Clock-dependent chromatin accessibility rhythms regulate circadian transcription

May 28, 2024PLoS genetics

Daily biological clock rhythms control how DNA is accessed to regulate daily gene activity

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Abstract

Chromatin accessibility oscillates significantly at promoter and enhancer regions of hundreds of genes during the circadian cycle.

At dawn and dusk, chromatin accessibility at specific gene regions correlates with peak transcriptional activity.
Genes with higher accessibility at dusk are enriched with E-box motifs, while those at dawn are enriched with VRI/PDP1-box motifs.
A complete loss of chromatin accessibility rhythms occurs in per01 null mutants, indicating the role of the Period protein in chromatin compaction.
The findings suggest that chromatin organization is crucial for the regulation of circadian rhythms in clock neurons.
Variations in chromatin accessibility may contribute to the diverse patterns of circadian gene expression observed.

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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 at dawn and dusk over the circadian cycle. We observed significant 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 in per01 null mutants, with chromatin consistently accessible at both dawn and dusk, underscoring the critical role of Period protein in driving chromatin compaction during the repression phase at dawn. 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.

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Clock-dependent chromatin accessibility rhythms regulate circadian transcription

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