The ELF4–ELF3–LUX complex links the circadian clock to diurnal control of hypocotyl growth

Abstract

In plants, the circadian clock functions as an endogenous pacemaker that anticipates and responds to a changing environment in order to optimize the timing of physiological and developmental events. Nusinow et al. elucidate the mechanism by which the circadian clock controls growth of the model plant Arabidopsis thaliana. A novel trimeric complex called the evening complex is regulated by the clock and has a peak of expression at dusk. The complex represses the expression of two transcription factors, PIF4 and PIF5, which are part of a light-signalling cascade that controls the timing of plant growth in response to light conditions. The circadian clock is required for adaptive responses to daily and seasonal changes in environmental conditions1,2,3. Light and the circadian clock interact to consolidate the phase of hypocotyl cell elongation to peak at dawn under diurnal cycles in Arabidopsis thaliana4,5,6,7. Here we identify a protein complex (called the evening complex)—composed of the proteins encoded by EARLY FLOWERING 3 (ELF3), ELF4 and the transcription-factor-encoding gene LUX ARRHYTHMO (LUX; also known as PHYTOCLOCK 1)—that directly regulates plant growth8,9,10,11,12. ELF3 is both necessary and sufficient to form a complex between ELF4 and LUX, and the complex is diurnally regulated, peaking at dusk. ELF3, ELF4 and LUX are required for the proper expression of the growth-promoting transcription factors encoded by PHYTOCHROME INTERACTING FACTOR 4 (PIF4) and PIF5 (also known as PHYTOCHROME INTERACTING FACTOR 3-LIKE 6) under diurnal conditions4,6,13. LUX targets the complex to the promoters of PIF4 and PIF5 in vivo. Mutations in PIF4 and/or PIF5 are epistatic to the loss of the ELF4–ELF3–LUX complex, suggesting that regulation of PIF4 and PIF5 is a crucial function of the complex. Therefore, the evening complex underlies the molecular basis for circadian gating of hypocotyl growth in the early evening.