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Unique cell-type-specific patterns of DNA methylation in the root meristem

Nature Plants volume 2, Article number: 16058 (2016) Cite this article

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Abstract

DNA methylation is an epigenetic modification that differs between plant organs and tissues, but the extent of variation between cell types is not known. Here, we report single-base-resolution whole-genome DNA methylomes, mRNA transcriptomes and small RNA transcriptomes for six cell populations covering the major cell types of the Arabidopsis root meristem. We identify widespread cell-type-specific patterns of DNA methylation, especially in the CHH sequence context, where H is A, C or T. The genome of the columella root cap is the most highly methylated Arabidopsis cell characterized so far. It is hypermethylated within transposable elements (TEs), accompanied by increased abundance of transcripts encoding RNA-directed DNA methylation (RdDM) pathway components and 24-nt small RNAs (smRNAs). The absence of the nucleosome remodeller DECREASED DNA METHYLATION 1 (DDM1), required for maintenance of DNA methylation, and low abundance of histone transcripts involved in heterochromatin formation suggests that a loss of heterochromatin may occur in the columella, thus allowing access of RdDM factors to the whole genome, and producing an excess of 24-nt smRNAs in this tissue. Together, these maps provide new insights into the epigenomic diversity that exists between distinct plant somatic cell types.

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Figure 1: Cell-type-specific patterns of DNA methylation in the root meristem.
Figure 2: Differentially methylated regions (DMRs) among six root cell types.
Figure 3: DNA methylation in genes and TEs.
Figure 4: Transcript levels of DNA-methylation-related genes.
Figure 5: Loss of DDM1 in the columella.

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Acknowledgements

We thank K. Slotkin (Ohio State Univ., USA) and J.A.H. Murray (Univ. Cardiff, UK) for kindly providing DDM1–GFP seeds and ProCYCD5–GFP seeds, respectively. T.K. was supported by the Japan Society for the Promotion of Sciences Research Abroad Fellowship. T.S was supported by the Jean Rogerson Postgraduate Scholarship. This research was supported by grants from the National Science Foundation (MCB-1344299 to J.R.E and IOS-1021619 to P.N.B.), by the National Institutes of Health (GM R01-043778 to P.N.B.) and by the Gordon and Betty Moore Foundation (GBMF3034 to J.R.E and GBMF3405 to P.N.B.). R.L. was supported by the Australian Research Council (FT120100862). R.J.S. was supported by the National Institutes of Health (R00GM100000). J.R.E. and P.N.B. are investigators of the Howard Hughes Medical Institute.

Author information

Author notes

  1. Taiji Kawakatsu, Tim Stuart and Manuel Valdes: These authors contributed equally to this work.

Authors and Affiliations

  1. Plant Biology Laboratory, The Salk Institute for Biological Studies, La Jolla, 92037, California, USA

    Taiji Kawakatsu, Robert J. Schmitz & Joseph R. Ecker

  2. Genomic Analysis Laboratory, The Salk Institute for Biological Studies, La Jolla, 92037, California, USA

    Taiji Kawakatsu, Robert J. Schmitz, Joseph R. Nery, Mark A. Urich, Ryan Lister & Joseph R. Ecker

  3. Genetically Modified Organism Research Center, National Institute of Agrobiological Sciences, Tsukuba, 305-8602, Ibaraki, Japan

    Taiji Kawakatsu

  4. ARC Centre of Excellence in Plant Energy Biology, The University of Western Australia, Perth, 6009, Western Australia, Australia

    Tim Stuart & Ryan Lister

  5. Department of Biology, Duke University, Durham, 27708, North Carolina, USA

    Manuel Valdes, Natalie Breakfield, Xinwei Han & Philip N. Benfey

  6. Department of Genetics, University of Georgia, Athens, 30602, Georgia, USA

    Robert J. Schmitz

  7. Howard Hughes Medical Institute, Duke University, Durham, 27708, North Carolina, USA

    Philip N. Benfey

  8. Howard Hughes Medical Institute, The Salk Institute for Biological Studies, La Jolla, 92037, California, USA

    Joseph R. Ecker

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Contributions

P.N.B., J.R.E. and R.L. designed and supervised research. N.B., X.H. and M.V. collected cells. T.K., R.L., J.R.N. and M.A.U. conducted MethylC-seq experiments. R.L., J.R.N. and M.A.U. conducted RNA-seq experiments. T.K. and R.L. performed sequencing data processing. T.K., R.L., R.J.S. and T.S. performed statistical and bioinformatic analyses. R.J.S. performed imaging analyses. P.N.B., J.R.E., T.K., R.L. and T.S. prepared the manuscript.

Corresponding authors

Correspondence to Ryan Lister, Philip N. Benfey or Joseph R. Ecker.

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Kawakatsu, T., Stuart, T., Valdes, M. et al. Unique cell-type-specific patterns of DNA methylation in the root meristem. Nature Plants 2, 16058 (2016). https://doi.org/10.1038/nplants.2016.58

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