Plant Transgenerational Epigenetics

Annual Review of Genetics

Volumn 50, Issue , 2016, Pages 467-491

  Quadrana, Leandro ^a   Colot, Vincent ^a  

^a CNRS   (France)

Author keywords

DNA methylation; Epiallele; Epimutation; Inheritance; Mutation

Indexed keywords

ARABIDOPSIS; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; DEMETHYLATION; DNA METHYLATION; ENVIRONMENTAL CHANGE; EPIGENETICS; GENETIC VARIABILITY; GENOME-WIDE ASSOCIATION STUDY; NONHUMAN; PHENOTYPIC VARIATION; PRIORITY JOURNAL; REPRODUCTION; REVIEW; GENETIC EPIGENESIS; GENETIC VARIATION; GENETICS; MUTATION; PLANT; PLANT GENOME;

PLANT DNA;

DNA METHYLATION; DNA, PLANT; EPIGENESIS, GENETIC; GENETIC VARIATION; GENOME, PLANT; MUTATION; PLANTS; REPRODUCTION;

EID: 85000799134     PISSN: 00664197     EISSN: 15452948     Source Type: Book Series    
DOI: 10.1146/annurev-genet-120215-035254     Document Type: Review

References (163)

1. Ahmed I, Sarazin A, Bowler C, Colot V, Quesneville H. 2011. Genome-wide evidence for local DNA methylation spreading from small RNA-targeted sequences in Arabidopsis. Nucleic Acids Res. 39(16):6919-31
2. Arteaga-Vazquez MA, Chandler VL. 2010. Paramutation in maize: RNA mediated trans-generational gene silencing. Curr. Opin. Genet. Dev. 20(2):156-63
3. Baubec T, Colombo DF, Wirbelauer C, Schmidt J, Burger L, et al. 2015. Genomic profiling of DNA methyltransferases reveals a role for DNMT3B in genic methylation. Nature 520(7546):243-47
4. BaulcombeDC, Dean C. 2014. Epigenetic regulation in plant responses to the environment. Cold Spring Harb. Perspect. Biol. 6(9):a019471
5. Becker C, Hagmann J, Müller J, Koenig D, Stegle O, et al. 2011. Spontaneous epigenetic variation in the Arabidopsis thaliana methylome. Nature 480(7376):245-49
6. Bender J. 2004. DNA methylation of the endogenous PAI genes in Arabidopsis. Cold Spring Harb. Symp. Quant. Biol. 69:145-53
7. Berry S, Dean C. 2015. Environmental perception and epigenetic memory: mechanistic insight through FLC. Plant J. 83:133-48
8. Bestor TH, Chandler VL, Feinberg AP. 1994. Epigenetic effects in eukaryotic gene expression. Dev. Genet. 15(6):458-62
9. Bewick AJ, Ji L, Niederhuth CE, Willing E-M, Hofmeister BT, et al. 2016. On the origin and evolutionary consequences of gene body DNA methylation. PNAS 113:9111-16
10. Bird A. 2007. Perceptions of epigenetics. Nature 447:396-98
11. Blevins T, Podicheti R, Mishra V, Marasco M, Wang J, 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
12. Bond DM, Baulcombe DC. 2015. Epigenetic transitions leading to heritable, RNA-mediated de novo silencing in Arabidopsis thaliana. PNAS 112(3):201413053
13. Bossdorf O, Richards CL, Pigliucci M. 2008. Epigenetics for ecologists. Ecol. Lett. 11(2):106-15
14. Brachi B, Morris GP, Borevitz JO. 2011. Genome-wide association studies in plants: the missing heritability is in the field. Genome Biol. 12(10):232
15. Briggs D, Walters SM. 1984. Plant Variation and Evolution. Cambridge, UK: Cambridge Univ. Press. 2nd ed
16. Brink RA. 1956. A genetic change associated with the R locus in maize which is directed and potentially reversible. Genetics 41(6):872
17. Calarco JP, Borges F, Donoghue MTA, Van Ex F, Jullien PE, et al. 2012. Reprogramming of DNA methylation in pollen guides epigenetic inheritance via small RNA. Cell 151(1):194-205
18. Cao J, Schneeberger K, Ossowski S, Günther T, Bender S, et al. 2011. Whole-genome sequencing of multiple Arabidopsis thaliana populations. Nat. Genet. 43(10):956-63
19. Chodavarapu RK, Feng S, Ding B, Simon SA, Lopez D, et al. 2012. Transcriptome and methylome interactions in rice hybrids. PNAS 109(30):12040-45
