Double-edged sword: The evolutionary consequences of the epigenetic silencing of transposable elements

Autoři: Jae Young Choi aff001;  Yuh Chwen G. Lee aff002
Působiště autorů: Center for Genomics and Systems Biology, Department of Biology, New York University, New York, New York State, United States of America aff001;  Department of Ecology and Evolutionary Biology, University of California, Irvine, California, United States of America aff002
Vyšlo v časopise: Double-edged sword: The evolutionary consequences of the epigenetic silencing of transposable elements. PLoS Genet 16(7): e32767. doi:10.1371/journal.pgen.1008872
Kategorie: Review
doi: 10.1371/journal.pgen.1008872


Transposable elements (TEs) are genomic parasites that selfishly replicate at the expense of host fitness. Fifty years of evolutionary studies of TEs have concentrated on the deleterious genetic effects of TEs, such as their effects on disrupting genes and regulatory sequences. However, a flurry of recent work suggests that there is another important source of TEs’ harmful effects—epigenetic silencing. Host genomes typically silence TEs by the deposition of repressive epigenetic marks. While this silencing reduces the selfish replication of TEs and should benefit hosts, a picture is emerging that the epigenetic silencing of TEs triggers inadvertent spreading of repressive marks to otherwise expressed neighboring genes, ultimately jeopardizing host fitness. In this Review, we provide a long-overdue overview of the recent genome-wide evidence for the presence and prevalence of TEs’ epigenetic effects, highlighting both the similarities and differences across mammals, insects, and plants. We lay out the current understanding of the functional and fitness consequences of TEs’ epigenetic effects, and propose possible influences of such effects on the evolution of both hosts and TEs themselves. These unique evolutionary consequences indicate that TEs’ epigenetic effect is not only a crucial component of TE biology but could also be a significant contributor to genome function and evolution.

Klíčová slova:

Arabidopsis thaliana – DNA methylation – Drosophila melanogaster – Epigenetics – Genome evolution – Heterochromatin – Invertebrate genomics – Small interfering RNAs


1. Elliott TA, Gregory TR. Do larger genomes contain more diverse transposable elements? BMC Evolutionary Biology. 2015;15: 69. doi: 10.1186/s12862-015-0339-8 25896861

2. Finnegan DJ. Transposable elements. Curr Opin Genet Dev. 1992;2: 861–867. doi: 10.1016/s0959-437x(05)80108-x 1335807

3. Maksakova IA, Romanish MT, Gagnier L, Dunn CA, van de Lagemaat LN, Mager DL. Retroviral Elements and Their Hosts: Insertional Mutagenesis in the Mouse Germ Line. PLoS Genet. 2006;2. doi: 10.1371/journal.pgen.0020002 16440055

4. Hancks DC, Kazazian HH. Roles for retrotransposon insertions in human disease. Mobile DNA. 2016;7: 9. doi: 10.1186/s13100-016-0065-9 27158268

5. Chuong EB, Elde NC, Feschotte C. Regulatory activities of transposable elements: from conflicts to benefits. Nature Reviews Genetics. 2017;18: 71–86. doi: 10.1038/nrg.2016.139 27867194

6. Feschotte C. Transposable elements and the evolution of regulatory networks. Nat Rev Genet. 2008;9: 397–405. doi: 10.1038/nrg2337 18368054

7. Langley CH, Montgomery E, Hudson R, Kaplan N, Charlesworth B. On the role of unequal exchange in the containment of transposable element copy number. Genet Res. 1988;52: 223–235. doi: 10.1017/s0016672300027695 2854088

8. Montgomery EA, Huang SM, Langley CH, Judd BH. Chromosome rearrangement by ectopic recombination in Drosophila melanogaster: genome structure and evolution. Genetics. 1991;129: 1085–98. 1783293

9. Hedges DJ, Deininger PL. Inviting instability: Transposable elements, double-strand breaks, and the maintenance of genome integrity. Mutat Res. 2007;616: 46–59. doi: 10.1016/j.mrfmmm.2006.11.021 17157332

10. Deans C, Maggert KA. What Do You Mean, “Epigenetic”? Genetics. 2015;199: 887–896. doi: 10.1534/genetics.114.173492 25855649

11. Berger SL, Kouzarides T, Shiekhattar R, Shilatifard A. An operational definition of epigenetics. Genes Dev. 2009;23: 781–783. doi: 10.1101/gad.1787609 19339683

12. Allis CD, Jenuwein T. The molecular hallmarks of epigenetic control. Nat Rev Genet. 2016;17: 487–500. doi: 10.1038/nrg.2016.59 27346641

13. Elgin SCR, Reuter G. Position-effect variegation, heterochromatin formation, and gene silencing in Drosophila. Cold Spring Harb Perspect Biol. 2013;5: a017780. doi: 10.1101/cshperspect.a017780 23906716

14. Bannister AJ, Kouzarides T. Regulation of chromatin by histone modifications. Cell Research. 2011;21: 381–395. doi: 10.1038/cr.2011.22 21321607

15. Pikaard CS, Mittelsten Scheid O. Epigenetic Regulation in Plants. Cold Spring Harb Perspect Biol. 2014;6. doi: 10.1101/cshperspect.a019315 25452385

16. Garrigues JM, Sidoli S, Garcia BA, Strome S. Defining heterochromatin in C. elegans through genome-wide analysis of the heterochromatin protein 1 homolog HPL-2. Genome Res. 2015;25: 76–88. doi: 10.1101/gr.180489.114 25467431

