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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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Centromere loss impacts DNA methylation in A. thaliana.A) Orthologous genes, anchored on the C. rubella genome, were used to calculate several statistics to investigate the impact of centromere loss on DNA methylation in A. thaliana. Capsella rubella centromeres 2, 4, and 8 (grey boxes) were lost during chromosomal fusion events that occurred on the branch leading to A. thaliana. Gene density, repeat density, and methylation densities were calculated for a 20 Kb window centered on the midpoint of each orthologous gene (10 kb up- and 10 kb downstream). Gene density and repeat density were calculated as fractions of each 20 kb window annotated as either a gene (ATG to STOP) or a repeat. Methylation densities were calculated as fractions of cytosines methylated in each context. Gene body methylation and gene expression (RPKM) were calculated for each ortholog. Gene body methylation was calculated as the fraction of methylated CG sites in a gene (ATG to STOP). Gene expression data from all samples within a species were used to calculate the RPKM values. For each statistic, local linear regression was performed to smooth the data in 250 kb bins. Smoothing parameter was relative to chromosome length.
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pgen-1004785-g003: Centromere loss impacts DNA methylation in A. thaliana.A) Orthologous genes, anchored on the C. rubella genome, were used to calculate several statistics to investigate the impact of centromere loss on DNA methylation in A. thaliana. Capsella rubella centromeres 2, 4, and 8 (grey boxes) were lost during chromosomal fusion events that occurred on the branch leading to A. thaliana. Gene density, repeat density, and methylation densities were calculated for a 20 Kb window centered on the midpoint of each orthologous gene (10 kb up- and 10 kb downstream). Gene density and repeat density were calculated as fractions of each 20 kb window annotated as either a gene (ATG to STOP) or a repeat. Methylation densities were calculated as fractions of cytosines methylated in each context. Gene body methylation and gene expression (RPKM) were calculated for each ortholog. Gene body methylation was calculated as the fraction of methylated CG sites in a gene (ATG to STOP). Gene expression data from all samples within a species were used to calculate the RPKM values. For each statistic, local linear regression was performed to smooth the data in 250 kb bins. Smoothing parameter was relative to chromosome length.

Mentions: Arabidopsis thaliana lost three centromeres relative to A. lyrata and C. rubella, and this loss has been estimated to account for about 10% of the genome size reduction in A. thaliana[46]. Using orthologous genes, it is possible to reconstruct the gene, repeat, and methylation density using the ancestral chromosome positions (Fig. 3). As expected, repeat density and cytosine methylation next to these degraded centromeres is reduced in A. thaliana, while gene density is higher (Fig. 3). Particularly notable is the decrease in CG gene body methylation (Fig. 3). Although gene body methylation is positively correlated with gene expression in several species [6], [7], [14], [15], [16], gene expression is not noticeably different in these regions between the three species (Fig. 3). Thus, the elimination of centromeres has had a measurable impact on repeat and methylation distribution in A. thaliana, but did not strongly affect the expression of ancestrally pericentromeric genes.


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)

Centromere loss impacts DNA methylation in A. thaliana.A) Orthologous genes, anchored on the C. rubella genome, were used to calculate several statistics to investigate the impact of centromere loss on DNA methylation in A. thaliana. Capsella rubella centromeres 2, 4, and 8 (grey boxes) were lost during chromosomal fusion events that occurred on the branch leading to A. thaliana. Gene density, repeat density, and methylation densities were calculated for a 20 Kb window centered on the midpoint of each orthologous gene (10 kb up- and 10 kb downstream). Gene density and repeat density were calculated as fractions of each 20 kb window annotated as either a gene (ATG to STOP) or a repeat. Methylation densities were calculated as fractions of cytosines methylated in each context. Gene body methylation and gene expression (RPKM) were calculated for each ortholog. Gene body methylation was calculated as the fraction of methylated CG sites in a gene (ATG to STOP). Gene expression data from all samples within a species were used to calculate the RPKM values. For each statistic, local linear regression was performed to smooth the data in 250 kb bins. Smoothing parameter was relative to chromosome length.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1004785-g003: Centromere loss impacts DNA methylation in A. thaliana.A) Orthologous genes, anchored on the C. rubella genome, were used to calculate several statistics to investigate the impact of centromere loss on DNA methylation in A. thaliana. Capsella rubella centromeres 2, 4, and 8 (grey boxes) were lost during chromosomal fusion events that occurred on the branch leading to A. thaliana. Gene density, repeat density, and methylation densities were calculated for a 20 Kb window centered on the midpoint of each orthologous gene (10 kb up- and 10 kb downstream). Gene density and repeat density were calculated as fractions of each 20 kb window annotated as either a gene (ATG to STOP) or a repeat. Methylation densities were calculated as fractions of cytosines methylated in each context. Gene body methylation and gene expression (RPKM) were calculated for each ortholog. Gene body methylation was calculated as the fraction of methylated CG sites in a gene (ATG to STOP). Gene expression data from all samples within a species were used to calculate the RPKM values. For each statistic, local linear regression was performed to smooth the data in 250 kb bins. Smoothing parameter was relative to chromosome length.
Mentions: Arabidopsis thaliana lost three centromeres relative to A. lyrata and C. rubella, and this loss has been estimated to account for about 10% of the genome size reduction in A. thaliana[46]. Using orthologous genes, it is possible to reconstruct the gene, repeat, and methylation density using the ancestral chromosome positions (Fig. 3). As expected, repeat density and cytosine methylation next to these degraded centromeres is reduced in A. thaliana, while gene density is higher (Fig. 3). Particularly notable is the decrease in CG gene body methylation (Fig. 3). Although gene body methylation is positively correlated with gene expression in several species [6], [7], [14], [15], [16], gene expression is not noticeably different in these regions between the three species (Fig. 3). Thus, the elimination of centromeres has had a measurable impact on repeat and methylation distribution in A. thaliana, but did not strongly affect the expression of ancestrally pericentromeric genes.

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