1932

Abstract

Within the life cycle of a living organism, another life cycle exists for the selfish genome inhabitants, which are called transposable elements (TEs). These mobile sequences invade, duplicate, amplify, and diversify within a genome, increasing the genome's size and generating new mutations. Cells act to defend their genome, but rather than permanently destroying TEs, they use chromatin-level repression and epigenetic inheritance to silence TE activity. This level of silencing is ephemeral and reversible, leading to a dynamic equilibrium between TE suppression and reactivation within a host genome. The coexistence of the TE and host genome can also lead to the domestication of the TE to serve in host genome evolution and function. In this review, we describe the life cycle of a TE, with emphasis on how epigenetic regulation is harnessed to control TEs for host genome stability and innovation.

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2022-11-30
2024-06-15
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Literature Cited

  1. 1.
    Adey A, Morrison HG, Asan, Xun X, Kitzman JO et al. 2010. Rapid, low-input, low-bias construction of shotgun fragment libraries by high-density in vitro transposition. Genome Biol 11:12R119
    [Google Scholar]
  2. 2.
    Agol VI, Gmyl AP. 2010. Viral security proteins: counteracting host defences. Nat. Rev. Microbiol. 8:12867–78
    [Google Scholar]
  3. 3.
    Amberger M, Ivics Z. 2020. Latest advances for the Sleeping Beauty transposon system: 23 years of insomnia but prettier than ever: refinement and recent innovations of the Sleeping Beauty transposon system enabling novel, nonviral genetic engineering applications. BioEssays 42:11e2000136
    [Google Scholar]
  4. 4.
    Aubin E, Llauro C, Garrigue J, Mirouze M, Panaud O, El Baidouri M. 2021. Characterization of interspecific gene flows at the genome-wide level in a natural ecosystem the Massane forest reveals new insights into horizontal transfer in plants. bioRxiv 2021.12.19.471934. https://doi.org/10.1101/2021.12.19.471934
    [Crossref]
  5. 5.
    Baduel P, Leduque B, Ignace A, Gy I, Gil J Jr. et al. 2021. Genetic and environmental modulation of transposition shapes the evolutionary potential of Arabidopsis thaliana. Genome Biol 22:1138
    [Google Scholar]
  6. 6.
    Batista RA, Moreno-Romero J, Qiu Y, van Boven J, Santos-González J et al. 2019. The MADS-box transcription factor PHERES1 controls imprinting in the endosperm by binding to domesticated transposons. eLife 8:e50541
    [Google Scholar]
  7. 7.
    Becker C, Hagmann J, Müller J, Koenig D, Stegle O et al. 2011. Spontaneous epigenetic variation in the Arabidopsis thaliana methylome. Nature 480:7376245–49
    [Google Scholar]
  8. 8.
    Bennetzen JL, SanMiguel P, Chen M, Tikhonov A, Francki M, Avramova Z. 1998. Grass genomes. PNAS 95:51975–78
    [Google Scholar]
  9. 9.
    Bhattacharyya MK, Smith AM, Ellis TH, Hedley C, Martin C. 1990. The wrinkled-seed character of pea described by Mendel is caused by a transposon-like insertion in a gene encoding starch-branching enzyme. Cell 60:1115–22
    [Google Scholar]
  10. 10.
    Boulard M, Rucli S, Edwards JR, Bestor TH. 2020. Methylation-directed glycosylation of chromatin factors represses retrotransposon promoters. PNAS 117:2514292–98
    [Google Scholar]
  11. 11.
    Brandt J, Veith AM, Volff J-N. 2005. A family of neofunctionalized Ty3/gypsy retrotransposon genes in mammalian genomes. Cytogenet. Genome Res. 110:1–4307–17
    [Google Scholar]
  12. 12.
    Bruno M, Mahgoub M, Macfarlan TS. 2019. The arms race between KRAB-zinc finger proteins and endogenous retroelements and its impact on mammals. Annu. Rev. Genet. 53:393–416
    [Google Scholar]
  13. 13.
    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 151:1194–205
    [Google Scholar]
  14. 14.
    Capy P, Gasperi G, Biémont C, Bazin C. 2000. Stress and transposable elements: co-evolution or useful parasites?. Heredity 85:Part 2101–6
    [Google Scholar]
  15. 15.
    Carlier F, Nguyen T-S, Mazur AK, Gladyshev E. 2021. Modulation of C-to-T mutation by recombination-independent pairing of closely positioned DNA repeats. Biophys. J. 120:204325–36
    [Google Scholar]
  16. 16.
    Cho J. 2018. Transposon-derived non-coding RNAs and their function in plants. Front. Plant Sci. 9:600
    [Google Scholar]
  17. 17.
    Choi JY, Lee YCG. 2020. Double-edged sword: the evolutionary consequences of the epigenetic silencing of transposable elements. PLOS Genet 16:7e1008872
    [Google Scholar]
  18. 18.
    Chuong EB, Elde NC, Feschotte C. 2017. Regulatory activities of transposable elements: from conflicts to benefits. Nat. Rev. Genet. 18:271–86
    [Google Scholar]
  19. 19.
    Chuong EB, Rumi MAK, Soares MJ, Baker JC. 2013. Endogenous retroviruses function as species-specific enhancer elements in the placenta. Nat. Genet. 45:3325–29
    [Google Scholar]
  20. 20.
    Cooley L, Kelley R, Spradling A. 1988. Insertional mutagenesis of the Drosophila genome with single P elements. Science 239:48441121–28
