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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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Species gene expression and mC relationships.A) Principal component analysis on fitted gene expression values (log2) and B) mC rates at aligned methylated positions. All contexts are considered (see Fig. 6B,C and Table S10 for further description of mC sites).
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pgen-1004785-g007: Species gene expression and mC relationships.A) Principal component analysis on fitted gene expression values (log2) and B) mC rates at aligned methylated positions. All contexts are considered (see Fig. 6B,C and Table S10 for further description of mC sites).

Mentions: Because several studies have shown that DNA methylation can change between tissues and in response to external stimuli [19], [20], we wanted to address whether these responses are conserved. Principal component analysis on the four types of samples, control shoots, cold-treated shoots, control roots and cold-treated roots, for all three species according to global RNA-seq measurements revealed that tissue is the most important factor, with over 7,000 genes being differentially expressed between roots and shoots (Fig. 7A, S11). Tissue-specific differences in gene expression are the largest source of expression variance in this data set (Fig. 7A). In contrast, species is the most important factor for differences in DNA methylation and explains 80% of the variance in our data (Fig. 7B, Fig. S12). Moreover, PC2 places A. lyrata closest to C. rubella instead of its congener A. thaliana, reflecting the methylation losses in A. thaliana (Fig. 7B).


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)

Species gene expression and mC relationships.A) Principal component analysis on fitted gene expression values (log2) and B) mC rates at aligned methylated positions. All contexts are considered (see Fig. 6B,C and Table S10 for further description of mC sites).
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1004785-g007: Species gene expression and mC relationships.A) Principal component analysis on fitted gene expression values (log2) and B) mC rates at aligned methylated positions. All contexts are considered (see Fig. 6B,C and Table S10 for further description of mC sites).
Mentions: Because several studies have shown that DNA methylation can change between tissues and in response to external stimuli [19], [20], we wanted to address whether these responses are conserved. Principal component analysis on the four types of samples, control shoots, cold-treated shoots, control roots and cold-treated roots, for all three species according to global RNA-seq measurements revealed that tissue is the most important factor, with over 7,000 genes being differentially expressed between roots and shoots (Fig. 7A, S11). Tissue-specific differences in gene expression are the largest source of expression variance in this data set (Fig. 7A). In contrast, species is the most important factor for differences in DNA methylation and explains 80% of the variance in our data (Fig. 7B, Fig. S12). Moreover, PC2 places A. lyrata closest to C. rubella instead of its congener A. thaliana, reflecting the methylation losses in A. thaliana (Fig. 7B).

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