Function and Evolution of DNA Methylation in Nasonia vitripennis
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{"title"=>"Function and Evolution of DNA Methylation in Nasonia vitripennis", "type"=>"journal", "authors"=>[{"first_name"=>"Xu", "last_name"=>"Wang", "scopus_author_id"=>"55988974100"}, {"first_name"=>"David", "last_name"=>"Wheeler", "scopus_author_id"=>"56425045400"}, {"first_name"=>"Amanda", "last_name"=>"Avery", "scopus_author_id"=>"55819951300"}, {"first_name"=>"Alfredo", "last_name"=>"Rago", "scopus_author_id"=>"55920940300"}, {"first_name"=>"Jeong Hyeon", "last_name"=>"Choi", "scopus_author_id"=>"12807976600"}, {"first_name"=>"John K.", "last_name"=>"Colbourne", "scopus_author_id"=>"7005213323"}, {"first_name"=>"Andrew G.", "last_name"=>"Clark", "scopus_author_id"=>"7404479646"}, {"first_name"=>"John H.", "last_name"=>"Werren", "scopus_author_id"=>"7006624294"}], "year"=>2013, "source"=>"PLoS Genetics", "identifiers"=>{"pui"=>"370217931", "issn"=>"15537390", "isbn"=>"1553-7404 (Electronic) 1553-7390 (Linking)", "doi"=>"10.1371/journal.pgen.1003872", "scopus"=>"2-s2.0-84887312009", "pmid"=>"24130511", "sgr"=>"84887312009"}, "id"=>"d6aad7fe-cb89-3a9e-b777-11841c9130b6", "abstract"=>"The parasitoid wasp Nasonia vitripennis is an emerging genetic model for functional analysis of DNA methylation. Here, we characterize genome-wide methylation at a base-pair resolution, and compare these results to gene expression across five developmental stages and to methylation patterns reported in other insects. An accurate assessment of DNA methylation across the genome is accomplished using bisulfite sequencing of adult females from a highly inbred line. One-third of genes show extensive methylation over the gene body, yet methylated DNA is not found in non-coding regions and rarely in transposons. Methylated genes occur in small clusters across the genome. Methylation demarcates exon-intron boundaries, with elevated levels over exons, primarily in the 5' regions of genes. It is also elevated near the sites of translational initiation and termination, with reduced levels in 5' and 3' UTRs. Methylated genes have higher median expression levels and lower expression variation across development stages than non-methylated genes. There is no difference in frequency of differential splicing between methylated and non-methylated genes, and as yet no established role for methylation in regulating alternative splicing in Nasonia. Phylogenetic comparisons indicate that many genes maintain methylation status across long evolutionary time scales. Nasonia methylated genes are more likely to be conserved in insects, but even those that are not conserved show broader expression across development than comparable non-methylated genes. Finally, examination of duplicated genes shows that those paralogs that have lost methylation in the Nasonia lineage following gene duplication evolve more rapidly, show decreased median expression levels, and increased specialization in expression across development. Methylation of Nasonia genes signals constitutive transcription across developmental stages, whereas non-methylated genes show more dynamic developmental expression patterns. We speculate that loss of methylation may result in increased developmental specialization in evolution and acquisition of methylation may lead to broader constitutive expression.", "link"=>"http://www.mendeley.com/research/function-evolution-dna-methylation-nasonia-vitripennis-1", "reader_count"=>108, "reader_count_by_academic_status"=>{"Unspecified"=>4, "Professor > Associate Professor"=>5, "Researcher"=>28, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>38, "Student > Postgraduate"=>2, "Student > Master"=>10, "Other"=>2, "Student > Bachelor"=>10, "Lecturer"=>1, "Professor"=>5}, "reader_count_by_user_role"=>{"Unspecified"=>4, "Professor > Associate Professor"=>5, "Researcher"=>28, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>38, "Student > Postgraduate"=>2, "Student > Master"=>10, "Other"=>2, "Student > Bachelor"=>10, "Lecturer"=>1, "Professor"=>5}, "reader_count_by_subject_area"=>{"Unspecified"=>6, "Environmental Science"=>3, "Biochemistry, Genetics and Molecular Biology"=>16, "Agricultural and Biological Sciences"=>81, "Neuroscience"=>1, "Physics and Astronomy"=>1}, "reader_count_by_subdiscipline"=>{"Neuroscience"=>{"Neuroscience"=>1}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>81}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>16}, "Unspecified"=>{"Unspecified"=>6}, "Environmental Science"=>{"Environmental Science"=>3}}, "reader_count_by_country"=>{"Netherlands"=>3, "Hungary"=>1, "United States"=>7, "Japan"=>1, "Brazil"=>1, "Australia"=>1, "Portugal"=>1, "Germany"=>1, "India"=>1}, "group_count"=>3}

