Transgenerational epigenetic inheritance

Annual Review of Genetics

Volumn 52, Issue , 2018, Pages 21-41

  Bošković, Ana ^a   Rando, Oliver J ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

development; epigenetics; germ cells; transgenerational inheritance

Indexed keywords

EPIGENETICS; GERM LINE; HUMAN CELL; INHERITANCE; REVIEW; STIMULUS; STOCHASTIC MODEL; DNA METHYLATION; GENETIC EPIGENESIS; GENETICS; GERM CELL; GROWTH, DEVELOPMENT AND AGING; TRENDS;

DNA METHYLATION; EPIGENESIS, GENETIC; EPIGENOMICS; GERM CELLS; INHERITANCE PATTERNS;

EID: 85057168659     PISSN: 00664197     EISSN: 15452948     Source Type: Book Series    
DOI: 10.1146/annurev-genet-120417-031404     Document Type: Review

References (158)

1. Alabert C, Groth A. 2012. Chromatin replication and epigenome maintenance.Nat. Rev. Mol. Cell Biol. 13:153-67
2. Alcazar RM, Lin R, Fire AZ. 2008. Transmission dynamics of heritable silencing induced by doublestranded RNA in Caenorhabditis elegans. Genetics 180:1275-88
3. Amodeo AA, Jukam D, Straight AF, Skotheim JM. 2015. Histone titration against the genome sets the DNA-to-cytoplasm threshold for the Xenopus midblastula transition. PNAS 112:E1086-95
4. Anderson LM, Riffle L, Wilson R, Travlos GS, Lubomirski MS, Alvord WG. 2006. Preconceptional fasting of fathers alters serum glucose in offspring of mice. Nutrition 22:327-31
5. Anway MD, Cupp AS, Uzumcu M, Skinner MK. 2005. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 308:1466-69
6. Aravin AA, Hannon GJ, Brennecke J. 2007. The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 318:761-64
7. Aravin AA, Sachidanandam R, Bourc'his D, Schaefer C, Pezic D, et al. 2008. A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol. Cell 31:785-99
8. Arney KL, Bao S, Bannister AJ, Kouzarides T, Surani MA. 2002. Histonemethylation defines epigenetic asymmetry in the mouse zygote. Int. J. Dev. Biol. 46:317-20
9. Arteaga-Vazquez MA, Chandler VL. 2010. Paramutation in maize: RNA mediated trans-generational gene silencing. Curr. Opin. Genet. Dev. 20:156-63
10. Ashe A, Sapetschnig A, Weick EM, Mitchell J, Bagijn MP, et al. 2012. piRNAs can trigger a multigenerational epigenetic memory in the germline of C. elegans. Cell 150:88-99
11. Autran D, Baroux C, Raissig MT, Lenormand T, Wittig M, et al. 2011. Maternal epigenetic pathways control parental contributions to Arabidopsis early embryogenesis. Cell 145:707-19
12. Bagijn MP, Goldstein LD, Sapetschnig A, Weick EM, Bouasker S, et al. 2012. Function, targets, and evolution of Caenorhabditis elegans piRNAs. Science 337:574-78
13. Bale TL. 2015. Epigenetic and transgenerational reprogramming of brain development. Nat. Rev. Neurosci. 16:332-44
14. Barton SC, Surani MA, Norris ML. 1984. Role of paternal andmaternal genomes in mouse development. Nature 311:374-76
15. Bateson W, Pellew C. 1915. On the genetics of "rogues" among culinary peas (Pisum sativum). J. Genet. 5:15-36
16. Batista PJ, Ruby JG, Claycomb JM, Chiang R, Fahlgren N, et al. 2008. PRG-1 and 21U-RNAs interact to form the piRNA complex required for fertility in C. elegans. Mol. Cell 31:67-78
17. Baulcombe DC. 1996. Mechanisms of pathogen-derived resistance to viruses in transgenic plants. Plant Cell 8:1833-44
18. Bonnefoy E, Orsi GA, Couble P, Loppin B. 2007. The essential role of Drosophila HIRA for de novo assembly of paternal chromatin at fertilization. PLOS Genet. 3:1991-2006
19. Borges F, Martienssen RA. 2015. The expanding world of small RNAs in plants. Nat. Rev.Mol. Cell Biol. 16:727-41
