BBX24 and BBX25 antagonize the function of thermosensor ELF3 to promote PIF4-mediated thermomorphogenesis in...

Temperature is a crucial environmental cue that governs plant growth and adaptation in natural habitats. PHYTOCHROME INTERACTING FACTOR 4 (PIF4) functions as a central regulator promoting thermomorphogenesis in Arabidopsis. An understanding of its precise regulation is essential for optimal thermomorphogenic growth. Here, we identified two BBX proteins, BBX24 and BBX25, as novel components of the PIF4-mediated thermosensory pathway that promote growth at elevated temperatures. Single and double mutants of bbx24 and bbx25 exhibit moderate to strong temperature-insensitive hypocotyl and cotyledon growth. Elevated temperatures induce BBX24 and BBX25 mRNA expression and protein accumulation. Genetic and biochemical analyses reveal that BBX24 and BBX25 enhance PIF4-mediated thermosensory growth by counteracting ELF3, a key component of the evening complex. Whereas ELF3 represses BBX24 and BBX25 gene expression at low ambient temperatures during the evening, the inhibition of ELF3 activity under elevated temperatures increases BBX24 and BBX25 activity. Moreover, BBX24 and BBX25 suppress ELF3 function through direct physical interaction, likely relieving its repression of PIF4 and enhancing thermomorphogenesis. These findings identify the ELF3-BBX24/BBX25-PIF4 axis as a key regulatory module controlling plant growth and development in response to temperature cues.