17. Ahringer J, Gasser SM. Repressive Chromatin in Caenorhabditis elegans: Establishment, Composition, and Function. Genetics. 2018;208: 491–511. doi: 10.1534/genetics.117.300386 29378810

18. Janssen A, Colmenares SU, Karpen GH. Heterochromatin: Guardian of the Genome. Annual Review of Cell and Developmental Biology. 2018;34: 265–288. doi: 10.1146/annurev-cellbio-100617-062653 30044650

19. Riddle NC, Minoda A, Kharchenko PV, Alekseyenko AA, Schwartz YB, Tolstorukov MY, et al. Plasticity in patterns of histone modifications and chromosomal proteins in Drosophila heterochromatin. Genome Res. 2011;21: 147–163. doi: 10.1101/gr.110098.110 21177972

20. Vogel MJ, Guelen L, de Wit E, Hupkes DP, Lodén M, Talhout W, et al. Human heterochromatin proteins form large domains containing KRAB-ZNF genes. Genome Res. 2006;16: 1493–1504. doi: 10.1101/gr.5391806 17038565

21. Wen B, Wu H, Shinkai Y, Irizarry RA, Feinberg AP. Large histone H3 lysine 9 dimethylated chromatin blocks distinguish differentiated from embryonic stem cells. Nat Genet. 2009;41: 246–250. doi: 10.1038/ng.297 19151716

22. West PT, Li Q, Ji L, Eichten SR, Song J, Vaughn MW, et al. Genomic distribution of H3K9me2 and DNA methylation in a maize genome. PLoS ONE. 2014;9: e105267. doi: 10.1371/journal.pone.0105267 25122127

23. Slotkin RK, Martienssen R. Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet. 2007;8: 272–285. doi: 10.1038/nrg2072 17363976

24. Morgan HD, Sutherland HG, Martin DI, Whitelaw E. Epigenetic inheritance at the agouti locus in the mouse. Nat Genet. 1999;23: 314–318. doi: 10.1038/15490 10545949

25. Iida S, Morita Y, Choi J-D, Park K-I, Hoshino A. Genetics and epigenetics in flower pigmentation associated with transposable elements in morning glories. Adv Biophys. 2004;38: 141–159.

26. Saze H, Kakutani T. Heritable epigenetic mutation of a transposon-flanked Arabidopsis gene due to lack of the chromatin-remodeling factor DDM1. EMBO J. 2007;26: 3641–3652. doi: 10.1038/sj.emboj.7601788 17627280

27. Martin A, Troadec C, Boualem A, Rajab M, Fernandez R, Morin H, et al. A transposon-induced epigenetic change leads to sex determination in melon. Nature. 2009;461: 1135–1138. doi: 10.1038/nature08498 19847267

28. Sun F-L, Haynes K, Simpson CL, Lee SD, Collins L, Wuller J, et al. cis-Acting determinants of heterochromatin formation on Drosophila melanogaster chromosome four. Mol Cell Biol. 2004;24: 8210–8220. doi: 10.1128/MCB.24.18.8210-8220.2004 15340080

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

30. Girton JR, Johansen KM. Chromatin structure and the regulation of gene expression: the lessons of PEV in Drosophila. Adv Genet. 2008;61: 1–43. doi: 10.1016/S0065-2660(07)00001-6 18282501

31. Talbert PB, Henikoff S. Spreading of silent chromatin: inaction at a distance. Nat Rev Genet. 2006;7: 793–803. doi: 10.1038/nrg1920 16983375

32. Shpiz S, Ryazansky S, Olovnikov I, Abramov Y, Kalmykova A. Euchromatic Transposon Insertions Trigger Production of Novel Pi- and Endo-siRNAs at the Target Sites in the Drosophila Germline. PLoS Genet. 2014;10: e1004138. doi: 10.1371/journal.pgen.1004138 24516406

33. Vaistij FE, Jones L, Baulcombe DC. Spreading of RNA targeting and DNA methylation in RNA silencing requires transcription of the target gene and a putative RNA-dependent RNA polymerase. Plant Cell. 2002;14: 857–867. doi: 10.1105/tpc.010480 11971140

34. Van Houdt H, Bleys A, Depicker A. RNA Target Sequences Promote Spreading of RNA Silencing. Plant Physiol. 2003;131: 245–253. doi: 10.1104/pp.009407 12529532

35. Ahmed I, Sarazin A, Bowler C, Colot V, Quesneville H. Genome-wide evidence for local DNA methylation spreading from small RNA-targeted sequences in Arabidopsis. Nucleic acids research. 2011;39: 6919–31. doi: 10.1093/nar/gkr324 21586580

36. Rebollo R, Karimi MM, Bilenky M, Gagnier L, Miceli-Royer K, Zhang Y, et al. Retrotransposon-Induced Heterochromatin Spreading in the Mouse Revealed by Insertional Polymorphisms. PLoS Genet. 2011;7: e1002301. doi: 10.1371/journal.pgen.1002301 21980304

37. Quadrana L, Silveira AB, Mayhew GF, LeBlanc C, Martienssen RA, Jeddeloh JA, et al. The Arabidopsis thaliana mobilome and its impact at the species level. eLife. 2016;5: e15716. doi: 10.7554/eLife.15716 27258693

38. Stuart T, Eichten SR, Cahn J, Karpievitch YV, Borevitz JO, Lister R. Population scale mapping of transposable element diversity reveals links to gene regulation and epigenomic variation. eLife. 2016;5: e20777. doi: 10.7554/eLife.20777 27911260

39. Choi JY, Purugganan MD. Evolutionary Epigenomics of Retrotransposon-Mediated Methylation Spreading in Rice. Mol Biol Evol. 2018;35: 365–382. doi: 10.1093/molbev/msx284 29126199