20. CleatonMAM,EdwardsCA, Ferguson-Smith AC. 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
21. Cokus SJ, Feng S, Zhang X, Chen Z, Merriman B, et al. 2008. Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452:215-19
22. Coleman-Derr D, ZilbermanD. 2012. Deposition of histone variantH2A.Z within gene bodies regulates responsive genes. PLOS Genet. 8(10):e1002988
23. Colomé-Tatché M, Cortijo S, Wardenaar R, Morgado L, Lahouze B, et al. 2012. Features of the Arabidopsis recombination landscape resulting from the combined loss of sequence variation and DNA methylation. PNAS 109(40):16240-45
24. Cortijo S,Wardenaar R, Colomé-TatchéM, Gilly A, Etcheverry M, et al. 2014. Mapping the epigenetic basis of complex traits. Science 343(6175):1145-48
25. Crisp PA, Ganguly D, Eichten SR, Borevitz JO, Pogson BJ. 2016. Reconsidering plant memory: intersections between stress recovery, RNA turnover, and epigenetics. Sci. Adv. 2(2):e1501340
26. Cubas P, Vincent C, Coen E. 1999. An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401(6749):157-61
27. Day T, Bonduriansky R. 2011. A unified approach to the evolutionary consequences of genetic and nongenetic inheritance. Am. Nat. 178(2):E18-36
28. Dowen RH, Pelizzola M, Schmitz RJ, Lister R, Dowen JM, et al. 2012. Widespread dynamic DNA methylation in response to biotic stress. PNAS 109(32):E2183-91
29. Du J, Johnson LM, Jacobsen SE, Patel DJ. 2015. DNA methylation pathways and their crosstalk with histone methylation. Nat. Rev. Mol. Cell Biol. 16(9):519-32
30. DubinMJ, Zhang P,MengD,RemigereauM-S, Osborne EJ, et al. 2015.DNAmethylation in Arabidopsis has a genetic basis and shows evidence of local adaptation. eLife 4:e05255
31. Durand S, Bouché N, Perez Strand E, Loudet O, Camilleri C. 2012. Rapid establishment of genetic incompatibility through natural epigenetic variation. Curr. Biol. 22(4):326-31
32. Eichten SR, Briskine R, Song J, Li Q, Swanson-Wagner R, et al. 2013. Epigenetic and genetic influences on DNA methylation variation in maize populations. Plant Cell 25(8):2783-97
33. Eichten SR, Ellis NA,Makarevitch I, Yeh C, Gent JI, et al. 2012. Spreading of heterochromatin is limited to specific families of maize retrotransposons. PLOS Genet. 8(12):e1003127
34. Eichten SR, Swanson-Wagner RA, Schnable JC, Waters AJ, Hermanson PJ, et al. 2011. Heritable epigenetic variation among maize inbreds. PLOS Genet. 7(11):e1002372
35. El-shami M, PontierD, Lahmy S, Braun L, Picart C, et al. 2007. ReiteratedWG/GWmotifs form functionally and evolutionarily conserved ARGONAUTE-binding platforms in RNAi-related components. Genes Dev. 21:2539-44
36. FedoroffN. 1989. The heritable activation of cryptic suppressor-mutator elements by an active element. Genetics 121(3):591-608
37. Fedoroff N, Schläppi M, Raina R. 1995. Epigenetic regulation of the maize Spm transposon. BioEssays 17(4):291-97
38. Fujimoto R, Kinoshita Y, Kawabe A, Kinoshita T, Takashima K, et al. 2008. Evolution and control of imprinted FWA genes in the genus Arabidopsis. PLOS Genet. 4(4):e1000048
39. Gao Z, Liu H, Daxinger L, Pontes O, He X, et al. 2010. An RNA Polymerase II-and AGO4-associated protein acts in RNA-directed DNA methylation. Nature 465(7294):106-9
40. Gehring M. 2013. Genomic imprinting: insights from plants. Annu. Rev. Genet. 47(1):187-208
41. Gendrel A, Heard E. 2014. Noncoding RNAs and epigenetic mechanisms during X-chromosome inactivation. Annu. Rev. Cell Dev. Biol. 30:561-80
42. Gent JI, Ellis NA, Guo L, Harkess AE, Yao Y, et al. 2013. CHH islands: de novo DNA methylation in near-gene chromatin regulation in maize. Genome Res. 23(4):628-37
43. Geoghegan JL, SpencerHG. 2013. Exploring epiallele stability in a population-epigenetic model. Theor. Popul. Biol. 83:136-44
