Transgenerational epigenetic inheritance: Myths and mechanisms

Cell

Volumn 157, Issue 1, 2014, Pages 95-109

  Heard, Edith ^a,b   Martienssen, Robert A ^c,d  

^a INSTITUT CURIE   (France)

^b Centre de Recherche Interdisciplinaire en Biologie   (France)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d PSL RESEARCH UNIVERSITY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; HISTONE; UNTRANSLATED RNA;

CHROMATIN; DNA METHYLATION; DNA SEQUENCE; EPIGENETICS; FEEDBACK SYSTEM; GENE EXPRESSION; GENE MUTATION; GENE SEQUENCE; GENE SILENCING; GENETIC TRAIT; GENETIC VARIABILITY; GENOME IMPRINTING; GENOTYPE ENVIRONMENT INTERACTION; HISTONE MODIFICATION; HUMAN; HUMAN GENOME; INHERITANCE; MOLECULAR EVOLUTION; NONHUMAN; NUCLEAR REPROGRAMMING; PLANT BREEDING; PRIORITY JOURNAL; REVIEW; RNA INTERFERENCE; TRANSGENE; TRANSGENERATIONAL EPIGENETIC INHERITANCE; TRANSPOSON; ARTICLE; GERMLINE MUTATION;

ANIMALS; DNA METHYLATION; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION; GENE-ENVIRONMENT INTERACTION; GERM CELLS; HUMANS; PLANTS;

EID: 84897139220     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2014.02.045     Document Type: Review

References (138)

1. F. Andrés, and G. Coupland The genetic basis of flowering responses to seasonal cues Nat. Rev. Genet. 13 2012 627 639
2. M.D. Anway, A.S. Cupp, M. Uzumcu, and M.K. Skinner Epigenetic transgenerational actions of endocrine disruptors and male fertility Science 308 2005 1466 1469
3. M.A. Arteaga-Vazquez, and V.L. Chandler Paramutation in maize: RNA mediated trans-generational gene silencing Curr. Opin. Genet. Dev. 20 2010 156 163
4. M. Arteaga-Vazquez, L. Sidorenko, F.A. Rabanal, R. Shrivistava, K. Nobuta, P.J. Green, B.C. Meyers, and V.L. Chandler RNA-mediated trans-communication can establish paramutation at the b1 locus in maize Proc. Natl. Acad. Sci. USA 107 2010 12986 12991
5. A. Ashe, A. Sapetschnig, E.-M. Weick, J. Mitchell, M.P. Bagijn, A.C. Cording, A.-L. Doebley, L.D. Goldstein, N.J. Lehrbach, and J. Le Pen et al. piRNAs can trigger a multigenerational epigenetic memory in the germline of C elegans Cell 150 2012 88 99
6. J.E. Barbour, I.T. Liao, J.L. Stonaker, J.P. Lim, C.C. Lee, S.E. Parkinson, J. Kermicle, S.A. Simon, B.C. Meyers, and R. Williams-Carrier et al. required to maintain repression2 is a novel protein that facilitates locus-specific paramutation in maize Plant Cell 24 2012 1761 1775
7. C. Becker, and D. Weigel Epigenetic variation: origin and transgenerational inheritance Curr. Opin. Plant Biol. 15 2012 562 567
8. C. Becker, J. Hagmann, J. Müller, D. Koenig, O. Stegle, K. Borgwardt, and D. Weigel Spontaneous epigenetic variation in the Arabidopsis thaliana methylome Nature 480 2011 245 249
9. A. Bird Perceptions of epigenetics Nature 447 2007 396 398
10. J. Brennecke, C.D. Malone, A.A. Aravin, R. Sachidanandam, A. Stark, and G.J. Hannon An epigenetic role for maternally inherited piRNAs in transposon silencing Science 322 2008 1387 1392
11. R.A. Brink, E.D. Styles, and J.D. Axtell Paramutation: directed genetic change. Paramutation occurs in somatic cells and heritably alters the functional state of a locus Science 159 1968 161 170
12. U. Brykczynska, M. Hisano, S. Erkek, L. Ramos, E.J. Oakeley, T.C. Roloff, C. Beisel, D. Schübeler, M.B. Stadler, and A.H. Peters Repressive and active histone methylation mark distinct promoters in human and mouse spermatozoa Nat. Struct. Mol. Biol. 17 2010 679 687
13. K. Brzeska, J. Brzeski, J. Smith, and V.L. Chandler Transgenic expression of CBBP, a CXC domain protein, establishes paramutation in maize Proc. Natl. Acad. Sci. USA 107 2010 5516 5521
14. B.A. Buckley, K.B. Burkhart, S.G. Gu, G. Spracklin, A. Kershner, H. Fritz, J. Kimble, A. Fire, and S. Kennedy A nuclear Argonaute promotes multigenerational epigenetic inheritance and germline immortality Nature 489 2012 447 451
