Transgenerational epigenetics is defined in opposition to developmental epigenetics and implies an absence of resetting of epigenetic states between generations. Unlike mammals, plants appear to be particularly prone to this type of inheritance. In this review, we summarize our knowledge about transgenerational epigenetics in plants, which entails heritable changes in DNA methylation. We emphasize the role of transposable elements and other repeat sequences in the creation of epimutable alleles. We also argue that because reprogramming of DNA methylation across generations seems limited in plants, the inheritance of DNA methylation defects results from the failure to reinforce rather than reset this modification during sexual reproduction. We compare genome-wide assessments of heritable DNA methylation variation and its phenotypic impact in natural populations to those made using near-isogenic populations derived from crosses between parents with experimentally induced DNA methylation differences. Finally, we question the role of the environment in inducing transgenerational epigenetic variation and briefly present theoretical models under which epimutability is expected to be selected for.


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Literature Cited

  1. Ahmed I, Sarazin A, Bowler C, Colot V, Quesneville H. 1.  2011. Genome-wide evidence for local DNA methylation spreading from small RNA-targeted sequences in Arabidopsis. Nucleic Acids Res 39:166919–31 [Google Scholar]
  2. Arteaga-Vazquez MA, Chandler VL. 2.  2010. Paramutation in maize: RNA mediated trans-generational gene silencing. Curr. Opin. Genet. Dev. 20:2156–63 [Google Scholar]
  3. Baubec T, Colombo DF, Wirbelauer C, Schmidt J, Burger L. 3.  et al. 2015. Genomic profiling of DNA methyltransferases reveals a role for DNMT3B in genic methylation. Nature 520:7546243–47 [Google Scholar]
  4. Baulcombe DC, Dean C. 4.  2014. Epigenetic regulation in plant responses to the environment. Cold Spring Harb. Perspect. Biol. 6:9a019471 [Google Scholar]
  5. Becker C, Hagmann J, Müller J, Koenig D, Stegle O. 5.  et al. 2011. Spontaneous epigenetic variation in the Arabidopsis thaliana methylome. Nature 480:7376245–49 [Google Scholar]
  6. Bender J. 6.  2004. DNA methylation of the endogenous PAI genes in Arabidopsis. Cold Spring Harb. Symp. Quant. Biol. 69:145–53 [Google Scholar]
  7. Berry S, Dean C. 7.  2015. Environmental perception and epigenetic memory: mechanistic insight through FLC. Plant J 83:133–48 [Google Scholar]
  8. Bestor TH, Chandler VL, Feinberg AP. 8.  1994. Epigenetic effects in eukaryotic gene expression. Dev. Genet. 15:6458–62 [Google Scholar]
  9. Bewick AJ, Ji L, Niederhuth CE, Willing E-M, Hofmeister BT. 9.  et al. 2016. On the origin and evolutionary consequences of gene body DNA methylation. PNAS 113:9111–16 [Google Scholar]
  10. Bird A. 10.  2007. Perceptions of epigenetics. Nature 447:396–98 [Google Scholar]
  11. Blevins T, Podicheti R, Mishra V, Marasco M, Wang J. 11.  et al. 2015. Identification of Pol IV and RDR2-dependent precursors of 24 nt siRNAs guiding de novo DNA methylation in Arabidopsis. eLife 4:1–22 [Google Scholar]
  12. Bond DM, Baulcombe DC. 12.  2015. Epigenetic transitions leading to heritable, RNA-mediated de novo silencing in Arabidopsis thaliana. PNAS 112:3201413053 [Google Scholar]
  13. Bossdorf O, Richards CL, Pigliucci M. 13.  2008. Epigenetics for ecologists. Ecol. Lett. 11:2106–15 [Google Scholar]
  14. Brachi B, Morris GP, Borevitz JO. 14.  2011. Genome-wide association studies in plants: the missing heritability is in the field. Genome Biol. 12:10232 [Google Scholar]
  15. Briggs D, Walters SM. 15.  1984. Plant Variation and Evolution Cambridge, UK: Cambridge Univ. Press, 2nd ed.. [Google Scholar]
  16. Brink RA. 16.  1956. A genetic change associated with the R locus in maize which is directed and potentially reversible. Genetics 41:6872 [Google Scholar]
