Limits...
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.


Related in: MedlinePlus

aHeatmap showing methylation state of orthologous genes (horizontal axis) to A. thaliana for each species (vertical axis). Species are organized according to phylogenetic relationship. b Percentage of genes in each species that are gbM (mCG only in coding sequences). The Brassicaceae are highlighted in gold. c The levels of mCG in upstream, across, and downstream of gbM genes for all species. Species in gold belong to the Brassicaceae and illustrate the decreased levels and loss of mCG. d gbM genes are more highly expressed, whereas mCG over the TSS (mCG-TSS) has reduced gene expression
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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

Fig4: aHeatmap showing methylation state of orthologous genes (horizontal axis) to A. thaliana for each species (vertical axis). Species are organized according to phylogenetic relationship. b Percentage of genes in each species that are gbM (mCG only in coding sequences). The Brassicaceae are highlighted in gold. c The levels of mCG in upstream, across, and downstream of gbM genes for all species. Species in gold belong to the Brassicaceae and illustrate the decreased levels and loss of mCG. d gbM genes are more highly expressed, whereas mCG over the TSS (mCG-TSS) has reduced gene expression

Mentions: Between species, the DNA methylation status of gbM can be conserved across orthologs [46]. The DNA methylation state of orthologous genes across all species was compared using A. thaliana as an anchor (Fig. 4a). A. lyrata and C. rubella are the most closely related to A. thaliana and also have the greatest conservation of DNA methylation status, with many A. thaliana gbM gene orthologs also being gbM genes in these species (~86.3 % and ~79.8 % of A. thaliana gbM genes, respectively). However, they also had many gbM genes that had unmethylated A. thaliana orthologs (~18.6 % and ~13.9 % of A. thaliana genes, respectively). Although gbM is generally “conserved” between species, this conservation breaks down over evolutionary distance with gains and losses of gbM in different lineages. In terms of total number of gbM genes, M. truncatula and Mimulus guttatus had the greatest number (Additional file 2: Table S2). However, when the percentage of gbM genes in the genome is taken into account (Fig. 4b), M. truncatula appeared similar to other species, whereas M. guttatus remained an outlier with ~60.7 % of all genes classified as gbM genes. The reason why M. guttatus has unusually large numbers of gbM loci is unknown and will require further investigation. In contrast, there has been considerable loss of gbM genes in Brassica rapa and Brassica oleracea, and a complete loss in E. salsugineum. This suggests that over longer evolutionary distance, the DNA methylation status of gbM varies considerably and is dispensable as it is lost entirely in E. salsugineum.Fig. 4


Widespread natural variation of DNA methylation within angiosperms
aHeatmap showing methylation state of orthologous genes (horizontal axis) to A. thaliana for each species (vertical axis). Species are organized according to phylogenetic relationship. b Percentage of genes in each species that are gbM (mCG only in coding sequences). The Brassicaceae are highlighted in gold. c The levels of mCG in upstream, across, and downstream of gbM genes for all species. Species in gold belong to the Brassicaceae and illustrate the decreased levels and loss of mCG. d gbM genes are more highly expressed, whereas mCG over the TSS (mCG-TSS) has reduced gene expression
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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

Fig4: aHeatmap showing methylation state of orthologous genes (horizontal axis) to A. thaliana for each species (vertical axis). Species are organized according to phylogenetic relationship. b Percentage of genes in each species that are gbM (mCG only in coding sequences). The Brassicaceae are highlighted in gold. c The levels of mCG in upstream, across, and downstream of gbM genes for all species. Species in gold belong to the Brassicaceae and illustrate the decreased levels and loss of mCG. d gbM genes are more highly expressed, whereas mCG over the TSS (mCG-TSS) has reduced gene expression
Mentions: Between species, the DNA methylation status of gbM can be conserved across orthologs [46]. The DNA methylation state of orthologous genes across all species was compared using A. thaliana as an anchor (Fig. 4a). A. lyrata and C. rubella are the most closely related to A. thaliana and also have the greatest conservation of DNA methylation status, with many A. thaliana gbM gene orthologs also being gbM genes in these species (~86.3 % and ~79.8 % of A. thaliana gbM genes, respectively). However, they also had many gbM genes that had unmethylated A. thaliana orthologs (~18.6 % and ~13.9 % of A. thaliana genes, respectively). Although gbM is generally “conserved” between species, this conservation breaks down over evolutionary distance with gains and losses of gbM in different lineages. In terms of total number of gbM genes, M. truncatula and Mimulus guttatus had the greatest number (Additional file 2: Table S2). However, when the percentage of gbM genes in the genome is taken into account (Fig. 4b), M. truncatula appeared similar to other species, whereas M. guttatus remained an outlier with ~60.7 % of all genes classified as gbM genes. The reason why M. guttatus has unusually large numbers of gbM loci is unknown and will require further investigation. In contrast, there has been considerable loss of gbM genes in Brassica rapa and Brassica oleracea, and a complete loss in E. salsugineum. This suggests that over longer evolutionary distance, the DNA methylation status of gbM varies considerably and is dispensable as it is lost entirely in E. salsugineum.Fig. 4

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.


Related in: MedlinePlus