The Evening Complex Establishes Repressive Chromatin Domains via H2A.Z-Nucleosome Deposition in Arabidopsis

The Evening Complex (EC) is a core component of the circadian clock, which represses target gene expression at the end of the day and integrates temperature information in order to coordinate environmental and endogenous signals. Despite its importance, the mechanism of EC function remains unknown. Here we show that the EC recruits repressive chromatin domains to regulate the evening transcriptome. The EC component EARLY FLOWERING 3 (ELF3) directly interacts with a protein from the Swi2/Snf2-Related 1 (SWR1) complex to control deposition of H2A.Z-nucleosomes at the EC target genes. The SWR1 components display a circadian oscillation in gene expression with a peak at dusk, suggesting that the circadian clock controls the expression and function of SWR1. In turn, SWR1 is required for the circadian clockwork as defects in SWR1 activity alters morning-expressed genes. The EC-SWR1 complex binds to the promoters of the core clock genes PSEUDORESPONSE REGULATOR 7 (PRR7) and PRR9 and catalyzes H2A.Z deposition coincident with their repression at dusk. This provides a mechanism by which the circadian clock temporally establishes repressive chromatin domains to shape oscillatory gene expression around dusk. HTA11 ChIP-seq and Mnase-seq were generated in Arabidopsis seedlings growing at 17 ºC