An autoregulatory negative feedback loop controls thermomorphogenesis in Arabidopsis

Plant growth and development are acutely sensitive to high ambient temperature caused in part due to climate change. However, the mechanism of high ambient temperature signaling is not well defined. Here, we show that HECATEs (HEC1 and HEC2), two helix-loop-helix transcription factors, inhibit thermomorphogenesis. While the expression of HEC1 and HEC2 is increased and HEC2 protein is stabilized at high ambient temperature, hec1hec2 double mutant showed exaggerated thermomorphogenesis. Analyses of the four PHYTOCHROME INTERACTING FACTOR (PIF1, PIF3, PIF4 and PIF5) mutants and overexpression lines showed that they all contribute to promote thermomorphogenesis. Furthermore, genetic analysis showed that pifQ is epistatic to hec1hec2. HECs and PIFs oppositely control the expression of many genes in response to high ambient temperature. PIFs activate the expression of HECs in response to high ambient temperature. HEC2 in turn interacts with PIF4 both in yeast and in vivo. In the absence of HECs, PIF4 binding to its own promoter as well as the target gene promoters was enhanced, indicating that HECs control PIF4 activity via heterodimerization. Overall, these data suggest that PIF4-HEC forms an autoregulatory composite negative feedback loop that controls growth genes to modulate thermomorphogenesis.Author summary: Global warming caused by climate change affects all terrestrial life forms including crop yield. Proper response to high ambient temperature is crucial for survival of plants. However, our understanding of how plants respond to high ambient temperature is still rudimentary. Here we show that the HECATE and the PHYTOCHROME INTERACTING FACTORs (PIFs) family of basic helix loop helix proteins antagonistically regulate thermomorphogenesis. PIFs transcriptionally activate the expression of HECs in response to high ambient temperature. HEC2 in turn physically heterodimerizes with PIF4 and inhibit its function. Because PIF4 controls its own expression, this PIF-HEC negative feedback loop fine tunes thermomorphogenesis in a temperature-dependent manner. Our data contribute to a deeper understanding of how plants respond to high ambient temperature and are expected to help develop next generation crops that are resilient to global warming.