Diurnal control of H3K27me1 deposition shapes expression of a subset of cell cycle and DNA damage response genes.

Abstract

Rhythmic oscillation of biological processes helps organisms adapt their physiological responses to the most appropriate time of the day. Chromatin remodeling has been described as one of the molecular mechanisms controlling these oscillations. The importance of these changes in transcriptional activation as well as in the maintenance of heterochromatic regions has been widely demonstrated. However, little is still known on how diurnal changes can impact the global status of chromatin modifications and, hence, control gene expression. In plants, the repressive mark H3K27me1, deposited by ARABIDOPSIS TRITHORAX-RELATED PROTEIN 5 and 6 (ATXR5 and 6) methyltransferases, is largely associated with transposable elements but also covers lowly expressed genes. Here we show that this histone modification is preferentially deposited during the night. In euchromatic regions, it is found along the bodies of DNA damage response genes (DDR), where it is needed for their proper expression. The absence of H3K27me1 translates into an enhanced expression of DDR genes that follows a rhythmic oscillation pattern. This evidences a link between chromatin modifications and their synchronization with the diurnal cycle in order to accurately modulate the activation of biological processes to the most appropriate time of the day.