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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 Methylation levels for mCG (blue) (mCG only in coding sequences), mCHG (green) (mCG and mCHG in coding sequences), and mCHH (maroon) (mCG, mCHG, and mCHH in coding sequences) were plotted upstream, across, and downstream of mCHG and mCHH genes. b Gene expression of mCHG and mCHH genes vs. all genes. c The percentage of mCHG and mCHH genes per species. Species are arranged by phylogenetic relationship
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Fig5: a Methylation levels for mCG (blue) (mCG only in coding sequences), mCHG (green) (mCG and mCHG in coding sequences), and mCHH (maroon) (mCG, mCHG, and mCHH in coding sequences) were plotted upstream, across, and downstream of mCHG and mCHH genes. b Gene expression of mCHG and mCHH genes vs. all genes. c The percentage of mCHG and mCHH genes per species. Species are arranged by phylogenetic relationship

Mentions: Non-CG methylation exists within genes and is known to suppress gene expression [16, 18, 77–79]. Differences in annotation quality could lead to some transposons being misannotated as genes and thus as targets of non-CG methylation. However, work in both A. thaliana and G. max have shown that some percentage of protein-coding genes do indeed contain non-CG methylation [3, 12]. In many species there were genes with significant amounts of mCHG and little to no mCHH. High levels of mCHG within Z. mays genes is known to occur, especially in intronic sequences due in part to the presence of transposons [80]. Based on this difference in DNA methylation, mCHG and mCHH genes were maintained as separate categories (Additional files 4 and 5: Table S4). The DNA methylation profiles of mCHG and mCHH genes often resembled that of repeats (Fig. 5a, Additional file 3: Figure S18). Both mCHG and mCHH genes are associated with reduced expression levels (Fig. 5b, Additional file 3: Figure S19). As mCHG methylation is present in mCHH genes, this may indicate that mCHG alone is sufficient for reduced gene expression. It was also observed that Cucumis sativus has an unusual pattern of mCHH in many highly expressed genes, although this pattern was not observed in a second C. sativus sample and will require further study to understand the basis for this difference (Additional file 3: Figure S20). The number of genes possessing non-CG types of DNA methylation ranged from as low as ~3 % of genes (M. esculenta) to as high as ~32 % of genes (F. vesca) (Fig. 5c). In all the Poaceae, mCHG genes made up at least ~5 % of genes and typically more. In contrast, mCHG genes were relatively rare in the Brassicaceae where mCHH genes were the predominant type of non-CG genes.Fig. 5


Widespread natural variation of DNA methylation within angiosperms
a Methylation levels for mCG (blue) (mCG only in coding sequences), mCHG (green) (mCG and mCHG in coding sequences), and mCHH (maroon) (mCG, mCHG, and mCHH in coding sequences) were plotted upstream, across, and downstream of mCHG and mCHH genes. b Gene expression of mCHG and mCHH genes vs. all genes. c The percentage of mCHG and mCHH genes per species. Species are arranged by phylogenetic relationship
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC5037628&req=5

Fig5: a Methylation levels for mCG (blue) (mCG only in coding sequences), mCHG (green) (mCG and mCHG in coding sequences), and mCHH (maroon) (mCG, mCHG, and mCHH in coding sequences) were plotted upstream, across, and downstream of mCHG and mCHH genes. b Gene expression of mCHG and mCHH genes vs. all genes. c The percentage of mCHG and mCHH genes per species. Species are arranged by phylogenetic relationship
Mentions: Non-CG methylation exists within genes and is known to suppress gene expression [16, 18, 77–79]. Differences in annotation quality could lead to some transposons being misannotated as genes and thus as targets of non-CG methylation. However, work in both A. thaliana and G. max have shown that some percentage of protein-coding genes do indeed contain non-CG methylation [3, 12]. In many species there were genes with significant amounts of mCHG and little to no mCHH. High levels of mCHG within Z. mays genes is known to occur, especially in intronic sequences due in part to the presence of transposons [80]. Based on this difference in DNA methylation, mCHG and mCHH genes were maintained as separate categories (Additional files 4 and 5: Table S4). The DNA methylation profiles of mCHG and mCHH genes often resembled that of repeats (Fig. 5a, Additional file 3: Figure S18). Both mCHG and mCHH genes are associated with reduced expression levels (Fig. 5b, Additional file 3: Figure S19). As mCHG methylation is present in mCHH genes, this may indicate that mCHG alone is sufficient for reduced gene expression. It was also observed that Cucumis sativus has an unusual pattern of mCHH in many highly expressed genes, although this pattern was not observed in a second C. sativus sample and will require further study to understand the basis for this difference (Additional file 3: Figure S20). The number of genes possessing non-CG types of DNA methylation ranged from as low as ~3 % of genes (M. esculenta) to as high as ~32 % of genes (F. vesca) (Fig. 5c). In all the Poaceae, mCHG genes made up at least ~5 % of genes and typically more. In contrast, mCHG genes were relatively rare in the Brassicaceae where mCHH genes were the predominant type of non-CG genes.Fig. 5

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.