20. Brennecke J, Aravin AA, Stark A, Dus M, Kellis M, et al. 2007. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128:1089-103
21. Brennecke J, Malone CD, Aravin AA, Sachidanandam R, Stark A, Hannon GJ. 2008. An epigenetic role for maternally inherited piRNAs in transposon silencing. Science 322:1387-92
22. Brink RA. 1958. Paramutation at the R locus in maize. Cold Spring Harb. Symp. Quant. Biol. 23:379-91
23. Buckley BA, Burkhart KB, Gu SG, Spracklin G, Kershner A, et al. 2012. A nuclear Argonaute promotes multigenerational epigenetic inheritance and germline immortality. Nature 489:447-51
24. Calarco JP, Borges F, Donoghue MT, Van Ex F, Jullien PE, et al. 2012. Reprogramming of DNA methylation in pollen guides epigenetic inheritance via small RNA. Cell 151:194-205
25. Campos EI, Stafford JM, Reinberg D. 2014. Epigenetic inheritance: Histone bookmarks across generations. Trends Cell Biol. 24:664-74
26. Carone BR, Fauquier L, Habib N, Shea JM, Hart CE, et al. 2010. Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell 143:1084-96
27. Cavrak VV, Lettner N, Jamge S, Kosarewicz A, Bayer LM, Mittelsten Scheid O. 2014. How a retrotransposon exploits the plant's heat stress response for its activation. PLOS Genet. 10:e1004115
28. Chan SW, Zhang X, Bernatavichute YV, Jacobsen SE. 2006. Two-step recruitment of RNA-directed DNA methylation to tandem repeats. PLOS Biol. 4:e363
29. Chen Q, Yan M, Cao Z, Li X, Zhang Y, et al. 2016. Sperm tsRNAs contribute to intergenerational inheritance of an acquired metabolic disorder. Science 351:397-400
30. Coleman RT, Struhl G. 2017. Causal role for inheritance of H3K27me3 in maintaining the OFF state of a Drosophila HOX gene. Science 356:eaai8236
31. Curley JP, Mashoodh R, Champagne FA. 2010. Epigenetics and the origins of paternal effects. Horm. Behav. 59:306-14
32. Dias BG, Ressler KJ. 2014. Parental olfactory experience influences behavior and neural structure in subsequent generations. Nat. Neurosci. 17:89-96
33. Dumesic PA, Natarajan P, Chen C, Drinnenberg IA, Schiller BJ, et al. 2013. Stalled spliceosomes are a signal for RNAi-mediated genome defense. Cell 152:957-68
34. Erkek S, Hisano M, Liang CY, Gill M, Murr R, et al. 2013. Molecular determinants of nucleosome retention at CpG-rich sequences in mouse spermatozoa. Nat. Struct. Mol. Biol. 20:868-75
35. Feng S, Jacobsen SE, ReikW. 2010. Epigenetic reprogramming in plant and animal development. Science 330:622-27
36. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC. 1998. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806-11
37. Gapp K, Jawaid A, Sarkies P, Bohacek J, Pelczar P, et al. 2014. Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice. Nat. Neurosci. 17:667-69
38. Gehring M, Bubb KL, Henikoff S. 2009. Extensive demethylation of repetitive elements during seed development underlies gene imprinting. Science 324:1447-51
39. Ghildiyal M, Zamore PD. 2009. Small silencing RNAs: An expanding universe. Nat. Rev. Genet. 10:94-108
40. Gowen JW, Gay EH. 1933. Effect of temperature on eversporting eye color in Drosophila melanogaster. Science 77:312
41. GrandjeanV, Fourre S, De Abreu DA, Derieppe MA, Remy JJ, Rassoulzadegan M. 2015. RNA-mediated paternal heredity of diet-induced obesity and metabolic disorders. Sci. Rep. 5:18193
42. Greer EL, Maures TJ, Ucar D, Hauswirth AG, Mancini E, et al. 2011. Transgenerational epigenetic inheritance of longevity in Caenorhabditis elegans. Nature 479:365-71
43. Gu W, Lee HC, Chaves D, Youngman EM, Pazour GJ, et al. 2013. CapSeq and CIP-TAP identify Pol II start sites and reveal capped small RNAs as C. elegans piRNA precursors. Cell 151:1488-500
