Diurnal 3D genome organization remodeling orchestrates rhythmic gene expression in rice [DAP-seq]

Genome-wide rhythmic occupancy of RNA polymerase II (RNAPII) is highly coordinated with rhythmic genes expression. Rhythmic RNAPII binding dynamically modulates diurnal 3D genome architecture remodeling with 91% of the chromatin interactions were altered. The rhythmic genes cluster at the 8:00 (AM) circadian phase form spatial interacting clusters in turn assist coordinated rhythmic gene expression, while non-rhythmic genes tend to tether together and contribute to expression at 20:00 (PM) circadian window. Target genes and associated cis-binding motifs of transcription factors enrichment points to the existence of subnuclear organization hub enriched around the TFs. RNAPII-associated chromatin interaction domains (CIDs) are under circadian control, and static CIDs with common node genes but changed connecting genes along the circadian cycle, reveal they may function as distinct clock components in the interconnected circuits between morning and evening. Core circadian clock genes related chromatin connectivity networks reveal a compact and highly connected chromatin architecture serving to coordinate gene expression in the morning, whereas a scattered, loose chromatin architecture coordinates PM gene expression. Our findings uncover novel diurnal fundamental genome folding principles in plants, and reveal the distinct higher-order chromosome organization that is crucial for coordinating diurnal dynamics of transcriptional regulation. Overall design: Here, we generated genome-wide occupancy of RNA polymerase II (RNAPII) by ChIP-seq, whole-transcriptome by RNA-seq, and chromatin accessibility by FAIRE-seq throughout the six-time course. We also performed RNAPII long-read ChIA-PET from the same tissues used for ChIP-seq, RNA-seq, and FAIRE-seq at 8:00 and 20:00. Together, we constructed comprehensive high-resolution dynamic chromatin architecture, and disected its effects on diurnal gene expression.