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

Li Deng,C Robertson Mcclung,Shuangqi Wang,Zhilin Cao,Meng Ma,Wei Zhang,Lun Zhao,Minrong Guo,Xingwang Li,Baibai Gao,Yongqing Yang,Qinghua Zhang,Hao Lou,Liang Xie,Ying Zhang,Qing Zhang,Guoliang Li

doi:10.1186/s13059-021-02594-7

Abstract

BackgroundThe daily cycling of plant physiological processes is speculated to arise from the coordinated rhythms of gene expression. However, the dynamics of diurnal 3D genome architecture and their potential functions underlying the rhythmic gene expression remain unclear.ResultsHere, we reveal the genome-wide rhythmic occupancy of RNA polymerase II (RNAPII), which precedes mRNA accumulation by approximately 2 h. Rhythmic RNAPII binding dynamically correlates with RNAPII-mediated chromatin architecture remodeling at the genomic level of chromatin interactions, spatial clusters, and chromatin connectivity maps, which are associated with the circadian rhythm of gene expression. Rhythmically expressed genes within the same peak phases of expression are preferentially tethered by RNAPII for coordinated transcription. RNAPII-associated chromatin spatial clusters (CSCs) show high plasticity during the circadian cycle, and rhythmically expressed genes in the morning phase and non-rhythmically expressed genes in the evening phase tend to be enriched in RNAPII-associated CSCs to orchestrate expression. Core circadian clock genes are associated with RNAPII-mediated highly connected chromatin connectivity networks in the morning in contrast to the scattered, sporadic spatial chromatin connectivity in the evening; this indicates that they are transcribed within physical proximity to each other during the AM circadian window and are located in discrete “transcriptional factory” foci in the evening, linking chromatin architecture to coordinated transcription outputs.ConclusionOur findings uncover fundamental diurnal genome folding principles in plants and reveal a distinct higher-order chromosome organization that is crucial for coordinating diurnal dynamics of transcriptional regulation.

Highlights

The daily cycling of plant physiological processes is speculated to arise from the coordinated rhythms of gene expression
We found that RNA polymerase II (RNAPII) signals increased sharply at transcription start sites (TSS), decreased on entering gene body regions, and peaked at polyadenylation site (PAS) (Fig. 1b)
We examined the temporal relationships between RNAPII recruitment and RNA accumulation and found that the phase distribution of RNAPII peaks and peak abundance of rhythmic transcripts clustered around the morning phase (Fig. 1c, d; Fig. S2b, 3b) and that rhythmic RNAPII peak intensity was significantly correlated with rhythmic transcript expression levels (Pearson rank correlation = 0.69, over the six time points; Fig. 1e, Fig. S2c)

Summary

Introduction

The daily cycling of plant physiological processes is speculated to arise from the coordinated rhythms of gene expression. Diurnal oscillations of gene expression are presumed to drive daily cycles of plant physiological processes through core circadian genes involved in interlocked transcriptional/translational negative feedback loops [1,2,3,4,5,6,7,8]. Interlocking transcriptional loops generate cycles of transcription with various expression phases depending on the alternative usage of cis-elements in the promoters and enhancers of specific target genes [12, 13]. In Arabidopsis, genome-wide identification of circadian clock associated 1 (CCA1), the timing of CAB expression 1 (TOC1; known as PRR1), pseudoresponse regulator 5 (PRR5), and PRR7 targets revealed phase-specific circadian clock regulatory elements in target gene promoters and temporal regulation of specific output pathways [14,15,16,17]. RNAPII plays an essential role in initiating nascent transcription [23, 24]; whether RNAPII occupancy is under diurnal control to regulate circadian transcription in plants remains poorly understood

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Conclusion