40. Eichten SR, Ellis NA, Makarevitch I, Yeh C-T, Gent JI, Guo L, et al. Spreading of Heterochromatin Is Limited to Specific Families of Maize Retrotransposons. PLOS Genet. 2012;8: e1003127. doi: 10.1371/journal.pgen.1003127 23271981

41. Eichten SR, Briskine R, Song J, Li Q, Swanson-Wagner R, Hermanson PJ, et al. Epigenetic and Genetic Influences on DNA Methylation Variation in Maize Populations. The Plant Cell. 2013;25: 2783–2797. doi: 10.1105/tpc.113.114793 23922207

42. Gent JI, Ellis NA, Guo L, Harkess AE, Yao Y, Zhang X, et al. CHH islands: de novo DNA methylation in near-gene chromatin regulation in maize. Genome Res. 2013;23: 628–637. doi: 10.1101/gr.146985.112 23269663

43. Noshay JM, Anderson SN, Zhou P, Ji L, Ricci W, Lu Z, et al. Monitoring the interplay between transposable element families and DNA methylation in maize. PLOS Genetics. 2019;15: e1008291. doi: 10.1371/journal.pgen.1008291 31498837

44. Sienski G, Dönertas D, Brennecke J. Transcriptional silencing of transposons by Piwi and maelstrom and its impact on chromatin state and gene expression. Cell. 2012;151: 964–980. doi: 10.1016/j.cell.2012.10.040 23159368

45. Lee YCG. The Role of piRNA-Mediated Epigenetic Silencing in the Population Dynamics of Transposable Elements in Drosophila melanogaster. PLoS Genet. 2015;11: e1005269. doi: 10.1371/journal.pgen.1005269 26042931

46. Lee YCG, Karpen GH. Pervasive epigenetic effects of Drosophila euchromatic transposable elements impact their evolution. eLife. 2017;6. doi: 10.7554/eLife.25762 28695823

47. Ahmed I, Sarazin A, Bowler C, Colot V, Quesneville H. Genome-wide evidence for local DNA methylation spreading from small RNA-targeted sequences in Arabidopsis. Nucleic Acids Res. 2011;39: 6919–6931. doi: 10.1093/nar/gkr324 21586580

48. Schmitz RJ, He Y, Valdés-López O, Khan SM, Joshi T, Urich MA, et al. Epigenome-wide inheritance of cytosine methylation variants in a recombinant inbred population. Genome Res. 2013;23: 1663–1674. doi: 10.1101/gr.152538.112 23739894

49. Dubin MJ, Zhang P, Meng D, Remigereau M-S, Osborne EJ, Casale FP, et al. DNA methylation in Arabidopsis has a genetic basis and shows evidence of local adaptation. eLife. 2015;4: e05255. doi: 10.7554/eLife.05255 25939354

50. Kawakatsu T, Huang SC, Jupe F, Sasaki E, Schmitz RJ, Urich MA, et al. Epigenomic Diversity in a Global Collection of Arabidopsis thaliana Accessions. Cell. 2016;166: 492–505. doi: 10.1016/j.cell.2016.06.044 27419873

51. Hollister JD, Gaut BS. Epigenetic silencing of transposable elements: A trade-off between reduced transposition and deleterious effects on neighboring gene expression. Genome Research. 2009;19: 1419–1428. doi: 10.1101/gr.091678.109 19478138

52. Vonholdt BM, Takuno S, Gaut BS. Recent retrotransposon insertions are methylated and phylogenetically clustered in japonica rice (Oryza sativa spp. japonica). Mol Biol Evol. 2012;29: 3193–3203. doi: 10.1093/molbev/mss129 22593226

53. Charlesworth B, Langley CH. The Population Genetics of Drosophila Transposable Elements. Annual Review of Genetics. 1989;23: 251–287. doi: 10.1146/ 2559652

54. Lee YCG, Langley CH. Transposable elements in natural populations of Drosophila melanogaster. Philosophical Transactions of the Royal Society of London B: Biological Sciences. 2010;365. Available:

55. Barrón MG, Fiston-Lavier A-S, Petrov DA, González J. Population Genomics of Transposable Elements in Drosophila. Annual Review of Genetics. 2014;48: 561–581. doi: 10.1146/annurev-genet-120213-092359 25292358

56. Ninova M, Godneeva B, Chen Y-CA, Luo Y, Prakash SJ, Jankovics F, et al. The SUMO Ligase Su(var)2-10 Controls Hetero- and Euchromatic Gene Expression via Establishing H3K9 Trimethylation and Negative Feedback Regulation. Molecular Cell. 2020;77: 571–585.e4. doi: 10.1016/j.molcel.2019.09.033 31901448

57. Hollister JD, Smith LM, Guo Y-L, Ott F, Weigel D, Gaut BS. Transposable elements and small RNAs contribute to gene expression divergence between Arabidopsis thaliana and Arabidopsis lyrata. PNAS. 2011;108: 2322–2327. doi: 10.1073/pnas.1018222108 21252301

58. Meng D, Dubin M, Zhang P, Osborne EJ, Stegle O, Clark RM, et al. Limited Contribution of DNA Methylation Variation to Expression Regulation in Arabidopsis thaliana. PLoS Genet. 2016;12: e1006141. doi: 10.1371/journal.pgen.1006141 27398721

59. Vogel MJ, Pagie L, Talhout W, Nieuwland M, Kerkhoven RM, Steensel B van. High-resolution mapping of heterochromatin redistribution in a Drosophila position-effect variegation model. Epigenetics & Chromatin. 2009;2: 1. doi: 10.1186/1756-8935-2-1 19178722