  17. Calarco JP, Borges F, Donoghue MTA, Van Ex F, Jullien PE. 17.  et al. 2012. Reprogramming of DNA methylation in pollen guides epigenetic inheritance via small RNA. Cell 151:1194–205 [Google Scholar]
  18. Cao J, Schneeberger K, Ossowski S, Günther T, Bender S. 18.  et al. 2011. Whole-genome sequencing of multiple Arabidopsis thaliana populations. Nat. Genet. 43:10956–63 [Google Scholar]
  19. Chodavarapu RK, Feng S, Ding B, Simon SA, Lopez D. 19.  et al. 2012. Transcriptome and methylome interactions in rice hybrids. PNAS 109:3012040–45 [Google Scholar]
  20. Cleaton MAM, Edwards CA, Ferguson-Smith AC. 20.  2014. Phenotypic outcomes of imprinted gene models in mice: elucidation of pre- and postnatal functions of imprinted genes. Annu. Rev. Genom. Hum. Genet. 15:93–126 [Google Scholar]
  21. Cokus SJ, Feng S, Zhang X, Chen Z, Merriman B. 21.  et al. 2008. Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452:215–19 [Google Scholar]
  22. Coleman-Derr D, Zilberman D. 22.  2012. Deposition of histone variant H2A.Z within gene bodies regulates responsive genes. PLOS Genet 8:10e1002988 [Google Scholar]
  23. Colomé-Tatché M, Cortijo S, Wardenaar R, Morgado L, Lahouze B. 23.  et al. 2012. Features of the Arabidopsis recombination landscape resulting from the combined loss of sequence variation and DNA methylation. PNAS 109:4016240–45 [Google Scholar]
  24. Cortijo S, Wardenaar R, Colomé-Tatché M, Gilly A, Etcheverry M. 24.  et al. 2014. Mapping the epigenetic basis of complex traits. Science 343:61751145–48 [Google Scholar]
  25. Crisp PA, Ganguly D, Eichten SR, Borevitz JO, Pogson BJ. 25.  2016. Reconsidering plant memory: intersections between stress recovery, RNA turnover, and epigenetics. Sci. Adv. 2:2e1501340 [Google Scholar]
  26. Cubas P, Vincent C, Coen E. 26.  1999. An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401:6749157–61 [Google Scholar]
  27. Day T, Bonduriansky R. 27.  2011. A unified approach to the evolutionary consequences of genetic and nongenetic inheritance. Am. Nat. 178:2E18–36 [Google Scholar]
  28. Dowen RH, Pelizzola M, Schmitz RJ, Lister R, Dowen JM. 28.  et al. 2012. Widespread dynamic DNA methylation in response to biotic stress. PNAS 109:32E2183–91 [Google Scholar]
  29. Du J, Johnson LM, Jacobsen SE, Patel DJ. 29.  2015. DNA methylation pathways and their crosstalk with histone methylation. Nat. Rev. Mol. Cell Biol. 16:9519–32 [Google Scholar]
  30. Dubin MJ, Zhang P, Meng D, Remigereau M-S, Osborne EJ. 30.  et al. 2015. DNA methylation in Arabidopsis has a genetic basis and shows evidence of local adaptation. eLife 4:e05255 [Google Scholar]
  31. Durand S, Bouché N, Perez Strand E, Loudet O, Camilleri C. 31.  2012. Rapid establishment of genetic incompatibility through natural epigenetic variation. Curr. Biol. 22:4326–31 [Google Scholar]
  32. Eichten SR, Briskine R, Song J, Li Q, Swanson-Wagner R. 32.  et al. 2013. Epigenetic and genetic influences on DNA methylation variation in maize populations. Plant Cell 25:82783–97 [Google Scholar]
  33. Eichten SR, Ellis NA, Makarevitch I, Yeh C, Gent JI. 33.  et al. 2012. Spreading of heterochromatin is limited to specific families of maize retrotransposons. PLOS Genet. 8:12e1003127 [Google Scholar]
  34. Eichten SR, Swanson-Wagner RA, Schnable JC, Waters AJ, Hermanson PJ. 34.  et al. 2011. Heritable epigenetic variation among maize inbreds. PLOS Genet. 7:11e1002372 [Google Scholar]
  35. El-shami M, Pontier D, Lahmy S, Braun L, Picart C. 35.  et al. 2007. Reiterated WG/GW motifs form functionally and evolutionarily conserved ARGONAUTE-binding platforms in RNAi-related components. Genes Dev 21:2539–44 [Google Scholar]
  36. Fedoroff N. 36.  1989. The heritable activation of cryptic suppressor-mutator elements by an active element. Genetics 121:3591–608 [Google Scholar]