44. Guerrero-Bosagna C, SkinnerMK. 2014. Environmentally induced epigenetic transgenerational inheritance of male infertility. Curr. Opin. Genet. Dev. 26:79-88
45. GuoH, Zhu P, Yan L, Li R, Hu B, et al. 2014. TheDNAmethylation landscape of human early embryos. Nature 511:606-10
46. Gurdon JB. 2006. From nuclear transfer to nuclear reprogramming: The reversal of cell differentiation. Annu. Rev. Cell Dev. Biol. 22:1-22
47. Hackett JA, Sengupta R, Zylicz JJ, Murakami K, Lee C, et al. 2013. Germline DNA demethylation dynamics and imprint erasure through 5-hydroxymethylcytosine. Science 339:448-52
48. Hackett JA, Surani MA. 2013. DNA methylation dynamics during the mammalian life cycle. Philos. Trans. R. Soc. B 368:20110328
49. Haig D. 2004. Genomic imprinting and kinship: How good is the evidence Annu. Rev. Genet. 38:553-85
50. Haig D, Wilkins JF. 2000. Genomic imprinting, sibling solidarity and the logic of collective action. Philos. Trans. R. Soc. B 355:1593-97
51. Hanna CW, Taudt A, Huang J, Gahurova L, Kranz A, et al. 2018. MLL2 conveys transcriptionindependent H3K4 trimethylation in oocytes. Nat. Struct. Mol. Biol. 25:73-82
52. Hartmann-Goldstein IJ. 1967. On the relationship between heterochromatization and variegation in Drosophila, with special reference to temperature-sensitive periods. Genet. Res. 10:143-59
53. Harvey ZH, Chen Y, Jarosz DF. 2017. Protein-based inheritance: Epigenetics beyond the chromosome. Mol. Cell 69:195-202
54. Heard E, Martienssen RA. 2014. Transgenerational epigenetic inheritance: Myths and mechanisms. Cell 157:95-109
55. Hermant C, Boivin A, Teysset L, Delmarre V, Asif-Laidin A, et al. 2015. Paramutation in Drosophila requires both nuclear and cytoplasmic actors of the piRNA pathway and induces cis-spreading of piRNA production. Genetics 201:1381-96
56. Hirsch S, Baumberger R, Grossniklaus U. 2012. Epigenetic variation, inheritance, and selection in plant populations. Cold Spring Harb. Symp. Quant. Biol. 77:97-104
57. Holoch D, Moazed D. 2015. RNA-mediated epigenetic regulation of gene expression. Nat. Rev. Genet. 16:71-84
58. Hsieh TF, Ibarra CA, Silva P, Zemach A, Eshed-Williams L, et al. 2009. Genome-wide demethylation of Arabidopsis endosperm. Science 324:1451-54
59. Huang X, Fejes Toth K, Aravin AA. 2017. piRNA biogenesis in Drosophila melanogaster. Trends Genet. 33:882-94
60. Huypens P, Sass S, Wu M, Dyckhoff D, Tschop M, et al. 2016. Epigenetic germline inheritance of diet-induced obesity and insulin resistance. Nat. Genet. 48:497-99
61. Ingouff M, Hamamura Y, Gourgues M, Higashiyama T, Berger F. 2007. Distinct dynamics of HISTONE3 variants between the two fertilization products in plants. Curr. Biol. 17:1032-37
62. Inoue A, Jiang L, Lu F, Suzuki T, Zhang Y. 2017. Maternal H3K27me3 controls DNA methylationindependent imprinting. Nature 547:419-24
63. Inoue A, Zhang Y. 2014. Nucleosome assembly is required for nuclear pore complex assembly in mouse zygotes. Nat. Struct. Mol. Biol. 21:609-16
64. Ito H, Gaubert H, Bucher E, Mirouze M, Vaillant I, Paszkowski J. 2011. An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress. Nature 472:115-19
65. Jablonka E, Lamb MJ. 1989. The inheritance of acquired epigenetic variations. J. Theor. Biol. 139:69-83
66. Jablonka E, Lamb MJ. 1995. Epigenetic Inheritance and Evolution: The Lamarckian Dimension.Oxford, UK: Oxford Univ. Press
67. Jacobsen SE, Meyerowitz EM. 1997. Hypermethylated SUPERMAN epigenetic alleles in Arabidopsis. Science 277:1100-3
