Chromosoma

, Volume 115, Issue 1, pp 27–35

DNA methylation and epigenetic inheritance during plant gametogenesis

Mini-Review

Abstract

In plants, newly acquired epigenetic states of transcriptional gene activity are readily transmitted to the progeny. This is in contrast to mammals, where only rare cases of transgenerational inheritance of new epigenetic traits have been reported (FASEB J 12:949–957, 1998; Nat Genet 23:314–318, 1999; Proc Natl Acad Sci U S A 100:2538–2543, 2003). Epigenetic inheritance in plants seems to rely on cytosine methylation maintained through meiosis and postmeiotic mitoses, giving rise to gametophytes. In particular, maintenance of CpG methylation (mCpG) appears to play a central role, guiding the distribution of other epigenetic signals such as histone H3 methylation and non-CpG DNA methylation. The evolutionarily conserved DNA methyltransferase MET1 is responsible for copying mCpG patterns through DNA replication in the gametophytic phase. The importance of gametophytic MET1 activity is illustrated by the phenotypes of met1 mutants that are severely compromised in the accuracy of epigenetic inheritance during gametogenesis. This includes elimination of imprinting at paternally silent loci such as FWA or MEDEA (MEA). The importance of DNA methylation in gametophytic imprinting has been reinforced by the discovery of DEMETER (DME), encoding putative DNA glycosylase involved in the removal of mC. DME opposes transcriptional silencing associated with imprinting activities of the MEA/FIE polycomb group complex.

References

  1. Arabidopsis Sequencing Consortium (2000) The complete sequence of a heterochromatic island from a higher eukaryote. Cell 100:377–386CrossRefGoogle Scholar
  2. Bartee L, Malagnac F, Bender J (2001) Arabidopsis cmt3 chromomethylase mutations block non-CG methylation and silencing of an endogenous gene. Genes Dev 15:1753–1758PubMedCrossRefGoogle Scholar
  3. Birve A, Sengupta AK, Beuchle D, Larsson J, Kennison JA, Rasmuson-Lestander A, Muller J (2001) Su(z)12, a novel Drosophila Polycomb group gene that is conserved in vertebrates and plants. Development 128:3371–3379PubMedGoogle Scholar
  4. Brzeski J, Jerzmanowski A (2003) Deficient in DNA methylation 1 (DDM1) defines a novel family of chromatin-remodeling factors. J Biol Chem 278:823–828PubMedCrossRefGoogle Scholar
  5. Cao X, Jacobsen SE (2002a) Role of the Arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr Biol 12:1138–1144PubMedCrossRefGoogle Scholar
  6. Cao X, Jacobsen SE (2002b) Locus-specific control of asymmetric and CpNpG methylation by the DRM and CMT3 methyltransferase genes. Proc Natl Acad Sci U S A 99:16491–16498PubMedCrossRefGoogle Scholar
  7. Cao X, Aufsatz W, Zilberman D, Mette MF, Huang MS, Matzke M, Jacobsen SE (2003) Role of the DRM and CMT3 methyltransferases in RNA-directed DNA methylation. Curr Biol 13:2212–2217PubMedCrossRefGoogle Scholar
  8. Chan SW, Zilberman D, Xie Z, Johansen LK, Carrington JC, Jacobsen SE (2004) RNA silencing genes control de novo DNA methylation. Science 303:1336PubMedCrossRefGoogle Scholar
  9. Chaudhury AM, Ming L, Miller C, Craig S, Dennis ES, Peacock WJ (1997) Fertilization-independent seed development in Arabidopsis thaliana. Proc Natl Acad Sci U S A 94:4223–4228PubMedCrossRefGoogle Scholar
