Clock-dependent chromatin accessibility rhythms regulate circadian transcription

Aug 30, 2023bioRxiv : the preprint server for biology

Daily biological clock rhythms control how DNA is accessed for gene activity

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Abstract

Chromatin accessibility exhibits significant circadian oscillations at promoter and enhancer regions of hundreds of genes.

Chromatin accessibility peaks at either dusk or dawn, correlating with the peak activity of specific genes.
Genes with increased accessibility at dusk are associated with E-box motifs, linked to the PER/CLK feedback loop.
Genes more accessible at dawn are enriched with VRI/PDP1-box motifs, suggesting regulation by the VRI/PDP1 feedback loop.
In null mutants, chromatin accessibility rhythms are completely lost, indicating the essential role of Period protein in chromatin compaction.
Variations in chromatin accessibility may influence circadian gene expression patterns in clock neurons.

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Chromatin organization plays a crucial role in gene regulation by controlling the accessibility of DNA to transcription machinery. While significant progress has been made in understanding the regulatory role of clock proteins in circadian rhythms, how chromatin organization affects circadian rhythms remains poorly understood. Here, we employed ATAC-seq (Assay for Transposase-Accessible Chromatin with Sequencing) on FAC-sorted Drosophila clock neurons to assess genome-wide chromatin accessibility over the circadian cycle. We observed significant circadian oscillations in chromatin accessibility at promoter and enhancer regions of hundreds of genes, with enhanced accessibility either at dusk or dawn, which correlated with their peak transcriptional activity. Notably, genes with enhanced accessibility at dusk were enriched with E-box motifs, while those more accessible at dawn were enriched with VRI/PDP1-box motifs, indicating that they are regulated by the core circadian feedback loops, PER/CLK and VRI/PDP1, respectively. Further, we observed a complete loss of chromatin accessibility rhythms innull mutants, with chromatin consistently accessible throughout the circadian cycle, underscoring the critical role of Period protein in driving chromatin compaction during the repression phase. Together, this study demonstrates the significant role of chromatin organization in circadian regulation, revealing how the interplay between clock proteins and chromatin structure orchestrates the precise timing of biological processes throughout the day. This work further implies that variations in chromatin accessibility might play a central role in the generation of diverse circadian gene expression patterns in clock neurons. per1

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Clock-dependent chromatin accessibility rhythms regulate circadian transcription

Abstract

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