15. Burbank, L. (1906). The training of the human plant. The Century Magazine, May, 1906. pp. 127-137.
16. K.B. Burkhart, S. Guang, B.A. Buckley, L. Wong, A.F. Bochner, and S. Kennedy A pre-mRNA-associating factor links endogenous siRNAs to chromatin regulation PLoS Genet. 7 2011 e1002249
17. N.O. Burton, K.B. Burkhart, and S. Kennedy Nuclear RNAi maintains heritable gene silencing in Caenorhabditis elegans Proc. Natl. Acad. Sci. USA 108 2011 19683 19688
18. J.P. Calarco, F. Borges, M.T. Donoghue, F. Van Ex, P.E. Jullien, T. Lopes, R. Gardner, F. Berger, J.A. Feijó, J.D. Becker, and R.A. Martienssen Reprogramming of DNA methylation in pollen guides epigenetic inheritance via small RNA Cell 151 2012 194 205
19. B.R. Carone, L. Fauquier, N. Habib, J.M. Shea, C.E. Hart, R. Li, C. Bock, C. Li, H. Gu, and P.D. Zamore et al. Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals Cell 143 2010 1084 1096
20. S.E. Castel, and R.A. Martienssen RNA interference in the nucleus: roles for small RNAs in transcription, epigenetics and beyond Nat. Rev. Genet. 14 2013 100 112
21. D.L. Chalker, and M.C. Yao DNA elimination in ciliates: transposon domestication and genome surveillance Annu. Rev. Genet. 45 2011 227 246
22. F.A. Champagne, and J.P. Curley Epigenetic mechanisms mediating the long-term effects of maternal care on development Neurosci. Biobehav. Rev. 33 2009 593 600
23. V.L. Chandler Paramutation: from maize to mice Cell 128 2007 641 645
24. V.L. Chandler Paramutation's properties and puzzles Science 330 2010 628 629
25. M. Colomé-Tatché, S. Cortijo, R. Wardenaar, L. Morgado, B. Lahouze, A. Sarazin, M. Etcheverry, A. Martin, S. Feng, and E. Duvernois-Berthet et al. Features of the Arabidopsis recombination landscape resulting from the combined loss of sequence variation and DNA methylation Proc. Natl. Acad. Sci. USA 109 2012 16240 16245
26. S. Cortijo, R. Wardenaar, M. Colomé-Tatché, A. Gilly, M. Etcheverry, K. Labadie, E. Caillieux, F. Hospital, J.-M. Aury, and P. Wincker et al. Mapping the epigenetic basis of complex traits Science 2014 10.1126/science.1248127 Published online February 6, 2014
27. K.M. Creasey, J. Zhai, F. Borges, F. Van Ex, M. Regulski, B.C. Meyers, and R. Martienssen miRNAs trigger widespread epigenetically-activated siRNAs from transposons in Arabidopsis Nature 2014 10.1038/nature13069 Published online March 16, 2014
28. P. Cubas, C. Vincent, and E. Coen An epigenetic mutation responsible for natural variation in floral symmetry Nature 401 1999 157 161
29. L. Daxinger, and E. Whitelaw Understanding transgenerational epigenetic inheritance via the gametes in mammals Nat. Rev. Genet. 13 2012 153 162
30. A. de Vanssay, A.L. Bougé, A. Boivin, C. Hermant, L. Teysset, V. Delmarre, C. Antoniewski, and S. Ronsseray Paramutation in Drosophila linked to emergence of a piRNA-producing locus Nature 490 2012 112 115
31. D.M. Dietz, Q. Laplant, E.L. Watts, G.E. Hodes, S.J. Russo, J. Feng, R.S. Oosting, V. Vialou, and E.J. Nestler Paternal transmission of stress-induced pathologies Biol. Psychiatry 70 2011 408 414
32. S. Durand, N. Bouché, E. Perez Strand, O. Loudet, and C. Camilleri Rapid establishment of genetic incompatibility through natural epigenetic variation Curr. Biol. 22 2012 326 331