  37. Fedoroff N, Schläppi M, Raina R. 37.  1995. Epigenetic regulation of the maize Spm transposon. BioEssays 17:4291–97 [Google Scholar]
  38. Fujimoto R, Kinoshita Y, Kawabe A, Kinoshita T, Takashima K. 38.  et al. 2008. Evolution and control of imprinted FWA genes in the genus Arabidopsis. PLOS Genet. 4:4e1000048 [Google Scholar]
  39. Gao Z, Liu H, Daxinger L, Pontes O, He X. 39.  et al. 2010. An RNA Polymerase II- and AGO4-associated protein acts in RNA-directed DNA methylation. Nature 465:7294106–9 [Google Scholar]
  40. Gehring M. 40.  2013. Genomic imprinting: insights from plants. Annu. Rev. Genet. 47:1187–208 [Google Scholar]
  41. Gendrel A, Heard E. 41.  2014. Noncoding RNAs and epigenetic mechanisms during X-chromosome inactivation. Annu. Rev. Cell Dev. Biol. 30:561–80 [Google Scholar]
  42. Gent JI, Ellis NA, Guo L, Harkess AE, Yao Y. 42.  et al. 2013. CHH islands: de novo DNA methylation in near-gene chromatin regulation in maize. Genome Res. 23:4628–37 [Google Scholar]
  43. Geoghegan JL, Spencer HG. 43.  2013. Exploring epiallele stability in a population-epigenetic model. Theor. Popul. Biol. 83:136–44 [Google Scholar]
  44. Geoghegan JL, Spencer HG. 44.  2013. The adaptive invasion of epialleles in a heterogeneous environment. Theor. Popul. Biol. 88:1–8 [Google Scholar]
  45. Geoghegan JL, Spencer HG. 45.  2013. The evolutionary potential of paramutation: a population-epigenetic model. Theor. Popul. Biol. 88:9–19 [Google Scholar]
  46. Gilly A, Etcheverry M, Madoui M-A, Guy J, Quadrana L. 46.  et al. 2014. TE-tracker: systematic identification of transposition events through whole-genome resequencing. BMC Bioinform. 15:1377 [Google Scholar]
  47. Hagmann J, Becker C, Müller J, Stegle O, Meyer RC. 47.  et al. 2015. Century-scale methylome stability in a recently diverged Arabidopsis thaliana lineage. PLOS Genet. 11:1e1004920 [Google Scholar]
  48. Heard E, Martienssen RA. 48.  2014. Transgenerational epigenetic inheritance: myths and mechanisms. Cell 157:195–109 [Google Scholar]
  49. Holeski LM, Jander G, Agrawal AA. 49.  2012. Transgenerational defense induction and epigenetic inheritance in plants. Trends Ecol. Evol. 27:11618–26 [Google Scholar]
  50. Holliday R. 50.  1987. The inheritance of epigenetic defects. Science 238:11163–70 [Google Scholar]
  51. Hollister JD, Gaut BS. 51.  2009. Epigenetic silencing of transposable elements: a trade-off between reduced transposition and deleterious effects on neighboring gene expression. Genome Res. 19:81419–28 [Google Scholar]
  52. Hsieh T-F, Ibarra CA, Silva P, Zemach A, Eshed-Williams L. 52.  et al. 2009. Genome-wide demethylation of Arabidopsis endosperm. Science 324:59331451–54 [Google Scholar]
  53. Ibarra CA, Feng X, Schoft VK, Hsieh T-F, Uzawa R. 53.  et al. 2012. Active DNA demethylation in plant companion cells reinforces transposon methylation in gametes. Science 337:61001360–64 [Google Scholar]
  54. Inagaki S, Miura-Kamio A, Nakamura Y, Lu F, Cui X. 54.  et al. 2010. Autocatalytic differentiation of epigenetic modifications within the Arabidopsis genome. EMBO J. 29:203496–3506 [Google Scholar]
  55. Ito T, Tarutani Y, To TK, Kassam M, Duvernois-Berthet E. 55.  et al. 2015. Genome-wide negative feedback drives transgenerational DNA methylation dynamics in Arabidopsis. PLOS Genet. 11:4e1005154 [Google Scholar]
  56. Iwasaki M, Paszkowski J. 56.  2014. Identification of genes preventing transgenerational transmission of stress-induced epigenetic states. PNAS 111:238547–52 [Google Scholar]
  57. Jablonka E, Lamb MJ. 57.  1989. The inheritance of acquired epigenetic variations. Int. J. Epidemiol. 44:41094–103 [Google Scholar]
  58. Jiang C, Mithani A, Belfield EJ, Mott R, Hurst LD, Harberd NP. 58.  2014. Environmentally responsive genome-wide accumulation of de novo Arabidopsis thaliana mutations and epimutations. Genome Res. 24:1821–29 [Google Scholar]
  59. Johannes F, Colomé-Tatché M. 59.  2011. Concerning epigenetics and inbreeding. Nat. Rev. Genet. 12:5376 [Google Scholar]
