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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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Related in: MedlinePlus

Impact of repeat expansion on DNA methylation at genomic features.A) Feature annotation of all cytosines and methylated cytosines. Annotations are shown for all three contexts. B) Genome average of methylation rates for each genomic feature. Methylation rates are normalized to the outgroup species C. rubella. C) Fraction of intron bases annotated as transposable element or other repeat sequence. D) Total number of intron bases (millions) that are annotated as a particular transposable element class. E) Methylation rate distribution across gene bodies of orthologous genes and flanking sequences (1.5 kb up - and downstream). Orthologs that lacked methylation in both their gene body and flanking sequences were excluded. Distributions are plotted by context.
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pgen-1004785-g002: Impact of repeat expansion on DNA methylation at genomic features.A) Feature annotation of all cytosines and methylated cytosines. Annotations are shown for all three contexts. B) Genome average of methylation rates for each genomic feature. Methylation rates are normalized to the outgroup species C. rubella. C) Fraction of intron bases annotated as transposable element or other repeat sequence. D) Total number of intron bases (millions) that are annotated as a particular transposable element class. E) Methylation rate distribution across gene bodies of orthologous genes and flanking sequences (1.5 kb up - and downstream). Orthologs that lacked methylation in both their gene body and flanking sequences were excluded. Distributions are plotted by context.

Mentions: Global patterns of DNA methylation in A. lyrata and C. rubella are similar to those reported before for A. thaliana, with highest levels in regions near the centromeres, which are populated by TEs and repeats, but contain few genes [6], [14], [15] (Fig. 1). There is little correlation between DNA methylation density and gene expression at the 500 kb scale (Fig. 1). Centromeric regions are plagued with TEs, and as expected, methylation is found preferentially at sites annotated as residing in TEs (Fig. 2A). Methylation at CHG and CHH sites, which account for over half of methylated sites in all three species, occurs almost exclusively in TEs (Fig. 2A).


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)

Impact of repeat expansion on DNA methylation at genomic features.A) Feature annotation of all cytosines and methylated cytosines. Annotations are shown for all three contexts. B) Genome average of methylation rates for each genomic feature. Methylation rates are normalized to the outgroup species C. rubella. C) Fraction of intron bases annotated as transposable element or other repeat sequence. D) Total number of intron bases (millions) that are annotated as a particular transposable element class. E) Methylation rate distribution across gene bodies of orthologous genes and flanking sequences (1.5 kb up - and downstream). Orthologs that lacked methylation in both their gene body and flanking sequences were excluded. Distributions are plotted by context.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1004785-g002: Impact of repeat expansion on DNA methylation at genomic features.A) Feature annotation of all cytosines and methylated cytosines. Annotations are shown for all three contexts. B) Genome average of methylation rates for each genomic feature. Methylation rates are normalized to the outgroup species C. rubella. C) Fraction of intron bases annotated as transposable element or other repeat sequence. D) Total number of intron bases (millions) that are annotated as a particular transposable element class. E) Methylation rate distribution across gene bodies of orthologous genes and flanking sequences (1.5 kb up - and downstream). Orthologs that lacked methylation in both their gene body and flanking sequences were excluded. Distributions are plotted by context.
Mentions: Global patterns of DNA methylation in A. lyrata and C. rubella are similar to those reported before for A. thaliana, with highest levels in regions near the centromeres, which are populated by TEs and repeats, but contain few genes [6], [14], [15] (Fig. 1). There is little correlation between DNA methylation density and gene expression at the 500 kb scale (Fig. 1). Centromeric regions are plagued with TEs, and as expected, methylation is found preferentially at sites annotated as residing in TEs (Fig. 2A). Methylation at CHG and CHH sites, which account for over half of methylated sites in all three species, occurs almost exclusively in TEs (Fig. 2A).

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