33. S.R. Eichten, R. Briskine, J. Song, Q. Li, R. Swanson-Wagner, P.J. Hermanson, A.J. Waters, E. Starr, P.T. West, and P. Tiffin et al. Epigenetic and genetic influences on DNA methylation variation in maize populations Plant Cell 25 2013 2783 2797
34. R.A. Enke, Z. Dong, and J. Bender Small RNAs prevent transcription- coupled loss of histone H3 lysine 9 methylation in Arabidopsis thaliana PLoS Genet. 7 2011 e1002350
35. K.F. Erhard Jr., S.E. Parkinson, S.M. Gross, J.E. Barbour, J.P. Lim, and J.B. Hollick Maize RNA polymerase IV defines trans-generational epigenetic variation Plant Cell 25 2013 808 819
36. C. Eun, Z.J. Lorkovic, T. Sasaki, U. Naumann, A.J. Matzke, and M. Matzke Use of forward genetic screens to identify genes required for RNA-directed DNA methylation in Arabidopsis thaliana Cold Spring Harb. Symp. Quant. Biol. 77 2012 195 204
37. A.C. Ferguson-Smith, and M.E. Patti You are what your dad ate Cell Metab. 13 2011 115 117
38. M. Gehring, K.L. Bubb, and S. Henikoff Extensive demethylation of repetitive elements during seed development underlies gene imprinting Science 324 2009 1447 1451
39. S.J. Gould The Panda's Thumb 1980 W.W. Norton & Company New York
40. I.K. Greaves, M. Groszmann, H. Ying, J.M. Taylor, W.J. Peacock, and E.S. Dennis Trans chromosomal methylation in Arabidopsis hybrids Proc. Natl. Acad. Sci. USA 109 2012 3570 3575
41. E.L. Greer, T.J. Maures, D. Ucar, A.G. Hauswirth, E. Mancini, J.P. Lim, B.A. Benayoun, Y. Shi, and A. Brunet Transgenerational epigenetic inheritance of longevity in Caenorhabditis elegans Nature 479 2011 365 371
42. S.G. Gu, J. Pak, S. Guang, J.M. Maniar, S. Kennedy, and A. Fire Amplification of siRNA in Caenorhabditis elegans generates a transgenerational sequence-targeted histone H3 lysine 9 methylation footprint Nat. Genet. 44 2012 157 164
43. J.F. Gutierrez-Marcos, and H.G. Dickinson Epigenetic reprogramming in plant reproductive lineages Plant Cell Physiol. 53 2012 817 823
44. J.R. Haag, and C.S. Pikaard Multisubunit RNA polymerases IV and V: purveyors of non-coding RNA for plant gene silencing Nat. Rev. Mol. Cell Biol. 12 2011 483 492
45. J.A. Hackett, and M.A. Surani Beyond DNA: programming and inheritance of parental methylomes Cell 153 2013 737 739
46. J.A. Hackett, J.J. Zylicz, and M.A. Surani Parallel mechanisms of epigenetic reprogramming in the germline Trends Genet. 28 2012 164 174
47. C.N. Hales, and D.J. Barker Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis Int. J. Epidemiol. 42 2013 1215 1222
48. S.S. Hammoud, D.A. Nix, H. Zhang, J. Purwar, D.T. Carrell, and B.R. Cairns Distinctive chromatin in human sperm packages genes for embryo development Nature 460 2009 473 478
49. W. Harvey Exercitationes de Generatione Animalium 1651 Londini, Typis Du-Gardianis; Impensis O. Pulleyn London
50. T. Hilbricht, S. Varotto, V. Sgaramella, D. Bartels, F. Salamini, and A. Furini Retrotransposons and siRNA have a role in the evolution of desiccation tolerance leading to resurrection of the plant Craterostigma plantagineum New Phytol. 179 2008 877 887
51. M.P. Hitchins, R.W. Rapkins, C.T. Kwok, S. Srivastava, J.J. Wong, L.M. Khachigian, P. Polly, J. Goldblatt, and R.L. Ward Dominantly inherited constitutional epigenetic silencing of MLH1 in a cancer-affected family is linked to a single nucleotide variant within the 5'UTR Cancer Cell 20 2011 200 213
