Planta

, Volume 222, Issue 2, pp 301–306

DNA methylation increases throughout Arabidopsis development

  • L. Ruiz-García
  • M. T. Cervera
  • J. M. Martínez-Zapater
Original Article

Abstract

We used amplified fragment length polymorphisms (AFLP) to analyze the stability of DNA methylation throughout Arabidopsis development. AFLP can detect genome-wide changes in cytosine methylation produced by DNA demethylation agents, such as 5-azacytidine, or specific mutations at the DDM1 locus. In both cases, cytosine demethylation is associated with a general increase in the presence of amplified fragments. Using this approach, we followed DNA methylation at methylation sensitive restriction sites throughout Arabidopsis development. The results show a progressive DNA methylation trend from cotyledons to vegetative organs to reproductive organs.

Keywords

Arabidopsis 5-azacytidine ddm1 mutant DNA methylation pattern Plant development 

Abbreviations

AFLP

Amplified fragment length polymorphism

5-azaC

5-azacytidine

5-mC

5-methylcytosine

References

  1. Bastow R, Mylne JS, Lister C, Lippman Z, Martienssen RA, Dean C (2004) Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427:164–167CrossRefPubMedGoogle Scholar
  2. Bender J, Fink GR (1995) Epigenetic control of an endogenous gene family is revealed by a novel blue fluorescent mutant of Arabidopsis. Cell 83:725–734CrossRefPubMedGoogle Scholar
  3. Bitonti MB, Cozza R, Chiappetta A, Giannino D, Castiglione MR, Dewitte W, Mariotti D, Van Onckelen H, Innocenti AM (2002) Distinct nuclear organization, DNA methylation pattern and cytokinin distribution mark juvenile, juvenile-like and adult vegetative apical meristems in peach (Prunus persica (L.) Batsch). J Exp Bot 53:1047–1054CrossRefPubMedGoogle 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 90:287–291PubMedGoogle Scholar
  5. Cervera MT, Ruiz-García L, Martínez-Zapater JM (2002) Analysis of DNA methylation-sensitive AFLP markers. Mol Genet Genomics 268:543–552Google Scholar
  6. Creusot F, Acs G, Christman JK (1982) Inhibition of DNA methyltransferase and induction of Friend erythroleukemia cell differentiation by 5-azacytidine and 5-aza-2′-deoxycytidine. J Biol Chem 257:2041–2048PubMedGoogle 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. Donald M, Clark VH, Bird A (1999) Absence of genome-wide changes in DNA methylation during development of the zebrafish. Nat Genet 23:139–140CrossRefPubMedGoogle Scholar
  9. 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
  10. Finnegan EJ, Genger RK, Peacock WJ, Dennis ES (1998a) DNA methylation in plants. Annu Rev Plant Physiol Plant Mol Biol 49:223–247Google Scholar
  11. Finnegan EJ, Genger RK, Kovac K, Peacock WJ, Dennis ES (1998b) DNA methylation and the promotion of flowering by vernalization. Proc Natl Acad Sci USA 95:5824–5829CrossRefPubMedGoogle Scholar
  12. Finnegan EJ, Peacock WJ, Dennis ES (2000) DNA methylation, a key regulator of plant development and other processes. Curr Opin Genet Dev 10:217–223PubMedGoogle Scholar
  13. Finnegan EJ, Sheldon CC, Jardinaud F, Peacock WJ, Dennis ES (2004) A cluster of Arabidopsis genes with a coordinate response to an environmental stimulus. Current Biol 14:911–916CrossRefGoogle Scholar
  14. Fraga M, Cañal MJ, Rodriguez R (2002) Phase-change related epigenetic and physiological changes in Pinus radiata D. Don. Planta 215:672–678CrossRefPubMedGoogle Scholar
  15. 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
  16. Goto T, Monk M (1998) Regulation of X-chromosome inactivation in development in mice and humans. Microbiol Mol Biol Reviews 62:362–378Google Scholar
  17. Hsieh CL (2000) Dynamics of DNA methylation pattern. Curr Opin Genet Dev 10:224–228CrossRefPubMedGoogle Scholar
  18. Jacobsen SE, Meyerowitz EM (1997) Hypermethylated SUPERMAN epigenetic alleles in Arabidopsis. Science 277:1100–1103CrossRefPubMedGoogle Scholar
  19. Jacobsen SE, Sakai H, Finnegan EJ, Cao X, Meyerowitz EM (2000) Ectopic hypermethylation of flower-specific genes in Arabidopsis. Curr Biol 10:179–186CrossRefPubMedGoogle Scholar
