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Evolution of DNA methylation patterns in the Brassicaceae is driven by differences in genome organization.

Seymour DK, Koenig D, Hagmann J, Becker C, Weigel D - PLoS Genet. (2014)

Bottom Line: DNA methylation is an ancient molecular modification found in most eukaryotes.We found that the lineage-specific expansion and contraction of transposon and repeat sequences is the main driver of interspecific differences in DNA methylation.Outside of repeat-associated methylation, there is a surprising degree of conservation in methylation at single nucleotides located in gene bodies.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Biology, Max Planck Institute for Developmental Biology, Tübingen, Germany.

ABSTRACT
DNA methylation is an ancient molecular modification found in most eukaryotes. In plants, DNA methylation is not only critical for transcriptionally silencing transposons, but can also affect phenotype by altering expression of protein coding genes. The extent of its contribution to phenotypic diversity over evolutionary time is, however, unclear, because of limited stability of epialleles that are not linked to DNA mutations. To dissect the relative contribution of DNA methylation to transposon surveillance and host gene regulation, we leveraged information from three species in the Brassicaceae that vary in genome architecture, Capsella rubella, Arabidopsis lyrata, and Arabidopsis thaliana. We found that the lineage-specific expansion and contraction of transposon and repeat sequences is the main driver of interspecific differences in DNA methylation. The most heavily methylated portions of the genome are thus not conserved at the sequence level. Outside of repeat-associated methylation, there is a surprising degree of conservation in methylation at single nucleotides located in gene bodies. Finally, dynamic DNA methylation is affected more by tissue type than by environmental differences in all species, but these responses are not conserved. The majority of DNA methylation variation between species resides in hypervariable genomic regions, and thus, in the context of macroevolution, is of limited phenotypic consequence.

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Site-level comparison of methylation.A) Annotation of all cytosines within a species (covered C) compared to the annotation of cytosines found in the three-way whole genome alignments (aligned C). B) Total number of mC by context for aligned site classes. Site classes are as follows: mC - methylated sites within a species. Conserved (3 species) - sites that are methylated in all three species. Gain - sites that are methylated in a single species. Loss - sites that have lost methylation in a single species. C) Total number of conserved mC and non-conserved mC by context. D) Density plot describing the distribution of variable sites in the genome (10 kb windows). For each window the following statistic was calculated: species-specific methylation gains/sum of species-specific methylation gains and losses. E) Windows with a high density of gains have more transposons and repetitive sequences. Density of transposons plotted against density of methylation gains (10 kb window). F) Methylation gains are enriched at the beginning and end of genes. Fraction of mC in each site class is plotted by exon position in a gene.
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pgen-1004785-g006: Site-level comparison of methylation.A) Annotation of all cytosines within a species (covered C) compared to the annotation of cytosines found in the three-way whole genome alignments (aligned C). B) Total number of mC by context for aligned site classes. Site classes are as follows: mC - methylated sites within a species. Conserved (3 species) - sites that are methylated in all three species. Gain - sites that are methylated in a single species. Loss - sites that have lost methylation in a single species. C) Total number of conserved mC and non-conserved mC by context. D) Density plot describing the distribution of variable sites in the genome (10 kb windows). For each window the following statistic was calculated: species-specific methylation gains/sum of species-specific methylation gains and losses. E) Windows with a high density of gains have more transposons and repetitive sequences. Density of transposons plotted against density of methylation gains (10 kb window). F) Methylation gains are enriched at the beginning and end of genes. Fraction of mC in each site class is plotted by exon position in a gene.

Mentions: We used the cross-species alignments to identify 15.1 million conserved CG, CHG and CHH sites, which are located particularly in exons (Fig. 6A, Table S5). Although only a small portion, 2%, had significant methylation, most were shared between at least two species, with A. thaliana having the fewest methylated sites, reflecting the general decrease in global DNA methylation in this species (Fig. 6B–D, Table S10). Sites methylated in multiple species are further enriched in exons, with very few of these conserved sites being CHG or CHH sites (Fig. 6B,C, Fig. S6).


