Open chromatin interaction maps reveal functional regulatory elements and chromatin architecture variations during wheat evolution

Abstract

Background Bread wheat (Triticum aestivum) is an allohexaploid that is generated by two subsequent allopolyploidization events. The large genome size (16 Gb) and polyploid complexity impede our understanding of how regulatory elements and their interactions shape chromatin structure and gene expression in wheat. The open chromatin enrichment and network Hi-C (OCEAN-C) is a powerful antibody-independent method to detect chromatin interactions between open chromatin regions throughout the genome. Results Here we generate open chromatin interaction maps for hexaploid wheat and its tetraploid and diploid relatives using OCEAN-C. The anchors of chromatin loops show high chromatin accessibility and are concomitant with several active histone modifications, with 67% of them interacting with multiple loci. Binding motifs of various transcription factors are significantly enriched in the hubs of open chromatin interactions (HOCIs). The genes linked by HOCIs represent higher expression level and lower coefficient expression variance than the genes linked by other loops, which suggests HOCIs may coordinate co-expression of linked genes. Thousands of interchromosomal loops are identified, while limited interchromosomal loops (0.4%) are identified between homoeologous genes in hexaploid wheat. Moreover, we find structure variations contribute to chromatin interaction divergence of homoeologs and chromatin topology changes between different wheat species. The genes with discrepant chromatin interactions show expression alteration in hexaploid wheat compared with its tetraploid and diploid relatives. Conclusions Our results reveal open chromatin interactions in different wheat species, which provide new insights into the role of open chromatin interactions in gene expression during the evolution of polyploid wheat.

Dispersed emergence and protracted domestication of polyploid wheat uncovered by mosaic ancestral haploblock inference

“…We inferred centAHGs for all 14 chromosomes in the A&B subgenomes (Supplementary Data 9 ). Interestingly, the partition of centAHG was roughly consistent with the A/B compartment of the wheat genome inferred in a previous study 49 (Fig. 5b , Supplementary Fig.…”

“… a Positioning of centAHGs on chromosome 1 A, based on the time of transition among AHG types between adjacent windows (upper), length of consecutive windows of the same type of AHG (middle) and ratio between inter- and intra- AHG type genetic diversity (lower) of all 386 accessions. b The consistency between the partition of the centAHG and the A/B compartment from a previously published study 49 on chr6A. c Proportion of centAHGs among four taxonomic groups that could be traced back through the route of WE-DT-LR-CV of 14 A&B chromosomes shown by stacked bar chart.…”

Systematic mining and functional analysis of factors regulating wheat spike development for breeding selection

“…As such, gene co-expression networks provide different filter for identification of key regulators, as demonstrated in previous studies based on stage-specific transcriptome and population-wide RNA-seq (Wang et al, 2017;Li et al, 2018;VanGessel et al, 2022). Aside from gene expression per se, chromatin features have also been explored in wheat for different tissues, revealing their association with the regulation of tissue-specific or stress-induced gene expression and subgenome-biased expression patterns of homeologs (Li et al, 2019b;Concia et al, 2020;Yuan et al, 2022;Zhao et al, 2023). Integrating gene expression, chromatin features, and transcription factor binding sites has enabled the prediction of gene regulatory networks, as exemplified by recent studies in wheat (Chen et al, 2023;Tang et al, 2023).…”

FAIRE‐MS reveals mitotic retention of transcriptional regulators on a proteome‐wide scale

“…30 This technique has been successfully used to reveal functional regulatory elements and chromatin architecture variations during wheat evolution. 31 In this study, we developed a new in vitro method called FAIRE-MS that combines FAIRE-based chromatin-associated protein pull-down and highresolution mass spectrometry (MS). We utilized it to quantify changes in chromatin-binding transcriptional regulators across the interphase and mitotic phases of the A549 human cell cycle.…”

“…By integrating FAIRE‐seq and Hi‐C, researchers recently developed a method called open chromatin enrichment and network Hi‐C (OCEAN‐C) to detect global open chromatin interactions 30 . This technique has been successfully used to reveal functional regulatory elements and chromatin architecture variations during wheat evolution 31 . In this study, we developed a new in vitro method called FAIRE‐MS that combines FAIRE‐based chromatin‐associated protein pull‐down and high‐resolution mass spectrometry (MS).…”