44. Geoghegan JL, Spencer HG. 2013. The adaptive invasion of epialleles in a heterogeneous environment. Theor. Popul. Biol. 88:1-8
45. Geoghegan JL, SpencerHG. 2013. The evolutionary potential of paramutation: a population-epigenetic model. Theor. Popul. Biol. 88:9-19
46. Gilly A, Etcheverry M, Madoui M-A, Guy J, Quadrana L, et al. 2014. TE-tracker: systematic identification of transposition events through whole-genome resequencing. BMC Bioinform. 15(1):377
47. Hagmann J, Becker C, Müller J, Stegle O, Meyer RC, et al. 2015. Century-scale methylome stability in a recently diverged Arabidopsis thaliana lineage. PLOS Genet. 11(1):e1004920
48. Heard E,Martienssen RA. 2014. Transgenerational epigenetic inheritance: myths and mechanisms. Cell 157(1):95-109
49. Holeski LM, Jander G, Agrawal AA. 2012. Transgenerational defense induction and epigenetic inheritance in plants. Trends Ecol. Evol. 27(11):618-26
50. Holliday R. 1987. The inheritance of epigenetic defects. Science 238(11):163-70
51. Hollister JD, Gaut BS. 2009. Epigenetic silencing of transposable elements: a trade-off between reduced transposition and deleterious effects on neighboring gene expression. Genome Res. 19(8):1419-28
52. Hsieh T-F, Ibarra CA, Silva P, Zemach A, Eshed-Williams L, et al. 2009. Genome-wide demethylation of Arabidopsis endosperm. Science 324(5933):1451-54
53. Ibarra CA, Feng X, Schoft VK, Hsieh T-F, Uzawa R, et al. 2012. Active DNA demethylation in plant companion cells reinforces transposon methylation in gametes. Science. 337(6100):1360-64
54. Inagaki S, Miura-Kamio A, Nakamura Y, Lu F, Cui X, et al. 2010. Autocatalytic differentiation of epigenetic modifications within the Arabidopsis genome. EMBO J. 29(20):3496-3506
55. ItoT,Tarutani Y,ToTK, KassamM,Duvernois-Berthet E, et al. 2015. Genome-wide negative feedback drives transgenerational DNA methylation dynamics in Arabidopsis. PLOS Genet. 11(4):e1005154
56. Iwasaki M, Paszkowski J. 2014. Identification of genes preventing transgenerational transmission of stress-induced epigenetic states. PNAS 111(23):8547-52
57. Jablonka E, Lamb MJ. 1989. The inheritance of acquired epigenetic variations. Int. J. Epidemiol. 44(4):1094-103
58. Jiang C, Mithani A, Belfield EJ, Mott R, Hurst LD, Harberd NP. 2014. Environmentally responsive genome-wide accumulation of de novo Arabidopsis thaliana mutations and epimutations. Genome Res. 24:1821-29
59. Johannes F,Colomé-TatchéM. 2011. Concerning epigenetics and inbreeding. Nat. Rev. Genet. 12(5):376
60. Johannes F, Colot V, Jansen RC. 2008. Epigenome dynamics: a quantitative genetics perspective. Nat. Rev. Genet. 9(11):883-90
61. Johannes F, Porcher E, Teixeira FK, Saliba-Colombani V, Albuisson J, et al. 2009. Assessing the impact of transgenerational epigenetic variation on complex traits. PLOS Genet. 5(6):e1000530
62. Johnson LM, Du J, Hale CJ, Bischof S, Feng S, et al. 2014. SRA-and SET-domain-containing proteins link RNA polymerase V occupancy to DNA methylation. Nature 507(7490):124-28
63. Jullien PE, Susaki D, YelagandulaR,Higashiyama T, Berger F. 2012.DNAmethylation dynamics during sexual reproduction in Arabidopsis thaliana. Curr. Biol. 22(19):1825-30
64. Kankel MW, Ramsey DE, Stokes TL, Flowers SK, Haag JR, et al. 2003. Arabidopsis MET1 cytosine methyltransferase mutants. Genetics 163(3):1109-22
65. Kanno T, Mette MF,Kreil DP,AufsatzW,Matzke M, Matzke AJM. 2004. Involvement of putative SNF2 chromatin remodeling protein DRD1 in RNA-directed DNA methylation. Curr. Biol. 14(9):801-5
66. 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(2):492-505
67. Kawashima T, Berger F. 2014. Epigenetic reprogramming in plant sexual reproduction. Nat. Rev. Genet. 15(9):613-24