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  • {"files"=>["https://ndownloader.figshare.com/files/1231658"], "description"=>"<p>(A) Distributions across genomic features for all 14 million CpG sites (Top left), 8 million covered CpG sites (Top middle) and methylated CpG sites (mCpGs, Top right). Plotted in the bottom panel are the distributions for percentage of mCpGs and methylation percentage at covered CpG sites. (B) Percentage of mCpGs in the 1 kbp upstream, 1 kbp downstream, UTR and intronic regions for methylated (blue), non-methylated (red) and all genes (purple). (C) Percentage of mCpGs in introns for methylated (blue), non-methylated (red) and all genes (purple), binned by the nearest distance to the exon-intron junctions. (D) Percentage of mCpGs across exons for methylated (blue), non-methylated (red) and all genes (purple). (E) Percentage of mCpGs in the coding region starting from first codon for methylated (blue), non-methylated (red) and all genes (purple). (F) Methylation level in 1 kbp upstream, 1 kbp 5′-UTR, first 2 kbp coding, 1 kbp 3′-UTR and 1 kbp downstream regions for 1,540 expressed transposable element genes (TE genes) and 16,186 non-TE genes. Dark blue line: percentage of mCpGs for non-TE genes; light blue line: average methylation percentage across covered CpGs for non-TE genes; red line: percentage of mCpGs for TE genes. (G) Methylation level in 1 kbp upstream, 1 kbp 5′-UTR, first 2 kbp coding, 1 kbp 3′-UTR and 1 kbp downstream regions for 4,751 methylated non-TE genes and 12,975 non-methylated non-TE genes. Dark blue line: percentage of mCpGs for methylated genes; light blue line: average methylation percentage across covered CpGs for methylated genes; red line: percentage of mCpGs for non-methylated genes. (H–I) Plot of Percentage of methylated CpG sites in the 5′UTR, the first four exons and introns (H) and 3′UTR, the last four exons and introns (I) for methylated (blue) and non-methylated genes (red). All exons, introns and UTRs were rescaled to the same length.</p>", "links"=>[], "tags"=>["cpg", "dna", "methylation", "genome", "protein-coding"], "article_id"=>819152, "categories"=>["Biological Sciences"], "users"=>["Xu Wang", "David Wheeler", "Amanda Avery", "Alfredo Rago", "Jeong-Hyeon Choi", "John K. Colbourne", "Andrew G. Clark", "John H. Werren"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003872.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Distribution_of_CpG_DNA_methylation_in_the_Nasonia_genome_across_protein_coding_genes_/819152", "title"=>"Distribution of CpG DNA methylation in the <i>Nasonia</i> genome across protein-coding genes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-10 06:25:57"}
  • {"files"=>["https://ndownloader.figshare.com/files/1231670"], "description"=>"<p>(A) Scatterplot for gene length (log<sub>10</sub>) and percentage of methylated CpG sites for methylation genes in the entire transcript region (left) and in 5′ 1 kbp coding region (right). The fitted lines using non-parametric local regression are shown in red. (B) Left: Distance between neighboring methylated genes (MM), non-methylated genes (NN) and methylated-non-methylated genes (MN or NM). The expected distributions for the three classes calculated by permuting the methylation status (N = 5,000) were plotted (MM: blue; NN: red; MN or NM: purple). The observed mean distance for each group was shown using arrows. Right: Distribution of the distance for the four classes (MM, NN, MN and NM). (C) Distribution of observed (orange) and expected (blue) counts for consecutive run of methylated genes. The expected counts were computed assuming the methylation status is randomly distributed.</p>", "links"=>[], "tags"=>["methylation", "exon"], "article_id"=>819155, "categories"=>["Biological Sciences"], "users"=>["Xu Wang", "David Wheeler", "Amanda Avery", "Alfredo Rago", "Jeong-Hyeon Choi", "John K. Colbourne", "Andrew G. Clark", "John H. Werren"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003872.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_DNA_methylation_and_gene_length_exon_number_and_gene_locations_/819155", "title"=>"DNA methylation and gene length, exon number and gene locations.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-10 06:25:57"}
