Genome-Wide Negative Feedback Drives Transgenerational DNA Methylation Dynamics in Arabidopsis

1. Kelly WG (2014) Transgenerational epigenetics in the germline cycle of Caenorhabditis elegans. Epigenetics Chromatin 7 : 6. doi: 10.1186/1756-8935-7-6 24678826

2. Heard E, Martienssen RA (2014) Transgenerational epigenetic inheritance: myths and mechanisms. Cell 157 : 95–109. doi: 10.1016/j.cell.2014.02.045 24679529

3. Kakutani T (2002) Epi-alleles in plants: inheritance of epigenetic information over generations. Plant Cell Physiol 43 : 1106–1111. 12407189

4. Richards EJ (2011) Natural epigenetic variation in plant species: a view from the field. Curr Opin Plant Biol 14 : 204–209. doi: 10.1016/j.pbi.2011.03.009 21478048

5. Weigel D, Colot V (2012) Epialleles in plant evolution. Genome Biol 13 : 249. doi: 10.1186/gb-2012-13-10-249 23058244

6. Schmitz RJ, Schultz MD, Lewsey MG, O'Malley RC, Urich MA, Libiger O, et al. (2011) Transgenerational epigenetic instability is a source of novel methylation variants. Science 334 : 369–373. doi: 10.1126/science.1212959 21921155

7. Becker C, Hagmann J, Müller J, Koenig D, Stegle O, Borgwardt K, et al. (2011) Spontaneous epigenetic variation in the Arabidopsis thaliana methylome. Nature 480 : 245–249. doi: 10.1038/nature10555 22057020

8. 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 : 8449–8454. 8710891

9. Kankel MW, Ramsey DE, Stokes TL, Flowers SK, Haag JR, Jeddeloh JA, et al. (2003) Arabidopsis MET1 cytosine methyltransferase mutants. Genetics. 163 : 1109–1122. 12663548

10. Zemach A, Kim MY, Hsieh PH, Coleman-Derr D, Eshed-Williams L, Thao K, et al. (2013) The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell 153 : 193–205. doi: 10.1016/j.cell.2013.02.033 23540698

11. Stroud H, Do T, Du J, Zhong X, Feng S, Johnson L, et al. (2014) Non-CG methylation patterns shape the epigenetic landscape in Arabidopsis. Nat Struct Mol Biol 21 : 64–72. doi: 10.1038/nsmb.2735 24336224

12. Johnson LM, Bostick M, Zhang X, Kraft E, Henderson I, Callis J, et al. (2007) The SRA methyl-cytosine-binding domain links DNA and histone methylation. Curr Biol 17 : 379–384. 17239600

13. Inagaki S, Miura-Kamio A, Nakamura Y, Lu F, Cui X, Cao X, et al. (2010) Autocatalytic differentiation of epigenetic modifications within the Arabidopsis genome. EMBO J 29 : 3496–3506. doi: 10.1038/emboj.2010.227 20834229

14. Du J, Zhong X, Bernatavichute YV, Stroud H, Feng S, Caro E, et al. (2012) Dual binding of chromomethylase domains to H3K9me2-containing nucleosomes directs DNA methylation in plants. Cell 151 : 167–180. doi: 10.1016/j.cell.2012.07.034 23021223

15. Saze H, Shiraishi A, Miura A, Kakutani T (2008) Control of genic DNA methylation by a jmjC domain-containing protein in Arabidopsis thaliana. Science 319 : 462–465. doi: 10.1126/science.1150987 18218897

16. Mette MF, Aufsatz W, van der Winden J, Matzke MA, Matzke AJ. (2000) Transcriptional silencing and promoter methylation triggered by double-stranded RNA. EMBO J 19 : 5194–5201. 11013221

17. Cao X, Aufsatz W, Zilberman D, Mette MF, Huang MS, Matzke M, et al. (2003) Role of the DRM and CMT3 methyltransferases in RNA-directed DNA methylation. Curr Biol 13 : 2212–2217. 14680640

18. Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11 : 204–220. doi: 10.1038/nrg2719 20142834

19. Furner IJ, Matzke M (2011) Methylation and demethylation of the Arabidopsis genome. Curr Opin Plant Biol 14 : 137–141. doi: 10.1016/j.pbi.2010.11.004 21159546