  60. Johannes F, Colot V, Jansen RC. 60.  2008. Epigenome dynamics: a quantitative genetics perspective. Nat. Rev. Genet. 9:11883–90 [Google Scholar]
  61. Johannes F, Porcher E, Teixeira FK, Saliba-Colombani V, Albuisson J. 61.  et al. 2009. Assessing the impact of transgenerational epigenetic variation on complex traits. PLOS Genet. 5:6e1000530 [Google Scholar]
  62. Johnson LM, Du J, Hale CJ, Bischof S, Feng S. 62.  et al. 2014. SRA- and SET-domain-containing proteins link RNA polymerase V occupancy to DNA methylation. Nature 507:7490124–28 [Google Scholar]
  63. Jullien PE, Susaki D, Yelagandula R, Higashiyama T, Berger F. 63.  2012. DNA methylation dynamics during sexual reproduction in Arabidopsis thaliana. Curr. Biol. 22:191825–30 [Google Scholar]
  64. Kankel MW, Ramsey DE, Stokes TL, Flowers SK, Haag JR. 64.  et al. 2003. Arabidopsis MET1 cytosine methyltransferase mutants. Genetics 163:31109–22 [Google Scholar]
  65. Kanno T, Mette MF, Kreil DP, Aufsatz W, Matzke M, Matzke AJM. 65.  2004. Involvement of putative SNF2 chromatin remodeling protein DRD1 in RNA-directed DNA methylation. Curr. Biol. 14:9801–5 [Google Scholar]
  66. Kawakatsu T, Huang SC, Jupe F, Sasaki E, Schmitz RJ. 66.  et al. 2016. Epigenomic diversity in a global collection of Arabidopsis thaliana accessions. Cell 166:2492–505 [Google Scholar]
  67. Kawashima T, Berger F. 67.  2014. Epigenetic reprogramming in plant sexual reproduction. Nat. Rev. Genet. 15:9613–24 [Google Scholar]
  68. Kohli RM, Zhang Y. 68.  2013. Tet enzymes, TDG and the dynamics of DNA demethylation. Nature 502:7472472–79 [Google Scholar]
  69. Kooke R, Johannes F, Wardenaar R, Becker F, Etcheverry M. 69.  et al. 2015. Epigenetic basis of morphological variation and phenotypic plasticity in Arabidopsis thaliana. Plant Cell 27:2337–48 [Google Scholar]
  70. Kronholm I, Collins S. 70.  2015. Epigenetic mutations can both help and hinder adaptive evolution. Mol. Ecol. 25:81856–68 [Google Scholar]
  71. Latzel V, Allan E, Bortolini Silveira A, Colot V, Fischer M, Bossdorf O. 71.  2013. Epigenetic diversity increases the productivity and stability of plant populations. Nat. Commun. 4:2875 [Google Scholar]
  72. Law JA, Ausin I, Johnson LM, Vashisht AA, Zhu JK. 72.  et al. 2010. A protein complex required for polymerase V transcripts and RNA-directed DNA methylation in Arabidopsis. Curr. Biol. 20:10951–56 [Google Scholar]
  73. Law JA, Du J, Hale CJ, Feng S, Krajewski K. 73.  et al. 2013. Polymerase IV occupancy at RNA-directed DNA methylation sites requires SHH1. Nature 498:7454385–89 [Google Scholar]
  74. Law JA, Jacobsen SE. 74.  2010. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat. Rev. Genet. 11:3204–20 [Google Scholar]
  75. Li CF, Pontes O, El-Shami M, Henderson IR, Bernatavichute YV. 75.  et al. 2006. An ARGONAUTE4-containing nuclear processing center colocalized with Cajal bodies in Arabidopsis thaliana. Cell 126:193–106 [Google Scholar]
  76. Li Q, Eichten SR, Hermanson PJ, Springer NM. 76.  2014. Inheritance patterns and stability of DNA methylation variation in maize near-isogenic lines. Genetics 196:3667–76 [Google Scholar]
  77. Li X, Zhu J, Hu F, Ge S, Ye M. 77.  et al. 2012. Single-base resolution maps of cultivated and wild rice methylomes and regulatory roles of DNA methylation in plant gene expression. BMC Genom. 13:1300 [Google Scholar]
  78. Lippman Z, Gendrel A-V, Black M, Vaughn MW, Dedhia N. 78.  et al. 2004. Role of transposable elements in heterochromatin and epigenetic control. Nature 430:6998471–76 [Google Scholar]
  79. Lister R, Malley RCO, Tonti-Filippini J, Gregory BD, Berry CC. 79.  et al. 2008. Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 133:523–36 [Google Scholar]
  80. Long Q, Rabanal FA, Meng D, Huber CD, Farlow A. 80.  et al. 2013. Massive genomic variation and strong selection in Arabidopsis thaliana lines from Sweden. Nat. Genet. 45:8884–90 [Google Scholar]