  10. Choi Y, Gehring M, Johnson L, Hannon M, Harada JJ, Goldberg RB, Jacobsen SE, Fischer RL (2002) DEMETER, a DNA glycosylase domain protein, is required for endosperm gene imprinting and seed viability in Arabidopsis. Cell 110:33–42PubMedCrossRefGoogle Scholar
  11. Choi Y, Harada JJ, Goldberg RB, Fischer RL (2004) An invariant aspartic acid in the DNA glycosylase domain of DEMETER is necessary for transcriptional activation of the imprinted MEDEA gene. Proc Natl Acad Sci U S A 101:7481–7486PubMedCrossRefGoogle Scholar
  12. Delaval K, Feil R (2004) Epigenetic regulation of mammalian genomic imprinting. Curr Opin Genet Dev 14:188–195PubMedCrossRefGoogle Scholar
  13. Finnegan EJ, Peacock WJ, Dennis ES (1996) Reduced DNA methylation in Arabidopsis thaliana results in abnormal plant development. Proc Natl Acad Sci U S A 93:8449–8454PubMedCrossRefGoogle Scholar
  14. Fransz PF, Armstrong S, de Jong JH, Parnell LD, van Drunen C, Dean C, Zabel P, Bisseling T, Jones GH (2000) Integrated cytogenetic map of chromosome arm 4S of A. thaliana: structural organization of heterochromatic knob and centromere region. Cell 100:367–376PubMedCrossRefGoogle Scholar
  15. Fransz P, Soppe W, Schubert I (2003) Heterochromatin in interphase nuclei of Arabidopsis thaliana. Chromosome Res 11:227–240PubMedCrossRefGoogle Scholar
  16. Gendrel AV, Lippman Z, Yordan C, Colot V, Martienssen RA (2002) Dependence of heterochromatic histone H3 methylation patterns on the Arabidopsis gene DDM1. Science 297:1871–1873PubMedCrossRefGoogle Scholar
  17. Gong Z, Morales-Ruiz T, Ariza RR, Roldan-Arjona T, David L, Zhu JK (2002) ROS1, a repressor of transcriptional gene silencing in Arabidopsis, encodes a DNA glycosylase/lyase. Cell 111:803–814PubMedCrossRefGoogle Scholar
  18. Grossniklaus U, Vielle-Calzada JP, Hoeppner MA, Gagliano WB (1998) Maternal control of embryogenesis by MEDEA, a polycomb group gene in Arabidopsis. Science 280:446–450PubMedCrossRefGoogle Scholar
  19. Hirochika H, Okamoto H, Kakutani T (2000) Silencing of retrotransposons in Arabidopsis and reactivation by the ddm1 mutation. Plant Cell 12:357–369PubMedCrossRefGoogle Scholar
  20. Jackson JP, Lindroth AM, Cao X, Jacobsen SE (2002) Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416:556–560PubMedCrossRefGoogle Scholar
  21. Jacobsen SE, Sakai H, Finnegan EJ, Cao X, Meyerowitz EM (2000) Ectopic hypermethylation of flower-specific genes in Arabidopsis. Curr Biol 10:179–186PubMedCrossRefGoogle Scholar
  22. Jeddeloh JA, Bender J, Richards EJ (1998) The DNA methylation locus DDM1 is required for maintenance of gene silencing in Arabidopsis. Genes Dev 12:1714–1725PubMedGoogle Scholar
  23. Jeddeloh JA, Stokes TL, Richards EJ (1999) Maintenance of genomic methylation requires a SWI2/SNF2-like protein. Nat Genet 22:94–97PubMedCrossRefGoogle Scholar
  24. Johnson L, Cao X, Jacobsen S (2002) Interplay between two epigenetic marks. DNA methylation and histone H3 lysine 9 methylation. Curr Biol 12:1360–1367PubMedCrossRefGoogle Scholar
  25. Jost JP, Oakeley EJ, Zhu B, Benjamin D, Thiry S, Siegmann M, Jost YC (2001) 5-Methylcytosine DNA glycosylase participates in the genome-wide loss of DNA methylation occurring during mouse myoblast differentiation. Nucleic Acids Res 29:4452–4461PubMedCrossRefGoogle Scholar
  26. Kakutani T, Munakata K, Richards EJ, Hirochika H (1999) Meiotically and mitotically stable inheritance of DNA hypomethylation induced by ddm1 mutation of Arabidopsis thaliana. Genetics 151:831–838PubMedGoogle Scholar
