Evolutionary Ecology

, Volume 24, Issue 3, pp 541–553 | Cite as

Experimental alteration of DNA methylation affects the phenotypic plasticity of ecologically relevant traits in Arabidopsis thaliana

  • Oliver Bossdorf
  • Davide Arcuri
  • Christina L. Richards
  • Massimo Pigliucci
Original Paper

Abstract

Heritable phenotypic variation in plants can be caused not only by underlying genetic differences, but also by variation in epigenetic modifications such as DNA methylation. However, we still know very little about how relevant such epigenetic variation is to the ecology and evolution of natural populations. We conducted a greenhouse experiment in which we treated a set of natural genotypes of Arabidopsis thaliana with the demethylating agent 5-azacytidine and examined the consequences of this treatment for plant traits and their phenotypic plasticity. Experimental demethylation strongly reduced the growth and fitness of plants and delayed their flowering, but the degree of this response varied significantly among genotypes. Differences in genotypes’ responses to demethylation were only weakly related to their genetic relatedness, which is consistent with the idea that natural epigenetic variation is independent of genetic variation. Demethylation also altered patterns of phenotypic plasticity, as well as the amount of phenotypic variation observed among plant individuals and genotype means. We have demonstrated that epigenetic variation can have a dramatic impact on ecologically important plant traits and their variability, as well as on the fitness of plants and their ecological interactions. Epigenetic variation may thus be an overlooked factor in the evolutionary ecology of plant populations.

Keywords

Arabidopsis thaliana 5-azacytidine DNA methylation Epigenetics Natural variation Phenotypic plasticity 

Supplementary material

10682_2010_9372_MOESM1_ESM.pdf (20 kb)
Supplementary material 1 (PDF 19 kb)

