Diurnal RNAPII-tethered chromatin interactions are associated with rhythmic gene expression in rice

Area of Science:

• Plant molecular biology
• Circadian biology
• Epigenetics and genome architecture

Background:

• Daily plant physiological processes are thought to be driven by coordinated gene expression rhythms.
• The dynamics of diurnal 3D genome architecture and its role in rhythmic gene expression are not well understood.

Purpose of the Study:

• To investigate the genome-wide dynamics of RNA polymerase II (RNAPII) occupancy and its relationship with 3D genome architecture.
• To elucidate how these dynamics contribute to the circadian regulation of gene expression in plants.

Main Methods:

• Genome-wide analysis of RNA polymerase II (RNAPII) occupancy.
• Chromatin interaction analysis to map 3D genome architecture.
• Correlation analysis between RNAPII binding, chromatin structure, and gene expression rhythms.

Main Results:

• Genome-wide RNAPII occupancy rhythms precede mRNA accumulation by approximately 2 hours.
• Rhythmic RNAPII binding correlates with dynamic remodeling of chromatin architecture, including spatial clusters and connectivity.
• Rhythmically expressed genes are preferentially tethered by RNAPII within specific expression phase clusters.
• Chromatin spatial clusters (CSCs) exhibit plasticity, with morning-expressed genes and evening-expressed non-rhythmic genes enriched in RNAPII-associated CSCs.
• Core circadian clock genes show distinct chromatin connectivity patterns, forming highly connected networks in the morning and scattered foci in the evening.

Conclusions:

• This study reveals fundamental principles of diurnal genome folding in plants.
• A distinct higher-order chromosome organization is crucial for coordinating diurnal transcriptional regulation.