60. Wakimoto BT, Hearn MG. The effects of chromosome rearrangements on the expression of heterochromatic genes in chromosome 2L of Drosophila melanogaster. Genetics. 1990;125: 141–154. 2111264

61. Yasuhara JC, Wakimoto BT. Molecular landscape of modified histones in Drosophila heterochromatic genes and euchromatin-heterochromatin transition zones. PLoS Genet. 2008;4: e16. doi: 10.1371/journal.pgen.0040016 18208336

62. Hearn MG, Hedrick A, Grigliatti TA, Wakimoto BT. The Effect of Modifiers of Position-Effect Variegation on the Variegation of Heterochromatic Genes of Drosophila Melanogaster. Genetics. 1991;128: 785–797. 1916244

63. Caizzi R, Moschetti R, Piacentini L, Fanti L, Marsano RM, Dimitri P. Comparative Genomic Analyses Provide New Insights into the Evolutionary Dynamics of Heterochromatin in Drosophila. PLoS Genet. 2016;12: e1006212. doi: 10.1371/journal.pgen.1006212 27513559

64. de Wit E, Greil F, van Steensel B. High-resolution mapping reveals links of HP1 with active and inactive chromatin components. PLoS Genet. 2007;3: e38. doi: 10.1371/journal.pgen.0030038 17335352

65. Bellen HJ, Levis RW, He Y, Carlson JW, Evans-Holm M, Bae E, et al. The Drosophila Gene Disruption Project: Progress Using Transposons With Distinctive Site Specificities. Genetics. 2011;188: 731–743. doi: 10.1534/genetics.111.126995 21515576

66. Bellen HJ, Levis RW, Liao G, He Y, Carlson JW, Tsang G, et al. The BDGP Gene Disruption Project: Single Transposon Insertions Associated With 40% of Drosophila Genes. Genetics. 2004;167: 761–781. doi: 10.1534/genetics.104.026427 15238527

67. Brennecke J, Malone CD, Aravin AA, Sachidanandam R, Stark A, Hannon GJ. An epigenetic role for maternally inherited piRNAs in transposon silencing. Science. 2008;322: 1387–1392. doi: 10.1126/science.1165171 19039138

68. Lee YCG, Ogiyama Y, Martins NMC, Beliveau BJ, Acevedo D, Wu C -ting, et al. Pericentromeric heterochromatin is hierarchically organized and spatially contacts H3K9me2 islands in euchromatin. PLoS Genetics. 2020;16: e1008673. doi: 10.1371/journal.pgen.1008673 32203508

69. Charlesworth B, Charlesworth D. The Population Dynamics of Transposable Elements. Genetics Research. 1983;42: 1–27. doi: 10.1017/S0016672300021455

70. Langley CH, Brookfield JF, Kaplan N. Transposable elements in mendelian populations. I. A theory. Genetics. 1983;104: 457–471. 17246142

71. Mukai T. The Genetic Structure of Natural Populations of DROSOPHILA MELANOGASTER. VII Synergistic Interaction of Spontaneous Mutant Polygenes Controlling Viability. Genetics. 1969;61: 749–761. 17248439

72. Halligan DL, Keightley PD. Spontaneous Mutation Accumulation Studies in Evolutionary Genetics. Annual Review of Ecology, Evolution, and Systematics. 2009;40: 151–172. doi: 10.1146/annurev.ecolsys.39.110707.173437

73. Sohail M, Vakhrusheva OA, Sul JH, Pulit SL, Francioli LC, Consortium G of the N, et al. Negative selection in humans and fruit flies involves synergistic epistasis. Science. 2017;356: 539–542. doi: 10.1126/science.aah5238 28473589

74. Petrov DA, Aminetzach YT, Davis JC, Bensasson D, Hirsh AE. Size Matters: Non-LTR Retrotransposable Elements and Ectopic Recombination in Drosophila. Mol Biol Evol. 2003;20: 880–892. doi: 10.1093/molbev/msg102 12716993

75. Clark AG, Eisen MB, Smith DR, Bergman CM, Oliver B, Markow TA, et al. Evolution of genes and genomes on the Drosophila phylogeny. Nature. 2007;450: 203–218. doi: 10.1038/nature06341 17994087

76. Kofler R, Nolte V, Schlötterer C. Tempo and Mode of Transposable Element Activity in Drosophila. PLoS Genet. 2015;11: e1005406. doi: 10.1371/journal.pgen.1005406 26186437

77. Hu TT, Pattyn P, Bakker EG, Cao J, Cheng J-F, Clark RM, et al. The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nature Genetics. 2011;43: 476–481. doi: 10.1038/ng.807 21478890

78. Baulcombe DC, Dean C. Epigenetic Regulation in Plant Responses to the Environment. Cold Spring Harb Perspect Biol. 2014;6: a019471. doi: 10.1101/cshperspect.a019471 25183832

79. Feil R, Fraga MF. Epigenetics and the environment: emerging patterns and implications. Nat Rev Genet. 2012;13: 97–109. doi: 10.1038/nrg3142 22215131

80. Cvijović I, Good BH, Jerison ER, Desai MM. Fate of a mutation in a fluctuating environment. PNAS. 2015;112: E5021–E5028. doi: 10.1073/pnas.1505406112 26305937

81. Kent TV, Uzunović J, Wright SI. Coevolution between transposable elements and recombination. Philos Trans R Soc Lond, B, Biol Sci. 2017;372. doi: 10.1098/rstb.2016.0458 29109221