  81. López Sánchez A, Stassen J, Furci L, Smith L, Ton J. 81.  2016. The role of DNA (de)methylation in immune responsiveness of Arabidopsis. Plant J. In press [Google Scholar]
  82. Luna E, Bruce TJA, Roberts MR, Flors V, Ton J. 82.  2012. Next-generation systemic acquired resistance. Plant Physiol. 158:2844–53 [Google Scholar]
  83. Manning K, Tör M, Poole M, Hong Y, Thompson AJ. 83.  et al. 2006. A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat. Genet. 38:8948–52 [Google Scholar]
  84. Marí-Ordóñez A, Marchais A, Etcheverry M, Martin A, Colot V, Voinnet O. 84.  2013. Reconstructing de novo silencing of an active plant retrotransposon. Nat. Genet. 45:1029–39 [Google Scholar]
  85. Martienssen RA. 85.  1998. Transposons, DNA methylation and gene control. Trends Genet. 14:7263–64 [Google Scholar]
  86. Martienssen RA, Colot V. 86.  2001. DNA methylation and epigenetic inheritance in plants and filamentous fungi. Science 293:55321070–74 [Google Scholar]
  87. Martin A, Troadec C, Boualem A, Rajab M, Fernandez R. 87.  et al. 2009. A transposon-induced epigenetic change leads to sex determination in melon. Nature 461:72671135–38 [Google Scholar]
  88. Mathieu O, Reinders J, Caikovski M, Smathajitt C, Paszkowski J. 88.  et al. 2007. Transgenerational stability of the Arabidopsis epigenome is coordinated by CG methylation. Cell 130:5851–62 [Google Scholar]
  89. Matzke MA, Mosher RA. 89.  2014. RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat. Rev. Genet. 15:6394–408 [Google Scholar]
  90. McClintock B. 90.  1965. The control of gene action in maize. Brookhaven Symp. Biol. 18:162–84 [Google Scholar]
  91. McCue AD, Nuthikattu S, Reeder SH, Slotkin RK. 91.  2012. Gene expression and stress response mediated by the epigenetic regulation of a transposable element small RNA. PLOS Genet. 8:2e1002474 [Google Scholar]
  92. McCue AD, Panda K, Nuthikattu S, Choudury SG, Thomas EN, Slotkin RK. 92.  2015. ARGONAUTE 6 bridges transposable element mRNA-derived siRNAs to the establishment of DNA methylation. EMBO J. 34:120–35 [Google Scholar]
  93. Meng D, Dubin M, Zhang P, Osborne EJ, Stegle O. 93.  et al. 2016. Limited contribution of DNA methylation variation to expression regulation in Arabidopsis thaliana. PLOS Genet. 12:7e1006141 [Google Scholar]
  94. Mirouze M, Reinders J, Bucher E, Nishimura T, Schneeberger K. 94.  et al. 2009. Selective epigenetic control of retrotransposition in Arabidopsis. Nature 461:7262427–30 [Google Scholar]
  95. Miura A, Yonebayashi S, Watanabe K, Toyama T, Shimada H, Kakutani T. 95.  2001. Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis. Nature 411:6834212–14 [Google Scholar]
  96. Miura K, Agetsuma M, Kitano H, Yoshimura A, Matsuoka M. 96.  et al. 2009. A metastable DWARF1 epigenetic mutant affecting plant stature in rice. PNAS 106:2711218–23 [Google Scholar]
  97. Mosher RA, Melnyk CW, Kelly KA, Dunn RM, Studholme DJ, Baulcombe DC. 97.  2009. Uniparental expression of PolIV-dependent siRNAs in developing endosperm of Arabidopsis. Nature 460:7252283–86 [Google Scholar]
  98. Myant K, Stancheva I. 98.  2008. LSH cooperates with DNA methyltransferases to repress transcription. Mol. Cell. Biol. 28:1215–26 [Google Scholar]
  99. Niederhuth CE, Bewick AJ, Ji L, Alabady MS, Do Kim K. 99.  et al. 2015. Widespread natural variation of DNA methylation within angiosperms. bioRxiv doi: http://dx.doi.org/10.1101/045880 [Google Scholar]
  100. Nuthikattu S, McCue AD, Panda K, Fultz D, DeFraia C. 100.  et al. 2013. The initiation of epigenetic silencing of active transposable elements is triggered by RDR6 and 21–22 nucleotide small interfering RNAs. Plant Physiol. 162:1116–31 [Google Scholar]
  101. Ong-Abdullah M, Ordway JM, Jiang N, Ooi S-E, Kok S. 101.  et al. 2015. Loss of Karma transposon methylation underlies the mantled somaclonal variant of oil palm. Nature 525:7570533–37 [Google Scholar]
