Ambient temperature signal feeds into the circadian clock transcriptional circuitry through the EC night-time repressor in Arabidopsis thaliana

Abstract

An interlocking multiloop model has been generally accepted to describe the transcriptional circuitry of core clock genes, through which robust circadian rhythms are generated in Arabidopsis thaliana. The circadian clock must have the ability to integrate ambient temperature signals into the clock transcriptional circuitry to regulate clock function properly. Clarification of the underlying mechanism is a longstanding subject in the field. Here, we provide evidence that temperature signals feed into the clock transcriptional circuitry through the evening complex (EC) night-time repressor consisting of EARLY FLOWERING 3 (ELF3, ELF4) and LUX ARRHYTHMO (LUX; also known as PCL1). Chromatin immunoprecipitation assays showed that PSEUDO-RESPONSE REGULATOR7 (PRR7), GIGANTEA (GI) and LUX are direct targets of the night-time repressor. Consequently, transcription of PRR9/PRR7, GI and LUX is commonly regulated through the night-time repressor in response to both moderate changes in temperature (Δ6°C) and differences in the steady-state growth-compatible temperature (16-28°C). A warmer temperature inhibits EC function more, whereas a cooler temperature stimulates it more. Consequently, the expression of these target genes is up-regulated in response to a warm temperature specifically during the dark period, whereas they are reversibly down-regulated in response to a cool temperature. Transcription of another EC target, the PIF4 (PHYTOCHROME-INTERACTING FACTOR 4) gene, is modulated through the same thermoregulatory mechanism. The last finding revealed the sophisticated physiological mechanism underlying the clock-controlled output pathway, which leads to the PIF4-mediated temperature-adaptive regulation of hypocotyl elongation.

Keywords: Arabidopsis thaliana; Circadian clock; Hypocotyl elongation; Pseudo-response regulator; Response to temperature; Transcription circuitry.