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      Identification and caste-dependent expression patterns of DNA methylation associated genes in Bombus terrestris

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          Abstract

          DNA methylation has been proposed to play critical roles in caste fate and behavioral plasticity in bumblebees, however, there is little information on its regulatory mechanisms. Here, we identified six important genes mediating the modification of DNA methylation and determined their expression patterns in the bumblebee Bombus terrestris. There is a complete functional DNA methylation system, including four DNA methyltransferases (DNMT1a, DNMT1b, DNMT2, and DNMT3), a DNA demethylase (Ten-eleven translocation), and a methyl-CpG-binding domain protein in B. terrestris. Most of these genes were highly expressed in fat bodies and gonads but lowly expressed in antennae and brains of bumblebee adults. Besides, these genes exhibited caste-specific expression patterns in bumblebees, with higher transcription levels in queens than workers and drones. Whereas their expression levels showed no remarkable difference in queenright and queenless workers. These results suggested potential roles of DNA methylation-related genes in caste differentiation in bumblebees.

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          Most cited references41

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          TET enzymes, TDG and the dynamics of DNA demethylation.

          DNA methylation has a profound impact on genome stability, transcription and development. Although enzymes that catalyse DNA methylation have been well characterized, those that are involved in methyl group removal have remained elusive, until recently. The transformative discovery that ten-eleven translocation (TET) family enzymes can oxidize 5-methylcytosine has greatly advanced our understanding of DNA demethylation. 5-Hydroxymethylcytosine is a key nexus in demethylation that can either be passively depleted through DNA replication or actively reverted to cytosine through iterative oxidation and thymine DNA glycosylase (TDG)-mediated base excision repair. Methylation, oxidation and repair now offer a model for a complete cycle of dynamic cytosine modification, with mounting evidence for its significance in the biological processes known to involve active demethylation.
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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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              Gene body-specific methylation on the active X chromosome.

              Differential DNA methylation is important for the epigenetic regulation of gene expression. Allele-specific methylation of the inactive X chromosome has been demonstrated at promoter CpG islands, but the overall pattern of methylation on the active X(Xa) and inactive X (Xi) chromosomes is unknown. We performed allele-specific analysis of more than 1000 informative loci along the human X chromosome. The Xa displays more than two times as much allele-specific methylation as Xi. This methylation is concentrated at gene bodies, affecting multiple neighboring CpGs. Before X inactivation, all of these Xa gene body-methylated sites are biallelically methylated. Thus, a bipartite methylation-demethylation program results in Xa-specific hypomethylation at gene promoters and hypermethylation at gene bodies. These results suggest a relationship between global methylation and expression potentiality.
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                Author and article information

                Contributors
                anshiheng@aliyun.com
                wangxh@ioz.ac.cn
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                5 February 2018
                5 February 2018
                2018
                : 8
                : 2332
                Affiliations
                [1 ]GRID grid.108266.b, College of Plant Protection, , Henan Agricultural University, ; Zhengzhou, 450002 China
                [2 ]ISNI 0000000119573309, GRID grid.9227.e, Institute of Zoology, , Chinese Academy of Sciences, ; Beijing, 100101 China
                [3 ]ISNI 0000 0004 0646 9053, GRID grid.418260.9, Institute of Plant and Environment Protection, , Beijing Academy of Agriculture and Forestry Sciences, ; Beijing, 100097 China
                Article
                20831
                10.1038/s41598-018-20831-1
                5799256
                29402971
                1ca357b9-5f43-4048-b17d-e9f3c454f8aa
                © The Author(s) 2018

                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/.

                History
                : 4 July 2017
                : 24 January 2018
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