68. Kohli RM, Zhang Y. 2013. Tet enzymes, TDG and the dynamics of DNA demethylation. Nature 502(7472):472-79
69. Kooke R, Johannes F,Wardenaar R, Becker F, Etcheverry M, et al. 2015. Epigenetic basis of morphological variation and phenotypic plasticity in Arabidopsis thaliana. Plant Cell 27(2):337-48
70. Kronholm I, Collins S. 2015. Epigenetic mutations can both help and hinder adaptive evolution. Mol. Ecol. 25(8):1856-68
71. Latzel V, Allan E, Bortolini Silveira A, Colot V, Fischer M, Bossdorf O. 2013. Epigenetic diversity increases the productivity and stability of plant populations. Nat. Commun. 4:2875
72. Law JA, Ausin I, Johnson LM, Vashisht AA, Zhu JK, et al. 2010. A protein complex required for polymerase V transcripts and RNA-directed DNA methylation in Arabidopsis. Curr. Biol. 20(10):951-56
73. Law JA, Du J, Hale CJ, Feng S, Krajewski K, et al. 2013. Polymerase IV occupancy at RNA-directed DNA methylation sites requires SHH1. Nature 498(7454):385-89
74. Law JA, Jacobsen SE. 2010. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat. Rev. Genet. 11(3):204-20
75. Li CF, Pontes O, El-Shami M, Henderson IR, Bernatavichute YV, et al. 2006. An ARGONAUTE4-containing nuclear processing center colocalized with Cajal bodies in Arabidopsis thaliana. Cell 126(1):93-106
76. Li Q, Eichten SR, Hermanson PJ, Springer NM. 2014. Inheritance patterns and stability of DNA methylation variation in maize near-isogenic lines. Genetics 196(3):667-76
77. Li X, Zhu J, Hu F, Ge S, Ye M, 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(1):300
78. Lippman Z, Gendrel A-V, Black M, VaughnMW, Dedhia N, et al. 2004. Role of transposable elements in heterochromatin and epigenetic control. Nature 430(6998):471-76
79. Lister R, Malley RCO, Tonti-Filippini J, Gregory BD, Berry CC, et al. 2008. Highly integrated singlebase resolution maps of the epigenome in Arabidopsis. Cell 133:523-36
80. Long Q, Rabanal FA, Meng D, Huber CD, Farlow A, et al. 2013. Massive genomic variation and strong selection in Arabidopsis thaliana lines from Sweden. Nat. Genet. 45(8):884-90
81. López Sánchez A, Stassen J, Furci L, Smith L,Ton J. 2016. The role ofDNA(de)methylation in immune responsiveness of Arabidopsis. Plant J. In press
82. Luna E, Bruce TJA, Roberts MR, Flors V, Ton J. 2012. Next-generation systemic acquired resistance. Plant Physiol. 158(2):844-53
83. Manning K, Tör M, Poole M, Hong Y, Thompson AJ, et al. 2006. A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat. Genet. 38(8):948-52
84. Marí-Ordonez A, Marchais A, Etcheverry M, Martin A, Colot V, Voinnet O. 2013. Reconstructing de novo silencing of an active plant retrotransposon. Nat. Genet. 45:1029-39
85. Martienssen RA. 1998. Transposons, DNA methylation and gene control. Trends Genet. 14(7):263-64
86. Martienssen RA, Colot V. 2001. DNA methylation and epigenetic inheritance in plants and filamentous fungi. Science 293(5532):1070-74
87. Martin A, Troadec C, Boualem A, Rajab M, Fernandez R, et al. 2009. A transposon-induced epigenetic change leads to sex determination in melon. Nature 461(7267):1135-38
88. Mathieu O, Reinders J, CaikovskiM, Smathajitt C, Paszkowski J, et al. 2007. Transgenerational stability of the Arabidopsis epigenome is coordinated by CG methylation. Cell 130(5):851-62
89. Matzke MA, Mosher RA. 2014. RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat. Rev. Genet. 15(6):394-408
90. McClintock B. 1965. The control of gene action in maize. Brookhaven Symp. Biol. 18:162-84
91. McCue AD, Nuthikattu S, Reeder SH, Slotkin RK. 2012. Gene expression and stress response mediated by the epigenetic regulation of a transposable element small RNA. PLOS Genet. 8(2):e1002474