52. Z. Hochberg, R. Feil, M. Constancia, M. Fraga, C. Junien, J.C. Carel, P. Boileau, Y. Le Bouc, C.L. Deal, and K. Lillycrop et al. Child health, developmental plasticity, and epigenetic programming Endocr. Rev. 32 2011 159 224
53. L.M. Holeski, G. Jander, and A.A. Agrawal Transgenerational defense induction and epigenetic inheritance in plants Trends Ecol. Evol. 27 2012 618 626
54. J.B. Hollick Paramutation: a trans-homolog interaction affecting heritable gene regulation Curr. Opin. Plant Biol. 15 2012 536 543
55. T.F. Hsieh, C.A. Ibarra, P. Silva, A. Zemach, L. Eshed-Williams, R.L. Fischer, and D. Zilberman Genome-wide demethylation of Arabidopsis endosperm Science 324 2009 1451 1454
56. X.A. Huang, H. Yin, S. Sweeney, D. Raha, M. Snyder, and H. Lin A major epigenetic programming mechanism guided by piRNAs Dev. Cell 24 2013 502 516
57. C.A. Ibarra, X. Feng, V.K. Schoft, T.F. Hsieh, R. Uzawa, J.A. Rodrigues, A. Zemach, N. Chumak, A. Machlicova, and T. Nishimura et al. Active DNA demethylation in plant companion cells reinforces transposon methylation in gametes Science 337 2012 1360 1364
58. M. Ingouff, Y. Hamamura, M. Gourgues, T. Higashiyama, and F. Berger Distinct dynamics of HISTONE3 variants between the two fertilization products in plants Curr. Biol. 17 2007 1032 1037
59. D.V. Irvine, M. Zaratiegui, N.H. Tolia, D.B. Goto, D.H. Chitwood, M.W. Vaughn, L. Joshua-Tor, and R.A. Martienssen Argonaute slicing is required for heterochromatic silencing and spreading Science 313 2006 1134 1137
60. H. Ito, H. Gaubert, E. Bucher, M. Mirouze, I. Vaillant, and J. Paszkowski An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress Nature 472 2011 115 119
61. E. Jablonka, and G. Raz Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution Q. Rev. Biol. 84 2009 131 176
62. Y. Jacob, E. Bergamin, M.T. Donoghue, V. Mongeon, C. Le Blanc, P. Voigt, C. Underwood, J.S. Brunzelle, S.D. Michaels, and D. Reinberg et al. Selective methylation of histone H3 variant H3.1 regulates heterochromatin replication Science 2014 10.1126/science.1248357 Published online March 14, 2014
63. V. Jauvion, M. Rivard, N. Bouteiller, T. Elmayan, and H. Vaucheret RDR2 partially antagonizes the production of RDR6-dependent siRNA in sense transgene-mediated PTGS PLoS ONE 7 2012 e29785
64. L. Jiang, J. Zhang, J.J. Wang, L. Wang, L. Zhang, G. Li, X. Yang, X. Ma, X. Sun, and J. Cai et al. Sperm, but not oocyte, DNA methylome is inherited by zebrafish early embryos Cell 153 2013 773 784
65. R.L. Jirtle, and M.K. Skinner Environmental epigenomics and disease susceptibility Nat. Rev. Genet. 8 2007 253 262
66. F. Johannes, E. Porcher, F.K. Teixeira, V. Saliba-Colombani, M. Simon, N. Agier, A. Bulski, J. Albuisson, F. Heredia, and P. Audigier et al. Assessing the impact of transgenerational epigenetic variation on complex traits PLoS Genet. 5 2009 e1000530
67. P.E. Jullien, D. Susaki, R. Yelagandula, T. Higashiyama, and F. Berger DNA methylation dynamics during sexual reproduction in Arabidopsis thaliana Curr. Biol. 22 2012 1825 1830