  102. Ossowski S, Schneeberger K, Lucas-Lledó JI, Warthmann N, Clark RM. 102.  et al. 2010. The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana. Science 327:596192–94 [Google Scholar]
  103. Pál C. 103.  1998. Plasticity, memory and the adaptive landscape of the genotype. Proc. R. Soc. B 265:14031319–23 [Google Scholar]
  104. Pál C, Miklós I. 104.  1999. Epigenetic inheritance, genetic assimilation and speciation. J. Theor. Biol. 200:19–37 [Google Scholar]
  105. Penterman J, Zilberman D, Huh JH, Ballinger T, Henikoff S, Fischer RL. 105.  2007. DNA demethylation in the Arabidopsis genome. PNAS 104:166752–57 [Google Scholar]
  106. Pontier D, Picart C, Roudier F, Garcia D, Lahmy S. 106.  et al. 2012. NERD, a plant-specific GW protein, defines an additional RNAi-dependent chromatin-based pathway in Arabidopsis. Mol. Cell 48:1121–32 [Google Scholar]
  107. Quadrana L, Almeida J, Asís R, Duffy T, Dominguez PG. 107.  et al. 2014. Natural occurring epialleles determine vitamin E accumulation in tomato fruits. Nat. Commun. 5:3027 [Google Scholar]
  108. Quadrana L, Silveira AB, Mayhew GF, Leblanc C, Martienssen RA. 108.  et al. 2016. The Arabidopsis thaliana mobilome and its impact at the species level. eLife 5:1–25 [Google Scholar]
  109. Regulski M, Lu Z, Kendall J, Donoghue MTA, Reinders J. 109.  et al. 2013. The maize methylome influences mRNA splice sites and reveals widespread paramutation-like switches guided by small RNA. Genome Res. 23:101651–62 [Google Scholar]
  110. Reinders J, Wulff BBH, Mirouze M, Mari-Ordoñez A, Dapp M. 110.  et al. 2009. Compromised stability of DNA methylation and transposon immobilization in mosaic Arabidopsis epigenomes. Genes Dev. 23:8939–50 [Google Scholar]
  111. Richards EJ. 111.  2006. Inherited epigenetic variation—revisiting soft inheritance. Nat. Rev. Genet. 7:5395–401 [Google Scholar]
  112. Riddle NC, Richards EJ. 112.  2002. The control of natural variation in cytosine methylation in Arabidopsis. Genetics 162:1355–63 [Google Scholar]
  113. Rigal M, Becker C, Pélissier T, Pogorelcnik R, Devos J. 113.  et al. 2016. Epigenome confrontation triggers immediate reprogramming of DNA methylation and transposon silencing in Arabidopsis thaliana F1 epihybrids. PNAS 113:14E2083–92 [Google Scholar]
  114. Rigal M, Kevei Z, Pélissier T, Mathieu O. 114.  2012. DNA methylation in an intron of the IBM1 histone demethylase gene stabilizes chromatin modification patterns. EMBO J. 31:132981–93 [Google Scholar]
  115. Riggs AD. 115.  1975. X inactivation, differentiation, and DNA methylation. Cytogenet. Genome Res. 14:19–25 [Google Scholar]
  116. Roux F, Colomé-Tatché M, Edelist C, Wardenaar R, Guerche P. 116.  et al. 2011. Genome-wide epigenetic perturbation jump-starts patterns of heritable variation found in nature. Genetics 188:41015–17 [Google Scholar]
  117. Saze H, Shiraishi A, Miura A, Kakutani T. 117.  2008. Control of genic DNA methylation by a jmjC domain-containing protein in Arabidopsis thaliana. Science 319:5862462–65 [Google Scholar]
  118. Schmitz RJ, He Y, Valdes-Lopez O, Khan SM, Joshi T. 118.  et al. 2013. Epigenome-wide inheritance of cytosine methylation variants in a recombinant inbred population. Genome Res. 23:1663–74 [Google Scholar]
  119. Schmitz RJ, Schultz MD, Lewsey MG, O'Malley RC, Urich MA. 119.  et al. 2011. Transgenerational epigenetic instability is a source of novel methylation variants. Science 334:6054369–73 [Google Scholar]
  120. Schmitz RJ, Schultz MD, Urich MA, Nery JR, Pelizzola M. 120.  et al. 2013. Patterns of population epigenomic diversity. Nature 495:7440193–98 [Google Scholar]
  121. Secco D, Wang C, Shou H, Schultz MD, Chiarenza S. 121.  et al. 2015. Stress induced gene expression drives transient DNA methylation changes at adjacent repetitive elements. eLife 4:1–26 [Google Scholar]
