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

Abstract

Temperature serves as a crucial environmental cue governing the growth and adaptation of plants in their natural habitat. The B-BOX proteins play a vital role in the light-mediated regulation of growth and development. However, their role in the thermosensory signaling pathway remains poorly understood. Here, we identified two B-BOX (BBX) proteins, BBX24 and BBX25, as novel components of the thermosensory pathway to promote warm temperature-mediated growth in Arabidopsis. The bbx24 and bbx25 single mutants showed moderate temperature insensitivity, while the bbx24bbx25 double mutants displayed strong temperature-insensitive hypocotyl and cotyledon growth. Warm temperatures induce BBX24 and BBX25 mRNA expression and protein accumulation. Genetic and biochemical analysis revealed that BBX24/BBX25 promotes thermomorphogenesis by stabilizing PHYTOCHROME INTERACTING FACTOR 4 (PIF4), a key component of the thermosensory pathway, probably through direct physical interaction. Interestingly, our study also revealed that the thermosensor EARLY FLOWERING 3 (ELF3), a potent inhibitor of PIF4 function, acts upstream of BBX24/BBX25, wherein ELF3 inhibits BBX24/BBX25 gene expression at low ambient temperatures in the evening. However, warm temperatures render ELF3 inactive, enhancing BBX24/BBX25 activity and stabilizing PIF4 protein and thermomorphogenic growth. Together, this study unravels ELF3/BBX24/BBX25-PIF4 as a key regulatory module that controls growth and development under varying temperature cues.