20. Pikaard CS, Haag JR, Pontes OM, Blevins T, Cocklin R (2012) A transcription fork model for Pol IV and Pol V-dependent RNA-directed DNA methylation. Cold Spring Harb Symp Quant Biol 77 : 205–212. doi: 10.1101/sqb.2013.77.014803 23567894

21. Zilberman D, Cao X, Johansen LK, Xie Z, Carrington JC, Jacobsen SE (2004) Role of Arabidopsis ARGONAUTE4 in RNA-directed DNA methylation triggered by inverted repeats. Curr Biol 14 : 1214–1220. 15242620

22. Henderson IR, Deleris A, Wong W, Zhong X, Chin HG, Horwitz GA, et al. (2010) The de novo cytosine methyltransferase DRM2 requires intact UBA domains and a catalytically mutated paralog DRM3 during RNA-directed DNA methylation in Arabidopsis thaliana. PLoS Genet 6: e1001182. doi: 10.1371/journal.pgen.1001182 21060858

23. Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan SW, Chen H, et al. (2006) Genome-wide high-resolution mapping and functional analysis of DNA methylation in arabidopsis. Cell 126 : 1189–1201. 16949657

24. Stroud H, Greenberg MV, Feng S, Bernatavichute YV, Jacobsen SE (2013) Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome. Cell 152 : 352–364. doi: 10.1016/j.cell.2012.10.054 23313553

25. Vongs A, Kakutani T, Martienssen RA, Richards EJ (1993) Arabidopsis thaliana DNA methylation mutants. Science 260 : 1926–1928. 8316832

26. Lippman Z, Gendrel AV, Black M, Vaughn MW, Dedhia N, McCombie WR, et al. (2004) Role of transposable elements in heterochromatin and epigenetic control. Nature 430 : 471–476. 15269773

27. Jeddeloh JA, Stokes TL, Richards EJ (1999) Maintenance of genomic methylation requires a SWI2/SNF2-like protein. Nat Genet 22 : 94–97. 10319870

28. Dennis K, Fan T, Geiman T, Yan Q, Muegge K (2001) Lsh, a member of the SNF2 family, is required for genome-wide methylation. Genes Dev 15 : 2940–2944. 11711429

29. Tao Y, Xi S, Shan J, Maunakea A, Che A, Briones V, et al. (2011) Lsh, chromatin remodeling family member, modulates genome-wide cytosine methylation patterns at nonrepeat sequences. Proc Natl Acad Sci U S A 108 : 5626–5631. doi: 10.1073/pnas.1017000108 21427231

30. Kakutani T, Jeddeloh JA, Flowers SK, Munakata K, Richards EJ (1996) Developmental abnormalities and epimutations associated with DNA hypomethylation mutations. Proc Natl Acad Sci U S A 22 : 12406–12411. 8901594

31. Kakutani T (1997) Genetic characterization of late-flowering traits induced by DNA hypomethylation mutation in Arabidopsis thaliana. Plant J 12 : 1447–1451. 9450349

32. 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 : 212–214. 11346800

33. 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 : 591–602. 11238379

34. Tsukahara S, Kobayashi A, Kawabe A, Mathieu O, Miura A, Kakutani T (2009) Bursts of retrotransposition reproduced in Arabidopsis. Nature 461 : 423–426. doi: 10.1038/nature08351 19734880

35. Yi H, Richards EJ (2009) Gene duplication and hypermutation of the pathogen Resistance gene SNC1 in the Arabidopsis bal variant. Genetics 183 : 1227–1234. doi: 10.1534/genetics.109.105569 19797048

36. Soppe WJ, Jacobsen SE, Alonso-Blanco C, Jackson JP, Kakutani T, Koornneef M, et al. (2000) The late flowering phenotype of fwa mutants is caused by gain-of-function epigenetic alleles of a homeodomain gene. Mol Cell 4 : 791–802. 11090618

37. Saze H, Kakutani T (2007) Heritable epigenetic mutation of a transposon-flanked Arabidopsis gene due to lack of the chromatin-remodeling factor DDM1. EMBO J 26 : 3641–3652. 17627280

38. Kinoshita Y, Saze H, Kinoshita T, Miura A, Soppe WJ, Koornneef M, et al. (2007) Control of FWA gene silencing in Arabidopsis thaliana by SINE-related direct repeats. Plant J 49 : 38–45. 17144899