  20. Jones PA, Taylor SM, Wilson VL (1983) Inhibition of DNA methylation by 5-azacytidine. Recent Res Cancer Res 84:202–211Google Scholar
  21. Kakutani T (1997) Genetic characterization of late-flowering traits induced by DNA hypomethylation mutation in Arabidopsis thaliana. Plant J 12:1447–1451CrossRefPubMedGoogle Scholar
  22. Kakutani T, Jeddeloh JA, Richards EJ (1995) Characterization of an Arabidopsis thaliana DNA hypomethylation mutant. Nucleic Acids Res 23:130–137PubMedGoogle Scholar
  23. Koornneef M, Hanhart CJ, van der Veen JH (1991) A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Mol Gen Genet 229:57–66CrossRefPubMedGoogle Scholar
  24. Korch C, Hagblom P (1986) In-vivo-modified gonococcal plasmid pJD1. A model system for analysis of restriction enzyme sensitivity to DNA modifications. Eur J Biochem 161:519–524CrossRefPubMedGoogle Scholar
  25. Lund G, Messing J, Viotti A (1995) Endosperm-specific demethylation and activation of specific alleles of alpha-tubulin genes of Zea mays L. Mol Gen Genet 246:716–722Google Scholar
  26. Lyko F, Ramsahoye BH, Jainisch R (2000) DNA methylation in Drosophila melanogaster. Nature 408:538–540CrossRefPubMedGoogle Scholar
  27. Martienssen RA, Richards EJ (1995) DNA methylation in eukaryotes. Curr Opin Genet Dev 5:234–242CrossRefPubMedGoogle Scholar
  28. McClelland M, Nelson M, Raschke E (1994) Effect of site-specific modification on restriction endonucleases and DNA modification methyltransferases. Nucleic Acids Res 22:3640–3659PubMedGoogle Scholar
  29. Melquist S, Luff B, Bender J (1999) Arabidopsis PAI gene arrangements, cytosine methylation and expression. Genetics 153:401–413PubMedGoogle Scholar
  30. Messeguer R, Ganal MW, Steffens JC, Tanksley SD (1991) Characterization of the level, target sites and inheritance of cytosine methylation in tomato nuclear DNA. Plant Mol Biol 16:753–770CrossRefPubMedGoogle Scholar
  31. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassay with tobacco tissue cultures. Physiol Plant 15:473–479Google Scholar
  32. Okamoto H, Hirochika H (2001) Silencing of transposable elements in plants. Trends Plant Sci 6:527–534CrossRefPubMedGoogle Scholar
  33. Razin A, Cedar H (1994) DNA methylation and genomic imprinting. Cell 77:473–476PubMedGoogle Scholar
  34. Razin A, Riggs AD (1980) DNA methylation and gene regulation. Science 210:604–610PubMedGoogle Scholar
  35. Ronemus MJ, Galbiati M, Ticknor C, Chen J, Dellaporta SL (1996) Demethylation-induced developmental pleiotropy in Arabidopsis. Science 273:654–657PubMedGoogle Scholar
  36. Soppe W, Jacobsen SE, Alonso-Blanco C, Jackson JP, Kakutani T, Koornneef M, Peeters AJ (2000) The late flowering phenotype of fwa mutants is caused by gain-of-function epigenetic alleles of a homeodomain gene. Mol Cell 6:791–802PubMedGoogle Scholar
  37. Vongs A, Kakutani T, Martienssen RA, Richards EJ (1993) Arabidopsis thaliana DNA methylation mutants. Science 260:1926–1928PubMedGoogle Scholar
  38. Xiong LZ, Xu CG, Saghai Maroof MA, Zhang Q (1999) Patterns of cytosine methylation in an elite rice hybrid and its parental lines, detected by a methylation-sensitive amplification polymorphism technique. Mol Gen Genet 261:439–446PubMedGoogle Scholar
  39. Yoder JA, Soman NS, Verdine GL, Bestor TH (1997) DNA (cytosine-5)-methyltransferases in mouse cells and tissues. Studies with a mechanism-based probe. J Mol Biol 270:385–395CrossRefPubMedGoogle Scholar
  40. Zluvova J, Janousek B, Vyskot B (2001) Immunohistochemical study of DNA methylation dynamics during plant development. J Exp Bot 52:2265–2273CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • L. Ruiz-García
    • 1
  • M. T. Cervera
    • 1
  • J. M. Martínez-Zapater
    • 1
  1. 1.Departamento de Genética Molecular de PlantasCentro Nacional de Biotecnología, CSIC. Campus de la Universidad Autónoma de MadridMadridSpain
  2. 2.Genética Forestal. Centro de Investigaciones Forestales, Instituto Nacional de Investigación y Tecnología Agraria y AlimentariaMadridSpain

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