68. Jiang L, Zhang J, Wang JJ, Wang L, Zhang L, et al. 2013. Sperm, but not oocyte, DNA methylome is inherited by zebrafish early embryos. Cell 153:773-84
69. Jimenez-Chillaron JC, Isganaitis E, Charalambous M, Gesta S, Pentinat-Pelegrin T, et al. 2009. Intergenerational transmission of glucose intolerance and obesity by in utero undernutrition in mice. Diabetes 58:460-68
70. Katan-Khaykovich Y, Struhl K. 2005. Heterochromatin formation involves changes in histone modifications over multiple cell generations. EMBO J. 24:2138-49
71. Kaufman PD, Rando OJ. 2010. Chromatin as a potential carrier of heritable information. Curr. Opin. Cell Biol. 22:284-90
72. Kawakatsu T, Huang SC, Jupe F, Sasaki E, Schmitz RJ, et al. 2016. Epigenomic diversity in a global collection of Arabidopsis thaliana accessions. Cell 166:492-505
73. Kawashima T, Berger F. 2014. Epigenetic reprogramming in plant sexual reproduction. Nat. Rev. Genet. 15:613-24
74. Kelly WG, Aramayo R. 2007. Meiotic silencing and the epigenetics of sex. Chromosome Res. 15:633-51
75. Khurana JS, Wang J, Xu J, Koppetsch BS, Thomson TC, et al. 2011. Adaptation to P element transposon invasion in Drosophila melanogaster. Cell 147:1551-63
76. Klattenhoff C, Xi H, Li C, Lee S, Xu J, et al. 2009. The Drosophila HP1 homolog Rhino is required for transposon silencing and piRNA production by dual-strand clusters. Cell 138:1137-49
77. Klosin A, Casas E, Hidalgo-Carcedo C, Vavouri T, Lehner B. 2017. Transgenerational transmission of environmental information in C. elegans. Science 356:320-23
78. Kobayashi H, Sakurai T, Imai M, Takahashi N, Fukuda A, et al. 2012. Contribution of intragenic DNA methylation in mouse gametic DNA methylomes to establish oocyte-specific heritable marks. PLOS Genet. 8:e1002440
79. Kussell E, Leibler S. 2005. Phenotypic diversity, population growth, and information in fluctuating environments. Science 309:2075-78
80. Lane M, Robker RL, Robertson SA. 2014. Parenting from before conception. Science 345:756-60
81. Lee HC, Gu W, Shirayama M, Youngman E, Conte D Jr., Mello CC. 2013. C. elegans piRNAs mediate the genome-wide surveillance of germline transcripts. Cell 150:78-87
82. Li XZ, Roy CK, Dong X, Bolcun-Filas E, Wang J, et al. 2013. An ancient transcription factor initiates the burst of piRNA production during early meiosis in mouse testes. Mol. Cell 50:67-81
83. Lindbo JA, Silva-Rosales L, Proebsting WM, Dougherty WG. 1993. Induction of a highly specific antiviral state in transgenic plants: Implications for regulation of gene expression and virus resistance. Plant Cell 5:1749-59
84. Luo GZ, Blanco MA, Greer EL, He C, Shi Y. 2015. DNA N6-methyladenine: A new epigenetic mark in eukaryotes Nat. Rev. Mol. Cell Biol. 16:705-10
85. Lyon MF. 1961. Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature 190:372-73
86. Madhani HD. 2013. The frustrated gene: Origins of eukaryotic gene expression. Cell 155:744-49
87. Malone CD, Hannon GJ. 2009. Small RNAs as guardians of the genome. Cell 136:656-68
88. Marquet R, Isel C, Ehresmann C, Ehresmann B. 1995. tRNAs as primer of reverse transcriptases. Biochimie 77:113-24
89. Martinez G, Choudury SG, Slotkin RK. 2017. tRNA-derived small RNAs target transposable element transcripts. Nucleic Acids Res. 45:5142-52
90. Martinez G, Panda K, KohlerC, Slotkin RK. 2016. Silencing in sperm cells is directed byRNAmovement from the surrounding nurse cell. Nat. Plants 2:16030
91. Matzke MA, Matzke A. 1995. How and why do plants inactivate homologous (trans)genes Plant Physiol. 107:679-85
