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

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          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.

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          Most cited references 39

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          Evolution by gene duplication: an update

           Jianzhi Zhang (2003)
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            The DNA methyltransferases of mammals.

             T Bestor (2000)
            The biological significance of 5-methylcytosine was in doubt for many years, but is no longer. Through targeted mutagenesis in mice it has been learnt that every protein shown by biochemical tests to be involved in the establishment, maintenance or interpretation of genomic methylation patterns is encoded by an essential gene. A human genetic disorder (ICF syndrome) has recently been shown to be caused by mutations in the DNA methyltransferase 3B (DNMT3B) gene. A second human disorder (Rett syndrome) has been found to result from mutations in the MECP2 gene, which encodes a protein that binds to methylated DNA. Global genome demethylation caused by targeted mutations in the DNA methyltransferase-1 (Dnmt1) gene has shown that cytosine methylation plays essential roles in X-inactivation, genomic imprinting and genome stabilization. The majority of genomic 5-methylcytosine is now known to enforce the transcriptional silence of the enormous burden of transposons and retroviruses that have accumulated in the mammalian genome. It has also become clear that programmed changes in methylation patterns are less important in the regulation of mammalian development than was previously believed. Although a number of outstanding questions have yet to be answered (one of these questions involves the nature of the cues that designate sites for methylation at particular stages of gametogenesis and early development), studies of DNA methyltransferases are likely to provide further insights into the biological functions of genomic methylation patterns.
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              The DNA methyltransferase DNMT3C protects male germ cells from transposon activity.

              DNA methylation is prevalent in mammalian genomes and plays a central role in the epigenetic control of development. The mammalian DNA methylation machinery is thought to be composed of three DNA methyltransferase enzymes (DNMT1, DNMT3A, and DNMT3B) and one cofactor (DNMT3L). Here, we describe the discovery of Dnmt3C, a de novo DNA methyltransferase gene that evolved via a duplication of Dnmt3B in rodent genomes and was previously annotated as a pseudogene. We show that DNMT3C is the enzyme responsible for methylating the promoters of evolutionarily young retrotransposons in the male germ line and that this specialized activity is required for mouse fertility. DNMT3C reveals the plasticity of the mammalian DNA methylation system and expands the scope of the mechanisms involved in the epigenetic control of retrotransposons.
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                Author and article information

                Contributors
                lucie.marandel@inrae.fr
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                22 January 2020
                22 January 2020
                2020
                : 10
                Affiliations
                [1 ]ISNI 0000 0001 2289 818X, GRID grid.5571.6, INRAE, Univ Pau & Pays de l′Adour, E2S-UPPA, UMR1419 Nutrition Metabolism and Aquaculture, Aquapôle, ; F-64310 Saint-Pée-sur-Nivelle, France
                [2 ]ISNI 0000 0004 1792 6029, GRID grid.429211.d, State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, ; Wuhan, Hubei 430072 China
                [3 ]ISNI 0000 0004 1797 8419, GRID grid.410726.6, University of Chinese Academy of Sciences, ; Beijing, 100049 China
                Article
                57753
                10.1038/s41598-020-57753-w
                6976628
                31969623
                © The Author(s) 2020

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                Funding
                Funded by: FundRef https://doi.org/10.13039/501100004543, China Scholarship Council (CSC);
                Award ID: 201506330063
                Award Recipient :
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                © The Author(s) 2020

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                phylogeny, molecular evolution, gene expression

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