39. Sasaki T, Kobayashi A, Saze H, Kakutani T (2012) RNAi-independent de novo DNA methylation revealed in Arabidopsis mutants of chromatin remodeling gene DDM1. Plant J 70 : 750–758. doi: 10.1111/j.1365-313X.2012.04911.x 22269081

40. Jacobsen SE, Meyerowitz E (1997) Hypermethylated SUPERMAN Epigenetic Alleles in Arabidopsis. Science 277 : 1100–1103. 9262479

41. Kishimoto N, Sakai H, Jackson J, Jacobsen SE, Meyerowitz EM, Dennis ES, et al. (2001) Site specificity of the Arabidopsis METI DNA methyltransferase demonstrated through hypermethylation of the superman locus. Plant Mol Biol 46 : 171–183. 11442057

42. Mathieu O, Reinders J, Caikovski M, Smathajitt C, Paszkowski J (2007) Transgenerational stability of the Arabidopsis epigenome is coordinated by CG methylation. Cell 130 : 851–862. 17803908

43. Rigal M, Kevei Z, Pélissier T, Mathieu O (2012) DNA methylation in an intron of the IBM1 histone demethylase gene stabilizes chromatin modification patterns. EMBO J 31 : 2981–2993. doi: 10.1038/emboj.2012.141 22580822

44. Coleman-Derr D, Zilberman D (2012) Deposition of histone variant H2A.Z within gene bodies regulates responsive genes. PLoS Genet 8: e1002988. doi: 10.1371/journal.pgen.1002988 23071449

45. 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 : 831–838. 9927473

46. Colomé-Tatché M, Cortijo S, Wardenaar R, Morgado L, Lahouze B, Sarazin A, et al. (2012) Features of the Arabidopsis recombination landscape resulting from the combined loss of sequence variation and DNA methylation. Proc Natl Acad Sci U S A 109 : 16240–16245. doi: 10.1073/pnas.1212955109 22988127

47. Teixeira FK, Heredia F, Sarazin A, Roudier F, Boccara M, Ciaudo C, et al. (2009) A role for RNAi in the selective correction of DNA methylation defects. Science 323 : 1600–1604. doi: 10.1126/science.1165313 19179494

48. Huettel B, Kanno T, Daxinger L, Aufsatz W, Matzke AJ, Matzke M (2006) Endogenous targets of RNA-directed DNA methylation and Pol IV in Arabidopsis. EMBO J 25 : 2828–2836. 16724114

49. Arteaga-Vazquez MA, Chandler VL. (2010) Paramutation in maize: RNA mediated trans-generational gene silencing. Curr Opin Genet Dev 20 : 156–163. doi: 10.1016/j.gde.2010.01.008 20153628

50. Hollick JB. (2012) Paramutation: a trans-homolog interaction affecting heritable gene regulation. Curr Opin Plant Biol 15 : 536–543. doi: 10.1016/j.pbi.2012.09.003 23017240

51. Greaves IK, Groszmann M, Ying H, Taylor JM, Peacock WJ, Dennis ES (2012) Trans chromosomal methylation in Arabidopsis hybrids. Proc Natl Acad Sci U S A 109 : 3570–3575. doi: 10.1073/pnas.1201043109 22331882

52. Deleris A, Stroud H, Bernatavichute Y, Johnson E, Klein G, Schubert D, et al. (2012) Loss of the DNA methyltransferase MET1 Induces H3K9 hypermethylation at PcG target genes and redistribution of H3K27 trimethylation to transposons in Arabidopsis thaliana. PLoS Genet 8: e1003062. doi: 10.1371/journal.pgen.1003062 23209430

53. Ross JP, Rand KN, Molloy PL (2010) Hypomethylation of repeated DNA sequences in cancer. Epigenomics 2 : 245–269. doi: 10.2217/epi.10.2 22121873

54. Ehrlich M (2009) DNA hypomethylation in cancer cells. Epigenomics 1 : 239–259. doi: 10.2217/epi.09.33 20495664

55. Dimitri P, Pisano C (1989) Position effect variegation in Drosophila melanogaster: relationship between suppression effect and the amount of Y chromosome. Genetics 122 : 793–800. 2503420

56. Locke J, Kotarski MA, Tartof KD (1988) Dosage-dependent modifiers of position effect variegation in Drosophila and a mass action model that explains their effect. Genetics 120 : 181–198. 3146523

