Abstract

Chromatin loops connect regulatory elements to their target genes. They serve as bridges between transcriptional regulation and phenotypic variation in mammals. However, spatial organization of regulatory elements and its impact on gene expression in plants remain unclear. Here, we characterize epigenetic features of active promoter proximal regions and candidate distal regulatory elements to construct high-resolution chromatin interaction maps for maize via long-read chromatin interaction analysis by paired-end tag sequencing (ChIA-PET). The maps indicate that chromatin loops are formed between regulatory elements, and that gene pairs between promoter proximal regions tend to be co-expressed. The maps also demonstrated the topological basis of quantitative trait loci which influence gene expression and phenotype. Many promoter proximal regions are involved in chromatin loops with distal regulatory elements, which regulate important agronomic traits. Collectively, these maps provide a high-resolution view of 3D maize genome architecture, and its role in gene expression and phenotypic variation.

Highlights

  • Chromatin loops connect regulatory elements to their target genes

  • We explore the regulatory role of mutations occurring in distal regulatory elements related to gene expression and phenotypic variations with adapted long-read ChIA-PET, and construct high-resolution chromatin interaction maps of maize promoter proximal regions and distal regulatory elements associated with RNA polymerase II occupancy and histone mark H3K4me[3]

  • By integrating expression quantitative trait locus and genome-wide association study (GWAS) data, we demonstrate that long-range chromatin interactions between variant regulatory elements and their target genes contribute to variations in gene expression, metabolic phenotypes, and agronomic traits

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Summary

Introduction

Chromatin loops connect regulatory elements to their target genes. They serve as bridges between transcriptional regulation and phenotypic variation in mammals. Many promoter proximal regions are involved in chromatin loops with distal regulatory elements, which regulate important agronomic traits. These maps provide a high-resolution view of 3D maize genome architecture, and its role in gene expression and phenotypic variation. We explore the regulatory role of mutations occurring in distal regulatory elements related to gene expression and phenotypic variations with adapted long-read ChIA-PET, and construct high-resolution chromatin interaction maps of maize promoter proximal regions and distal regulatory elements associated with RNA polymerase II occupancy and histone mark H3K4me[3]. By integrating expression quantitative trait locus (eQTL) and genome-wide association study (GWAS) data, we demonstrate that long-range chromatin interactions between variant regulatory elements and their target genes contribute to variations in gene expression, metabolic phenotypes, and agronomic traits. Our results highlight the significance of 3D organization of regulatory elements and suggest that the topology of long-range genetic variations may affect gene expression as well as phenotype variation

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