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Evolutionary patterns of genic DNA methylation vary across land plants

Nature Plants volume 2, Article number: 15222 (2016) Cite this article

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Abstract

Little is known about patterns of genic DNA methylation across the plant kingdom or about the evolutionary processes that shape them. To characterize gene-body methylation (gbM) within exons, we have gathered single-base resolution methylome data that span the phylogenetic breadth of land plants. We find that a basal land plant, Marchantia polymorpha, lacks any evident signal of gbM within exons, but conifers have high levels of both CG and CHG (where H is A, C or T) methylation in expressed genes. To begin to understand the evolutionary forces that shape gbM, we first tested for correlations in methylation levels across orthologues1,2. Genic CG methylation levels, but not CHG or CHH levels, are correlated across orthologues for species as distantly related as ferns and angiosperms. Hence, relative levels of CG methylation are a consistent property across genes, even for species that diverged ∼400 million years ago3,4. In contrast, genic CHG methylation correlates with genome size, suggesting that the host epigenetic response to transposable elements also affects genes. Altogether, our data indicate that the evolutionary forces acting on DNA methylation vary substantially across species, genes and methylation contexts.

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Figure 1: A phylogeny of the sampled species with average levels of genic methylation.
Figure 2: Histograms of gbM among genes.
Figure 3: Correlations of mC level across orthologues in the CG context.
Figure 4: Plots of genome size (x axis) against the percentage of mCs in the CG, CHG and CHH contexts.

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Acknowledgements

The authors would like to thank J. Bousquet (University of Laval, Canada), J. Der (Cal State Fullerton, USA), C. Depamphilis (Penn State University, USA), K. Ishizaki (Kobe University, Japan), T. Kohchi (Kyoto University, Japan), C. Langley (University of California Davis, USA) and D. Stevenson (New York Botanical Garden, USA) for plant DNA and tissue. R. Gaut (University of Californa Irvine, USA) generated the BSseq libraries; C. Finet (University of Lyon, France) shared the alignment of amino acid sequences from his study; A. Delcher (John Hopkins University, USA) provided Glimmer software. J. A. Fawcett (Graduate University for Advanced Studies, Japan), A. Bousios (University of Sussex, UK), S. Hug, K. Roessler, Q. Liu and A. Gonzalez-Gonzalez provided helpful suggestions. S.T. is supported by an internal grant from SOKENDAI and JSPS Grant-in-Aid for Young Scientists (B) (grant no. 15K18585); J.-H.R. is supported by the National Natural Science Foundation of China (grant no. 31330008) and B.S.G. is supported by NSF Grant IOS-1542703.

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Authors and Affiliations

  1. SOKENDAI (The Graduate University for Advanced Studies), Hayama, 240-0193, Kanagawa, Japan

    Shohei Takuno

  2. State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing, China

    Jin-Hua Ran

  3. Department of Ecology and Evolutionary Biology, University of California, 321 Steinhaus Hall, Irvine, 92697-2525, California, USA

    Jin-Hua Ran & Brandon S. Gaut

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  1. Shohei Takuno
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J.-H.R. and B.S.G. conceived of the project; S.T. and J.-H.R. analysed data; S.T., J.-H.R. and B.S.G. wrote the paper. All authors approved the manuscript.

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Correspondence to Jin-Hua Ran or Brandon S. Gaut.

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Takuno, S., Ran, JH. & Gaut, B. Evolutionary patterns of genic DNA methylation vary across land plants. Nature Plants 2, 15222 (2016). https://doi.org/10.1038/nplants.2015.222

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