CCA1 and ELF3 Interact in the Control of Hypocotyl Length and Flowering Time in Arabidopsis    

Abstract

The circadian clock is an endogenous oscillator with a period of approximately 24 h that allows organisms to anticipate, and respond to, changes in the environment. In Arabidopsis (Arabidopsis thaliana), the circadian clock regulates a wide variety of physiological processes, including hypocotyl elongation and flowering time. CIRCADIAN CLOCK ASSOCIATED1 (CCA1) is a central clock component, and CCA1 overexpression causes circadian dysfunction, elongated hypocotyls, and late flowering. EARLY FLOWERING3 (ELF3) modulates light input to the clock and is also postulated to be part of the clock mechanism. elf3 mutations cause light-dependent arrhythmicity, elongated hypocotyls, and early flowering. Although both genes affect similar processes, their relationship is not clear. Here, we show that CCA1 represses ELF3 by associating with its promoter, completing a CCA1-ELF3 negative feedback loop that places ELF3 within the oscillator. We also show that ELF3 acts downstream of CCA1, mediating the repression of PHYTOCHROME-INTERACTING FACTOR4 (PIF4) and PIF5 in the control of hypocotyl elongation. In the regulation of flowering, our findings show that ELF3 and CCA1 either cooperate or act in parallel through the CONSTANS/ FLOWERING LOCUS T pathway. In addition, we show that CCA1 represses GIGANTEA and SUPPRESSOR OF CONSTANS1 by direct interaction with their promoters, revealing additional connections between the circadian clock and the flowering pathways.

EARLY FLOWERING3 Redundancy Fine-Tunes Photoperiod Sensitivity

“…ELF3 is also reported to influence the daily transcriptional rhythm of CO in a similar manner, through protein-level regulation of the indirect CO activator GI (Yu et al, 2008). Regulation through GI could also potentially explain CO-independent effects of ELF3 (Lu et al, 2012). Whether similar mechanisms could also explain the early flowering of elf4 and lux mutants has not been addressed.…”

“…In turn, the expression of EC genes and formation of the EC itself are also tightly regulated by the circadian clock through multiple regulatory mechanisms (Herrero et al, 2012;Choudhary et al, 2015). The ELF3, ELF4, and LUX promoters are bound by the key clock protein CCA1, a morning phased myb transcription factor that acts together with its paralog LATE ELONGATED HYPOCOTYL (LHY) to repress evening-phased genes during the day (Lu et al, 2012;Adams et al, 2015;Nagel et al, 2015;Kamioka et al, 2016). Autoregulation of the EC may also be achieved through binding of the LUX protein to its own promoter .…”

Phosphorylation of Histone H2A at Serine 95: A Plant-Specific Mark Involved in Flowering Time Regulation and H2A.Z Deposition

“…A recent study showed that MLK4 copurified with components of the evening complex of the circadian clock in a phytochrome B-dependent manner (Huang et al, 2016), suggesting that MLK4 might phosphorylate the components of this complex, which may, in turn, regulate GI expression. CCA1 binds to GI and represses its expression (Lu et al, 2012). Although mutations in CCA1 resulted in slightly early flowering, the cca1 mLk4 double mutant exhibited late flowering, suggesting that the appropriate flowering time requires both CCA1 and MLK4.…”

PIFs: Systems Integrators in Plant Development

“…The expression of the EC is diurnally regulated and peaks at dusk. PIF4/5 expression in ELF3-deficient mutants is antiphasic, consistent with EC acting as repressor of PIF4/5 during the evening Lu et al, 2012). CCA1 also participates in the control of PIF4/5 expression under diurnal conditions based on the finding that plants overexpressing CCA1 have constitutively high levels of PIF4 and PIF5 transcript (Nozue et al, 2007), although this might be indirect given that CCA1 has been shown to directly bind and repress ELF3 expression (Lu et al, 2012).…”

“…In diurnal conditions, PIF4 and PIF5 transcript levels start to rise at midday through the night, with a peak at dawn (Nozue et al, 2007). The evening complex (EC) formed by ELF3, ELF4, and LUX is necessary for this expression pattern Herrero et al, 2012;Lu et al, 2012). LUX has been found to directly bind to PIF4/5 promoters through the LUX binding site (GATA/TCG) and recruit ELF3 and ELF4.…”