References

  1. Berger SL (2007) The complex language of chromatin regulation during transcription. Nature 447:407–412CrossRefPubMedGoogle Scholar
  2. Bird A (2007) Perceptions of epigenetics. Nature 447:396–398CrossRefPubMedGoogle Scholar
  3. Bossdorf O, Richards CL, Pigliucci M (2008) Epigenetics for ecologists. Ecol Lett 11:106–115PubMedGoogle Scholar
  4. Burn JE, Bagnall DJ, Metzger JD, Dennis ES, Peacock WJ (1993) DNA methylation, vernalization, and the initiation of flowering. Proc Natl Acad Sci USA 90:287–291CrossRefPubMedGoogle Scholar
  5. Cervera MT, Ruiz-Garcia L, Martinez-Zapater JM (2002) Analysis of DNA methylation in Arabidopsis thaliana based on methylation-sensitive AFLP markers. Mol Genet Genom 268:543–552CrossRefGoogle Scholar
  6. Chen ZJ (2007) Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annu Rev Plant Biol 58:377–406CrossRefPubMedGoogle Scholar
  7. Cubas P, Vincent C, Coen E (1999) An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401:157–161CrossRefPubMedGoogle Scholar
  8. Endler JA (1986) Natural selection in the wild. Princeton University Press, PrincetonGoogle Scholar
  9. Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics. Pearson, HarlowGoogle Scholar
  10. Felsenstein J (2005) PHYLIP version 3.6. Distributed by the author, Department of Genome Sciences, University of WashingtonGoogle Scholar
  11. Fieldes MA (1994) Heritable effects of 5-azacytidine treatments on the growth and development of flax (Linum usitatissimum) genotrophs and genotypes. Genome 37:1–11CrossRefPubMedGoogle Scholar
  12. Fieldes MA, Amyot LM (1999a) Evaluating the potential of using 5-Azacytidine as an epimutagen. Can J Bot 77:1617–1622CrossRefGoogle Scholar
  13. Fieldes MA, Amyot LM (1999b) Epigenetic control of the early flowering in flax lines induced by 5-Azacytidine applied to germinating seeds. J Hered 90:199–206CrossRefGoogle Scholar
  14. Fieldes MA, Schaeffer SM, Krech MJ, Brown JCL (2005) DNA hypomethylation in 5-azacytidine-induced early-flowering lines of flax. Theor Appl Genet 111:136–149CrossRefPubMedGoogle Scholar
  15. Finnegan EJ, Peacock WJ, Dennis ES (1996) Reduced DNA methylation in Arabidopsis thaliana results in abnormal plant development. Proc Natl Acad Sci USA 93:8449–8454CrossRefPubMedGoogle Scholar
  16. Finnegan EJ, Genger RK, Kovac K, Peacock WJ, Dennis ES (1998) DNA methylation and the promotion of flowering by vernalization. Proc Natl Acad Sci USA 95:5824–5829CrossRefPubMedGoogle Scholar
  17. Genger RK, Peacock WJ, Dennis ES, Finnegan EJ (2003) Opposing effects of reduced DNA methylation on flowering time in Arabidopsis thaliana. Planta 216:461–466PubMedGoogle Scholar
  18. Goslee SC, Urban DL (2007) The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw 22:7 (www.jstatsoft.org)Google Scholar
  19. Grant-Downton RT, Dickinson HG (2005) Epigenetics and its implications for plant biology. 1. The epigenetic network in plants. Ann Bot 96:1143–1164CrossRefPubMedGoogle Scholar
  20. Grant-Downton RT, Dickinson HG (2006) Epigenetics and its implications for plant biology. 2. The ‘epigenetic epiphany’: epigenetics, evolution and beyond. Ann Bot 97:11–27CrossRefPubMedGoogle Scholar
  21. Jablonka E, Lamb MJ (2005) Evolution in Four Dimensions. MIT Press, CambridgeGoogle Scholar
  22. Johannes F, Colot V, Jansen RC (2008) Epigenome dynamics: a quantitative genetics perspective. Nature Rev Genet 9:883–890CrossRefPubMedGoogle Scholar
  23. Johannes F, Porcher E, Teixeira FK, Saliba-Colombani V, Simon M, Agier N, Bulski A, Albuisson J, Heredia F, Audigier P, Bouchez D, Dillmann C, Guerche P, Hospital F, Colot V (2009) Assessing the impact of transgenerational epigenetic variation on complex traits. PLoS Genet 5:e1000530CrossRefPubMedGoogle Scholar
  24. Jones PA (1985) Altering gene expression with 5-Azacytidine. Cell 40:485–486CrossRefPubMedGoogle Scholar
  25. Kalisz S, Purugganan MD (2004) Epialleles via DNA methylation: consequences for plant evolution. Trends Ecol Evol 19:309–314CrossRefPubMedGoogle Scholar
  26. Keyte AL, Percifield R, Liu B, Wendel JF (2006) Infraspecific DNA methylation polymorphism in cotton (Gossypium hirsutum L.). J Hered 97:444–450CrossRefPubMedGoogle Scholar
  27. Kondo H, Miura T, Wada KC, Takeno K (2007) Induction of flowering by 5-azacytidine in some plant species: relationship between the stability of photoperiodically induced flowering and flower-inducing effect of DNA demethylation. Physiol Plant 131:462–469CrossRefPubMedGoogle Scholar
  28. Koornneef M, Alonso-Blanco C, Vreugdenhil D (2004) Naturally occurring genetic variation in Arabidopsis thaliana. Annu Rev Plant Biol 55:141–172CrossRefPubMedGoogle Scholar
  29. Linhart YB, Grant MC (1996) Evolutionary significance of local differentiation in plants. Annu Rev Ecol Syst 27:237–277CrossRefGoogle Scholar
  30. Liu B, Wendel JF (2003) Epigenetic phenomena and the evolution of plant allopolyploids. Mol Phylogenet Evol 29:365–379CrossRefPubMedGoogle Scholar
  31. McCullagh P, Nelder JA (1989) Generalized linear models. CRC Press, Boca RatonGoogle Scholar
  32. Meyerowitz EM, Somerville CR (2002) The Arabidopsis book. American Society of Plant Biologists, Rockville. Available from http://www.aspb.org/publications/arabidopsis/
  33. Miller GE (1991) Asymptotic test statistics for coefficients of variation. Commun Stat Theor M 20:3351–3363CrossRefGoogle Scholar
  34. Mitchell-Olds T (2001) Arabidopsis thaliana and its wild relatives: a model system for ecology and evolution. Trends Ecol Evol 16:693–700CrossRefGoogle Scholar
  35. Osborn TC, Pires JC, Birchler JA, Auger DL, Chen ZJ, Lee HS, Comai L, Madlung A, Doerge RW, Colot V, Martienssen RA (2003) Understanding mechanisms of novel gene expression in polyploids. Trends Genet 19:141–147CrossRefPubMedGoogle Scholar
  36. Pigliucci M (1998) Ecological and evolutionary genetics of Arabidopsis. Trends Plant Sci 3:485–489CrossRefGoogle Scholar
  37. Rapp RA, Wendel J (2005) Epigenetics and plant evolution. New Phytol 168:81–91CrossRefPubMedGoogle Scholar
  38. Richards EJ (2006) Inherited epigenetic variation–revisiting soft inheritance. Nature Rev Genet 7:395–401CrossRefPubMedGoogle Scholar
  39. Riddle NC, Richards EJ (2002) The control of natural variation in cytosine methylation in Arabidopsis. Genetics 162:355–363PubMedGoogle Scholar
  40. Tatra GS, Miranda J, Chinnappa CC, Reid DM (2000) Effect of light quality and 5-azacytidine on genomic methylation and stem elongation in two ecotypes of Stellaria longipes. Physiol Plant 109:313–321CrossRefGoogle Scholar
  41. R Development Core Team (2007) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available from http://R-project.org
  42. Vaughn MW, Tanurdzic M, Lippman Z, Jiang H, Carrasquillo R, Rabinowicz PD, Dedhia N, McCombie WR, Agier N, Bulski A, Colot V, Doerge RW, Martienssen RA (2007) Epigenetic natural variation in Arabidopsis thaliana. PLoS Biol 5:e174CrossRefPubMedGoogle Scholar
  43. Zhang X, Shiu S, Cal A, Borevitz JO (2008) Global analysis of genetic, epigenetic and transcriptional polymorphisms in Arabidopsis thaliana using whole genome tiling arrays. PLoS Genet 4:e1000032CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Oliver Bossdorf
    • 1
  • Davide Arcuri
    • 2
  • Christina L. Richards
    • 3
  • Massimo Pigliucci
    • 4
  1. 1.Institute of Plant SciencesUniversity of BernBernSwitzerland
  2. 2.Dipartimento di Biotecnologie (Bio.M.A.A.)Università Mediterranea di Reggio CalabriaReggio CalabriaItaly
  3. 3.Department of Integrative BiologyUniversity of South FloridaTampaUSA
  4. 4.Department of PhilosophyCity University of New York-Lehman CollegeBronxUSA

Personalised recommendations