92. McCue AD, Panda K, Nuthikattu S, Choudury SG, Thomas EN, Slotkin RK. 2015. ARGONAUTE 6 bridges transposable element mRNA-derived siRNAs to the establishment of DNA methylation. EMBO J. 34(1):20-35
93. Meng D, Dubin M, Zhang P, Osborne EJ, Stegle O, et al. 2016. Limited contribution of DNA methylation variation to expression regulation in Arabidopsis thaliana. PLOS Genet. 12(7):e1006141
94. MirouzeM,Reinders J, BucherE,Nishimura T, SchneebergerK, et al. 2009. Selective epigenetic control of retrotransposition in Arabidopsis. Nature 461(7262):427-30
95. 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(6834):212-14
96. Miura K, Agetsuma M, Kitano H, Yoshimura A, Matsuoka M, et al. 2009. A metastable DWARF1 epigenetic mutant affecting plant stature in rice. PNAS 106(27):11218-23
97. Mosher RA, Melnyk CW, Kelly KA, Dunn RM, Studholme DJ, Baulcombe DC. 2009. Uniparental expression of PolIV-dependent siRNAs in developing endosperm of Arabidopsis. Nature 460(7252):283-86
98. Myant K, Stancheva I. 2008. LSH cooperates with DNA methyltransferases to repress transcription. Mol. Cell. Biol. 28(1):215-26
99. Niederhuth CE, Bewick AJ, Ji L, Alabady MS, Do Kim K, et al. 2015. Widespread natural variation of DNA methylation within angiosperms. bioRxiv doi: http://dx.doi.org/10.1101/045880
100. Nuthikattu S, McCue AD, PandaK, Fultz D, DeFraia C, 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(1):116-31
101. Ong-Abdullah M, Ordway JM, Jiang N, Ooi S-E, Kok S, et al. 2015. Loss of Karma transposon methylation underlies the mantled somaclonal variant of oil palm. Nature 525(7570):533-37
102. Ossowski S, Schneeberger K, Lucas-Lledo JI, Warthmann N, Clark RM, et al. 2010. The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana. Science 327(5961):92-94
103. Pál C. 1998. Plasticity, memory and the adaptive landscape of the genotype. Proc. R. Soc. B 265(1403):1319-23
104. Pál C, Mikl ós I. 1999. Epigenetic inheritance, genetic assimilation and speciation. J. Theor. Biol. 200:19-37
105. Penterman J, Zilberman D, Huh JH, Ballinger T, Henikoff S, Fischer RL. 2007. DNA demethylation in the Arabidopsis genome. PNAS 104(16):6752-57
106. Pontier D, Picart C, Roudier F, Garcia D, Lahmy S, et al. 2012. NERD, a plant-specific GW protein, defines an additional RNAi-dependent chromatin-based pathway in Arabidopsis. Mol. Cell 48(1):121-32
107. Quadrana L, Almeida J, Asís R, Duffy T, Dominguez PG, et al. 2014. Natural occurring epialleles determine vitamin E accumulation in tomato fruits. Nat. Commun. 5:3027
108. Quadrana L, Silveira AB,Mayhew GF, Leblanc C,Martienssen RA, et al. 2016. The Arabidopsis thaliana mobilome and its impact at the species level. eLife. 5:1-25
109. Regulski M, Lu Z, Kendall J, Donoghue MTA, Reinders J, et al. 2013. The maize methylome influences mRNA splice sites and reveals widespread paramutation-like switches guided by small RNA. Genome Res. 23(10):1651-62
110. Reinders J, Wulff BBH, Mirouze M, Mari-Ordonez A, Dapp M, et al. 2009. Compromised stability of DNA methylation and transposon immobilization in mosaic Arabidopsis epigenomes. Genes Dev. 23(8):939-50
111. Richards EJ. 2006. Inherited epigenetic variation-revisiting soft inheritance. Nat. Rev. Genet. 7(5):395-401
112. Riddle NC, Richards EJ. 2002. The control of natural variation in cytosine methylation in Arabidopsis. Genetics 162(1):355-63
113. Rigal M, Becker C, Pélissier T, Pogorelcnik R, Devos J, et al. 2016. Epigenome confrontation triggers immediate reprogramming of DNA methylation and transposon silencing in Arabidopsis thaliana F1 epihybrids. PNAS 113(14):E2083-92
