Evolutionary history of DNA methylation related genes in chordates: new insights from multiple whole genome duplications

Abstract

DNA methylation is an important epigenetic mechanism involved in many biological processes, i.e. gametogenesis and embryonic development. However, increased copy numbers of DNA methylation related genes (dnmt, tet and tdg) have been found during chordate evolution due to successive whole genome duplication (WGD) events. Their evolutionary history and phylogenetic relationships remain unclear. The present study is the first to clarify the evolutionary history of DNA methylation genes in chordates. In particular, our results highlight the fixation of several dnmt3-related genes following successive WGD throughout evolution. The rainbow trout genome offered a unique opportunity to study the early evolutionary fates of duplicated genes due to a recent round of WGD at the radiation of salmonids. Differences highlighted in transcriptional patterns of these genes during gametogenesis and ontogenesis in trout indicated that they might be subjected to sub- or neo-functionalisation after WDG. The fixation of multiple dnmt3 genes in genomes after WGD could contribute to the diversification and plastic adaptation of the teleost.

Flanking sequence preference modulates de novo DNA methylation in the mouse genome

“…Together with our molecular dynamics simulations, these results support a sequence-dependent conformation of the R836 side chain, and pinpoint R836 as a critical residue in mediating the flanking sequence preferences observed for DNMT3A. Interestingly, this arginine is conserved throughout all genes annotated as Dnmt3a in jawed vertebrates, teleost species and in the jawless vertebrate Lamprey ( 64 ). The lysine in DNMT3B on the other hand, is only conserved in jawed vertebrates, while Arg, Lys or Asparagine can be found at the same position in other species ( 64 ).…”

“…Interestingly, this arginine is conserved throughout all genes annotated as Dnmt3a in jawed vertebrates, teleost species and in the jawless vertebrate Lamprey ( 64 ). The lysine in DNMT3B on the other hand, is only conserved in jawed vertebrates, while Arg, Lys or Asparagine can be found at the same position in other species ( 64 ). It will be interesting to investigate if DNA methylation is influenced by flanking-sequence preference in these species, and if this can be explained by a conserved role of the side chain at this position.…”

Pervasive non-CpG methylation at zebrafish mosaic satellite repeats

“…2 and Additional File 1: Figure S5). This is in accord with steady state transcript abundance of zebrafish de novo DNMT3 enzymes that are low in post-fertilization embryos and higher during later developmental stages, indicating their possible roles in the maintenance of this unique form of methylation [28,29] (Additional File 1: Figure S5). The observed temporal mCH dynamics are independent of mCG changes at these regions and are uncoupled from global developmental mCG patterning in zebrafish, which progressively increases from 16 cell stage to match the paternal methylome at the ZGA onset [20,21] (Additional File 1: Figure S5).…”

“…H3K9me3 has been shown to mark the zebrafish genome pre-ZGA and to progressively increase from ZGA onwards [35,38], however, we find that at a sub-population of MOSAT_DR sites, H3K9me3 is stable during development (256 cell to shield) (Additional File1: Figure S5). This contrasts the observation in mammals, where H3K9me3 and mCH are generally inversely correlated at CG-poor regions [8,29,39]. To interrogate if H3K9me3 could play a role in recruiting or maintaining mCH at MOSAT repeats, we investigated the correlation between mCH and H3K9me3 through development.…”

A Comprehensive Integrated Genetic Map of the Complete Karyotype of Solea senegalensis (Kaup 1858)

“…It is believed that approximately 15% of the paralogs generated by TGD have been maintained in the teleost genome [ 46 ], a percentage very similar of that of the number of duplicated FISH signals obtained in this study and which could explain the adaptive plasticity of this group. Recently, it has been described that the fixation of extra copies of de novo DNA methyl transferases ( dnmt3 ) genes may have contributed to the diversification and adaptive plasticity of the teleost [ 47 ]. Teleosts, including S. senegalensis , have a high number of functional dnmt3 paralogs where up to 6 dnmt3 paralogs with different tissue and developmental specific expression patterns have been described [ 48 ].…”