A Comparative Epigenomic Analysis of Polyploidy-Derived Genes in Soybean and Common Bean

Abstract

Soybean (Glycine max) and common bean (Phaseolus vulgaris) share a paleopolyploidy (whole-genome duplication [WGD]) event, approximately 56.5 million years ago, followed by a genus Glycine-specific polyploidy, approximately 10 million years ago. Cytosine methylation is an epigenetic mark that plays an important role in the regulation of genes and transposable elements (TEs); however, the role of DNA methylation in the fate/evolution of genes following polyploidy and speciation has not been fully explored. Whole-genome bisulfite sequencing was used to produce nucleotide resolution methylomes for soybean and common bean. We found that, in soybean, CG body-methylated genes were abundant in WGD genes, which were, on average, more highly expressed than single-copy genes and had slower evolutionary rates than unmethylated genes, suggesting that WGD genes evolve more slowly than single-copy genes. CG body-methylated genes were also enriched in shared single-copy genes (single copy in both species) that may be responsible for the broad and high expression patterns of this class of genes. In addition, diverged methylation patterns in non-CG contexts between paralogs were due mostly to TEs in or near genes, suggesting a role for TEs and non-CG methylation in regulating gene expression post polyploidy. Reference methylomes for both soybean and common bean were constructed, providing resources for investigating epigenetic variation in legume crops. Also, the analysis of methylation patterns of duplicated and single-copy genes has provided insights into the functional consequences of polyploidy and epigenetic regulation in plant genomes.

Methylome evolution in plants

“…It has important roles in regulating the expression of transposable elements (TEs), repeat sequences, and genes. Extensive experimental work has shown that changes in DNA methylation are associated with plant phenotypes [5–20], genome stability [21–25], polyploidization [26], recombination [27–31], and heterosis [32–40], and that such changes actively mediate environmental signaling [41–43], pathogen responses [44–46], and priming [47–49]. For these reasons, DNA methylation has emerged as a potentially important factor in plant evolution [50–53] and as a possible molecular target for the improvement of commercial crops [54, 55].…”

Creating Order from Chaos: Epigenome Dynamics in Plants with Complex Genomes

“…Analysis of the soybean methylome reveals that many duplicates have similar levels of DNA methylation, but ;6% of the pairs have divergent non-CG methylation levels that are associated with altered expression . Many of the methylation differences in the duplicate soybean genes can be attributed to transposon insertions that are present in one member of the pair Kim et al, 2015). These studies along with data from specific wheat (Triticum aestivum) loci (Shitsukawa et al, 2007;Hu et al, 2013;Zhang et al, 2015) and maize (West et al, 2014) suggest that DNA methylation does not play a major global role in differentiating subgenomes, but it can contribute to locus-specific divergence of retained duplicates.…”

“…The above example of maize and Arabidopsis simply exhibits differences in two species. A growing set of chromatin profiles in crop species reveals more interesting patterns of heterochromatin and a variety of ways that the epigenome is used to organize complex genome structures He et al, 2010;Gent et al, 2013;Makarevitch et al, 2013;Regulski et al, 2013;Schmitz et al, 2013;Zhong et al, 2013;Baker et al, 2015;Kim et al, 2015). Much of the variation among species in genome size and complexity is attributable to two factors: bursts of TEs and/or whole-genome duplications (WGDs).…”

Epigenetic perspectives on the evolution and domestication of polyploid plant and crops

“…Genome-wide studies investigating the methylome of diverse accessions of key crop species have indicated that the majority of these modifications are conserved within a species (see ref. in [91,92]) [93,94]. Between accessions, there are thousands of differentially methylated regions (DMRs), and 10–20% of these DMRs are negatively associated with gene expression.…”