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

Abstract

Background 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 profiling to characterize the combinatorial patterns of chromatin signatures is a powerful means to detect functional elements and clarify regulatory activities in human studies. Results In 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. Conclusions We 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. Electronic supplementary material The online version of this article (10.1186/s13059-019-1746-8) contains supplementary material, which is available to authorized users.

Differential chromatin accessibility landscape reveals structural and functional features of the allopolyploid wheat chromosomes

“…Differences in nucleosome depleted regions between high and low expressed genes have also been reported in Arabidopsis, rice, and maize [4,15,16], linking an open chromatin state with higher gene expression. Consistent with the DNS-seq results in both plant and animal genomes, DNase I hyper-sensitive regions with open chromatin are often associated with proximal cis-regulatory elements [4,[15][16][17][18][19]. However, a substantial fraction of DNase I hyper-sensitive sites, some harboring distal cis-regulatory elements, were detected in intergenic regions [7,18,20,21].…”

“…The hexaploid wheat genome (genome formula AABBDD) was formed by two recent hybridizations of three diploid progenitors [23][24][25][26], which diverged about 5.5 million years ago [27]. Previous studies demonstrated that the long-term post-hybridization adjustment of gene regulation as a consequence of increased gene dosage was accompanied by epigenetic, structural, and gene expression modifications [18,[28][29][30][31][32]. Analysis of syntenic gene triplets in the allopolyploid genome showed that a gene expression bias towards one of the homoeologous copies was associated with changes in histone epigenetic marks, DNA methylation, and chromatin sensitivity to DNAse I and Transposase Tn5 treatments within the proximal cis-regulatory regions or gene body, thus connecting the chromatin and epigenetic states with imbalanced expression of duplicated genes [18,29,30].…”

Polycomb Repressive Complex 2-mediated histone modification H3K27me3 is associated with embryogenic potential in Norway spruce

“…2A ). These observations are consistent with previous studies in angiosperms, moss, and unicellular algae ( Zhang et al , 2007 ; Makarevitch et al , 2013 ; Widiez et al , 2014 ; Baker et al , 2015 ; Hussey et al , 2017 ; Latrasse et al , 2017 ; Mikulski et al , 2017 ; Chica et al , 2017 ; Lü et al , 2018 ; Qi et al , 2018 ; Li et al , 2019 ). This shows that (i) the CUT&RUN method can be successfully applied to large genomes, such as that of Norway spruce, and (ii) despite the significant differences in genome size between angiosperms and gymnosperms, deposition of H3K27me3 is detected in similar genomic features across different plant species.…”

“…Here, we surveyed the differences of H3K27me3 deposition in EC and NEC of Norway spruce. Most genome-wide analyses of histone modifications in plants have been accomplished in species with relatively small genomes, with the exception of maize, barley, and wheat ( Zhang et al , 2007 ; Makarevitch et al , 2013 ; Widiez et al , 2014 ; Baker et al , 2015 ; Hussey et al , 2017 ; Latrasse et al , 2017 ; Chica et al , 2017 ; Lü et al , 2018 ; Qi et al , 2018 ; Li et al , 2019 ; Montgomery et al , 2020 ). In contrast to many angiosperm studies, genome-wide chromatin profiling in other plant species has been limited to moss, liverwort, and unicellular algae ( Widiez et al , 2014 ; Mikulski et al , 2017 ; Montgomery et al , 2020 ).…”

Identification of key tissue-specific, biological processes by integrating enhancer information in maize gene regulatory networks

“…Recent combined analyses of DNA methylation, chromatin accessibility and histone marks have led to the genome-wide characterization of thousands of putative active enhancers in plants [8,4,9,10,11,12,13].…”