The bread wheat epigenomic map reveals distinct chromatin architectural and evolutionary features of functional genetic elements

Zijuan Li,Wenli Zhang,Yilin Xie,Kande Lin,Xiaojuan Ran,Yili Zhuang,Yiping Tong,Luhuan Ye,Wan Teng,Yijing Zhang,Yongbiao Xue,Jingyu Guo,Meiyue Wang

doi:10.1186/s13059-019-1746-8

Abstract

BackgroundBread wheat is an allohexaploid species with a 16-Gb genome that has large intergenic regions, which presents a big challenge for pinpointing regulatory elements and further revealing the transcriptional regulatory mechanisms. Chromatin profiling to characterize the combinatorial patterns of chromatin signatures is a powerful means to detect functional elements and clarify regulatory activities in human studies.ResultsIn the present study, through comprehensive analyses of the open chromatin, DNA methylome, seven major chromatin marks, and transcriptomic data generated for seedlings of allohexaploid wheat, we detected distinct chromatin architectural features surrounding various functional elements, including genes, promoters, enhancer-like elements, and transposons. Thousands of new genic regions and cis-regulatory elements are identified based on the combinatorial pattern of chromatin features. Roughly 1.5% of the genome encodes a subset of active regulatory elements, including promoters and enhancer-like elements, which are characterized by a high degree of chromatin openness and histone acetylation, an abundance of CpG islands, and low DNA methylation levels. A comparison across sub-genomes reveals that evolutionary selection on gene regulation is targeted at the sequence and chromatin feature levels. The divergent enrichment of cis-elements between enhancer-like sequences and promoters implies these functional elements are targeted by different transcription factors.ConclusionsWe herein present a systematic epigenomic map for the annotation of cis-regulatory elements in the bread wheat genome, which provides new insights into the connections between chromatin modifications and cis-regulatory activities in allohexaploid wheat.

Highlights

Bread wheat is an allohexaploid species with a 16-Gb genome that has large intergenic regions, which presents a big challenge for pinpointing regulatory elements and further revealing the transcriptional regulatory mechanisms
Chromatin architecture of bread wheat seedlings To systematically analyze the epigenomic features in bread wheat, we profiled the open chromatin associated with DNase I-hypersensitive sites (DHSs), the DNA methylome at a single-base resolution based on bisulfite sequencing, and the genomic distribution of seven histone modifications according to chromatin immunoprecipitation followed by high-throughput sequencing (ChIP-sequencing) in seedlings
We used specific antibodies to detect histone H3 lysine 4 tri-methylation (H3K4me3), a modification that generally occurs in promoters; H3K27me3 associated with repression; lysine 9 acetylation (H3K9ac) and H3K27ac associated with active regulation, mostly in promoters and enhancers; H3K36me3 associated with transcribed regions; H3K9me2 responsible for the repression of transposable elements (TEs); and H3K4me1, which is preferentially associated with enhancers in vertebrates, but in gene body regions in Arabidopsis thaliana [16] (Fig. 1a and Additional file 1: Figure S1)

Summary

Introduction

Bread wheat is an allohexaploid species with a 16-Gb genome that has large intergenic regions, which presents a big challenge for pinpointing regulatory elements and further revealing the transcriptional regulatory mechanisms. A previous study indicated that the noncoding regions account for approximately 93% of the 16-Gb genome [1] Studies in both higher plants and animals revealed abundant highly conserved regulatory elements in noncoding regions with essential regulatory activities [2, 3], the detection of which is critical for a comprehensive characterization of the regulatory networks. Various types of chromatin modifications regulating gene activity have been described and applied for pinpointing cis-regulatory elements, including histone acetylation; mono-, di-, and trimethylations; and DNA methylation [5]. The integration of epigenomic architecture and sequence features has become a powerful means for pinpointing the regulatory elements in the genome and for revealing the regulatory mechanism, helping to accurately narrow down the chromosomal locations of candidate functional regions [4, 5, 8,9,10,11]

Methods

Results

Conclusion