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Widespread natural variation of DNA methylation within angiosperms

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ABSTRACT

Background: DNA methylation is an important feature of plant epigenomes, involved in the formation of heterochromatin and affecting gene expression. Extensive variation of DNA methylation patterns within a species has been uncovered from studies of natural variation. However, the extent to which DNA methylation varies between flowering plant species is still unclear. To understand the variation in genomic patterning of DNA methylation across flowering plant species, we compared single base resolution DNA methylomes of 34 diverse angiosperm species.

Results: By analyzing whole-genome bisulfite sequencing data in a phylogenetic context, it becomes clear that there is extensive variation throughout angiosperms in gene body DNA methylation, euchromatic silencing of transposons and repeats, as well as silencing of heterochromatic transposons. The Brassicaceae have reduced CHG methylation levels and also reduced or loss of CG gene body methylation. The Poaceae are characterized by a lack or reduction of heterochromatic CHH methylation and enrichment of CHH methylation in genic regions. Furthermore, low levels of CHH methylation are observed in a number of species, especially in clonally propagated species.

Conclusions: These results reveal the extent of variation in DNA methylation in angiosperms and show that DNA methylation patterns are broadly a reflection of the evolutionary and life histories of plant species.

Electronic supplementary material: The online version of this article (doi:10.1186/s13059-016-1059-0) contains supplementary material, which is available to authorized users.

No MeSH data available.


Genome-wide methylation levels for a mCG, b mCHG, and c mCHH. d Using the genome-wide methylation levels, the proportion that each context contributes towards the total methylation (mC) was calculated. e The distribution of per-site methylation levels for mCG, f mCHG, and g mCHH. Species are organized according to their phylogenetic relationship
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Fig1: Genome-wide methylation levels for a mCG, b mCHG, and c mCHH. d Using the genome-wide methylation levels, the proportion that each context contributes towards the total methylation (mC) was calculated. e The distribution of per-site methylation levels for mCG, f mCHG, and g mCHH. Species are organized according to their phylogenetic relationship

Mentions: We compared single-base resolution methylomes from the leaves of 34 angiosperm species that have genome assemblies [49–52] (Additional file 1: Table S1). MethylC-seq [40, 53] was used to sequence 26 species and an additional eight species with previously published methylomes were downloaded and reanalyzed [12, 15, 36, 48, 54–56]. Different metrics were used to make comparisons at a whole-genome level. The genome-wide weighted DNA methylation level [57] combines data from the number of instances of methylated cytosine sites relative to all sequenced cytosine sites, giving a single value for each context that can be compared across species (Fig. 1a–c). The proportion that each DNA methylation context makes up of all DNA methylation indicates the predominance of specific DNA methylation pathways (Fig. 1d). The per-site DNA methylation level is the distribution of DNA methylation levels at individual methylated sites and indicates within a population of cells, the proportion that are methylated (Fig. 1e–g, Additional file 1: Figure S1). Symmetry is a comparison of per-site DNA methylation levels at cytosines on the Watson versus the Crick strand for the symmetrical CG and CHG contexts (Additional file 1: Figures S2 and S3). As CMT3 is responsible for maintaining the symmetrical DNA methylation of CHG sites [27], we can use A. thaliana cmt3 mutants to establish thresholds with which to identify sites as symmetrical or asymmetrical and [58] quantify the asymmetry of mCHG sites (Additional file 1: Figure S4). Per-site DNA methylation and symmetry provide information into how well DNA methylation is maintained and how ubiquitously the sites are methylated across cell types within sequenced tissues [59].Fig. 1


Widespread natural variation of DNA methylation within angiosperms
Genome-wide methylation levels for a mCG, b mCHG, and c mCHH. d Using the genome-wide methylation levels, the proportion that each context contributes towards the total methylation (mC) was calculated. e The distribution of per-site methylation levels for mCG, f mCHG, and g mCHH. Species are organized according to their phylogenetic relationship
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC5037628&req=5

Fig1: Genome-wide methylation levels for a mCG, b mCHG, and c mCHH. d Using the genome-wide methylation levels, the proportion that each context contributes towards the total methylation (mC) was calculated. e The distribution of per-site methylation levels for mCG, f mCHG, and g mCHH. Species are organized according to their phylogenetic relationship
Mentions: We compared single-base resolution methylomes from the leaves of 34 angiosperm species that have genome assemblies [49–52] (Additional file 1: Table S1). MethylC-seq [40, 53] was used to sequence 26 species and an additional eight species with previously published methylomes were downloaded and reanalyzed [12, 15, 36, 48, 54–56]. Different metrics were used to make comparisons at a whole-genome level. The genome-wide weighted DNA methylation level [57] combines data from the number of instances of methylated cytosine sites relative to all sequenced cytosine sites, giving a single value for each context that can be compared across species (Fig. 1a–c). The proportion that each DNA methylation context makes up of all DNA methylation indicates the predominance of specific DNA methylation pathways (Fig. 1d). The per-site DNA methylation level is the distribution of DNA methylation levels at individual methylated sites and indicates within a population of cells, the proportion that are methylated (Fig. 1e–g, Additional file 1: Figure S1). Symmetry is a comparison of per-site DNA methylation levels at cytosines on the Watson versus the Crick strand for the symmetrical CG and CHG contexts (Additional file 1: Figures S2 and S3). As CMT3 is responsible for maintaining the symmetrical DNA methylation of CHG sites [27], we can use A. thaliana cmt3 mutants to establish thresholds with which to identify sites as symmetrical or asymmetrical and [58] quantify the asymmetry of mCHG sites (Additional file 1: Figure S4). Per-site DNA methylation and symmetry provide information into how well DNA methylation is maintained and how ubiquitously the sites are methylated across cell types within sequenced tissues [59].Fig. 1

View Article: PubMed Central - PubMed

ABSTRACT

Background: DNA methylation is an important feature of plant epigenomes, involved in the formation of heterochromatin and affecting gene expression. Extensive variation of DNA methylation patterns within a species has been uncovered from studies of natural variation. However, the extent to which DNA methylation varies between flowering plant species is still unclear. To understand the variation in genomic patterning of DNA methylation across flowering plant species, we compared single base resolution DNA methylomes of 34 diverse angiosperm species.

Results: By analyzing whole-genome bisulfite sequencing data in a phylogenetic context, it becomes clear that there is extensive variation throughout angiosperms in gene body DNA methylation, euchromatic silencing of transposons and repeats, as well as silencing of heterochromatic transposons. The Brassicaceae have reduced CHG methylation levels and also reduced or loss of CG gene body methylation. The Poaceae are characterized by a lack or reduction of heterochromatic CHH methylation and enrichment of CHH methylation in genic regions. Furthermore, low levels of CHH methylation are observed in a number of species, especially in clonally propagated species.

Conclusions: These results reveal the extent of variation in DNA methylation in angiosperms and show that DNA methylation patterns are broadly a reflection of the evolutionary and life histories of plant species.

Electronic supplementary material: The online version of this article (doi:10.1186/s13059-016-1059-0) contains supplementary material, which is available to authorized users.

No MeSH data available.