Widespread natural variation of DNA methylation within angiosperms

Chad E Niederhuth¹, Adam J Bewick¹, Lexiang Ji², Magdy S Alabady³, Kyung Do Kim⁴, Qing Li⁵, Nicholas A Rohr¹, Aditi Rambani⁶, John M Burke³, Joshua A Udall⁵, Chiedozie Egesi⁷, Jeremy Schmutz^{8

9}, Jane Grimwood⁸, Scott A Jackson⁴, Nathan M Springer⁶, Robert J Schmitz¹⁰

Affiliations

¹ Department of Genetics, University of Georgia, 120 East Green Street, Athens, GA, 30602, USA.
² Institute of Bioinformatics, University of Georgia, Athens, GA, 30602, USA.
³ Department of Plant Biology, University of Georgia, Athens, GA, 30602, USA.
⁴ Center for Applied Genetic Technologies, University of Georgia, Athens, GA, 30602, USA.
⁵ Department of Plant Biology, Microbial and Plant Genomics Institute, University of Minnesota, Saint Paul, MN, 55108, USA.
⁶ Plant and Wildlife Science Department, Brigham Young University, Provo, UT, 84602, USA.
⁷ National Root Crops Research Institute (NRCRI), Umudike, Km 8 Ikot Ekpene Road, PMB 7006, Umuahia, 440001, Nigeria.
⁸ HudsonAlpha Institute for Biotechnology, Huntsville, AL, 35806, USA.
⁹ Department of Energy Joint Genome Institute, Walnut Creek, CA, USA.
¹⁰ Department of Genetics, University of Georgia, 120 East Green Street, Athens, GA, 30602, USA. schmitz@uga.edu.

PMID: 27671052
PMCID: PMC5037628
DOI: 10.1186/s13059-016-1059-0

Widespread natural variation of DNA methylation within angiosperms

Chad E Niederhuth et al. Genome Biol. 2016.

. 2016 Sep 27;17(1):194.

doi: 10.1186/s13059-016-1059-0.

Authors

Affiliations

¹ Department of Genetics, University of Georgia, 120 East Green Street, Athens, GA, 30602, USA.
² Institute of Bioinformatics, University of Georgia, Athens, GA, 30602, USA.
³ Department of Plant Biology, University of Georgia, Athens, GA, 30602, USA.
⁴ Center for Applied Genetic Technologies, University of Georgia, Athens, GA, 30602, USA.
⁵ Department of Plant Biology, Microbial and Plant Genomics Institute, University of Minnesota, Saint Paul, MN, 55108, USA.
⁶ Plant and Wildlife Science Department, Brigham Young University, Provo, UT, 84602, USA.
⁷ National Root Crops Research Institute (NRCRI), Umudike, Km 8 Ikot Ekpene Road, PMB 7006, Umuahia, 440001, Nigeria.
⁸ HudsonAlpha Institute for Biotechnology, Huntsville, AL, 35806, USA.
⁹ Department of Energy Joint Genome Institute, Walnut Creek, CA, USA.
¹⁰ Department of Genetics, University of Georgia, 120 East Green Street, Athens, GA, 30602, USA. schmitz@uga.edu.

PMID: 27671052
PMCID: PMC5037628
DOI: 10.1186/s13059-016-1059-0

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.

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Figures

**Fig. 1**
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

**Fig. 2**
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. c *Chromosome 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*)

**Fig. 3**
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*)

**Fig. 4**
a *Heatmap* 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

**Fig. 5**
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

**Fig. 6**
a Patterns of methylation across conserved non-coding sequences (CNS) for mCG (*blue*), mCHG (*green*), and mCHH (*maroon*). b Percentage of genes with mCHH islands 2 kb upstream or downstream. c Association of upstream mCHH islands with gene expression. Genes are divided into not-expressed (NE) and quartiles of increasing expression. ** indicates a difference in proportion from the fourth quartile at p < 0.01. d Patterns of upstream mCHH islands for mCG (*blue*), mCHG (*green*), and mCHH (*maroon*)

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Comment in

Prodigious plant methylomes.
Gehring M. Gehring M. Genome Biol. 2016 Sep 27;17(1):197. doi: 10.1186/s13059-016-1065-2. Genome Biol. 2016. PMID: 27677311 Free PMC article.

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Widespread natural variation of DNA methylation within angiosperms

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Widespread natural variation of DNA methylation within angiosperms

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Abstract

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