92. McClintock B. 1984. The significance of responses of the genome to challenge. Science 226:792-801
93. McGrath J, SolterD. 1984. Completion of mouse embryogenesis requires both the maternal and paternal genomes. Cell 37:179-83
94. Migicovsky Z, Yao Y, Kovalchuk I. 2014. Transgenerational phenotypic and epigenetic changes in response to heat stress in Arabidopsis thaliana. Plant Signal. Behav. 9:e27971
95. Miska EA, Ferguson-Smith AC. 2016. Transgenerational inheritance: Models and mechanisms of non-DNA sequence-based inheritance. Science 354:59-63
96. Morgan HD, Sutherland HG, Martin DI, Whitelaw E. 1999. Epigenetic inheritance at the agouti locus in the mouse. Nat. Genet. 23:314-18
97. Nakamura T, Liu YJ, Nakashima H, Umehara H, Inoue K, et al. 2012. PGC7 binds histone H3K9me2 to protect against conversion of 5mC to 5hmC in early embryos. Nature 486:415-19
98. Napoli C, Lemieux C, Jorgensen R. 1990. Introduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous genes in trans. Plant Cell 2:279-89
99. Ng SF, Lin RC, Laybutt DR, Barres R, Owens JA, Morris MJ. 2010. Chronic high-fat diet in fathers programs -cell dysfunction in female rat offspring. Nature 467:963-66
100. Okada T, Endo M, Singh MB, Bhalla PL. 2005. Analysis of the histone H3 gene family in Arabidopsis and identification of the male-gamete-specific variant AtMGH3. Plant J. 44:557-68
101. Ooi SL, Henikoff S. 2007. Germline histone dynamics and epigenetics. Curr. Opin. Cell Biol. 19:257-65
102. Ooi SL, Priess JR, Henikoff S. 2006. Histone H3.3 variant dynamics in the germline of Caenorhabditis elegans. PLOS Genet. 2:e97
103. Padmanabhan N, Jia D, Geary-Joo C, Wu X, Ferguson-Smith AC, et al. 2013. Mutation in folate metabolism causes epigenetic instability and transgenerational effects on development. Cell 155:81-93
104. Paszkowski J, Grossniklaus U. 2011. Selected aspects of transgenerational epigenetic inheritance and resetting in plants. Curr. Opin. Plant Biol. 14:195-203
105. Peng H, Shi J, Zhang Y, Zhang H, Liao S, et al. 2012. A novel class of tRNA-derived small RNAs extremely enriched in mature mouse sperm. Cell Res. 22:1609-12
106. Potok ME, Nix DA, Parnell TJ, Cairns BR. 2013. Reprogramming the maternal zebrafish genome after fertilization to match the paternal methylation pattern. Cell 153:759-72
107. Ptashne M. 2007. On the use of the word 'epigenetic.' Curr. Biol. 17:R233-36
108. Quadrana L, Colot V. 2016. Plant transgenerational epigenetics. Annu. Rev. Genet. 50:467-91
109. Radford EJ, ItoM, Shi H, Corish JA, Yamazawa K, et al. 2014. In utero undernourishment perturbs the adult sperm methylome and intergenerational metabolism. Science 345:1255903
110. Raissig MT, Baroux C, Grossniklaus U. 2011. Regulation and flexibility of genomic imprinting during seed development. Plant Cell 23:16-26
111. Rando OJ. 2012. Daddy issues: Paternal effects on phenotype. Cell 151:702-8
112. Rando OJ, Simmons RA. 2015. I'm eating for two: Parental dietary effects on offspring metabolism. Cell 161:93-105
113. Rassoulzadegan M, Grandjean V, Gounon P, Vincent S, Gillot I, Cuzin F. 2006. RNA-mediated non-Mendelian inheritance of an epigenetic change in the mouse. Nature 441:469-74
114. Ratcliff F, Harrison BD, Baulcombe DC. 1997. A similarity between viral defense and gene silencing in plants. Science 276:1558-60
115. Raychaudhuri N, Dubruille R, Orsi GA, Bagheri HC, Loppin B, Lehner CF. 2012. Transgenerational propagation and quantitative maintenance of paternal centromeres depends on Cid/Cenp-A presence in Drosophila sperm. PLOS Biol. 10:e1001434