57. Henikoff S (1996) Dosage-dependent modification of position-effect variegation in Drosophila. Bioessays 18 : 401–409. 8639163

58. Inagaki S, Kakutani T (2013) What triggers differential DNA methylation of genes and TEs: contribution of body methylation? Cold Spring Harb Symp Quant Biol 2012 77 : 155–160. doi: 10.1101/sqb.2013.77.016212 23302809

59. Turing AM (1953) The chemical basis of morphogenesis. Philos Trans R Soc Lond B Biol Sci 237 : 37–72.

60. Meinhardt H, Gierer A (2000) Pattern formation by local self-activation and lateral inhibition. Bioessays 22 : 753–760. 10918306

61. Hawkins JS, Kim H, Nason JD, Wing RA, Wendel JF (2006) Differential lineage-specific amplification of transposable elements is responsible for genome size variation in Gossypium. Genome Res 16 : 1252–1261. 16954538

62. Cullis CA (2005) Mechanisms and control of rapid genomic changes in flax. Ann Bot 95 : 201–206. 15596467

63. Woo HR, Richards EJ (2008) Natural variation in DNA methylation in ribosomal RNA genes of Arabidopsis thaliana. BMC Plant Biol 8 : 92. doi: 10.1186/1471-2229-8-92 18783613

64. Johannes F, Porcher E, Teixeira FK, Saliba-Colombani V, Simon M, Agier N, et al. (2009) Assessing the impact of transgenerational epigenetic variation on complex traits. PLoS Genet. 5: e1000530. doi: 10.1371/journal.pgen.1000530 19557164

65. Fu Y, Kawabe A, Etcheverry M, Ito T, Toyoda A, Fujiyama A, et al. (2013) Mobilization of a plant transposon by expression of the transposon-encoded anti-silencing factor. EMBO J 32 : 2407–2417. doi: 10.1038/emboj.2013.169 23900287

66. Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25. doi: 10.1186/gb-2009-10-3-r25 19261174

67. Schultz MD, Schmitz RJ, Ecker JR (2012) 'Leveling' the playing field for analyses of single-base resolution DNA methylomes. Trends Genet 28 : 583–585. doi: 10.1016/j.tig.2012.10.012 23131467

68. de Hoon MJ, Imoto S, Nolan J, Miyano S (2004) Open source clustering software. Bioinformatics 20 : 1453–1454. 14871861

69. Saldanha AJ (2004) Java Treeview—extensible visualization of microarray data. Bioinformatics 20 : 3246–3248. 15180930

70. Gendrel AV, Lippman Z, Martienssen R, Colot V (2005) Profiling histone modification patterns in plants using genomic tiling microarrays. Nat Protocols 2 : 213–218.

71. Hayashi-Takanaka Y, Yamagata K, Wakayama T, Stasevich TJ, Kainuma T, Tsurimoto T, et al. (2011) Tracking epigenetic histone modifications in single cells using Fab-based live endogenous modification labeling. Nucleic Acids Res. 39 : 6475–88. doi: 10.1093/nar/gkr343 21576221

72. Luo C, Sidote DJ, Zhang Y, Kerstetter RA, Michael TP, Lam E (2013) Integrative analysis of chromatin states in Arabidopsis identified potential regulatory mechanisms for natural antisense transcript production. Plant J 73 : 77–90.

73. Lamesch P, Berardini TZ, Li D, Swarbreck D, Wilks C, Sasidharan R, et al. (2012) The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res 40: D1202–1210. doi: 10.1093/nar/gkr1090 22140109

74. Nicol JW, Helt GA, Blanchard SG, Raja A, Loraine AE (2009) The Integrated Genome Browser: free software for distribution and exploration of genome-scale datasets. Bioinformatics 25 : 2730–2731. doi: 10.1093/bioinformatics/btp472 19654113

75. Ebbs ML, Bender J (2006) Locus-specific control of DNA methylation by the Arabidopsis SUVH5 histone methyltransferase. Plant Cell 18 : 1166–1176. 16582009

76. Penterman J, Zilberman D, Huh JH, Ballinger T, Henikoff S, Fischer RL (2007) DNA demethylation in the Arabidopsis genome. Proc Natl Acad Sci U S A 104 : 6752–6757. 17409185