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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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Methylation rates at orthologs.A) Pairwise comparison of the average methylation rates at orthologs. Average methylation rate was calculated as the average of all CG sites in the feature, including non-methylated CG sites. Pairwise comparisons are shown for upstream regions (1.5 kb), gene bodies, and downstream regions (1.5 kb). Spearman rank correlation coefficient (ρ) is included for each comparison.
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pgen-1004785-g005: Methylation rates at orthologs.A) Pairwise comparison of the average methylation rates at orthologs. Average methylation rate was calculated as the average of all CG sites in the feature, including non-methylated CG sites. Pairwise comparisons are shown for upstream regions (1.5 kb), gene bodies, and downstream regions (1.5 kb). Spearman rank correlation coefficient (ρ) is included for each comparison.

Mentions: In contrast to RdDM of TEs and other repeats, the function of CG gene body methylation is still enigmatic, although it correlates positively with gene expression and negatively with mean normalized expression variance, or the coefficient of variation, across tissues and treatments (Fig. S5) [6], [7], [14], [15], [16], [17]. CG gene body methylation is found in the majority of genes (Table S9), and its rate is highly correlated between orthologs, while CG methylation up- and downstream of genes is much less correlated (Fig. 5).


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)

Methylation rates at orthologs.A) Pairwise comparison of the average methylation rates at orthologs. Average methylation rate was calculated as the average of all CG sites in the feature, including non-methylated CG sites. Pairwise comparisons are shown for upstream regions (1.5 kb), gene bodies, and downstream regions (1.5 kb). Spearman rank correlation coefficient (ρ) is included for each comparison.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4230842&req=5

pgen-1004785-g005: Methylation rates at orthologs.A) Pairwise comparison of the average methylation rates at orthologs. Average methylation rate was calculated as the average of all CG sites in the feature, including non-methylated CG sites. Pairwise comparisons are shown for upstream regions (1.5 kb), gene bodies, and downstream regions (1.5 kb). Spearman rank correlation coefficient (ρ) is included for each comparison.
Mentions: In contrast to RdDM of TEs and other repeats, the function of CG gene body methylation is still enigmatic, although it correlates positively with gene expression and negatively with mean normalized expression variance, or the coefficient of variation, across tissues and treatments (Fig. S5) [6], [7], [14], [15], [16], [17]. CG gene body methylation is found in the majority of genes (Table S9), and its rate is highly correlated between orthologs, while CG methylation up- and downstream of genes is much less correlated (Fig. 5).

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