  • {"files"=>["https://ndownloader.figshare.com/files/1231675"], "description"=>"<p>(A) Distribution of RNA-seq expression level (log<sub>10</sub> FPKM) in adult female for methylated (blue), non-methylated (red) and all genes (purple). (B) Distribution of RNA-seq expression level (log<sub>10</sub> FPKM) in adult female for groups of genes binned by percentage of methylated CpG sites in 5′ 1 kbp coding region. Red: non-methylation genes; blue: methylated genes. (C) Histograms for distribution of expression coefficient of variation (log<sub>10</sub> expression CV) in five developmental stages (early embryo, late embryo, larvae, pupae and adult) for methylated (blue), non-methylated (red) and all genes (purple). (D) Distribution of expression breadth measurement (log<sub>10</sub> expression CV) in six developmental stages for groups of genes binned by percentage of methylated CpG sites in 5′ 1 kbp coding region. Red: non-methylation genes; blue: methylated genes. (E) Scatterplot of expression breadth (log<sub>2</sub> expression CV) on y-axis against median expression level (log<sub>2</sub> signal intensity) in tiling array on x-axis, color-coded by adult female methylation status (blue: methylated genes; red: non-methylated genes). Fitted lines using non-parametric local regression are shown for methylated and non-methylated genes respectively. (F) Top right panel: Stacked barplot for expressed methylated and non-methylated genes with 0 to 6 expressed stages. Red: unmethylation genes; blue: methylated genes. Top left and bottom panel: boxplot for distribution of adult female RNA-seq expression level (log<sub>10</sub> FPKM) for methylated (in blue), non-methylated (in red) and all genes (in purple) expressed in 0–5 developmental stages.</p>", "links"=>[], "tags"=>[], "article_id"=>819160, "categories"=>["Biological Sciences"], "users"=>["Xu Wang", "David Wheeler", "Amanda Avery", "Alfredo Rago", "Jeong-Hyeon Choi", "John K. Colbourne", "Andrew G. Clark", "John H. Werren"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003872.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_DNA_methylation_gene_expression_and_expression_breadth_/819160", "title"=>"DNA methylation, gene expression and expression breadth.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-10 06:25:57"}
  • {"files"=>["https://ndownloader.figshare.com/files/1231681"], "description"=>"<p>(A) Counts of alternatively spliced and non-alternatively spliced genes with different methylation status from OGS2 gene models (left) and RNA-seq data (right). AS: alternatively spliced; nAS: non-alternatively spliced. Methylated is shown in blue and non-methylated shown in red. (B) Distribution of fraction of major spliced forms for alternatively spliced methylated (blue) and non-methylated genes (red). (C) Gene expression, DNA methylation and alternative splicing profile for a non-methylated gene Nasvi2EG003411. Plotted at the top is the IGV browser screenshot showing adult female RNA-seq coverage (on log scale) and read alignments in the gene region. Plotted at the bottom are the CpG methylation profile at covered CpG sites from WGBS-seq data and the exon model of the alternatively spliced transcripts from OGS2 gene models. A vertical bar was drawn for each CpG at its position in the gene, color-coded by the methylation percentage in proportion to the bar length (blue: methylated Cs; red: non-methylated Cs). All 587 covered CpGs in the gene region were non-methylated. Two of the three OGS2 transcript variants, Nasvi2EG003411t1 (labelled as t1) and Nasvi2EG003411t3 (labelled as t3), were covered in the RNA-seq data with 47% and 41% of the transcript abundance, respectively. Two of the remaining minor transcript variants (other1 and other2) were also plotted.</p>", "links"=>[], "tags"=>["methylation"], "article_id"=>819164, "categories"=>["Biological Sciences"], "users"=>["Xu Wang", "David Wheeler", "Amanda Avery", "Alfredo Rago", "Jeong-Hyeon Choi", "John K. Colbourne", "Andrew G. Clark", "John H. Werren"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003872.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_DNA_methylation_and_alternative_splicing_/819164", "title"=>"DNA methylation and alternative splicing.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-10 06:25:57"}
