and SlphyA, physically interacts with both SlphyB1 and SlphyA, and acts in a regulatory module where SlphyB negatively regulates cold tolerance while SlphyA exerts a positive effect. Moreover, both cold stress and light signals promote the formation of SlWRKY2 condensates consistent with liquid-liquid phase separation. Functionally, SlWRKY2 directly interacts with and stabilizes the light-signaling regulator PHYTOCHROME-INTERACTING TRANSCRIPTION 4 (SlPIF4). Furthermore, SlWRKY2 directly activates SlPIF4 transcription, and the 2 factors function synergistically to enhance the expression of SlCBFs, as evidenced by genetic data indicating that SlPIF4 is required for SlWRKY2-dependent cold tolerance. Mechanistically, SlWRKY2 competes with SlphyB1 for interaction with SlPIF4. Our findings reveal the SlphyB1/A-SlWRKY2-SlPIF4 signaling module as a pivotal mechanism underlying light quality-dependent cold adaptation, advancing our understanding of how plants integrate environmental cues to fine-tune cold adaptation.