114. 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(13):2981-93
115. Riggs AD. 1975.Xinactivation, differentiation, andDNAmethylation. Cytogenet.Genome Res. 14(1):9-25
116. Roux F, Colomé-Tatché M, Edelist C,Wardenaar R, Guerche P, et al. 2011. Genome-wide epigenetic perturbation jump-starts patterns of heritable variation found in nature. Genetics 188(4):1015-17
117. Saze H, Shiraishi A, Miura A, Kakutani T. 2008. Control of genic DNA methylation by a jmjC domaincontaining protein in Arabidopsis thaliana. Science 319(5862):462-65
118. Schmitz RJ, He Y, Valdes-Lopez O, Khan SM, Joshi T, et al. 2013. Epigenome-wide inheritance of cytosine methylation variants in a recombinant inbred population. Genome Res. 23:1663-74
119. 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(6054):369-73
120. SchmitzRJ, SchultzMD, Urich MA,Nery JR, Pelizzola M, et al. 2013. Patterns of population epigenomic diversity. Nature 495(7440):193-98
121. 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 4:1-26
122. Seisenberger S, Peat JR, Hore TA, Santos F, Dean W, Reik W. 2013. Reprogramming DNA methylation in the mammalian life cycle: building and breaking epigenetic barriers. Philos. Trans. R. Soc. B 368(1609):20110330
123. Seymour DK,KoenigD,Hagmann J, Becker C, Weigel D. 2014. Evolution ofDNAmethylation patterns in the Brassicaceae is driven by differences in genome organization. PLOS Genet. 10(11):e1004785
124. Shen X, De Jonge J, Forsberg SKG, Pettersson ME, Sheng Z, et al. 2014. Natural CMT2 variation is associated with genome-wide methylation changes and temperature seasonality. PLOS Genet. 10(12):e1004842
125. Silveira AB, Trontin C, Cortijo S, Barau J, Del Bem LEV, et al. 2013. Extensive natural epigenetic variation at a de novo originated gene. PLOS Genet. 9(4):e1003437
126. 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(5):591-602
127. Slotkin RK, VaughnM, Borges F, TanurdžícM, Becker JD, et al. 2009. Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136(3):461-72
128. Stelpflug SC, Eichten SR, Hermanson PJ, Springer NM, Kaeppler SM. 2014. Consistent and heritable alterations of DNA methylation are induced by tissue culture in maize. Genetics 198(1):209-18
129. Stroud H, Ding B, Simon SA, Feng S, Bellizzi M, et al. 2013. Plants regenerated from tissue culture contain stable epigenome changes in rice. eLife 2:e00354
130. Stroud H, Do T, Du J, Zhong X, Feng S, et al. 2014. Non-CG methylation patterns shape the epigenetic landscape in Arabidopsis. Nat. Struct. Mol. Biol. 21(1):64-72
131. Stroud H, Greenberg MVC, Feng S, Bernatavichute YV, Jacobsen SE. 2013. Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome. Cell 152(1-2):352-64
132. Takuno S, Gaut BS. 2013. Gene body methylation is conserved between plant orthologs and is of evolutionary consequence. PNAS 110(5):1797-802
133. Takuno S, Ran J-H, Gaut BS. 2016. Evolutionary patterns of genic DNA methylation vary across land plants. Nat. Plants 2:15222
134. Tanurdzic M, Vaughn MW, Jiang H, Lee T-J, Slotkin RK, et al. 2008. Epigenomic consequences of immortalized plant cell suspension culture. PLOS Biol. 6(12):2880-95
135. Teixeira FK, Colot V. 2009. Gene body DNA methylation in plants: A means to an end or an end to a means? EMBO J. 28(8):997-98
136. 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(5921):1600-4
137. Thakore PI, Black JB, Hilton IB, Gersbach CA. 2016. Editing the epigenome: technologies for programmable transcription and epigenetic modulation. Nat. Methods 13(2):127-37
138. Tsukahara S, Kobayashi A, Kawabe A, Mathieu O, Miura A, Kakutani T. 2009. Bursts of retrotransposition reproduced in Arabidopsis. Nature 461(7262):423-26