  • {"files"=>["https://ndownloader.figshare.com/files/1231684"], "description"=>"<p>(A) Phylogenetic tree of eight insect species: <i>Nasonia vitripennis</i>, <i>Apis mellifera</i>, <i>Tribolium castaneum</i>, <i>Bombyx mori</i>, <i>Anopheles gambiae</i>, <i>Drosophila melanogaster</i>, <i>Pediculus humanus</i> and <i>Acyrthosiphon pisum</i>. The methylation status and correlating factors were plotted in (B–F) for four groups of genes: all 5,039 <i>Nasonia</i> single-copy genes with one or zero ortholog in seven other insect species, 2,374 genes with one orthologs in all eight insect species, 443 genes with one orthologs in <i>Apis</i> and <i>Nasonia</i> but missing in other six species, and 320 genes present only in <i>Nasonia</i>. The <i>y</i>-axes plotted in (B–F) are (B): proportion of methylated (blue) and non-methylated genes (red); (C): percentage of methylated CpG sites in methylated genes; (D): adult RNA-seq expression levels (log<sub>10</sub>FPKM); (E): coefficient of variation of expression level in tiling array across six developmental stages; (F): number of expressed tissues. (G) Top: Phylogenetic tree of three <i>Nasonia</i> species: <i>N. longicornis</i> (L), <i>N. giraulti</i> (G) and <i>N. vitripennis</i> (V). Bottom: boxplots of nucleotide substitution rates between V–L, V–G and L–G.</p>", "links"=>[], "tags"=>["methylation"], "article_id"=>819167, "categories"=>["Biological Sciences"], "users"=>["Xu Wang", "David Wheeler", "Amanda Avery", "Alfredo Rago", "Jeong-Hyeon Choi", "John K. Colbourne", "Andrew G. Clark", "John H. Werren"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003872.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_DNA_methylation_and_gene_conservation_/819167", "title"=>"DNA methylation and gene conservation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-10 06:25:57"}
  • {"files"=>["https://ndownloader.figshare.com/files/1231687"], "description"=>"<p>Differences between two paralogs that have changed in methylation status in the Nasonia lineage are shown. (A) Comparisons of expression pattern across developmental stages for duplicated genes in the <i>Nasonia</i> lineage where one gene is methylated (M) and the other lost methylation (N). These genes have 1∶1 orthologs in other hymenopteran species, and the ortholog is methylated in <i>Apis</i>. (B) Those paralogs that lost methylation show significant reductions in median expression level across development relative to the M paralog (N–M), significant increases in the range of expression level (N–M), and significantly greater divergence from the <i>Apis</i> ortholog (N–M).</p>", "links"=>[], "tags"=>[], "article_id"=>819170, "categories"=>["Biological Sciences"], "users"=>["Xu Wang", "David Wheeler", "Amanda Avery", "Alfredo Rago", "Jeong-Hyeon Choi", "John K. Colbourne", "Andrew G. Clark", "John H. Werren"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003872.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Paralog_analysis_/819170", "title"=>"Paralog analysis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-10 06:25:57"}
  • {"files"=>["https://ndownloader.figshare.com/files/1231688"], "description"=>"<p>mCpG: methylated CpG sites; mC: methylated cytosines.</p>", "links"=>[], "tags"=>["dna", "methylation", "cpg", "islands", "methylated"], "article_id"=>819171, "categories"=>["Biological Sciences"], "users"=>["Xu Wang", "David Wheeler", "Amanda Avery", "Alfredo Rago", "Jeong-Hyeon Choi", "John K. Colbourne", "Andrew G. Clark", "John H. Werren"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003872.t001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Summary_of_DNA_methylation_status_for_CpG_islands_and_methylated_CpG_clusters_/819171", "title"=>"Summary of DNA methylation status for CpG islands and methylated CpG clusters.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-10-10 06:25:57"}