  27. Kankel MW, Ramsey DE, Stokes TL, Flowers SK, Haag JR, Jeddeloh JA, Riddle NC, Verbsky ML, Richards EJ (2003) Arabidopsis MET1 cytosine methyltransferase mutants. Genetics 163:1109–1122PubMedGoogle Scholar
  28. Kinoshita T, Yadegari R, Harada JJ, Goldberg RB, Fischer RL (1999) Imprinting of the MEDEA polycomb gene in the Arabidopsis endosperm. Plant Cell 11:1945–1952PubMedCrossRefGoogle Scholar
  29. Kinoshita T, Miura A, Choi Y, Kinoshita Y, Cao X, Jacobsen SE, Fischer RL, Kakutani T (2004) One-way control of FWA imprinting in Arabidopsis endosperm by DNA methylation. Science 303:521–523PubMedCrossRefGoogle Scholar
  30. Köhler C, Hennig L, Bouveret R, Gheyselinck J, Grossniklaus U, Gruissem W (2003a) Arabidopsis MSI1 is a component of the MEA/FIE Polycomb group complex and required for seed development. EMBO J 22:4804–4814PubMedCrossRefGoogle Scholar
  31. Köhler C, Hennig L, Spillane C, Pien S, Gruissem W, Grossniklaus U (2003b) The Polycomb-group protein MEDEA regulates seed development by controlling expression of the MADS-box gene PHERES1. Genes Dev 17:1540–1553PubMedCrossRefGoogle Scholar
  32. Köhler C, Page DR, Gagliardini V, Grossniklaus U (2005) The Arabidopsis thaliana MEDEA Polycomb group protein controls expression of PHERES1 by parental imprinting. Nat Genet 37:28–30PubMedGoogle Scholar
  33. Lindroth AM, Cao X, Jackson JP, Zilberman D, McCallum CM, Henikoff S, Jacobsen, SE (2001) Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science 292:2077–2080PubMedCrossRefGoogle Scholar
  34. Lindroth AM, Shultis D, Jasencakova Z, Fuchs J, Johnson L, Schubert D, Patnaik D, Pradhan S, Goodrich J, Schubert I, Jenuwein T, Khorasanizadeh S, Jacobsen SE (2004) Dual histone H3 methylation marks at lysines 9 and 27 required for interaction with CHROMOMETHYLASE3. EMBO J 23:4286–4296PubMedCrossRefGoogle Scholar
  35. Lippman Z, Gendrel AV, Black M, Vaughn MW, Dedhia N, McCombie WR, Lavine K, Mittal V, May B, Kasschau KD, Carrington JC, Doerge RW, Colot V, Martienssen R (2004) Role of transposable elements in heterochromatin and epigenetic control. Nature 430:471–476PubMedCrossRefGoogle Scholar
  36. Luo M, Bilodeau P, Dennis ES, Peacock WJ, Chaudhury A (2000) Expression and parent-of-origin effects for FIS2, MEA, and FIE in the endosperm and embryo of developing Arabidopsis seeds. Proc Natl Acad Sci U S A 97:10637–10642PubMedCrossRefGoogle Scholar
  37. Malagnac F, Bartee L, Bender J (2002) An Arabidopsis SET domain protein required for maintenance but not establishment of DNA methylation. EMBO J 21:6842–6852PubMedCrossRefGoogle Scholar
  38. Martienssen RA, Colot V (2001) DNA methylation and epigenetic inheritance in plants and filamentous fungi. Science 293:1070–1074PubMedCrossRefGoogle Scholar
  39. Mathieu O, Probst AV, Paszkowski J (2005) Distinct regulation of histone H3 methylation at lysines 27 and 9 by CpG methylation in Arabidopsis. EMBO J 24:2783–2791PubMedCrossRefGoogle Scholar
  40. McCormick S (2004) Control of male gametophyte development. Plant Cell Suppl 16:S142–S153CrossRefGoogle Scholar
  41. Mittelsten Scheid O, Afsar K, Paszkowski J (1998) Release of epigenetic gene silencing by trans-acting mutations in Arabidopsis. Proc Natl Acad Sci U S A 95:632–637PubMedCrossRefGoogle Scholar
