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Widespread natural variation of DNA methylation within angiosperms

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.


a Genome-wide methylation levels are correlated to genome size for mCG (blue) and mCHG (green), but not for mCHH (maroon). Significant relationships are indicated. b Coding region (CDS) methylation levels is not correlated to genome size for mCG (blue), but is for mCHG (green) and mCHH (maroon). Significant relationships are indicated. cChromosome plots show the distribution of mCG (blue), mCHG (green), and mCHH (maroon) across the chromosome (100 kb windows) in relationship to genes. d For each species, the correlation (Pearson’s correlation) in 100 kb windows between gene number and mCG (blue), mCHG (green), and mCHH (maroon)
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Fig2: a Genome-wide methylation levels are correlated to genome size for mCG (blue) and mCHG (green), but not for mCHH (maroon). Significant relationships are indicated. b Coding region (CDS) methylation levels is not correlated to genome size for mCG (blue), but is for mCHG (green) and mCHH (maroon). Significant relationships are indicated. cChromosome plots show the distribution of mCG (blue), mCHG (green), and mCHH (maroon) across the chromosome (100 kb windows) in relationship to genes. d For each species, the correlation (Pearson’s correlation) in 100 kb windows between gene number and mCG (blue), mCHG (green), and mCHH (maroon)

Mentions: DNA methylation is often associated with heterochromatin. Two factors can drive increases in genome size, whole genome duplication (WGD) events, and in the copy number for repetitive elements. The majority of changes in genome size among the species we examined are due to changes in repeat content as the total gene number in these species only varies two-fold, whereas the genome size exhibits ~8.5-fold change. As genomes increase in size due to increased repeat content, it is expected that DNA methylation levels will increase as well. This was tested using phylogenetic generalized least squares (PGLS) [68] which takes into account the phylogenetic relationship and non-independence of species as more closely related species are more alike (Additional file 1: Table S3). Phylogenetic relationships were inferred from a species tree constructed using 50 single copy loci for use in PGLS (Additional file 1: Figure S8) [69]. A previous report had found a relationship between total methylation and genome size, but did not take into account the sequence context of that methylation [70]. Positive correlations were found between mCG and genome size (p value = 2.9 × 10–3) and between mCHG and genome size (p value = 2.2 × 10–6) (Fig. 2a), but no correlation was found with mCHH and genome size (Fig. 2a). This dataset was limited to one larger genome greater than 2 Gb, Z. mays, so we tested the effect that this had on the results. After removal of Z. mays, genome-wide mCHG methylation remained correlated with genome size, whereas mCG and mCHH showed no correlation (Additional file 1: Figure S9).Fig. 2


Widespread natural variation of DNA methylation within angiosperms
a Genome-wide methylation levels are correlated to genome size for mCG (blue) and mCHG (green), but not for mCHH (maroon). Significant relationships are indicated. b Coding region (CDS) methylation levels is not correlated to genome size for mCG (blue), but is for mCHG (green) and mCHH (maroon). Significant relationships are indicated. cChromosome plots show the distribution of mCG (blue), mCHG (green), and mCHH (maroon) across the chromosome (100 kb windows) in relationship to genes. d For each species, the correlation (Pearson’s correlation) in 100 kb windows between gene number and mCG (blue), mCHG (green), and mCHH (maroon)
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Related In: Results  -  Collection

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Fig2: a Genome-wide methylation levels are correlated to genome size for mCG (blue) and mCHG (green), but not for mCHH (maroon). Significant relationships are indicated. b Coding region (CDS) methylation levels is not correlated to genome size for mCG (blue), but is for mCHG (green) and mCHH (maroon). Significant relationships are indicated. cChromosome plots show the distribution of mCG (blue), mCHG (green), and mCHH (maroon) across the chromosome (100 kb windows) in relationship to genes. d For each species, the correlation (Pearson’s correlation) in 100 kb windows between gene number and mCG (blue), mCHG (green), and mCHH (maroon)
Mentions: DNA methylation is often associated with heterochromatin. Two factors can drive increases in genome size, whole genome duplication (WGD) events, and in the copy number for repetitive elements. The majority of changes in genome size among the species we examined are due to changes in repeat content as the total gene number in these species only varies two-fold, whereas the genome size exhibits ~8.5-fold change. As genomes increase in size due to increased repeat content, it is expected that DNA methylation levels will increase as well. This was tested using phylogenetic generalized least squares (PGLS) [68] which takes into account the phylogenetic relationship and non-independence of species as more closely related species are more alike (Additional file 1: Table S3). Phylogenetic relationships were inferred from a species tree constructed using 50 single copy loci for use in PGLS (Additional file 1: Figure S8) [69]. A previous report had found a relationship between total methylation and genome size, but did not take into account the sequence context of that methylation [70]. Positive correlations were found between mCG and genome size (p value = 2.9 × 10–3) and between mCHG and genome size (p value = 2.2 × 10–6) (Fig. 2a), but no correlation was found with mCHH and genome size (Fig. 2a). This dataset was limited to one larger genome greater than 2 Gb, Z. mays, so we tested the effect that this had on the results. After removal of Z. mays, genome-wide mCHG methylation remained correlated with genome size, whereas mCG and mCHH showed no correlation (Additional file 1: Figure S9).Fig. 2

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.