An autoregulatory negative feedback loop controls thermomorphogenesis in Arabidopsis

Abstract

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.

PIF7 controls leaf cell proliferation through an AN3 substitution repression mechanism

“…The PIF7 sequestration of AN3 potentially leads to the buildup of inactive heterodimers. Interestingly, a comparable regulatory mechanism has recently been described for HEC2 control of PIF4 in thermomorphogenesis ( 54 ). Here, HEC2 both stabilizes PIF4 and inhibits PIF4 function through heterodimerization.…”

Plant AFC2 kinase desensitizes thermomorphogenesis through modulation of alternative splicing

“…Therefore, plants already develop several brakes to restrict PIF4 activity. For example, transcription factors HECATEs (HEC1 and HEC2) directly interact with PIF4 and inhibit its transcriptional activity ( Lee et al., 2021 ). In this study, we revealed that alternative splicing was also an efficient way to attenuate PIF4-regulated thermomorphogenesis.…”

PIF4 and PIF4-Interacting Proteins: At the Nexus of Plant Light, Temperature and Hormone Signal Integrations

“…Recently, another elegant study showed that HEC1 and HEC2 inhibit thermomorphogenesis by forming a negative feedback loop with PIF4 [ 18 ]. hec1 hec2 double mutants exhibited much longer hypocotyls at 28 °C compared with Col-0 controls, while HEC2ox plants showed short hypocotyls.…”

“…hec1 hec2 double mutants exhibited much longer hypocotyls at 28 °C compared with Col-0 controls, while HEC2ox plants showed short hypocotyls. Furthermore, high temperature upregulated HEC2 expression levels and stabilized HEC2 protein levels [ 18 ]. Genetic analysis showed that PIFs are epistatic to HEC2 .…”

“…PIFs activate the expression of HECs at high temperature. HEC2 in turn interacts with PIF4 and forms a negative feedback loop ( Figure 5 B) [ 18 ].…”