Abstract
BackgroundPolyploidy 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.ResultsWe 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.ConclusionsOur 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.
Highlights
Polyploidy has played a prominent role in the evolution of plants and many other eukaryotic lineages
We found the A-subgenome in all three tetraploid wheats showed higher levels of modification of both histone markers than the B-subgenome except for extracted tetraploid wheat (ETW) of H3K27me3, and the evolution and domestication at hexaploid level had a distinct impact on the epigenetic modifications between the subgenomes compared to these processes at the tetraploid level
We found that 76.7–96.1% triad homoeologous genes maintained stable modification levels while 3.9–23.3% triads genes showed variable levels in the ploidy transition processes, suggesting predominant autonomy in modification of the AABB subgenomes accompanied with moderate trans-regulatory effects by the DD subgenome in hexaploid wheat
Summary
Polyploidy has played a prominent role in the evolution of plants and many other eukaryotic lineages. One major mechanism by which nascent polyploid plants can overcome these incompatibilities or conflicts and restore normal growth and development is via rapid changes in epigenetic regulation of gene expression and genome restabilization [14,15,16]. Beside DNA methylation, histone modifications play important roles in polyploid formation and stabilization [21, 24]. Notwithstanding these studies, to date the interplay of subgenome autonomy vs trans-genome interaction associated with histone modifications in a given allopolyploid following allopolyploidization or during the course of evolution and domestication remains poorly understood
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