Genome-wide chromatin accessibility analysis unveils open chromatin convergent evolution during polyploidization in cotton

Abstract

Allopolyploidization, resulting in divergent genomes in the same cell, is believed to trigger a “genome shock”, leading to broad genetic and epigenetic changes. However, little is understood about chromatin and gene-expression dynamics as underlying driving forces during allopolyploidization. Here, we examined the genome-wide DNase I-hypersensitive site (DHS) and its variations in domesticated allotetraploid cotton ( Gossypium hirsutum and Gossypium barbadense , AADD) and its extant AA ( Gossypium arboreum ) and DD ( Gossypium raimondii ) progenitors. We observed distinct DHS distributions between G. arboreum and G. raimondii . In contrast, the DHSs of the two subgenomes of G. hirsutum and G. barbadense showed a convergent distribution. This convergent distribution of DHS was also present in the wild allotetraploids Gossypium darwinii and G. hirsutum var. yucatanense , but absent from a resynthesized hybrid of G. arboreum and G. raimondii , suggesting that it may be a common feature in polyploids, and not a consequence of domestication after polyploidization. We revealed that putative cis -regulatory elements (CREs) derived from polyploidization-related DHSs were dominated by several families, including Dof, ERF48, and BPC1. Strikingly, 56.6% of polyploidization-related DHSs were derived from transposable elements (TEs). Moreover, we observed positive correlations between DHS accessibility and the histone marks H3K4me3, H3K27me3, H3K36me3, H3K27ac, and H3K9ac, indicating that coordinated interplay among histone modifications, TEs, and CREs drives the DHS landscape dynamics under polyploidization. Collectively, these findings advance our understanding of the regulatory architecture in plants and underscore the complexity of regulome evolution during polyploidization.

High-resolution Hi-C maps highlight multiscale chromatin architecture reorganization during cold stress in Brachypodium distachyon

“…To explore the factors driving TAD alterations during cold stress, we characterized TADs by performing chromatin immunoprecipitation and sequencing (ChIP-seq) of two histone modifications (H3K27ac and H3K27me3) in normal and cold-treated samples. Similar to the study of other plants [ 31 ], the active histone modification H3K27ac was enriched in active genes at the transcription start sites (TSSs) (Fig. S 6 ).…”

Haplotype phased genome of ‘Fairchild’ mandarin highlights influence of local chromatin state on gene expression

“…ERF48 binding motifs were also found to be enriched in differentially accessible chromatin regions between cotton ( Gossypium ) accessions before and after allopolyploidization, interspecific hybridization, and domestication [30], suggesting ERF48 motifs are a potential source of cis-regulatory variation across multiple plant species. ERF48 is a target of Polycomb repressive complex 2 which deposits H3K27me3 [30,31] and typically results in reduced transcriptional activity. Following this logic, we explored the relationship between levels of H3K27me3 at paternal alleles of AS-ACRs and the presence of the ERF48 motif.…”

“…ERF48 binding sites were also found to be enriched in differential DNAse hypersensitive regions discovered in a panel of cotton accessions spanning polyploidization and domestication in the species [30]. Han and colleagues speculate that PRC2 binds the guanine-rich binding site of ERF48, and that PRC2-mediated deposition of H3K27me3 may be involved in transitions between states of chromatin accessibility [30]. The sequence-specific DNA binding activity of H3K27me3 “writers” such as Polycomb repressive complex 2 (PRC2), and “erasers” such as JUMONJI DOMAIN-CONTAINING PROTEINS (JMJ) may underlie differential regulation of alleles with resulting ASE.…”

Genome‐wide DNase I‐hypersensitive site assay reveals distinct genomic distributions and functional features of open chromatin in autopolyploid sugarcane

“…For example, nearly 56–85% of open chromatin is located within 1 kb of any gene in Oryza sativa , Brachypodium distachyon , Setaria italica , Sorghum bicolor , and Arabidopsis thaliana (Han et al., 2020; Zhang, Wu, et al., 2012; Zhang, Zhang, et al., 2012). In contrast, the majority of open chromatin (50–60%) has been found to reside far away from genes (>1 kb of any gene) in plants with larger genome sizes (Han et al., 2022; Li, Wang, et al., 2019; Lu et al., 2019; Rodgers‐Melnick et al., 2016). These results suggest that the proportion of distal open chromatin is correlated with genome size.…”

“…DNase‐seq experiments, including nuclear isolation, DNase I digestion, and DNase‐seq library construction, were performed exactly as previously described by Han et al. (2022). For nuclear cleavage, the isolated nuclei were digested by DNase I with different Units.…”