68. T. Kakutani, J.A. Jeddeloh, S.K. Flowers, K. Munakata, and E.J. Richards Developmental abnormalities and epimutations associated with DNA hypomethylation mutations Proc. Natl. Acad. Sci. USA 93 1996 12406 12411
69. D.J. Katz, T.M. Edwards, V. Reinke, and W.G. Kelly A C elegans LSD1 demethylase contributes to germline immortality by reprogramming epigenetic memory Cell 137 2009 308 320
70. C. Keller, and M. Bühler Chromatin-associated ncRNA activities Chromosome Res. 21 2013 627 641
71. W.G. Kelly, and R. Aramayo Meiotic silencing and the epigenetics of sex Chromosome Res. 15 2007 633 651
72. J. Kiani, V. Grandjean, R. Liebers, F. Tuorto, H. Ghanbarian, F. Lyko, F. Cuzin, and M. Rassoulzadegan RNA-mediated epigenetic heredity requires the cytosine methyltransferase Dnmt2 PLoS Genet. 9 2013 e1003498
73. J.A. Law, and S.E. Jacobsen Establishing, maintaining and modifying DNA methylation patterns in plants and animals Nat. Rev. Genet. 11 2010 204 220
74. A. Le Thomas, A.K. Rogers, A. Webster, G.K. Marinov, S.E. Liao, E.M. Perkins, J.K. Hur, A.A. Aravin, and K.F. Tóth Piwi induces piRNA-guided transcriptional silencing and establishment of a repressive chromatin state Genes Dev. 27 2013 390 399
75. X. Li, M. Ito, F. Zhou, N. Youngson, X. Zuo, P. Leder, and A.C. Ferguson-Smith A maternal-zygotic effect gene, Zfp57, maintains both maternal and paternal imprints Dev. Cell 15 2008 547 557
76. Q. Li, S.R. Eichten, P.J. Hermanson, and N.M. Springer Inheritance patterns and stability of DNA methylation variation in maize near-isogenic lines Genetics 2013 10.1534/genetics.113.158980 Published online December 20, 2013
77. J.P. Lim, and A. Brunet Bridging the transgenerational gap with epigenetic memory Trends Genet. 29 2013 176 186
78. C.R. Linnen, Y.P. Poh, B.K. Peterson, R.D. Barrett, J.G. Larson, J.D. Jensen, and H.E. Hoekstra Adaptive evolution of multiple traits through multiple mutations at a single gene Science 339 2013 1312 1316
79. Z. Lippman, A.-V. Gendrel, M. Black, M.W. Vaughn, N. Dedhia, W.R. McCombie, K. Lavine, V. Mittal, B. May, and K.D. Kasschau et al. Role of transposable elements in heterochromatin and epigenetic control Nature 430 2004 471 476
80. D. Lisch Regulation of transposable elements in maize Curr. Opin. Plant Biol. 15 2012 511 516
81. D. Lisch How important are transposons for plant evolution? Nat. Rev. Genet. 14 2013 49 61
82. K. Manning, M. Tör, M. Poole, Y. Hong, A.J. Thompson, G.J. King, J.J. Giovannoni, and G.B. Seymour A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening Nat. Genet. 38 2006 948 952
83. A. Marí-Ordóñez, A. Marchais, M. Etcheverry, A. Martin, V. Colot, and O. Voinnet Reconstructing de novo silencing of an active plant retrotransposon Nat. Genet. 45 2013 1029 1039
84. R. Martienssen, A. Barkan, W.C. Taylor, and M. Freeling Somatically heritable switches in the DNA modification of Mu transposable elements monitored with a suppressible mutant in maize Genes Dev. 4 1990 331 343
85. O. Mathieu, J. Reinders, M. Caikovski, C. Smathajitt, and J. Paszkowski Transgenerational stability of the Arabidopsis epigenome is coordinated by CG methylation Cell 130 2007 851 862
86. B. McClintock Some parallels between gene control systems in maize and in bacteria Am. Nat. 95 1961 265 277
87. D.M. Messerschmidt Should I stay or should I go: protection and maintenance of DNA methylation at imprinted genes Epigenetics 7 2012 969 975
