3D genome architecture coordinates trans and cis regulation of differentially expressed ear and tassel genes in maize

Yonghao Sun,Guoliang Li,Fang Yang,Lulu Deng,Changxiong Ke,Ying Zhang,Linqian Han,Da Lin,Weize Xu,David Jackson,Liang Dong,Xingwang Li

doi:10.1186/s13059-020-02063-7

Yonghao Sun, Guoliang Li + Show 10 more

Open Access

https://doi.org/10.1186/s13059-020-02063-7

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Abstract

BackgroundMaize ears and tassels are two separate types of inflorescence which are initiated by similar developmental processes but gradually develop distinct architectures. However, coordinated trans and cis regulation of differentially expressed genes determining ear and tassel architecture within the 3D genome context is largely unknown.ResultsWe identify 56,055 and 52,633 open chromatin regions (OCRs) in developing maize ear and tassel primordia using ATAC-seq and characterize combinatorial epigenome features around these OCRs using ChIP-seq, Bisulfite-seq, and RNA-seq datasets. Our integrative analysis of coordinated epigenetic modification and transcription factor binding to OCRs highlights the cis and trans regulation of differentially expressed genes in ear and tassel controlling inflorescence architecture. We further systematically map chromatin interactions at high-resolution in corresponding tissues using in situ digestion-ligation-only Hi-C (DLO Hi-C). The extensive chromatin loops connecting OCRs and genes provide a 3D view on cis- and trans-regulatory modules responsible for ear- and tassel-specific gene expression. We find that intergenic SNPs tend to locate in distal OCRs, and our chromatin interaction maps provide a potential mechanism for trait-associated intergenic SNPs that may contribute to phenotypic variation by influencing target gene expression through chromatin loops.ConclusionsOur comprehensive epigenome annotations and 3D genome maps serve as valuable resource and provide a deep understanding of the complex regulatory mechanisms of genes underlying developmental and morphological diversities between maize ear and tassel.

Highlights

Maize ears and tassels are two separate types of inflorescence which are initiated by similar developmental processes but gradually develop distinct architectures
63% of the open chromatin regions (OCRs) were close to genes and were defined as local OCRs (LoOCRs: the genomic regions from 3 kb upstream of transcription start sites (TSS), spanning the gene body, to transcription termination sites (TTS) of genes)
Given the activity of cis-regulatory elements (CREs) in mammals is associated with certain epigenetic features [13, 51, 52], we investigated the chromatin signatures flanking LoOCRs and distal OCRs (dOCRs) in ear and tassel, by generating global maps of 3 types of histone modification, as well as DNA methylation (Fig. 1d, Additional file 2: Table S2)

Summary

Introduction

Maize ears and tassels are two separate types of inflorescence which are initiated by similar developmental processes but gradually develop distinct architectures. Open chromatin regions (OCRs) along the genome with depleted nucleosomes harbor various categories of cis-regulatory elements (CREs), including promoters, enhancers, and insulators, and are accessible to different trans-acting factors, such as transcription factors (TFs) that dynamically modulate gene expression [1,2,3,4,5,6,7]. Recent advances in studies of 3D genome organization found that regulatory elements, including enhancers, promoters, and insulators, frequently form chromatin loops and affect the expression of associated genes [15,16,17,18]. Recent studies of long-range regulatory element interactions in maize seedlings using ChIA-PET technology greatly improve the resolution and reveal the important roles of chromatin loops in gene expression and phenotypic variation [10, 26]. Gene pairs with loops between promoter proximal regions in maize tend to be transcriptionally coordinated, indicating they might be involved in the same developmental process [10, 26]

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