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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.


a Genome-wide methylation levels were correlated with repeat numbers for mCG (blue) and mCHG (green), but not for mCHH (maroon). Significant relationships are indicated. b Distribution of methylation levels for repeats in each species. c Patterns of methylation upstream, across, and downstream of repeats for mCG (blue), mCHG (green), and mCHH (maroon)
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Fig3: a Genome-wide methylation levels were correlated with repeat numbers for mCG (blue) and mCHG (green), but not for mCHH (maroon). Significant relationships are indicated. b Distribution of methylation levels for repeats in each species. c Patterns of methylation upstream, across, and downstream of repeats for mCG (blue), mCHG (green), and mCHH (maroon)

Mentions: Genome-wide mCG and mCHG levels are related to the proliferation of repetitive elements. The extent which heterochromatin and repeats are represented among the genomes studied does vary with the completeness of the assembled genomes. Despite this, however, correlations were found between repeat number and mCG (p value = 3.0 × 10–2) and mCHG levels (p value = 4.9 × 10–4) (Fig. 3a, Additional file 1: Table S3). This likely explains the correlation of DNA methylation with genome size, as large genomes often have more repetitive elements [71, 72]. No such correlation between mCHH levels and repeat numbers was found (p value = 1) (Fig. 3a). This was unexpected given that mCHH is generally associated with repetitive sequences in many plant species [32, 73]. Both CDS mCHG and mCHH correlated with the total number of repeats (p value = 8.7 × 10–3, p value = 1.5 × 10–2, respectively), but CDS mCG did not (p value = 1) (Additional file 3: Figure S15A). CDS mCHG and mCHH were also correlated with the presence of repeats within gene bodies (exons, introns, and untranslated regions: mCHG p value = 1.6 × 10–3, mCHH p value = 2.0 × 10–3), whereas mCG was not (p value = 1) (Additional files 1 and 3: Table S3 and Figure S15b). Plotting the percentage of genes containing repeats against the total number of repeats showed a relationship between the percentage of repeat content in genes and total number of repeats (p value = 2.4 × 10–6) (Additional file 3: Figure S15C). After Z. mays, B. vulgaris has the highest percentage of genes containing repeats, much more so than expected given the total repeat content. This may explain in part why it has the highest CDS methylation levels.Fig. 3


Widespread natural variation of DNA methylation within angiosperms
a Genome-wide methylation levels were correlated with repeat numbers for mCG (blue) and mCHG (green), but not for mCHH (maroon). Significant relationships are indicated. b Distribution of methylation levels for repeats in each species. c Patterns of methylation upstream, across, and downstream of repeats for mCG (blue), mCHG (green), and mCHH (maroon)
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Fig3: a Genome-wide methylation levels were correlated with repeat numbers for mCG (blue) and mCHG (green), but not for mCHH (maroon). Significant relationships are indicated. b Distribution of methylation levels for repeats in each species. c Patterns of methylation upstream, across, and downstream of repeats for mCG (blue), mCHG (green), and mCHH (maroon)
Mentions: Genome-wide mCG and mCHG levels are related to the proliferation of repetitive elements. The extent which heterochromatin and repeats are represented among the genomes studied does vary with the completeness of the assembled genomes. Despite this, however, correlations were found between repeat number and mCG (p value = 3.0 × 10–2) and mCHG levels (p value = 4.9 × 10–4) (Fig. 3a, Additional file 1: Table S3). This likely explains the correlation of DNA methylation with genome size, as large genomes often have more repetitive elements [71, 72]. No such correlation between mCHH levels and repeat numbers was found (p value = 1) (Fig. 3a). This was unexpected given that mCHH is generally associated with repetitive sequences in many plant species [32, 73]. Both CDS mCHG and mCHH correlated with the total number of repeats (p value = 8.7 × 10–3, p value = 1.5 × 10–2, respectively), but CDS mCG did not (p value = 1) (Additional file 3: Figure S15A). CDS mCHG and mCHH were also correlated with the presence of repeats within gene bodies (exons, introns, and untranslated regions: mCHG p value = 1.6 × 10–3, mCHH p value = 2.0 × 10–3), whereas mCG was not (p value = 1) (Additional files 1 and 3: Table S3 and Figure S15b). Plotting the percentage of genes containing repeats against the total number of repeats showed a relationship between the percentage of repeat content in genes and total number of repeats (p value = 2.4 × 10–6) (Additional file 3: Figure S15C). After Z. mays, B. vulgaris has the highest percentage of genes containing repeats, much more so than expected given the total repeat content. This may explain in part why it has the highest CDS methylation levels.Fig. 3

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.