82. Talbert PB, Henikoff S. Centromeres Convert but Don’t Cross. PLoS Biol. 2010;8: e1000326. doi: 10.1371/journal.pbio.1000326 20231873

83. Lazzerini-Denchi E, Sfeir A. Stop pulling my strings—what telomeres taught us about the DNA damage response. Nat Rev Mol Cell Biol. 2016;17: 364–378. doi: 10.1038/nrm.2016.43 27165790

84. Giraut L, Falque M, Drouaud J, Pereira L, Martin OC, Mézard C. Genome-Wide Crossover Distribution in Arabidopsis thaliana Meiosis Reveals Sex-Specific Patterns along Chromosomes. PLoS Genet. 2011;7. doi: 10.1371/journal.pgen.1002354 22072983

85. Szostak JW, Orr-Weaver TL, Rothstein RJ, Stahl FW. The double-strand-break repair model for recombination. Cell. 1983;33: 25–35. doi: 10.1016/0092-8674(83)90331-8 6380756

86. Keeney S, Giroux CN, Kleckner N. Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell. 1997;88: 375–384. doi: 10.1016/s0092-8674(00)81876-0 9039264

87. Berchowitz LE, Hanlon SE, Lieb JD, Copenhaver GP. A positive but complex association between meiotic double-strand break hotspots and open chromatin in Saccharomyces cerevisiae. Genome Res. 2009;19: 2245–2257. doi: 10.1101/gr.096297.109 19801530

88. Singhal S, Leffler EM, Sannareddy K, Turner I, Venn O, Hooper DM, et al. Stable recombination hotspots in birds. Science. 2015;350: 928–932. doi: 10.1126/science.aad0843 26586757

89. Auton A, Rui Li Y, Kidd J, Oliveira K, Nadel J, Holloway JK, et al. Genetic recombination is targeted towards gene promoter regions in dogs. PLoS Genet. 2013;9: e1003984. doi: 10.1371/journal.pgen.1003984 24348265

90. Choi K, Zhao X, Kelly KA, Venn O, Higgins JD, Yelina NE, et al. Arabidopsis meiotic crossover hotspots overlap with H2A.Z nucleosomes at gene promoters. Nat Genet. 2013;45. doi: 10.1038/ng.2766 24056716

91. Rodgers-Melnick E, Bradbury PJ, Elshire RJ, Glaubitz JC, Acharya CB, Mitchell SE, et al. Recombination in diverse maize is stable, predictable, and associated with genetic load. PNAS. 2015;112: 3823–3828. doi: 10.1073/pnas.1413864112 25775595

92. Choi K, Zhao X, Tock AJ, Lambing C, Underwood CJ, Hardcastle TJ, et al. Nucleosomes and DNA methylation shape meiotic DSB frequency in Arabidopsis thaliana transposons and gene regulatory regions. Genome Res. 2018;28: 532–546. doi: 10.1101/gr.225599.117 29530928

93. Underwood CJ, Choi K, Lambing C, Zhao X, Serra H, Borges F, et al. Epigenetic activation of meiotic recombination near Arabidopsis thaliana centromeres via loss of H3K9me2 and non-CG DNA methylation. Genome Res. 2018;28: 519–531. doi: 10.1101/gr.227116.117 29530927

94. Melamed-Bessudo C, Levy AA. Deficiency in DNA methylation increases meiotic crossover rates in euchromatic but not in heterochromatic regions in Arabidopsis. Proc Natl Acad Sci USA. 2012;109: E981–988. doi: 10.1073/pnas.1120742109 22460791

95. Peng JC, Karpen GH. Heterochromatic genome stability requires regulators of histone H3 K9 methylation. PLoS Genet. 2009;5: e1000435. doi: 10.1371/journal.pgen.1000435 19325889

96. Ellermeier C, Higuchi EC, Phadnis N, Holm L, Geelhood JL, Thon G, et al. RNAi and heterochromatin repress centromeric meiotic recombination. PNAS. 2010;107: 8701–8705. doi: 10.1073/pnas.0914160107 20421495

97. Janssen A, Colmenares SU, Lee T, Karpen GH. Timely double-strand break repair and pathway choice in pericentromeric heterochromatin depend on the histone demethylase dKDM4A. Genes Dev. 2019;33: 103–115. doi: 10.1101/gad.317537.118 30578303

98. Baldeyron C, Soria G, Roche D, Cook AJL, Almouzni G. HP1alpha recruitment to DNA damage by p150CAF-1 promotes homologous recombination repair. J Cell Biol. 2011;193: 81–95. doi: 10.1083/jcb.201101030 21464229

99. Maloisel L, Rossignol J-L. Suppression of crossing-over by DNA methylation in Ascobolus. Genes Dev. 1998;12: 1381–1389. doi: 10.1101/gad.12.9.1381 9573054

100. Engler P, Weng A, Storb U. Influence of CpG methylation and target spacing on V(D)J recombination in a transgenic substrate. Mol Cell Biol. 1993;13: 571–577. doi: 10.1128/mcb.13.1.571 8417353

101. Dooner HK. Genetic Fine Structure of the BRONZE Locus in Maize. Genetics. 1986;113: 1021–1036. 17246338

102. Xu X, Hsia AP, Zhang L, Nikolau BJ, Schnable PS. Meiotic recombination break points resolve at high rates at the 5’ end of a maize coding sequence. The Plant Cell. 1995;7: 2151–2161. doi: 10.1105/tpc.7.12.2151 8718625