88. D.M. Messerschmidt, W. de Vries, M. Ito, D. Solter, A. Ferguson-Smith, and B.B. Knowles Trim28 is required for epigenetic stability during mouse oocyte to embryo transition Science 335 2012 1499 1502
89. M. Mirouze, J. Reinders, E. Bucher, T. Nishimura, K. Schneeberger, S. Ossowski, J. Cao, D. Weigel, J. Paszkowski, and O. Mathieu Selective epigenetic control of retrotransposition in Arabidopsis Nature 461 2009 427 430
90. M. Mirouze, M. Lieberman-Lazarovich, R. Aversano, E. Bucher, J. Nicolet, J. Reinders, and J. Paszkowski Loss of DNA methylation affects the recombination landscape in Arabidopsis Proc. Natl. Acad. Sci. USA 109 2012 5880 5885
91. R.A. Mosher, C.W. Melnyk, K.A. Kelly, R.M. Dunn, D.J. Studholme, and D.C. Baulcombe Uniparental expression of PolIV-dependent siRNAs in developing endosperm of Arabidopsis Nature 460 2009 283 286
92. T. Nakamura, Y.J. Liu, H. Nakashima, H. Umehara, K. Inoue, S. Matoba, M. Tachibana, A. Ogura, Y. Shinkai, and T. Nakano PGC7 binds histone H3K9me2 to protect against conversion of 5mC to 5hmC in early embryos Nature 486 2012 415 419
93. N. Padmanabhan, D. Jia, C. Geary-Joo, X. Wu, A.C. Ferguson-Smith, E. Fung, M.C. Bieda, F.F. Snyder, R.A. Gravel, J.C. Cross, and E.D. Watson Mutation in folate metabolism causes epigenetic instability and transgenerational effects on development Cell 155 2013 81 93
94. R.C. Painter, C. Osmond, P. Gluckman, M. Hanson, D.I. Phillips, and T.J. Roseboom Transgenerational effects of prenatal exposure to the Dutch famine on neonatal adiposity and health in later life BJOG 115 2008 1243 1249
95. A. Pecinka, and O. Mittelsten Scheid Stress-induced chromatin changes: a critical view on their heritability Plant Cell Physiol. 53 2012 801 808
96. M.E. Potok, D.A. Nix, T.J. Parnell, and B.R. Cairns Reprogramming the maternal zebrafish genome after fertilization to match the paternal methylation pattern Cell 153 2013 759 772
97. M. Ptashne Epigenetics: core misconcept Proc. Natl. Acad. Sci. USA 110 2013 7101 7103
98. Y. Qi, X. He, X.-J. Wang, O. Kohany, J. Jurka, and G.J. Hannon Distinct catalytic and non-catalytic roles of ARGONAUTE4 in RNA-directed DNA methylation Nature 443 2006 1008 1012
99. E.J. Radford, E. Isganaitis, J. Jimenez-Chillaron, J. Schroeder, M. Molla, S. Andrews, N. Didier, M. Charalambous, K. McEwen, and G. Marazzi et al. An unbiased assessment of the role of imprinted genes in an intergenerational model of developmental programming PLoS Genet. 8 2012 e1002605
100. O.J. Rando Daddy issues: paternal effects on phenotype Cell 151 2012 702 708
101. M. Rassoulzadegan, V. Grandjean, P. Gounon, S. Vincent, I. Gillot, and F. Cuzin RNA-mediated non-mendelian inheritance of an epigenetic change in the mouse Nature 441 2006 469 474
102. A. Raval, S.M. Tanner, J.C. Byrd, E.B. Angerman, J.D. Perko, S.S. Chen, B. Hackanson, M.R. Grever, D.M. Lucas, and J.J. Matkovic et al. Downregulation of death-associated protein kinase 1 (DAPK1) in chronic lymphocytic leukemia Cell 129 2007 879 890
103. T.S. Ream, D.P. Woods, and R.M. Amasino The molecular basis of vernalization in different plant groups Cold Spring Harb. Symp. Quant. Biol. 77 2012 105 115
