Conservation and trans-regulation of histone modification in the A and B subgenomes of polyploid wheat during domestication and ploidy transition

Abstract

Background Polyploidy has played a prominent role in the evolution of plants and many other eukaryotic lineages. However, how polyploid genomes adapt to the abrupt presence of two or more sets of chromosomes via genome regulation remains poorly understood. Here, we analyzed genome-wide histone modification and gene expression profiles in relation to domestication and ploidy transition in the A and B subgenomes of polyploid wheat. Results We found that epigenetic modification patterns by two typical euchromatin histone markers, H3K4me3 and H3K27me3, for the great majority of homoeologous triad genes in A and B subgenomes were highly conserved between wild and domesticated tetraploid wheats and remained stable in the process of ploidy transitions from hexaploid to extracted tetraploid and then back to resynthesized hexaploid. However, a subset of genes was differentially modified during tetraploid and hexaploid wheat domestication and in response to ploidy transitions, and these genes were enriched for particular gene ontology (GO) terms. The extracted tetraploid wheat manifested higher overall histone modification levels than its hexaploid donor, and which were reversible and restored to normal levels in the resynthesized hexaploid. Further, while H3K4me3 marks were distally distributed along each chromosome and significantly correlated with subgenome expression as expected, H3K27me3 marks showed only a weak distal bias and did not show a significant correlation with gene expression. Conclusions Our results reveal overall high stability of histone modification patterns in the A and B subgenomes of polyploid wheat during domestication and in the process of ploidy transitions. However, modification levels of a subset of functionally relevant genes in the A and B genomes were trans-regulated by the D genome in hexaploid wheat.

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

“…Polyploidization induces rapid morphologic changes in wheat [ 45 ]. Changes of genetic sequences and epigenetic marks including DNA methylation and histone modifications are reported to be involved in gene regulation and phenotypic changes during wheat polyploidization [ 40 , 45 , 46 ]. By comparing hexaploid wheat with tetraploid and diploid relatives, we found a positive correlation between chromatin interaction changes and expression changes (Fig.…”

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

“…Allopolyploidization resulting in divergent genomes in a single cell is believed to trigger “genome shock” and to cause broad gene-expression aberrations, which could be detrimental to newly formed polyploidy ( 5 , 6 ). Continuous efforts have revealed that epigenetic modification changes ( 7 – 9 ), homologous recombination ( 10 ), three-dimensional chromatin conformation ( 11 , 12 ), transposable element (TE) reactivation ( 13 ), and small interfering RNA expression ( 14 ) are important factors driving gene-expression bias or novelty in plant polyploidization. However, there is still a lack of understanding of the mechanisms controlling gene transcription changes mediated by cis -regulatory elements (CREs) after plant polyploidization.…”

Domestication Impacts the Wheat-Associated Microbiota and the Rhizosphere Colonization by Seed- and Soil-Originated Microbiomes, Across Different Fields

“…Moreover, T. aestivum gene diversity significantly reduced as a result of subsequent polyploidy events. Its D genome was found to conserved more trait loci than in subgenomes A and B ( Berkman et al, 2011 ); however, it was also found that subgenome D can modify 42.8% of alternative splicing patterns (during gene expression, an alternative splicing process allows a single gene to code for numerous proteins) of subgenomes A and B ( Yu et al, 2020 ), meaning that domestication at the hexaploid level had a greater effect on genetic modifications between subgenomes than same processes at the tetraploid level ( Lv et al, 2021 ). This suggests that subsequent polyploidy events lead to the loss of more genetic information to recruit microorganisms from the bulk soil.…”