103. Zamudio N, Barau J, Teissandier A, Walter M, Borsos M, Servant N, et al. DNA methylation restrains transposons from adopting a chromatin signature permissive for meiotic recombination. Genes Dev. 2015;29: 1256–1270. doi: 10.1101/gad.257840.114 26109049

104. Cutter AD, Payseur BA. Genomic signatures of selection at linked sites: unifying the disparity among species. Nature Reviews Genetics. 2013;14: 262–274. doi: 10.1038/nrg3425 23478346

105. McMullen MD, Kresovich S, Villeda HS, Bradbury P, Li H, Sun Q, et al. Genetic properties of the maize nested association mapping population. Science. 2009;325: 737–740. doi: 10.1126/science.1174320 19661427

106. Singer T, Fan Y, Chang H-S, Zhu T, Hazen SP, Briggs SP. A High-Resolution Map of Arabidopsis Recombinant Inbred Lines by Whole-Genome Exon Array Hybridization. PLoS Genet. 2006;2. doi: 10.1371/journal.pgen.0020144 17044735

107. Comeron JM, Ratnappan R, Bailin S. The Many Landscapes of Recombination in Drosophila melanogaster. PLoS Genet. 2012;8: e1002905. doi: 10.1371/journal.pgen.1002905 23071443

108. Paigen K, Szatkiewicz JP, Sawyer K, Leahy N, Parvanov ED, Ng SHS, et al. The Recombinational Anatomy of a Mouse Chromosome. PLoS Genet. 2008;4. doi: 10.1371/journal.pgen.1000119 18617997

109. Cridland JM, Macdonald SJ, Long AD, Thornton KR. Abundance and distribution of transposable elements in two Drosophila QTL mapping resources. Molecular biology and evolution. 2013;30: 2311–27. doi: 10.1093/molbev/mst129 23883524

110. Laricchia KM, Zdraljevic S, Cook DE, Andersen EC. Natural Variation in the Distribution and Abundance of Transposable Elements Across the Caenorhabditis elegans Species. Mol Biol Evol. 2017;34: 2187–2202. doi: 10.1093/molbev/msx155 28486636

111. Rahman R, Chirn G, Kanodia A, Sytnikova YA, Brembs B, Bergman CM, et al. Unique transposon landscapes are pervasive across Drosophila melanogaster genomes. Nucl Acids Res. 2015;43: 10655–10672. doi: 10.1093/nar/gkv1193 26578579

112. Nellåker C, Keane TM, Yalcin B, Wong K, Agam A, Belgard TG, et al. The genomic landscape shaped by selection on transposable elements across 18 mouse strains. Genome Biology. 2012;13: R45. doi: 10.1186/gb-2012-13-6-r45 22703977

113. Anderson SN, Stitzer MC, Brohammer AB, Zhou P, Noshay JM, O’Connor CH, et al. Transposable elements contribute to dynamic genome content in maize. Plant J. 2019. doi: 10.1111/tpj.14489 31381222

114. Carpentier M-C, Manfroi E, Wei F-J, Wu H-P, Lasserre E, Llauro C, et al. Retrotranspositional landscape of Asian rice revealed by 3000 genomes. Nat Commun. 2019;10. doi: 10.1038/s41467-018-07974-5 30604755

115. Wicker T, Keller B. Genome-wide comparative analysis of copia retrotransposons in Triticeae, rice, and Arabidopsis reveals conserved ancient evolutionary lineages and distinct dynamics of individual copia families. Genome Res. 2007;17: 1072–1081. doi: 10.1101/gr.6214107 17556529

116. Bergman CM, Bensasson D. Recent LTR Retrotransposon Insertion Contrasts with Waves of Non-LTR Insertion Since Speciation in Drosophila Melanogaster. PNAS. 2007;104: 11340–11345. doi: 10.1073/pnas.0702552104 17592135

117. Penterman J, Zilberman D, Huh JH, Ballinger T, Henikoff S, Fischer RL. DNA demethylation in the Arabidopsis genome. PNAS. 2007;104: 6752–6757. doi: 10.1073/pnas.0701861104 17409185

118. Penterman J, Uzawa R, Fischer RL. Genetic Interactions between DNA Demethylation and Methylation in Arabidopsis. Plant Physiol. 2007;145: 1549–1557. doi: 10.1104/pp.107.107730 17951456

119. Tang K, Lang Z, Zhang H, Zhu J-K. The DNA demethylase ROS1 targets genomic regions with distinct chromatin modifications. Nature Plants. 2016;2: 1–10. doi: 10.1038/nplants.2016.169 27797352

120. Ahmad K, Henikoff S. Modulation of a Transcription Factor Counteracts Heterochromatic Gene Silencing in Drosophila. Cell. 2001;104: 839–847. doi: 10.1016/s0092-8674(01)00281-1 11290322

121. Sentmanat MF, Elgin SCR. Ectopic assembly of heterochromatin in Drosophila melanogaster triggered by transposable elements. Proc Natl Acad Sci USA. 2012;109: 14104–14109. doi: 10.1073/pnas.1207036109 22891327

122. Fodor BD, Shukeir N, Reuter G, Jenuwein T. Mammalian Su(var) genes in chromatin control. Annu Rev Cell Dev Biol. 2010;26: 471–501. doi: 10.1146/annurev.cellbio.042308.113225 19575672

123. Grewal SIS, Elgin SCR. Transcription and RNA interference in the formation of heterochromatin. Nature. 2007;447: 399–406. doi: 10.1038/nature05914 17522672

124. Eissenberg JC, Elgin SCR. HP1a: a structural chromosomal protein regulating transcription. Trends in Genetics. 2014;30: 103–110. doi: 10.1016/j.tig.2014.01.002 24555990