139. 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(21):6676-81
140. VaughnMW,TanurdzícM,Lippman Z, JiangH, Carrasquillo R, et al. 2007. Epigenetic natural variation in Arabidopsis thaliana. PLOS Biol. 5(7):e174
141. Verhoeven KJF, vanGurpTP. 2012. Transgenerational effects of stress exposure on offspring phenotypes in apomictic dandelion. PLOS ONE 7(6):e38605
142. Vining KJ, Pomraning KR, Wilhelm LJ, Priest HD, Pellegrini M, et al. 2012. Dynamic DNA cytosine methylation in the Populus trichocarpa genome: tissue-level variation and relationship to gene expression. BMC Genom. 13:27
143. Vojta A, Dobriníc P, Tadíc V, Bočkor L, Korác P, et al. 2016. Repurposing the CRISPR-Cas9 system for targeted DNA methylation. Nucleic Acids Res. 44(12):5615-28
144. Vongs A, Kakutani T, Martienssen RA, Richards EJ. 1993. Arabidopsis thaliana DNA methylation mutants. Science 260(5116):1926-28
145. Waddington CH. 1942. Canalization of development and the inheritance of acquired characters. Nature 3811:563-65
146. Weigel D, Colot V. 2012. Epialleles in plant evolution. Genome Biol. 13(10):249
147. Weigel D, NordborgM. 2015. Population genomics for understanding adaptation in wild plant species. Annu. Rev. Genet. 49(1):315-38
148. 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
149. Willing E-M, Rawat V, Mandáková T, Maumus F, James GV, et al. 2015. Genome expansion of Arabis alpina linked with retrotransposition and reduced symmetric DNA methylation. Nat. Plants 1:14023
150. WooH,Richards EJ. 2008. Natural variation inDNAmethylation in ribosomalRNAgenes of Arabidopsis thaliana. BMC Plant Biol. 8(1):1-12
151. Yang D-L, Zhang G, Tang K, Li J, Yang L, et al. 2016. Dicer-independent RNA-directed DNA methylation in Arabidopsis. Cell Res. 26(1):66-82
152. Ye R, Chen Z, Lian B, Rowley MJ, Xia N, et al. 2015. A Dicer-independent route for biogenesis of siRNAs that direct DNA methylation in Arabidopsis. Mol. Cell 61(2):222-35
153. Yi H, Riddle NC, Stokes TL, Woo HR, Richards EJ. 2004. Induced and natural epigenetic variation. Cold Spring Harb. Symp. Quant. Biol. 69:155-60
154. Yu A, Lepere G, Jay F, Wang J, Bapaume L, et al. 2013. Dynamics and biological relevance of DNA demethylation in Arabidopsis antibacterial defense. PNAS 110(6):2389-94
155. Zemach A, Kim MY, Hsieh PH, Coleman-Derr D, Eshed-Williams L, et al. 2013. The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell 153(1):193-205
156. Zemach A, McDaniel IE, Silva P, Zilberman D. 2010. Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science 328(5980):916-19
157. Zhai J, Bischof S, Wang H, Feng S, Lee T, et al. 2015. A one precursor one siRNA model for Pol IV-dependent siRNA biogenesis. Cell 163(2):445-55
158. Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan S-L, et al. 2006. Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126(6):1189-201
159. Zhang Y-Y, Fischer M, Colot V, Bossdorf O. 2013. Epigenetic variation creates potential for evolution of plant phenotypic plasticity. New Phytol. 197(1):314-22
160. Zheng B, Wang Z, Li S, Yu B, Liu JY, Chen X. 2009. Intergenic transcription by RNA polymerase II coordinates Pol IV and Pol V in siRNA-directed transcriptional gene silencing in Arabidopsis. Genes Dev. 23(24):2850-60
161. Zhong S, Fei Z, Chen Y, Zheng Y, Huang M, et al. 2013. Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening. Nat. Biotechnol. 31(2):154-59
162. ZilbermanD,Gehring M, Tran RK, Ballinger T,Henikoff S. 2006. Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat. Genet. 39(1):61-69
163. Zhong X, Du J, Hale CJ, Gallego-Bartolome J, Feng S, et al. 2014. Molecular mechanism of action of plant DRM de novo DNA methyltransferases. Cell. 157(5):1050-60