  42. Mittelsten Scheid O, Probst AV, Afsar K, Paszkowski J (2002) Two regulatory levels of transcriptional gene silencing in Arabidopsis. Proc Natl Acad Sci U S A 99:13659–13662PubMedCrossRefGoogle Scholar
  43. Miura A, Yonebayashi S, Watanabe K, Toyama T, Shimada H, Kakutani T (2001) Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis. Nature 411:212–214PubMedCrossRefGoogle Scholar
  44. Morel JB, Mourrain P, Beclin C, Vaucheret H (2000) DNA methylation and chromatin structure affect transcriptional and post-transcriptional transgene silencing in Arabidopsis. Curr Biol 10:1591–1594PubMedCrossRefGoogle Scholar
  45. Morgan HD, Sutherland HG, Martin DI, Whitelaw E (1999) Epigenetic inheritance at the agouti locus in the mouse. Nat Genet 23:314–318PubMedCrossRefGoogle Scholar
  46. Murfett J, Wang XJ, Hagen G, Guilfoyle TJ (2001) Identification of Arabidopsis histone deacetylase HDA6 mutants that affect transgene expression. Plant Cell 13:1047–1061PubMedCrossRefGoogle Scholar
  47. Naumann K, Fischer A, Hofmann I, Krauss V, Phalke S, Irmler K, Hause G, Aurich AC, Dorn R, Jenuwein T, Reuter G (2005) Pivotal role of AtSUVH2 in heterochromatic histone methylation and gene silencing in Arabidopsis. EMBO J 24:1418–1429PubMedCrossRefGoogle Scholar
  48. Oakeley EJ, Podesta A, Jost JP (1997) Developmental changes in DNA methylation of the two tobacco pollen nuclei during maturation. Proc Natl Acad Sci U S A 94:11721–11725PubMedCrossRefGoogle Scholar
  49. Ohad N, Margossian L, Hsu YC, Williams C, Repetti P, Fischer RL (1996) A mutation that allows endosperm development without fertilization. Proc Natl Acad Sci U S A 93:5319–5324PubMedCrossRefGoogle Scholar
  50. Ohad N, Yadegari R, Margossian L, Hannon M, Michaeli D, Harada JJ, Goldberg RB, Fischer RL (1999) Mutations in FIE, a WD polycomb group gene, allow endosperm development without fertilization. Plant Cell 11:407–416PubMedCrossRefGoogle Scholar
  51. Probst AV, Fransz PF, Paszkowski J, Scheid OM (2003) Two means of transcriptional reactivation within heterochromatin. Plant J 33:743–749PubMedCrossRefGoogle Scholar
  52. Rakyan VK, Chong S, Champ ME, Cuthbert PC, Morgan HD, Luu KV, Whitelaw E (2003) Transgenerational inheritance of epigenetic states at the murine Axin(Fu) allele occurs after maternal and paternal transmission. Proc Natl Acad Sci U S A 100:2538–2543PubMedCrossRefGoogle Scholar
  53. Rocha PS, Sheikh M, Melchiorre R, Fagard M, Boutet S, Loach R, Moffatt B, Wagner C, Vaucheret H, Furner I (2005) The Arabidopsis HOMOLOGY-DEPENDENT GENE SILENCING1 gene codes for an S-adenosyl-l-homocysteine hydrolase required for DNA methylation-dependent gene silencing. Plant Cell 17:404–417PubMedCrossRefGoogle Scholar
  54. Ronemus MJ, Galbiati M, Ticknor C, Chen J, Dellaporta SL (1996) Demethylation-induced developmental pleiotropy in Arabidopsis. Science 273:654–657PubMedCrossRefGoogle Scholar
  55. SanMiguel P, Tikhonov A, Jin YK, Motchoulskaia N, Zakharov D, Melake-Berhan A, Springer PS, Edwards KJ, Lee M, Avramova Z, Bennetzen JL (1996) Nested retrotransposons in the intergenic regions of the maize genome. Science 274:765–768PubMedCrossRefGoogle Scholar
  56. Saze H (2003) Maintenance of CpG methylation is essential for epigenetic inheritance during plant gametogenesis. PhD thesis, Friedrich Miescher Institute, Basel, SwitzerlandGoogle Scholar