125. Lynch M, Conery JS. The Origins of Genome Complexity. Science. 2003;302: 1401–1404. doi: 10.1126/science.1089370 14631042

126. Wright SI, Schoen DJ. Transposon dynamics and the breeding system. Genetica. 1999;107: 139–148. 10952207

127. Charlesworth D, Charlesworth B. Transposable elements in inbreeding and outbreeding populations. Genetics. 1995;140: 415–417. 7635305

128. Schaack S, Gilbert C, Feschotte C. Promiscuous DNA: horizontal transfer of transposable elements and why it matters for eukaryotic evolution. Trends Ecol Evol (Amst). 2010;25: 537–546. doi: 10.1016/j.tree.2010.06.001 20591532

129. Charlesworth B, Langley CH. The evolution of self-regulated transposition of transposable elements. Genetics. 1986;112: 359–383. 3000868

130. Blumenstiel JP, Erwin AA, Hemmer LW. What Drives Positive Selection in the Drosophila piRNA Machinery? The Genomic Autoimmunity Hypothesis. Yale J Biol Med. 2016;89: 499–512. 28018141

131. Wendel JF, Lisch D, Hu G, Mason AS. The long and short of doubling down: polyploidy, epigenetics, and the temporal dynamics of genome fractionation. Current Opinion in Genetics & Development. 2018;49: 1–7. doi: 10.1016/j.gde.2018.01.004 29438956

132. Bird KA, VanBuren R, Puzey JR, Edger PP. The causes and consequences of subgenome dominance in hybrids and recent polyploids. New Phytologist. 2018;220: 87–93. doi: 10.1111/nph.15256 29882360

133. Roessler K, Bousios A, Meca E, Gaut BS. Modeling Interactions between Transposable Elements and the Plant Epigenetic Response: A Surprising Reliance on Element Retention. Genome Biol Evol. 2018;10: 803–815. doi: 10.1093/gbe/evy043 29608716

134. Deniz Ö, Frost JM, Branco MR. Regulation of transposable elements by DNA modifications. Nature Reviews Genetics. 2019;20: 417–431. doi: 10.1038/s41576-019-0106-6 30867571

135. Du J, Leung A, Trac C, Lee M, Parks BW, Lusis AJ, et al. Chromatin variation associated with liver metabolism is mediated by transposable elements. Epigenetics & Chromatin. 2016;9: 28. doi: 10.1186/s13072-016-0078-0 27398095

136. Czech B, Munafò M, Ciabrelli F, Eastwood EL, Fabry MH, Kneuss E, et al. piRNA-Guided Genome Defense: From Biogenesis to Silencing. Annual Review of Genetics. 2018;52: 131–157. doi: 10.1146/annurev-genet-120417-031441 30476449

137. Aravin AA, Sachidanandam R, Bourc’his D, Schaefer C, Pezic D, Toth KF, et al. A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol Cell. 2008;31: 785–799. doi: 10.1016/j.molcel.2008.09.003 18922463

138. Kuramochi-Miyagawa S, Watanabe T, Gotoh K, Totoki Y, Toyoda A, Ikawa M, et al. DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes. Genes Dev. 2008;22: 908–917. doi: 10.1101/gad.1640708 18381894

139. Wolf D, Goff SP. TRIM28 mediates primer binding site-targeted silencing of murine leukemia virus in embryonic cells. Cell. 2007;131: 46–57. doi: 10.1016/j.cell.2007.07.026 17923087

140. Matsui T, Leung D, Miyashita H, Maksakova IA, Miyachi H, Kimura H, et al. Proviral silencing in embryonic stem cells requires the histone methyltransferase ESET. Nature. 2010;464: 927–931. doi: 10.1038/nature08858 20164836

141. Rowe HM, Jakobsson J, Mesnard D, Rougemont J, Reynard S, Aktas T, et al. KAP1 controls endogenous retroviruses in embryonic stem cells. Nature. 2010;463: 237–240. doi: 10.1038/nature08674 20075919

142. Schultz DC, Ayyanathan K, Negorev D, Maul GG, Rauscher FJ. SETDB1: a novel KAP-1-associated histone H3, lysine 9-specific methyltransferase that contributes to HP1-mediated silencing of euchromatic genes by KRAB zinc-finger proteins. Genes Dev. 2002;16: 919–932. doi: 10.1101/gad.973302 11959841

143. Dönertas D, Sienski G, Brennecke J. Drosophila Gtsf1 is an essential component of the Piwi-mediated transcriptional silencing complex. Genes Dev. 2013;27: 1693–1705. doi: 10.1101/gad.221150.113 23913922

144. Ohtani H, Iwasaki YW, Shibuya A, Siomi H, Siomi MC, Saito K. DmGTSF1 is necessary for Piwi–piRISC-mediated transcriptional transposon silencing in the Drosophila ovary. Genes Dev. 2013;27: 1656–1661. doi: 10.1101/gad.221515.113 23913921

145. Yu Y, Gu J, Jin Y, Luo Y, Preall JB, Ma J, et al. Panoramix enforces piRNA-dependent cotranscriptional silencing. Science. 2015;350: 339–342. doi: 10.1126/science.aab0700 26472911

146. Sienski G, Batki J, Senti K-A, Dönertas D, Tirian L, Meixner K, et al. Silencio/CG9754 connects the Piwi-piRNA complex to the cellular heterochromatin machinery. Genes Dev. 2015;29: 2258–2271. doi: 10.1101/gad.271908.115 26494711

