Chromatin spatial organization of wild type and mutant peanuts reveals high-resolution genomic architecture and interaction alterations

Xingguo Zhang,Baozhu Guo,Fangping Gong,Rajeev K Varshney,Kai Zhao,Manish K Pandey,Zhongfeng Li,Xingli Ma,Kunkun Zhao,Jianping Wang,Dongmei Yin

doi:10.1186/s13059-021-02520-x

Abstract

BackgroundThree-dimensional (3D) chromatin organization provides a critical foundation to investigate gene expression regulation and cellular homeostasis.ResultsHere, we present the first 3D genome architecture maps in wild type and mutant allotetraploid peanut lines, which illustrate A/B compartments, topologically associated domains (TADs), and widespread chromatin interactions. Most peanut chromosomal arms (52.3%) have active regions (A compartments) with relatively high gene density and high transcriptional levels. About 2.0% of chromosomal regions switch from inactive to active (B-to-A) in the mutant line, harboring 58 differentially expressed genes enriched in flavonoid biosynthesis and circadian rhythm functions. The mutant peanut line shows a higher number of genome-wide cis-interactions than its wild-type. The present study reveals a new TAD in the mutant line that generates different chromatin loops and harbors a specific upstream AP2EREBP-binding motif which might upregulate the expression of the GA2ox gene and decrease active gibberellin (GA) content, presumably making the mutant plant dwarf.ConclusionsOur findings will shed new light on the relationship between 3D chromatin architecture and transcriptional regulation in plants.

Highlights

Three-dimensional (3D) chromatin organization provides a critical foundation to investigate gene expression regulation and cellular homeostasis
We performed ATAC-seq to study open chromatin regions (Additional file 1: Table S2), and RNA sequencing (RNA-seq) analysis (Additional file 1: Table S3) using rRNA-depleted RNA extracted from tissues including leaf, stem, branch, flower, and seed at three developmental stages to facilitate investigation of chromatin topology-mediated transcriptional regulation in dwarf mutant H1314 and wild type H2014
The frequency of intra-chromosomal interactions decreased with increasing linear distance, and distances from 0 to 400 kb accounted for 80% interactions (Additional file 2: Fig. S1)

Summary

Introduction

Three-dimensional (3D) chromatin organization provides a critical foundation to investigate gene expression regulation and cellular homeostasis. Chromatin interaction and genome organization play an important role in gene expression regulation. Lack of information about chromatin spatial organization and chromosome structures in the plant genome have constrained understanding of gene regulation and cellular homeostasis. Accessible Chromatin sequencing (ATAC-seq) provided the opportunity to decipher (3D) genome architecture and to dissect the relationship between chromatin organization and gene expression in various biological processes. At the sub-megabase scale, mammalian chromatin can be further divided into topologically associated domains (TADs) [7,8,9,10] with their boundaries enriched for architectural proteins such as cohesion and CCCTC-binding factors (CTCF) and specific epigenetic marks [11, 12]. TADs have been shown to be largely conserved across different species, cell types and physiological conditions, and may act as functional units for transcription regulation [7, 13]

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Results

Discussion

Conclusion