Functional implication of the MYB transcription factor RVE8/LCL5 in the circadian control of histone acetylation

Abstract

Despite our increasing understanding of the molecular determinants essential for circadian clock function, we still lack a complete picture of the mechanisms contributing to clock progression in plants. Here, we explore the role of REVEILLE8/LHY-CCA1-LIKE5 (RVE8/LCL5) within the Arabidopsis circadian system. RVE8/LCL5 encodes a MYB-like transcription factor similar to CIRCADIAN CLOCK-ASSOCIATED1 (CCA1) and ELONGATED HYPOCOTYL (LHY), which are essential regulators of the Arabidopsis circadian clock. Consistent with the sequence similarity, the rhythmic expression of RVE8/LCL5 shows a morning acrophase comparable to that of CCA1 and LHY. Plants mis-expressing RVE8/LCL5 display a variety of circadian phenotypes, including altered circadian gene expression and photoperiodic flowering time. Similar to CCA1, RVE8/LCL5 regulates the expression of the oscillator gene TOC1 (TIMING OF CAB EXPRESSION1) by associating with the TOC1 promoter and by modulating the pattern of histone 3 (H3) acetylation. However, the mechanisms of RVE8/LCL5 and CCA1 activity in this regulation differ markedly. Indeed, the use of chromatin immunoprecipitation and pharmacological inhibition assays reveals that RVE8/LCL5 favours a hyper-acetylated state of H3 at the TOC1 promoter, which may facilitate the rising phase of TOC1. In contrast, CCA1 represses TOC1 expression by promoting histone deacetylation. Thus, despite the sequence homology and the similar morning phase of expression, RVE8/LCL5 and CCA1 have opposing regulatory functions within the Arabidopsis circadian clock, although CCA1 has a more predominant role. We propose that contrasting chromatin compaction and transcriptional modulation through the opposing activities of RVE8/LCL5 and CCA1 might provide a fine-tuning mechanism for precisely shaping the TOC1 circadian waveform in Arabidopsis.