147. Le Thomas A, Rogers AK, Webster A, Marinov GK, Liao SE, Perkins EM, et al. Piwi induces piRNA-guided transcriptional silencing and establishment of a repressive chromatin state. Genes Dev. 2013;27: 390–399. doi: 10.1101/gad.209841.112 23392610

148. Grewal SIS. RNAi-dependent formation of heterochromatin and its diverse functions. Curr Opin Genet Dev. 2010;20: 134–141. doi: 10.1016/j.gde.2010.02.003 20207534

149. McCue AD, Panda K, Nuthikattu S, Choudury SG, Thomas EN, Slotkin RK. ARGONAUTE 6 bridges transposable element mRNA-derived siRNAs to the establishment of DNA methylation. The EMBO Journal. 2015;34: 20–35. doi: 10.15252/embj.201489499 25388951

150. Zilberman D, Cao X, Jacobsen SE. ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science. 2003;299: 716–719. doi: 10.1126/science.1079695 12522258

151. Law JA, Ausin I, Johnson LM, Vashisht AA, Zhu J-K, Wohlschlegel JA, et al. A protein complex required for polymerase V transcripts and RNA- directed DNA methylation in Arabidopsis. Curr Biol. 2010;20: 951–956. doi: 10.1016/j.cub.2010.03.062 20409711

152. Wierzbicki AT, Ream TS, Haag JR, Pikaard CS. RNA polymerase V transcription guides ARGONAUTE4 to chromatin. Nat Genet. 2009;41: 630–634. doi: 10.1038/ng.365 19377477

153. El-Shami M, Pontier D, Lahmy S, Braun L, Picart C, Vega D, et al. Reiterated WG/GW motifs form functionally and evolutionarily conserved ARGONAUTE-binding platforms in RNAi-related components. Genes Dev. 2007;21: 2539–2544. doi: 10.1101/gad.451207 17938239

154. Goll MG, Bestor TH. Eukaryotic cytosine methyltransferases. Annu Rev Biochem. 2005;74: 481–514. doi: 10.1146/annurev.biochem.74.010904.153721 15952895

155. Zhong X, Du J, Hale CJ, Gallego-Bartolome J, Feng S, Vashisht AA, et al. Molecular mechanism of action of plant DRM de novo DNA methyltransferases. Cell. 2014;157: 1050–1060. doi: 10.1016/j.cell.2014.03.056 24855943

156. Cao X, Jacobsen SE. Role of the arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr Biol. 2002;12: 1138–1144. doi: 10.1016/s0960-9822(02)00925-9 12121623

157. Duhl DM, Vrieling H, Miller KA, Wolff GL, Barsh GS. Neomorphic agouti mutations in obese yellow mice. Nat Genet. 1994;8: 59–65. doi: 10.1038/ng0994-59 7987393

158. Xie Z, Johansen LK, Gustafson AM, Kasschau KD, Lellis AD, Zilberman D, et al. Genetic and Functional Diversification of Small RNA Pathways in Plants. PLoS Biol. 2004;2: e104. doi: 10.1371/journal.pbio.0020104 15024409

159. Kasschau KD, Fahlgren N, Chapman EJ, Sullivan CM, Cumbie JS, Givan SA, et al. Genome-Wide Profiling and Analysis of Arabidopsis siRNAs. PLoS Biol. 2007;5: e57. doi: 10.1371/journal.pbio.0050057 17298187

160. Gunawardane LS, Saito K, Nishida KM, Miyoshi K, Kawamura Y, Nagami T, et al. A slicer-mediated mechanism for repeat-associated siRNA 5’ end formation in Drosophila. Science. 2007;315: 1587–1590. doi: 10.1126/science.1140494 17322028

161. Brennecke J, Aravin AA, Stark A, Dus M, Kellis M, Sachidanandam R, et al. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell. 2007;128: 1089–1103. doi: 10.1016/j.cell.2007.01.043 17346786

162. Aravin AA, Sachidanandam R, Girard A, Fejes-Toth K, Hannon GJ. Developmentally regulated piRNA clusters implicate MILI in transposon control. Science. 2007;316: 744–747. doi: 10.1126/science.1142612 17446352

163. Kelleher ES, Barbash DA. Analysis of piRNA-Mediated Silencing of Active TEs in Drosophila melanogaster Suggests Limits on the Evolution of Host Genome Defense. Mol Biol Evol. 2013;30: 1816–1829. doi: 10.1093/molbev/mst081 23625890

164. Hirochika H, Okamoto H, Kakutani T. Silencing of Retrotransposons in Arabidopsis and Reactivation by the ddm1 Mutation. Plant Cell. 2000;12: 357–369. doi: 10.1105/tpc.12.3.357 10715322

165. Cheng C, Daigen M, Hirochika H. Epigenetic regulation of the rice retrotransposon Tos17. Mol Genet Genomics. 2006;276: 378–390. doi: 10.1007/s00438-006-0141-9 16821043

166. Noreen F, Akbergenov R, Hohn T, Richert-Pöggeler KR. Distinct expression of endogenous Petunia vein clearing virus and the DNA transposon dTph1 in two Petunia hybrida lines is correlated with differences in histone modification and siRNA production. Plant J. 2007;50: 219–229. doi: 10.1111/j.1365-313X.2007.03040.x 17444906

167. Czech B, Hannon GJ. One Loop to Rule Them All: The Ping-Pong Cycle and piRNA-Guided Silencing. Trends in Biochemical Sciences. 2016;41: 324–337. doi: 10.1016/j.tibs.2015.12.008 26810602

168. Matzke MA, Mosher RA. RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nature Reviews Genetics. 2014;15: 394–408. doi: 10.1038/nrg3683 24805120

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