  122. Seisenberger S, Peat JR, Hore TA, Santos F, Dean W, Reik W. 122.  2013. Reprogramming DNA methylation in the mammalian life cycle: building and breaking epigenetic barriers. Philos. Trans. R. Soc. B 368:160920110330 [Google Scholar]
  123. Seymour DK, Koenig D, Hagmann J, Becker C, Weigel D. 123.  2014. Evolution of DNA methylation patterns in the Brassicaceae is driven by differences in genome organization. PLOS Genet. 10:11e1004785 [Google Scholar]
  124. Shen X, De Jonge J, Forsberg SKG, Pettersson ME, Sheng Z. 124.  et al. 2014. Natural CMT2 variation is associated with genome-wide methylation changes and temperature seasonality. PLOS Genet. 10:12e1004842 [Google Scholar]
  125. Silveira AB, Trontin C, Cortijo S, Barau J, Del Bem LEV. 125.  et al. 2013. Extensive natural epigenetic variation at a de novo originated gene. PLOS Genet. 9:4e1003437 [Google Scholar]
  126. Singer T, Yordan C, Martienssen RA. 126.  2001. Robertson's Mutator transposons in A. thaliana are regulated by the chromatin-remodeling gene Decrease in DNA Methylation (DDM1). Genes Dev. 15:5591–602 [Google Scholar]
  127. Slotkin RK, Vaughn M, Borges F, Tanurdžić M, Becker JD. 127.  et al. 2009. Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136:3461–72 [Google Scholar]
  128. Stelpflug SC, Eichten SR, Hermanson PJ, Springer NM, Kaeppler SM. 128.  2014. Consistent and heritable alterations of DNA methylation are induced by tissue culture in maize. Genetics 198:1209–18 [Google Scholar]
  129. Stroud H, Ding B, Simon SA, Feng S, Bellizzi M. 129.  et al. 2013. Plants regenerated from tissue culture contain stable epigenome changes in rice. eLife 2:e00354 [Google Scholar]
  130. Stroud H, Do T, Du J, Zhong X, Feng S. 130.  et al. 2014. Non-CG methylation patterns shape the epigenetic landscape in Arabidopsis. Nat. Struct. Mol. Biol. 21:164–72 [Google Scholar]
  131. Stroud H, Greenberg MVC, Feng S, Bernatavichute YV, Jacobsen SE. 131.  2013. Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome. Cell 152:1–2352–64 [Google Scholar]
  132. Takuno S, Gaut BS. 132.  2013. Gene body methylation is conserved between plant orthologs and is of evolutionary consequence. PNAS 110:51797–802 [Google Scholar]
  133. Takuno S, Ran J-H, Gaut BS. 133.  2016. Evolutionary patterns of genic DNA methylation vary across land plants. Nat. Plants 2:15222 [Google Scholar]
  134. Tanurdzic M, Vaughn MW, Jiang H, Lee T-J, Slotkin RK. 134.  et al. 2008. Epigenomic consequences of immortalized plant cell suspension culture. PLOS Biol. 6:122880–95 [Google Scholar]
  135. Teixeira FK, Colot V. 135.  2009. Gene body DNA methylation in plants: A means to an end or an end to a means?. EMBO J. 28:8997–98 [Google Scholar]
  136. Teixeira FK, Heredia F, Sarazin A, Roudier F, Boccara M. 136.  et al. 2009. A role for RNAi in the selective correction of DNA methylation defects. Science 323:59211600–4 [Google Scholar]
  137. Thakore PI, Black JB, Hilton IB, Gersbach CA. 137.  2016. Editing the epigenome: technologies for programmable transcription and epigenetic modulation. Nat. Methods 13:2127–37 [Google Scholar]
  138. Tsukahara S, Kobayashi A, Kawabe A, Mathieu O, Miura A, Kakutani T. 138.  2009. Bursts of retrotransposition reproduced in Arabidopsis. Nature 461:7262423–26 [Google Scholar]
  139. van der Graaf A, Wardenaar R, Neumann DA, Taudt A, Shaw RG. 139.  et al. 2015. Rate, spectrum, and evolutionary dynamics of spontaneous epimutations. PNAS 112:216676–81 [Google Scholar]
  140. Vaughn MW, Tanurdzić M, Lippman Z, Jiang H, Carrasquillo R. 140.  et al. 2007. Epigenetic natural variation in Arabidopsis thaliana. PLOS Biol. 5:7e174 [Google Scholar]
  141. Verhoeven KJF, van Gurp TP. 141.  2012. Transgenerational effects of stress exposure on offspring phenotypes in apomictic dandelion. PLOS ONE 7:6e38605 [Google Scholar]