104. R. Rebollo, K. Miceli-Royer, Y. Zhang, S. Farivar, L. Gagnier, and D.L. Mager Epigenetic interplay between mouse endogenous retroviruses and host genes Genome Biol. 13 2012 R89
105. O. Rechavi, G. Minevich, and O. Hobert Transgenerational inheritance of an acquired small RNA-based antiviral response in C elegans Cell 147 2011 1248 1256
106. M. Regulski, Z. Lu, J. Kendall, M.T. Donoghue, J. Reinders, V. Llaca, S. Deschamps, A. Smith, D. Levy, and W.R. McCombie et al. The maize methylome influences mRNA splice sites and reveals widespread paramutation-like switches guided by small RNA Genome Res. 23 2013 1651 1662
107. J. Reinders, M. Mirouze, J. Nicolet, and J. Paszkowski Parent-of-origin control of transgenerational retrotransposon proliferation in Arabidopsis EMBO Rep. 14 2013 823 828
108. J.J. Remy Stable inheritance of an acquired behavior in Caenorhabditis elegans Curr. Biol. 20 2010 R877 R878
109. E.J. Richards Inherited epigenetic variation - revisiting soft inheritance Nat. Rev. Genet. 7 2006 395 401
110. N.V. Rozhkov, M. Hammell, and G.J. Hannon Multiple roles for Piwi in silencing Drosophila transposons Genes Dev. 27 2013 400 412
111. R.J. Schmitz, and J.R. Ecker Epigenetic and epigenomic variation in Arabidopsis thaliana Trends Plant Sci. 17 2012 149 154
112. R.J. Schmitz, M.D. Schultz, M.G. Lewsey, R.C. O'Malley, M.A. Urich, O. Libiger, N.J. Schork, and J.R. Ecker Transgenerational epigenetic instability is a source of novel methylation variants Science 334 2011 369 373
113. R.J. Schmitz, M.D. Schultz, M.A. Urich, J.R. Nery, M. Pelizzola, O. Libiger, A. Alix, R.B. McCosh, H. Chen, N.J. Schork, and J.R. Ecker Patterns of population epigenomic diversity Nature 495 2013 193 198
114. S. Schneider, W. Kaufmann, R. Buesen, and B. van Ravenzwaay Vinclozolin - the lack of a transgenerational effect after oral maternal exposure during organogenesis Reprod. Toxicol. 25 2008 352 360
115. V.K. Schoft, N. Chumak, M. Mosiolek, L. Slusarz, V. Komnenovic, L. Brownfield, D. Twell, T. Kakutani, and H. Tamaru Induction of RNA-directed DNA methylation upon decondensation of constitutive heterochromatin EMBO Rep. 10 2009 1015 1021
116. S. Seisenberger, S. Andrews, F. Krueger, J. Arand, J. Walter, F. Santos, C. Popp, B. Thienpont, W. Dean, and W. Reik The dynamics of genome-wide DNA methylation reprogramming in mouse primordial germ cells Mol. Cell 48 2012 849 862
117. S. Seisenberger, J.R. Peat, T.A. Hore, F. Santos, W. Dean, and W. Reik Reprogramming DNA methylation in the mammalian life cycle: building and breaking epigenetic barriers Philos. Trans. R. Soc. Lond. B Biol. Sci. 368 2013 20110330
118. K.H. Seong, D. Li, H. Shimizu, R. Nakamura, and S. Ishii Inheritance of stress-induced, ATF-2-dependent epigenetic change Cell 145 2011 1049 1061
119. C.C. Sheldon, M.J. Hills, C. Lister, C. Dean, E.S. Dennis, and W.J. Peacock Resetting of FLOWERING LOCUS C expression after epigenetic repression by vernalization Proc. Natl. Acad. Sci. USA 105 2008 2214 2219
120. M. Shirayama, M. Seth, H.-C. Lee, W. Gu, T. Ishidate, D. Conte, and C.C. Mello piRNAs initiate an epigenetic memory of nonself RNA in the C elegans germline Cell 150 2012 65 77
