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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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Conservation of methylated regions (MR).A) Annotation of all bases in MRs. B) Fraction of bases in MRs that occur either within or outside of the three-way whole genome alignments. C) Fraction of MR bases found within three-way whole genome alignments that occur in one, two, or three species. D) Conservation of MRs in the absence of sequence alignments. The total number of orthologous genes overlapping an MR in one, two, or three species is given, with location of MR overlap separated by genomic feature. Upstream region was defined as 1 kb before the start codon. Asterisk indicates two or three-way sharing of MRs that exceeds permutation values.
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pgen-1004785-g004: Conservation of methylated regions (MR).A) Annotation of all bases in MRs. B) Fraction of bases in MRs that occur either within or outside of the three-way whole genome alignments. C) Fraction of MR bases found within three-way whole genome alignments that occur in one, two, or three species. D) Conservation of MRs in the absence of sequence alignments. The total number of orthologous genes overlapping an MR in one, two, or three species is given, with location of MR overlap separated by genomic feature. Upstream region was defined as 1 kb before the start codon. Asterisk indicates two or three-way sharing of MRs that exceeds permutation values.

Mentions: Methylation of plant genomes is driven to a large extent by TEs, which are silenced via either the sRNA-mediated RdDM pathway [36] or the RdDM-independent pathway which relies on DDM1 [38]. Using a Hidden Markov Model algorithm, we identified methylated regions (MR) in each genome, which have a median length of 300 to 530 bp and cover between 26 and 73 Mb (Table S4). MRs are preferentially found in heterochromatic sequence next to centromeres, as they are enriched for TEs (Fig. S4, Fig. 4A). Since TEs are rapidly turned over, we expected MRs to be only poorly conserved. To test this assumption, we identified nearly 60 Mb of sequences with a 1∶1∶1 relationship in whole-genome alignments (Table S5) [47]. Less than 1% of the MR space is contained in the alignable portion of the genomes (Fig. 4B). In the rare cases where an MR spans alignable sequences, such sequences are almost always methylated in only one of the three species (Fig. 4C). We conclude that DNA methylation targets primarily the variable portion of the genome, which is subject to species-specific expansion and contraction of TEs.


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)

Conservation of methylated regions (MR).A) Annotation of all bases in MRs. B) Fraction of bases in MRs that occur either within or outside of the three-way whole genome alignments. C) Fraction of MR bases found within three-way whole genome alignments that occur in one, two, or three species. D) Conservation of MRs in the absence of sequence alignments. The total number of orthologous genes overlapping an MR in one, two, or three species is given, with location of MR overlap separated by genomic feature. Upstream region was defined as 1 kb before the start codon. Asterisk indicates two or three-way sharing of MRs that exceeds permutation values.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1004785-g004: Conservation of methylated regions (MR).A) Annotation of all bases in MRs. B) Fraction of bases in MRs that occur either within or outside of the three-way whole genome alignments. C) Fraction of MR bases found within three-way whole genome alignments that occur in one, two, or three species. D) Conservation of MRs in the absence of sequence alignments. The total number of orthologous genes overlapping an MR in one, two, or three species is given, with location of MR overlap separated by genomic feature. Upstream region was defined as 1 kb before the start codon. Asterisk indicates two or three-way sharing of MRs that exceeds permutation values.
Mentions: Methylation of plant genomes is driven to a large extent by TEs, which are silenced via either the sRNA-mediated RdDM pathway [36] or the RdDM-independent pathway which relies on DDM1 [38]. Using a Hidden Markov Model algorithm, we identified methylated regions (MR) in each genome, which have a median length of 300 to 530 bp and cover between 26 and 73 Mb (Table S4). MRs are preferentially found in heterochromatic sequence next to centromeres, as they are enriched for TEs (Fig. S4, Fig. 4A). Since TEs are rapidly turned over, we expected MRs to be only poorly conserved. To test this assumption, we identified nearly 60 Mb of sequences with a 1∶1∶1 relationship in whole-genome alignments (Table S5) [47]. Less than 1% of the MR space is contained in the alignable portion of the genomes (Fig. 4B). In the rare cases where an MR spans alignable sequences, such sequences are almost always methylated in only one of the three species (Fig. 4C). We conclude that DNA methylation targets primarily the variable portion of the genome, which is subject to species-specific expansion and contraction of TEs.

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