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.
Highlights
Temperature is one of the most influential environmental factors affecting all terrestrial life forms
We show that the HECATE and the PHYTOCHROME INTERACTING FACTORs (PIFs) family of basic helix loop helix proteins antagonistically regulate thermomorphogenesis
In our recent RNA-seq analysis of thermo-regulated gene expression [28], we found that HECATE 1 and 2 are both induced after high ambient temperature exposure (S1 Fig)
Summary
Temperature is one of the most influential environmental factors affecting all terrestrial life forms. High ambient temperature-mediated regulation of plant development is termed thermomorphogenesis, which is characterized by elongated hypocotyl, petiole and root, hyponastic growth, and early flowering [4,5]. These morphological changes help plants adapt to a new climate and complete reproduction. In the model plant Arabidopsis thaliana, the red-light photoreceptor phytochrome B (phyB) senses temperature by a process called thermal relaxation, where the active Pfr form of phyB is converted back to the inactive Pr form by high ambient temperature [8,9]. A prion-like domain in EARLY FLOWERING 3 (ELF3) is necessary for the conversion of the soluble active form to an inactive phase-separated form of ELF3 at high ambient temperature [10]. Similar to the bacterial RNA thermometer, an RNA thermoswitch within the 5’-untranslated region of PHYTOCHROME INTERCTING FACTOR 7 (PIF7) acts as a temperature sensor to regulate the translational efficiency of PIF7 mRNA [11]
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