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Research Article

Rate, spectrum, and evolutionary dynamics of spontaneous epimutations

Adriaan van der Graaf, René Wardenaar, Drexel A. Neumann, Aaron Taudt, Ruth G. Shaw, Ritsert C. Jansen, Robert J. Schmitz, Maria Colomé-Tatché, and Frank Johannes
  1. aGroningen Bioinformatics Centre, University of Groningen, 9747 AG Groningen, The Netherlands;
  2. bDepartment of Genetics, University of Georgia, Athens, GA 30602;
  3. cEuropean Institute for the Biology of Aging, University of Groningen, University Medical Centre Groningen, 9713 AV Groningen, The Netherlands; and
  4. dDepartment of Ecology, Evolution and Behavior, University of Minnesota, Minneapolis, MN 55455

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PNAS May 26, 2015 112 (21) 6676-6681; first published May 11, 2015; https://doi.org/10.1073/pnas.1424254112
Adriaan van der Graaf
aGroningen Bioinformatics Centre, University of Groningen, 9747 AG Groningen, The Netherlands;
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René Wardenaar
aGroningen Bioinformatics Centre, University of Groningen, 9747 AG Groningen, The Netherlands;
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Drexel A. Neumann
bDepartment of Genetics, University of Georgia, Athens, GA 30602;
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Aaron Taudt
c European Institute for the Biology of Aging, University of Groningen, University Medical Centre Groningen, 9713 AV Groningen, The Netherlands; and
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Ruth G. Shaw
dDepartment of Ecology, Evolution and Behavior, University of Minnesota, Minneapolis, MN 55455
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Ritsert C. Jansen
aGroningen Bioinformatics Centre, University of Groningen, 9747 AG Groningen, The Netherlands;
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Robert J. Schmitz
bDepartment of Genetics, University of Georgia, Athens, GA 30602;
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Maria Colomé-Tatché
c European Institute for the Biology of Aging, University of Groningen, University Medical Centre Groningen, 9713 AV Groningen, The Netherlands; and
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Frank Johannes
aGroningen Bioinformatics Centre, University of Groningen, 9747 AG Groningen, The Netherlands;
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  1. Edited by James A. Birchler, University of Missouri–Columbia, Columbia, MO, and approved April 14, 2015 (received for review December 19, 2014)

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Significance

Changes in the methylation status of cytosine nucleotides are a source of heritable epigenetic and phenotypic diversity in plants. Here we derive robust estimates of the rate at which cytosine methylation is spontaneously gained (forward epimutation) or lost (backward epimutation) in the genome of the model plant Arabidopsis thaliana. We show that the forward–backward dynamics of selectively neutral epimutations have a major impact on methylome evolution and shape genome-wide patterns of methylation diversity among natural populations in this species. The epimutation rates presented here can serve as reference values in future empirical and theoretical population epigenetic studies in plants.

Abstract

Stochastic changes in cytosine methylation are a source of heritable epigenetic and phenotypic diversity in plants. Using the model plant Arabidopsis thaliana, we derive robust estimates of the rate at which methylation is spontaneously gained (forward epimutation) or lost (backward epimutation) at individual cytosines and construct a comprehensive picture of the epimutation landscape in this species. We demonstrate that the dynamic interplay between forward and backward epimutations is modulated by genomic context and show that subtle contextual differences have profoundly shaped patterns of methylation diversity in A. thaliana natural populations over evolutionary timescales. Theoretical arguments indicate that the epimutation rates reported here are high enough to rapidly uncouple genetic from epigenetic variation, but low enough for new epialleles to sustain long-term selection responses. Our results provide new insights into methylome evolution and its population-level consequences.

  • epigenetics
  • epimutation
  • DNA methylation
  • evolution
  • Arabidopsis

Footnotes

  • ↵1A.v.d.G. and R.W. contributed equally to this work.

  • ↵2To whom correspondence may be addressed. Email: schmitz{at}uga.edu, m.colome.tatche{at}umcg.nl, or frank{at}johanneslab.org.
  • Author contributions: R.J.S., M.C.-T., and F.J. designed research; A.v.d.G., R.W., D.A.N., A.T., R.J.S., M.C.-T., and F.J. performed research; D.A.N., R.G.S., R.C.J., and R.J.S. contributed new reagents/analytic tools; A.v.d.G., R.W., A.T., M.C.-T., and F.J. analyzed data; and M.C.-T. and F.J. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: The sequence reported in this paper has been deposited in the Gene Expression Omnibus (GEO) database, www.ncbi.nlm.nih.gov/geo (accession no. GSE64463).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1424254112/-/DCSupplemental.

Freely available online through the PNAS open access option.

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Estimates of forward–backward epimutation rates
Adriaan van der Graaf, René Wardenaar, Drexel A. Neumann, Aaron Taudt, Ruth G. Shaw, Ritsert C. Jansen, Robert J. Schmitz, Maria Colomé-Tatché, Frank Johannes
Proceedings of the National Academy of Sciences May 2015, 112 (21) 6676-6681; DOI: 10.1073/pnas.1424254112

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Estimates of forward–backward epimutation rates
Adriaan van der Graaf, René Wardenaar, Drexel A. Neumann, Aaron Taudt, Ruth G. Shaw, Ritsert C. Jansen, Robert J. Schmitz, Maria Colomé-Tatché, Frank Johannes
Proceedings of the National Academy of Sciences May 2015, 112 (21) 6676-6681; DOI: 10.1073/pnas.1424254112
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Proceedings of the National Academy of Sciences: 112 (21)
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