The B-BOX protein BBX21 suppresses thermosensory growth under short- and long-day photoperiods by distinct mechanisms

Thermomorphogenesis is a plant adaptive response, enabling morphological adjustments to fluctuating ambient temperatures. In Arabidopsis, the bHLH family of transcription factor PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) plays a central role in promoting thermomorphogenesis, whose activity is negatively regulated by thermosensors EARLY FLOWERING 3 (ELF3) and PHYTOCHROME B (phyB). In response to warm temperatures, PIF4 transcript and protein levels increase to facilitate thermosensory growth. However, the regulatory mechanisms governing PIF4-mediated thermosensory growth remain partially elusive. Here, we demonstrate the role of a B-BOX protein, BBX21, in suppressing thermomorphogenesis through the PIF4 pathway. A mutation in BBX21 (bbx21) results in a longer hypocotyl phenotype accompanied by upregulation in thermoresponsive gene expression, whereas overexpression of BBX21 (BBX21-OE) results in an extremely short hypocotyl phenotype with dampened expression of temperature-responsive genes. Genetic analysis reveals that BBX21 acts upstream of PIF4 to regulate warm temperature-mediated hypocotyl growth. To limit excessive thermomorphogenesis, BBX21 inhibits PIF4 protein accumulation by repressing its transcript accumulation by directly binding to its promoter. Furthermore, our genetic and biochemical data show that the short hypocotyl phenotype of the BBX21-OE line is dependent on ELF3 and phyB. BBX21 enhances the ELF3 and phyB-mediated inhibition of PIF4 activity in SD and LD conditions, respectively, by enhancing their protein activity. Thus, this study elucidates the novel role of BBX21 in suppressing thermomorphogenesis, providing new insights into the molecular mechanism of PIF4-mediated regulation of hypocotyl growth in response to warm temperatures.