  • {"files"=>["https://ndownloader.figshare.com/files/1231705", "https://ndownloader.figshare.com/files/1231706", "https://ndownloader.figshare.com/files/1231707", "https://ndownloader.figshare.com/files/1231708", "https://ndownloader.figshare.com/files/1231709", "https://ndownloader.figshare.com/files/1231710", "https://ndownloader.figshare.com/files/1231711", "https://ndownloader.figshare.com/files/1231712", "https://ndownloader.figshare.com/files/1231713", "https://ndownloader.figshare.com/files/1231714", "https://ndownloader.figshare.com/files/1231715", "https://ndownloader.figshare.com/files/1231716", "https://ndownloader.figshare.com/files/1231717", "https://ndownloader.figshare.com/files/1231718", "https://ndownloader.figshare.com/files/1231719", "https://ndownloader.figshare.com/files/1231720", "https://ndownloader.figshare.com/files/1231721", "https://ndownloader.figshare.com/files/1231722", "https://ndownloader.figshare.com/files/1231723", "https://ndownloader.figshare.com/files/1231724", "https://ndownloader.figshare.com/files/1231725", "https://ndownloader.figshare.com/files/1231726", "https://ndownloader.figshare.com/files/1231727", "https://ndownloader.figshare.com/files/1231728", "https://ndownloader.figshare.com/files/1231729", "https://ndownloader.figshare.com/files/1231730", "https://ndownloader.figshare.com/files/1231731", "https://ndownloader.figshare.com/files/1231732", "https://ndownloader.figshare.com/files/1231733", "https://ndownloader.figshare.com/files/1231734", "https://ndownloader.figshare.com/files/1231735", "https://ndownloader.figshare.com/files/1231736", "https://ndownloader.figshare.com/files/1231737", "https://ndownloader.figshare.com/files/1231738", "https://ndownloader.figshare.com/files/1231739", "https://ndownloader.figshare.com/files/1231740", "https://ndownloader.figshare.com/files/1231741", "https://ndownloader.figshare.com/files/1231742", "https://ndownloader.figshare.com/files/1231743", "https://ndownloader.figshare.com/files/1231744", "https://ndownloader.figshare.com/files/1231745", "https://ndownloader.figshare.com/files/1231746", "https://ndownloader.figshare.com/files/1231747", "https://ndownloader.figshare.com/files/1231748", "https://ndownloader.figshare.com/files/1231749", "https://ndownloader.figshare.com/files/1231750", "https://ndownloader.figshare.com/files/1231751", "https://ndownloader.figshare.com/files/1231752", "https://ndownloader.figshare.com/files/1231753", "https://ndownloader.figshare.com/files/1231754"], "description"=>"<div><p>The parasitoid wasp <i>Nasonia vitripennis</i> is an emerging genetic model for functional analysis of DNA methylation. Here, we characterize genome-wide methylation at a base-pair resolution, and compare these results to gene expression across five developmental stages and to methylation patterns reported in other insects. An accurate assessment of DNA methylation across the genome is accomplished using bisulfite sequencing of adult females from a highly inbred line. One-third of genes show extensive methylation over the gene body, yet methylated DNA is not found in non-coding regions and rarely in transposons. Methylated genes occur in small clusters across the genome. Methylation demarcates exon-intron boundaries, with elevated levels over exons, primarily in the 5′ regions of genes. It is also elevated near the sites of translational initiation and termination, with reduced levels in 5′ and 3′ UTRs. Methylated genes have higher median expression levels and lower expression variation across development stages than non-methylated genes. There is no difference in frequency of differential splicing between methylated and non-methylated genes, and as yet no established role for methylation in regulating alternative splicing in <i>Nasonia</i>. Phylogenetic comparisons indicate that many genes maintain methylation status across long evolutionary time scales. <i>Nasonia</i> methylated genes are more likely to be conserved