  142. Vining KJ, Pomraning KR, Wilhelm LJ, Priest HD, Pellegrini M. 142.  et al. 2012. Dynamic DNA cytosine methylation in the Populus trichocarpa genome: tissue-level variation and relationship to gene expression. BMC Genom. 13:27 [Google Scholar]
  143. Vojta A, Dobrinić P, Tadić V, Bočkor L, Korać P. 143.  et al. 2016. Repurposing the CRISPR-Cas9 system for targeted DNA methylation. Nucleic Acids Res. 44:125615–28 [Google Scholar]
  144. Vongs A, Kakutani T, Martienssen RA, Richards EJ. 144.  1993. Arabidopsis thaliana DNA methylation mutants. Science 260:51161926–28 [Google Scholar]
  145. Waddington CH. 145.  1942. Canalization of development and the inheritance of acquired characters. Nature 3811:563–65 [Google Scholar]
  146. Weigel D, Colot V. 146.  2012. Epialleles in plant evolution. Genome Biol. 13:10249 [Google Scholar]
  147. Weigel D, Nordborg M. 147.  2015. Population genomics for understanding adaptation in wild plant species. Annu. Rev. Genet. 49:1315–38 [Google Scholar]
  148. Wibowo A, Becker C, Marconi G, Durr J, Price J. 148.  et al. 2016. Hyperosmotic stress memory 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 [Google Scholar]
  149. Willing E-M, Rawat V, Mandáková T, Maumus F, James GV. 149.  et al. 2015. Genome expansion of Arabis alpina linked with retrotransposition and reduced symmetric DNA methylation. Nat. Plants 1:14023 [Google Scholar]
  150. Woo H, Richards EJ. 150.  2008. Natural variation in DNA methylation in ribosomal RNA genes of Arabidopsis thaliana. BMC Plant Biol. 8:11–12 [Google Scholar]
  151. Yang D-L, Zhang G, Tang K, Li J, Yang L. 151.  et al. 2016. Dicer-independent RNA-directed DNA methylation in Arabidopsis. Cell Res. 26:166–82 [Google Scholar]
  152. Ye R, Chen Z, Lian B, Rowley MJ, Xia N. 152.  et al. 2015. A Dicer-independent route for biogenesis of siRNAs that direct DNA methylation in Arabidopsis. Mol. Cell 61:2222–35 [Google Scholar]
  153. Yi H, Riddle NC, Stokes TL, Woo HR, Richards EJ. 153.  2004. Induced and natural epigenetic variation. Cold Spring Harb. Symp. Quant. Biol. 69:155–60 [Google Scholar]
  154. Yu A, Lepère G, Jay F, Wang J, Bapaume L. 154.  et al. 2013. Dynamics and biological relevance of DNA demethylation in Arabidopsis antibacterial defense. PNAS 110:62389–94 [Google Scholar]
  155. Zemach A, Kim MY, Hsieh PH, Coleman-Derr D, Eshed-Williams L. 155.  et al. 2013. The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell 153:1193–205 [Google Scholar]
  156. Zemach A, McDaniel IE, Silva P, Zilberman D. 156.  2010. Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science 328:5980916–19 [Google Scholar]
  157. Zhai J, Bischof S, Wang H, Feng S, Lee T. 157.  et al. 2015. A one precursor one siRNA model for Pol IV-dependent siRNA biogenesis. Cell 163:2445–55 [Google Scholar]
  158. Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan SW-L. 158.  et al. 2006. Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126:61189–201 [Google Scholar]
  159. Zhang Y-Y, Fischer M, Colot V, Bossdorf O. 159.  2013. Epigenetic variation creates potential for evolution of plant phenotypic plasticity. New Phytol. 197:1314–22 [Google Scholar]
  160. Zheng B, Wang Z, Li S, Yu B, Liu JY, Chen X. 160.  2009. Intergenic transcription by RNA polymerase II coordinates Pol IV and Pol V in siRNA-directed transcriptional gene silencing in Arabidopsis. Genes Dev. 23:242850–60 [Google Scholar]
  161. Zhong S, Fei Z, Chen Y, Zheng Y, Huang M. 161.  et al. 2013. Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening. Nat. Biotechnol. 31:2154–59 [Google Scholar]
  162. Zilberman D, Gehring M, Tran RK, Ballinger T, Henikoff S. 162.  2006. Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat. Genet. 39:161–69 [Google Scholar]
  163. Zhong X, Du J, Hale CJ, Gallego-Bartolome J, Feng S. 163.  et al. 2014. Molecular mechanism of action of plant DRM de novo DNA methyltransferases. Cell 157:51050–60 [Google Scholar]

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