The ELF3-BBX24/BBX25-PIF4 module controls thermosensory growth in Arabidopsis

Temperature serves as a crucial environmental cue governing the growth and adaptation of plants in their natural habitat. PHYTOCHROME INTERACTING FACTOR 4 (PIF4) is a central regulator that promotes thermomorphogenesis in Arabidopsis. Understanding its precise regulation is critical for optimal thermomorphogenic growth. Here, we identified two BBX proteins, BBX24 and BBX25, as novel components of the PIF4-mediated thermosensory pathway and act to promote warm temperature-mediated growth. The bbx24 and bbx25 single and double mutants showed moderate to strong temperature-insensitive hypocotyl and cotyledon growth. Warm temperature induces BBX24 and BBX25 mRNA expression and protein accumulation. Genetic and biochemical analysis revealed that BBX24/BBX25 promotes PIF4-mediated thermosensory growth by counteracting a key component of the evening complex, ELF3. While ELF3 inhibits BBX24/BBX25 gene expression at low ambient temperatures in the evening, warm temperature-mediated inhibition of ELF3 activity results in enhanced BBX24/BBX25 activity. Moreover, BBX24/25 inhibit ELF3 function through direct physical interaction and likely relieves repression on PIF4, enhancing its activity and thermomorphogenesis. Together, this study unravels ELF3-BBX24/BBX25-PIF4 as a key regulatory module that controls growth and development under varying temperature cues.