in insects, but even those that are not conserved show broader expression across development than comparable non-methylated genes. Finally, examination of duplicated genes shows that those paralogs that have lost methylation in the <i>Nasonia</i> lineage following gene duplication evolve more rapidly, show decreased median expression levels, and increased specialization in expression across development. Methylation of <i>Nasonia</i> genes signals constitutive transcription across developmental stages, whereas non-methylated genes show more dynamic developmental expression patterns. We speculate that loss of methylation may result in increased developmental specialization in evolution and acquisition of methylation may lead to broader constitutive expression.</p></div>", "links"=>[], "tags"=>["dna", "methylation"], "article_id"=>819184, "categories"=>["Biological Sciences"], "users"=>["Xu Wang", "David Wheeler", "Amanda Avery", "Alfredo Rago", "Jeong-Hyeon Choi", "John K. Colbourne", "Andrew G. Clark", "John H. Werren"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003872.s001", "https://dx.doi.org/10.1371/journal.pgen.1003872.s002", "https://dx.doi.org/10.1371/journal.pgen.1003872.s003", "https://dx.doi.org/10.1371/journal.pgen.1003872.s004", "https://dx.doi.org/10.1371/journal.pgen.1003872.s005", "https://dx.doi.org/10.1371/journal.pgen.1003872.s006", "https://dx.doi.org/10.1371/journal.pgen.1003872.s007", "https://dx.doi.org/10.1371/journal.pgen.1003872.s008", "https://dx.doi.org/10.1371/journal.pgen.1003872.s009", "https://dx.doi.org/10.1371/journal.pgen.1003872.s010", "https://dx.doi.org/10.1371/journal.pgen.1003872.s011", "https://dx.doi.org/10.1371/journal.pgen.1003872.s012", "https://dx.doi.org/10.1371/journal.pgen.1003872.s013", "https://dx.doi.org/10.1371/journal.pgen.1003872.s014", "https://dx.doi.org/10.1371/journal.pgen.1003872.s015", "https://dx.doi.org/10.1371/journal.pgen.1003872.s016", "https://dx.doi.org/10.1371/journal.pgen.1003872.s017", "https://dx.doi.org/10.1371/journal.pgen.1003872.s018", "https://dx.doi.org/10.1371/journal.pgen.1003872.s019", "https://dx.doi.org/10.1371/journal.pgen.1003872.s020", "https://dx.doi.org/10.1371/journal.pgen.1003872.s021", "https://dx.doi.org/10.1371/journal.pgen.1003872.s022", "https://dx.doi.org/10.1371/journal.pgen.1003872.s023", "https://dx.doi.org/10.1371/journal.pgen.1003872.s024", "https://dx.doi.org/10.1371/journal.pgen.1003872.s025", "https://dx.doi.org/10.1371/journal.pgen.1003872.s026", "https://dx.doi.org/10.1371/journal.pgen.1003872.s027", "https://dx.doi.org/10.1371/journal.pgen.1003872.s028", "https://dx.doi.org/10.1371/journal.pgen.1003872.s029", "https://dx.doi.org/10.1371/journal.pgen.1003872.s030", "https://dx.doi.org/10.1371/journal.pgen.1003872.s031", "https://dx.doi.org/10.1371/journal.pgen.1003872.s032", "https://dx.doi.org/10.1371/journal.pgen.1003872.s033", "https://dx.doi.org/10.1371/journal.pgen.1003872.s034", "https://dx.doi.org/10.1371/journal.pgen.1003872.s035", "https://dx.doi.org/10.1371/journal.pgen.1003872.s036", "https://dx.doi.org/10.1371/journal.pgen.1003872.s037", "https://dx.doi.org/10.1371/journal.pgen.1003872.s038", "https://dx.doi.org/10.1371/journal.pgen.1003872.s039", "https://dx.doi.org/10.1371/journal.pgen.1003872.s040", "https://dx.doi.org/10.1371/journal.pgen.1003872.s041", "https://dx.doi.org/10.1371/journal.pgen.1003872.s042", "https://dx.doi.org/10.1371/journal.pgen.1003872.s043", "https://dx.doi.org/10.1371/journal.pgen.1003872.s044", "https://dx.doi.org/10.1371/journal.pgen.1003872.s045", "https://dx.doi.org/10.1371/journal.pgen.1003872.s046", "https://dx.doi.org/10.1371/journal.pgen.1003872.s047", "https://dx.doi.org/10.1371/journal.pgen.1003872.s048", "https://dx.doi.org/10.1371/journal.pgen.1003872.s049", "https://dx.doi.org/10.1371/journal.pgen.1003872.s050"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Function_and_Evolution_of_DNA_Methylation_in_Nasonia_vitripennis_/819184", "title"=>"Function and Evolution of DNA Methylation in <i>Nasonia vitripennis</i>", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-10-10 06:25:57"}

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Relative Metric

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