Evolution of DNA methylation patterns in the Brassicaceae is driven by differences in genome organization.

Seymour DK, Koenig D, Hagmann J, Becker C, Weigel D - PLoS Genet. (2014)

Site-level comparison of methylation.A) Annotation of all cytosines within a species (covered C) compared to the annotation of cytosines found in the three-way whole genome alignments (aligned C). B) Total number of mC by context for aligned site classes. Site classes are as follows: mC - methylated sites within a species. Conserved (3 species) - sites that are methylated in all three species. Gain - sites that are methylated in a single species. Loss - sites that have lost methylation in a single species. C) Total number of conserved mC and non-conserved mC by context. D) Density plot describing the distribution of variable sites in the genome (10 kb windows). For each window the following statistic was calculated: species-specific methylation gains/sum of species-specific methylation gains and losses. E) Windows with a high density of gains have more transposons and repetitive sequences. Density of transposons plotted against density of methylation gains (10 kb window). F) Methylation gains are enriched at the beginning and end of genes. Fraction of mC in each site class is plotted by exon position in a gene.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4230842&req=5

pgen-1004785-g006: Site-level comparison of methylation.A) Annotation of all cytosines within a species (covered C) compared to the annotation of cytosines found in the three-way whole genome alignments (aligned C). B) Total number of mC by context for aligned site classes. Site classes are as follows: mC - methylated sites within a species. Conserved (3 species) - sites that are methylated in all three species. Gain - sites that are methylated in a single species. Loss - sites that have lost methylation in a single species. C) Total number of conserved mC and non-conserved mC by context. D) Density plot describing the distribution of variable sites in the genome (10 kb windows). For each window the following statistic was calculated: species-specific methylation gains/sum of species-specific methylation gains and losses. E) Windows with a high density of gains have more transposons and repetitive sequences. Density of transposons plotted against density of methylation gains (10 kb window). F) Methylation gains are enriched at the beginning and end of genes. Fraction of mC in each site class is plotted by exon position in a gene.
Mentions: We used the cross-species alignments to identify 15.1 million conserved CG, CHG and CHH sites, which are located particularly in exons (Fig. 6A, Table S5). Although only a small portion, 2%, had significant methylation, most were shared between at least two species, with A. thaliana having the fewest methylated sites, reflecting the general decrease in global DNA methylation in this species (Fig. 6B–D, Table S10). Sites methylated in multiple species are further enriched in exons, with very few of these conserved sites being CHG or CHH sites (Fig. 6B,C, Fig. S6).

Bottom Line: DNA methylation is an ancient molecular modification found in most eukaryotes.We found that the lineage-specific expansion and contraction of transposon and repeat sequences is the main driver of interspecific differences in DNA methylation.Outside of repeat-associated methylation, there is a surprising degree of conservation in methylation at single nucleotides located in gene bodies.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Biology, Max Planck Institute for Developmental Biology, Tübingen, Germany.

ABSTRACT
DNA methylation is an ancient molecular modification found in most eukaryotes. In plants, DNA methylation is not only critical for transcriptionally silencing transposons, but can also affect phenotype by altering expression of protein coding genes. The extent of its contribution to phenotypic diversity over evolutionary time is, however, unclear, because of limited stability of epialleles that are not linked to DNA mutations. To dissect the relative contribution of DNA methylation to transposon surveillance and host gene regulation, we leveraged information from three species in the Brassicaceae that vary in genome architecture, Capsella rubella, Arabidopsis lyrata, and Arabidopsis thaliana. We found that the lineage-specific expansion and contraction of transposon and repeat sequences is the main driver of interspecific differences in DNA methylation. The most heavily methylated portions of the genome are thus not conserved at the sequence level. Outside of repeat-associated methylation, there is a surprising degree of conservation in methylation at single nucleotides located in gene bodies. Finally, dynamic DNA methylation is affected more by tissue type than by environmental differences in all species, but these responses are not conserved. The majority of DNA methylation variation between species resides in hypervariable genomic regions, and thus, in the context of macroevolution, is of limited phenotypic consequence.

Show MeSH
Related in: MedlinePlus