121. G. Sienski, D. Dönertas, and J. Brennecke Transcriptional silencing of transposons by Piwi and maelstrom and its impact on chromatin state and gene expression Cell 151 2012 964 980
122. A. Slaughter, X. Daniel, V. Flors, E. Luna, B. Hohn, and B. Mauch-Mani Descendants of primed Arabidopsis plants exhibit resistance to biotic stress Plant Physiol. 158 2012 835 843
123. R.K. Slotkin, and R. Martienssen Transposable elements and the epigenetic regulation of the genome Nat. Rev. Genet. 8 2007 272 285
124. R.K. Slotkin, M. Vaughn, F. Borges, M. Tanurdzić, J.D. Becker, J.A. Feijó, and R.A. Martienssen Epigenetic reprogramming and small RNA silencing of transposable elements in pollen Cell 136 2009 461 472
125. Z.D. Smith, M.M. Chan, T.S. Mikkelsen, H. Gu, A. Gnirke, A. Regev, and A. Meissner A unique regulatory phase of DNA methylation in the early mammalian embryo Nature 484 2012 339 344
126. J. Song, A. Angel, M. Howard, and C. Dean Vernalization - a cold-induced epigenetic switch J. Cell Sci. 125 2012 3723 3731
127. H. Stroud, T. Do, J. Du, X. Zhong, S. Feng, L. Johnson, D.J. Patel, and S.E. Jacobsen Non-CG methylation patterns shape the epigenetic landscape in Arabidopsis Nat. Struct. Mol. Biol. 21 2014 64 72
128. F.K. Teixeira, F. Heredia, A. Sarazin, F. Roudier, M. Boccara, C. Ciaudo, C. Cruaud, J. Poulain, M. Berdasco, and M.F. Fraga et al. A role for RNAi in the selective correction of DNA methylation defects Science 323 2009 1600 1604
129. V. Théodorou Susceptibility to stress-induced visceral sensitivity: a bad legacy for next generations Neurogastroenterol. Motil. 25 2013 927 930
130. M.W. Vaughn, M. Tanurdzić, Z. Lippman, H. Jiang, R. Carrasquillo, P.D. Rabinowicz, N. Dedhia, W.R. McCombie, N. Agier, and A. Bulski et al. Epigenetic natural variation in Arabidopsis thaliana PLoS Biol. 5 2007 e174
131. M.V. Veenendaal, R.C. Painter, S.R. de Rooij, P.M. Bossuyt, J.A. van der Post, P.D. Gluckman, M.A. Hanson, and T.J. Roseboom Transgenerational effects of prenatal exposure to the 1944-45 Dutch famine BJOG 120 2013 548 553
132. T.M. Vu, M. Nakamura, J.P. Calarco, D. Susaki, P.Q. Lim, T. Kinoshita, T. Higashiyama, R.A. Martienssen, and F. Berger RNA-directed DNA methylation regulates parental genomic imprinting at several loci in Arabidopsis Development 140 2013 2953 2960
133. J. Walter, B. Hutter, T. Khare, and M. Paulsen Repetitive elements in imprinted genes Cytogenet. Genome Res. 113 2006 109 115
134. T. Watanabe, S.i. Tomizawa, K. Mitsuya, Y. Totoki, Y. Yamamoto, S. Kuramochi-Miyagawa, N. Iida, Y. Hoki, P.J. Murphy, and A. Toyoda et al. Role for piRNAs and noncoding RNA in de novo DNA methylation of the imprinted mouse Rasgrf1 locus Science 332 2011 848 852
135. D. Weigel, and V. Colot Epialleles in plant evolution Genome Biol. 13 2012 249
136. C.F. Wolff Theoria Generationis 1759 Typis et sumtu Io. Christ. Hendel Germany
137. A. Yu, G. Lepère, F. Jay, J. Wang, L. Bapaume, Y. Wang, A.L. Abraham, J. Penterman, R.L. Fischer, O. Voinnet, and L. Navarro Dynamics and biological relevance of DNA demethylation in Arabidopsis antibacterial defense Proc. Natl. Acad. Sci. USA 110 2013 2389 2394
138. A. Zemach, M.Y. Kim, P.H. Hsieh, D. Coleman-Derr, L. Eshed-Williams, K. Thao, S.L. Harmer, and D. Zilberman The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin Cell 153 2013 193 205