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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 in DNA methylation.A) Fraction of mC that are variable between either tissue (root and shoot) or treatment (23°C and 4°C) comparisons. B) Fraction of DMRs that are variable between either tissue (root and shoot) or treatment (23°C and 4°C) comparisons. C) Fraction of DMPs in each context that reside either within a MR or DMR. D) Feature annotation of DMPs by context and DMR bases. E) Fraction of DMPs and DMR bases found within three-way whole genome alignments. F) Fraction of DMPs and DMR bases found within three-way whole genome alignments that occur in one, two, or three species.
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pgen-1004785-g008: Intraspecific variation in DNA methylation.A) Fraction of mC that are variable between either tissue (root and shoot) or treatment (23°C and 4°C) comparisons. B) Fraction of DMRs that are variable between either tissue (root and shoot) or treatment (23°C and 4°C) comparisons. C) Fraction of DMPs in each context that reside either within a MR or DMR. D) Feature annotation of DMPs by context and DMR bases. E) Fraction of DMPs and DMR bases found within three-way whole genome alignments. F) Fraction of DMPs and DMR bases found within three-way whole genome alignments that occur in one, two, or three species.

Mentions: To evaluate the degree to which within-species DNA methylation changes are conserved, we first estimated significant differential methylation at site and region levels. Four biologically appropriate comparisons were performed for each species to minimize multiple testing problems. Two tests identified differentially methylated positions (DMPs) between roots and shoots, and two tests identified DMPs between cold and control conditions regardless of tissue type. In each species, ten times as many DMPs were found between tissues than between treatments (Figure 8A, Table S11). Similar to DMPs, 20 to 50 times as many differentially methylated regions (DMRs) were detected between tissues than between treatments (Fig. 8B, Table S12).


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 in DNA methylation.A) Fraction of mC that are variable between either tissue (root and shoot) or treatment (23°C and 4°C) comparisons. B) Fraction of DMRs that are variable between either tissue (root and shoot) or treatment (23°C and 4°C) comparisons. C) Fraction of DMPs in each context that reside either within a MR or DMR. D) Feature annotation of DMPs by context and DMR bases. E) Fraction of DMPs and DMR bases found within three-way whole genome alignments. F) Fraction of DMPs and DMR bases found within three-way whole genome alignments that occur in one, two, or three species.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1004785-g008: Intraspecific variation in DNA methylation.A) Fraction of mC that are variable between either tissue (root and shoot) or treatment (23°C and 4°C) comparisons. B) Fraction of DMRs that are variable between either tissue (root and shoot) or treatment (23°C and 4°C) comparisons. C) Fraction of DMPs in each context that reside either within a MR or DMR. D) Feature annotation of DMPs by context and DMR bases. E) Fraction of DMPs and DMR bases found within three-way whole genome alignments. F) Fraction of DMPs and DMR bases found within three-way whole genome alignments that occur in one, two, or three species.
Mentions: To evaluate the degree to which within-species DNA methylation changes are conserved, we first estimated significant differential methylation at site and region levels. Four biologically appropriate comparisons were performed for each species to minimize multiple testing problems. Two tests identified differentially methylated positions (DMPs) between roots and shoots, and two tests identified DMPs between cold and control conditions regardless of tissue type. In each species, ten times as many DMPs were found between tissues than between treatments (Figure 8A, Table S11). Similar to DMPs, 20 to 50 times as many differentially methylated regions (DMRs) were detected between tissues than between treatments (Fig. 8B, Table S12).

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