  57. Saze H, Scheid OM, Paszkowski J (2003) Maintenance of CpG methylation is essential for epigenetic inheritance during plant gametogenesis. Nat Genet 34:65–69PubMedCrossRefGoogle Scholar
  58. Scott RJ, Spielman M, Bailey J, Dickinson HG (1998) Parent-of-origin effects on seed development in Arabidopsis thaliana. Development 125:3329–3341PubMedGoogle Scholar
  59. Sijen T, Kooter JM (2000) Post-transcriptional gene-silencing: RNAs on the attack or on the defense? Bioessays 22:520–531PubMedCrossRefGoogle Scholar
  60. Singer T, Yordan C, Martienssen RA (2001) Robertson's mutator transposons in A. thaliana are regulated by the chromatin-remodeling gene decrease in DNA methylation (DDM1). Genes Dev 15:591–602PubMedCrossRefGoogle Scholar
  61. Soppe WJ, 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 6:791–802PubMedCrossRefGoogle Scholar
  62. Soppe WJ, Jasencakova Z, Houben A, Kakutani T, Meister A, Huang MS, Jacobsen SE, Schubert I, Fransz PF (2002) DNA methylation controls histone H3 lysine 9 methylation and heterochromatin assembly in Arabidopsis. EMBO J 21:6549–6559PubMedCrossRefGoogle Scholar
  63. Steimer A, Amedeo P, Afsar K, Fransz P, Scheid OM, Paszkowski J (2000) Endogenous targets of transcriptional gene silencing in Arabidopsis. Plant Cell 12:1165–1178PubMedCrossRefGoogle Scholar
  64. Tariq M, Paszkowski J (2004) DNA and histone methylation in plants. Trends Genet 20:244–251PubMedCrossRefGoogle Scholar
  65. Tariq M, Saze H, Probst AV, Lichota J, Habu Y, Paszkowski J (2003) Erasure of CpG methylation in Arabidopsis alters patterns of histone H3 methylation in heterochromatin. Proc Natl Acad Sci U S A 100:8823–8827PubMedCrossRefGoogle Scholar
  66. Tompa R, McCallum CM, Delrow J, Henikoff JG, van Steensel B, Henikoff S (2002) Genome-wide profiling of DNA methylation reveals transposon targets of CHROMOMETHYLASE3. Curr Biol 12:65–68PubMedCrossRefGoogle Scholar
  67. Vaucheret H, Fagard M (2001) Transcriptional gene silencing in plants: targets, inducers and regulators. Trends Genet 17:29–35PubMedCrossRefGoogle Scholar
  68. Vielle-Calzada JP, Thomas J, Spillane C, Coluccio A, Hoeppner MA, Grossniklaus U (1999) Maintenance of genomic imprinting at the Arabidopsis medea locus requires zygotic DDM1 activity. Genes Dev 13:2971–2982PubMedCrossRefGoogle Scholar
  69. Vongs A, Kakutani T, Martienssen RA, Richards EJ (1993) Arabidopsis thaliana DNA methylation mutants. Science 260:1926–1928PubMedCrossRefGoogle Scholar
  70. Wilson ZA, Yang C (2004) Plant gametogenesis: conservation and contrasts in development. Reproduction 128:483–492PubMedCrossRefGoogle Scholar
  71. Wolff GL, Kodell RL, Moore SR, Cooney CA (1998) Maternal epigenetics and methyl supplements affect agouti gene expression in Avy/a mice. FASEB J 12:949–957PubMedGoogle Scholar
  72. Xiao W, Gehring M, Choi Y, Margossian L, Pu H, Harada JJ, Goldberg RB, Pennell RI, Fischer RL (2003) Imprinting of the MEA Polycomb gene is controlled by antagonism between MET1 methyltransferase and DME glycosylase. Dev Cell 5:891–901PubMedCrossRefGoogle Scholar
  73. Yadegari R, Drews GN (2004) Female gametophyte development. Plant Cell Suppl 16:S133–S141CrossRefGoogle Scholar
  74. Zilberman D, Cao X, Jacobsen SE (2003) ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science 299:716–719PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  1. 1.Laboratory of Plant GeneticsUniversity of Geneva, Science IIIGeneva 4Switzerland

Personalised recommendations