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      DNA Methylation Patterns in the Social Spider, Stegodyphus dumicola

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      Genes
      MDPI
      DNA methylation, gene expression, epigenetics

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          Abstract

          Variation in DNA methylation patterns among genes, individuals, and populations appears to be highly variable among taxa, but our understanding of the functional significance of this variation is still incomplete. We here present the first whole genome bisulfite sequencing of a chelicerate species, the social spider Stegodyphus dumicola. We show that DNA methylation occurs mainly in CpG context and is concentrated in genes. This is a pattern also documented in other invertebrates. We present RNA sequence data to investigate the role of DNA methylation in gene regulation and show that, within individuals, methylated genes are more expressed than genes that are not methylated and that methylated genes are more stably expressed across individuals than unmethylated genes. Although no causal association is shown, this lends support for the implication of DNA CpG methylation in regulating gene expression in invertebrates. Differential DNA methylation between populations showed a small but significant correlation with differential gene expression. This is consistent with a possible role of DNA methylation in local adaptation. Based on indirect inference of the presence and pattern of DNA methylation in chelicerate species whose genomes have been sequenced, we performed a comparative phylogenetic analysis. We found strong evidence for exon DNA methylation in the horseshoe crab Limulus polyphemus and in all spider and scorpion species, while most Parasitiformes and Acariformes species seem to have lost DNA methylation.

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          Most cited references37

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          Highly expressed genes in yeast evolve slowly.

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            The alternative role of DNA methylation in splicing regulation.

            Although DNA methylation was originally thought to only affect transcription, emerging evidence shows that it also regulates alternative splicing. Exons, and especially splice sites, have higher levels of DNA methylation than flanking introns, and the splicing of about 22% of alternative exons is regulated by DNA methylation. Two different mechanisms convey DNA methylation information into the regulation of alternative splicing. The first involves modulation of the elongation rate of RNA polymerase II (Pol II) by CCCTC-binding factor (CTCF) and methyl-CpG binding protein 2 (MeCP2); the second involves the formation of a protein bridge by heterochromatin protein 1 (HP1) that recruits splicing factors onto transcribed alternative exons. These two mechanisms, however, regulate only a fraction of such events, implying that more underlying mechanisms remain to be found.
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              Single base-resolution methylome of the silkworm reveals a sparse epigenomic map.

              Epigenetic regulation in insects may have effects on diverse biological processes. Here we survey the methylome of a model insect, the silkworm Bombyx mori, at single-base resolution using Illumina high-throughput bisulfite sequencing (MethylC-Seq). We conservatively estimate that 0.11% of genomic cytosines are methylcytosines, all of which probably occur in CG dinucleotides. CG methylation is substantially enriched in gene bodies and is positively correlated with gene expression levels, suggesting it has a positive role in gene transcription. We find that transposable elements, promoters and ribosomal DNAs are hypomethylated, but in contrast, genomic loci matching small RNAs in gene bodies are densely methylated. This work contributes to our understanding of epigenetics in insects, and in contrast to previous studies of the highly methylated genomes of Arabidopsis and human, demonstrates a strategy for sequencing the epigenomes of organisms such as insects that have low levels of methylation.
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                Author and article information

                Journal
                Genes (Basel)
                Genes (Basel)
                genes
                Genes
                MDPI
                2073-4425
                12 February 2019
                February 2019
                : 10
                : 2
                : 137
                Affiliations
                Department of Bioscience, Aarhus University, 8000 Aarhus C, Denmark; Liu.Shenglin@ 123456bios.au.dk (S.L.); anneaagaard@ 123456bios.au.dk (A.A.); Jesper.Bechsgaard@ 123456bios.au.dk (J.B.)
                Author notes
                [* ]Correspondence: Trine.Bilde@ 123456bios.au.dk ; Tel.: +45-87156565
                Author information
                https://orcid.org/0000-0003-3273-0174
                https://orcid.org/0000-0002-0341-161X
                Article
                genes-10-00137
                10.3390/genes10020137
                6409797
                30759892
                4e98712e-c97a-41f1-b2f1-d226791b52ca
                © 2019 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 11 December 2018
                : 25 January 2019
                Categories
                Article

                dna methylation,gene expression,epigenetics
                dna methylation, gene expression, epigenetics

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