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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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Intraspecific variation of transposon and gene body methylation.A) Comparison of the average methylation rates at annotated transposons and repeats between tissues (root and shoot) and treatments (23°C and 4°C). Average methylation rate is calculated as the average of methylation rates at all cytosines in the feature, including non-methylated cytosines. B) Methylation rate distribution across gene bodies of orthologous genes and flanking sequences (1.5 kb up- and 1.5 kb downstream). Orthologs that lacked methylation in both their gene body and flanking sequences are excluded. Distributions are plotted by context.
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pgen-1004785-g009: Intraspecific variation of transposon and gene body methylation.A) Comparison of the average methylation rates at annotated transposons and repeats between tissues (root and shoot) and treatments (23°C and 4°C). Average methylation rate is calculated as the average of methylation rates at all cytosines in the feature, including non-methylated cytosines. B) Methylation rate distribution across gene bodies of orthologous genes and flanking sequences (1.5 kb up- and 1.5 kb downstream). Orthologs that lacked methylation in both their gene body and flanking sequences are excluded. Distributions are plotted by context.

Mentions: Although DMPs and DMRs are not conserved across species, there is consistently more variability between root and shoot samples at a number of genomic features. Importantly, the methylation profile across transposons is quite different between tissues. Transposons are consistently more highly methylated in all sequence contexts in shoots (Fig. 9A). A similar trend is apparent for CHG and CHH sites in intergenic regions in A. lyrata, reflecting that TEs are closer to genes in this species (Fig. 9B) [46].


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)

Intraspecific variation of transposon and gene body methylation.A) Comparison of the average methylation rates at annotated transposons and repeats between tissues (root and shoot) and treatments (23°C and 4°C). Average methylation rate is calculated as the average of methylation rates at all cytosines in the feature, including non-methylated cytosines. B) Methylation rate distribution across gene bodies of orthologous genes and flanking sequences (1.5 kb up- and 1.5 kb downstream). Orthologs that lacked methylation in both their gene body and flanking sequences are excluded. Distributions are plotted by context.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1004785-g009: Intraspecific variation of transposon and gene body methylation.A) Comparison of the average methylation rates at annotated transposons and repeats between tissues (root and shoot) and treatments (23°C and 4°C). Average methylation rate is calculated as the average of methylation rates at all cytosines in the feature, including non-methylated cytosines. B) Methylation rate distribution across gene bodies of orthologous genes and flanking sequences (1.5 kb up- and 1.5 kb downstream). Orthologs that lacked methylation in both their gene body and flanking sequences are excluded. Distributions are plotted by context.
Mentions: Although DMPs and DMRs are not conserved across species, there is consistently more variability between root and shoot samples at a number of genomic features. Importantly, the methylation profile across transposons is quite different between tissues. Transposons are consistently more highly methylated in all sequence contexts in shoots (Fig. 9A). A similar trend is apparent for CHG and CHH sites in intergenic regions in A. lyrata, reflecting that TEs are closer to genes in this species (Fig. 9B) [46].

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