116. Rinn JL, ChangHY. 2012. Genome regulation by long noncoding RNAs. Annu. Rev. Biochem. 81:145-66
117. Rodgers AB, Morgan CP, Bronson SL, Revello S, Bale TL. 2013. Paternal stress exposure alters sperm microRNA content and reprograms offspring HPA stress axis regulation. J. Neurosci. 33:9003-12
118. Rodgers AB, Morgan CP, Leu NA, Bale TL. 2015. Transgenerational epigenetic programming via sperm microRNA recapitulates effects of paternal stress. PNAS 112:13699-704
119. Santenard A, Ziegler-Birling C, Koch M, Tora L, Bannister AJ, Torres-Padilla ME. 2010. Heterochromatin formation in the mouse embryo requires critical residues of the histone variant H3.3. Nat. Cell Biol. 12:853-62
120. Sasson IE, Vitins AP, Mainigi MA, Moley KH, Simmons RA. 2015. Pre-gestational versus gestational exposure to maternal obesity differentially programs the offspring in mice. Diabetologia 58:615-24
121. Schmitz RJ, Schultz MD, Lewsey MG, O'Malley RC, Urich MA, et al. 2011. Transgenerational epigenetic instability is a source of novel methylation variants. Science 334:369-73
122. Schoft VK, Chumak N, Mosiolek M, Slusarz L, Komnenovic V, et al. 2009. Induction of RNA-directed DNA methylation upon decondensation of constitutive heterochromatin. EMBO Rep. 10:1015-21
123. Schorn AJ, Gutbrod MJ, LeBlanc C, Martienssen R. 2017. LTR-retrotransposon control by tRNAderived small RNAs. Cell 170:61-71.e11
124. Schuettengruber B, Chourrout D, Vervoort M, Leblanc B, Cavalli G. 2007. Genome regulation by polycomb and trithorax proteins. Cell 128:735-45
125. Scott RJ, Spielman M, Bailey J, Dickinson HG. 1998. Parent-of-origin effects on seed development in Arabidopsis thaliana. Development 125:3329-41
126. Secco D, Wang C, Shou H, Schultz MD, Chiarenza S, et al. 2015. Stress induced gene expression drives transient DNA methylation changes at adjacent repetitive elements. eLife 4:e09343
127. Seong KH, Li D, Shimizu H, Nakamura R, Ishii S. 2011. Inheritance of stress-induced, ATF-2-dependent epigenetic change. Cell 145:1049-61
128. Serio TR, Lindquist SL. 1999. [PSI+]: An epigenetic modulator of translation termination efficiency. Annu. Rev. Cell Dev. Biol. 15:661-703
129. Sharma U, Conine CC, Shea JM, Boskovic A, Derr AG, et al. 2016. Biogenesis and function of tRNA fragments during sperm maturation and fertilization in mammals. Science 351:391-96
130. Shirayama M, Seth M, Lee HC, Gu W, Ishidate T, et al. 2012. piRNAs initiate an epigenetic memory of nonself RNA in the C. elegans germline. Cell 150:65-77
131. Shiu PK, Metzenberg RL. 2002. Meiotic silencing by unpaired DNA: Properties, regulation and suppression. Genetics 161:1483-95
132. Shivaprasad PV, Dunn RM, Santos BA, Bassett A, Baulcombe DC. 2012. Extraordinary transgressive phenotypes of hybrid tomato are influenced by epigenetics and small silencing RNAs. EMBO J. 31:257-66
133. Siklenka K, Erkek S, Godmann M, Lambrot R, McGraw S, et al. 2015. Disruption of histone methylation in developing sperm impairs offspring health transgenerationally. Science 350:aab2006
134. Slotkin RK, Vaughn M, Borges F, Tanurdzic M, Becker JD, et al. 2009. Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136:461-72
135. Smith ZD, Chan MM, Mikkelsen TS, Gu H, Gnirke A, et al. 2012. A unique regulatory phase of DNA methylation in the early mammalian embryo. Nature 484:339-44
136. Smith ZD, Shi J, Gu H, Donaghey J, Clement K, et al. 2017. Epigenetic restriction of extraembryonic lineages mirrors the somatic transition to cancer. Nature 549:543-47
