Chromatin states coordinate diurnal gene expression in the Drosophila retina

Abstract

Daily biological rhythms enable organisms to anticipate and respond to predictable diurnal environmental changes. While the circadian clock maintains rhythms under constant conditions, it remains unclear what gates the time-of-day expression of genes that are rhythmic under light:dark cycles. In the retina, restricting biological processes to specific times of the day is crucial for homeostasis because disrupting these rhythms causes retinal degeneration. We show that in light-sensitive photoreceptor neurons of Drosophila, the circadian transcription factors only account for the timing of a minority of rhythmic genes. Instead, integrative analysis of the daily chromatin landscape and transcription factor footprints reveals that promoter, enhancer, or repressive signatures strongly correspond with phase. Further, genetic modulation of the repressive and promoter chromatin states altered gene expression in a phase-specific manner. Together, our data support a model where the genome is organized into discrete chromatin signatures that collaborate with transcription factors to restrict diurnal transcription to distinct phases of the day.