137. Stam M, Belele C, Dorweiler JE, Chandler VL. 2002. Differential chromatin structure within a tandem array 100 kb upstream of the maize b1 locus is associated with paramutation. Genes Dev. 16:1906-18
138. Stroud H, Greenberg MV, Feng S, Bernatavichute YV, Jacobsen SE. 2013. Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome. Cell 152:352-64
139. Suter L, Widmer A. 2013. Environmental heat and salt stress induce transgenerational phenotypic changes in Arabidopsis thaliana. PLOS ONE 8:e60364
140. Svoboda P, Flemr M. 2010. The role of miRNAs and endogenous siRNAs in maternal-to-zygotic reprogramming and the establishment of pluripotency. EMBO Rep. 11:590-97
141. Takahashi K, Yamanaka S. 2006. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663-76
142. Tang WW, Kobayashi T, Irie N, Dietmann S, SuraniMA. 2016. Specification and epigenetic programming of the human germ line. Nat. Rev. Genet. 17:585-600
143. Teixeira FK, Heredia F, Sarazin A, Roudier F, Boccara M, et al. 2009. A role for RNAi in the selective correction of DNA methylation defects. Science 323:1600-4
144. Vagin VV, Sigova A, Li C, Seitz H, Gvozdev V, Zamore PD. 2006. A distinct small RNA pathway silences selfish genetic elements in the germline. Science 313:320-24
145. Vallaster MP, Kukreja S, Bing XY, Ngolab J, Zhao-Shea R, et al. 2017. Paternal nicotine exposure alters hepatic xenobiotic metabolism in offspring. eLife 6:e24771
146. van der Graaf A, Wardenaar R, Neumann DA, Taudt A, Shaw RG, et al. 2015. Rate, spectrum, and evolutionary dynamics of spontaneous epimutations. PNAS 112:6676-81
147. Vassoler FM, White SL, Schmidt HD, Sadri-Vakili G, Pierce RC. 2013. Epigenetic inheritance of a cocaine-resistance phenotype. Nat. Neurosci. 16:42-47
148. Volpe TA, Kidner C, Hall IM, Teng G, Grewal SI, MartienssenRA. 2002. Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297:1833-37
149. Vongs A, Kakutani T, Martienssen RA, Richards EJ. 1993. Arabidopsis thaliana DNA methylation mutants. Science 260:1926-28
150. Wang X, Moazed D. 2017. DNA sequence-dependent epigenetic inheritance of gene silencing and histone H3K9 methylation. Science 356:88-91
151. Watanabe T, Takeda A, Tsukiyama T, Mise K, Okuno T, et al. 2006. Identification and characterization of two novel classes of small RNAs in the mouse germline: Retrotransposon-derived siRNAs in oocytes and germline small RNAs in testes. Genes Dev. 20:1732-43
152. Waterland RA, Jirtle RL. 2003. Transposable elements: Targets for early nutritional effects on epigenetic gene regulation. Mol. Cell. Biol. 23:5293-300
153. Weigel D, Colot V. 2012. Epialleles in plant evolution. Genome Biol. 13:249
154. Wibowo A, Becker C, Marconi G, Durr J, Price J, et al. 2016. Hyperosmotic stressmemory in Arabidopsis is mediated by distinct epigenetically labile sites in the genome and is restricted in the male germline by DNA glycosylase activity. eLife 5:e13546
155. Yuan S, Schuster A, Tang C, Yu T, Ortogero N, et al. 2016. Sperm-borne miRNAs and endo-siRNAs are important for fertilization and preimplantation embryonic development. Development 143:635-47
156. Zeybel M, Hardy T, Wong YK, Mathers JC, Fox CR, et al. 2012. Multigenerational epigenetic adaptation of the hepatic wound-healing response. Nat. Med. 18:1369-77
157. Zierhut C, Jenness C, Kimura H, Funabiki H. 2014. Nucleosomal regulation of chromatin composition and nuclear assembly revealed by histone depletion. Nat. Struct. Mol. Biol. 21:617-25
158. Zilberman D, Cao X, Jacobsen SE. 2003. ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science 299:716-19