    [Google Scholar]
  21. 21.
    Cordaux R, Udit S, Batzer MA, Feschotte C. 2006. Birth of a chimeric primate gene by capture of the transposase gene from a mobile element. PNAS 103:218101–6
    [Google Scholar]
  22. 22.
    Cosby RL, Chang N-C, Feschotte C. 2019. Host-transposon interactions: conflict, cooperation, and cooption. Genes Dev 33:17–181098–116
    [Google Scholar]
  23. 23.
    Cosby RL, Judd J, Zhang R, Zhong A, Garry N et al. 2021. Recurrent evolution of vertebrate transcription factors by transposase capture. Science 371:6531eabc6405
    [Google Scholar]
  24. 24.
    Daniels SB, Peterson KR, Strausbaugh LD, Kidwell MG, Chovnick A. 1990. Evidence for horizontal transmission of the P transposable element between Drosophila species. Genetics 124:2339–55
    [Google Scholar]
  25. 25.
    Daron J, Glover N, Pingault L, Theil S, Jamilloux V et al. 2014. Organization and evolution of transposable elements along the bread wheat chromosome 3B. Genome Biol 15:12546
    [Google Scholar]
  26. 26.
    Déléris A, Berger F, Duharcourt S. 2021. Role of Polycomb in the control of transposable elements. Trends Genet 37:10882–89
    [Google Scholar]
  27. 27.
    Déléris A, Stroud H, Bernatavichute Y, Johnson E, Klein G et al. 2012. Loss of the DNA methyltransferase MET1 induces H3K9 hypermethylation at PcG target genes and redistribution of H3K27 trimethylation to transposons in Arabidopsis thaliana. PLOS Genet 8:11e1003062
    [Google Scholar]
  28. 28.
    Deniz Ö, Frost JM, Branco MR. 2019. Regulation of transposable elements by DNA modifications. Nat. Rev. Genet. 20:7417–31
    [Google Scholar]
  29. 29.
    Devos KM, Brown JKM, Bennetzen JL. 2002. Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. Genome Res 12:71075–79
    [Google Scholar]
  30. 30.
    Dietrich CR, Cui F, Packila ML, Li J, Ashlock DA et al. 2002. Maize Mu transposons are targeted to the 5ʹ untranslated region of the gl8 gene and sequences flanking Mu target-site duplications exhibit nonrandom nucleotide composition throughout the genome. Genetics 160:2697–716
    [Google Scholar]
  31. 31.
    Domínguez M, Dugas E, Benchouaia M, Leduque B, Jiménez-Gómez JM et al. 2020. The impact of transposable elements on tomato diversity. Nat. Commun. 11:14058
    [Google Scholar]
  32. 32.
    Duan C-G, Wang X, Xie S, Pan L, Miki D et al. 2017. A pair of transposon-derived proteins function in a histone acetyltransferase complex for active DNA demethylation. Cell Res 27:2226–40
    [Google Scholar]
  33. 33.
    El Baidouri M, Carpentier M-C, Cooke R, Gao D, Lasserre E et al. 2014. Widespread and frequent horizontal transfers of transposable elements in plants. Genome Res 24:5831–38
    [Google Scholar]
  34. 34.
    Elsner D, Meusemann K, Korb J. 2018. Longevity and transposon defense, the case of termite reproductives. PNAS 115:215504–9
    [Google Scholar]
  35. 35.
    Emerson RO, Thomas JH. 2011. Gypsy and the birth of the SCAN domain. J. Virol. 85:2212043–52
    [Google Scholar]
  36. 36.
    Feschotte C. 2008. Transposable elements and the evolution of regulatory networks. Nat. Rev. Genet. 9:5397–405
    [Google Scholar]
  37. 37.
    Fultz D, Slotkin RK. 2017. Exogenous transposable elements circumvent identity-based silencing, permitting the dissection of expression-dependent silencing. Plant Cell 29:2360–76
    [Google Scholar]
  38. 38.
    Galagan JE, Selker EU. 2004. RIP: the evolutionary cost of genome defense. Trends Genet. TIG 20:9417–23
    [Google Scholar]
  39. 39.
    Galli M, Feng F, Gallavotti A. 2020. Mapping regulatory determinants in plants. Front. Genet. 11:591194
    [Google Scholar]
  40. 40.
    George JA, DeBaryshe PG, Traverse KL, Celniker SE, Pardue M-L. 2006. Genomic organization of the Drosophila telomere retrotransposable elements. Genome Res 16:101231–40
    [Google Scholar]
  41. 41.
    Gilbert C, Feschotte C. 2018. Horizontal acquisition of transposable elements and viral sequences: patterns and consequences. Curr. Opin. Genet. Dev. 49:15–24
    [Google Scholar]
  42. 42.
    Gilbert C, Hernandez SS, Flores-Benabib J, Smith EN, Feschotte C. 2012. Rampant horizontal transfer of SPIN transposons in squamate reptiles. Mol. Biol. Evol. 29:2503–15
    [Google Scholar]
  43. 43.
    Girard A, Hannon GJ. 2008. Conserved themes in small-RNA-mediated transposon control. Trends Cell Biol 18:3136–48
    [Google Scholar]
  44. 44.
    Gladyshev E, Kleckner N. 2017. Recombination-independent recognition of DNA homology for repeat-induced point mutation. Curr. Genet. 63:3389–400
    [Google Scholar]
  45. 45.
    Goriaux C, Desset S, Renaud Y, Vaury C, Brasset E. 2014. Transcriptional properties and splicing of the flamenco piRNA cluster. EMBO Rep 15:4411–18
    [Google Scholar]
  46. 46.
    Gray MM, Sutter NB, Ostrander EA, Wayne RK. 2010. The IGF1 small dog haplotype is derived from Middle Eastern grey wolves. BMC Biol 8:16
    [Google Scholar]
  47. 47.
    Guo C, Jeong H-H, Hsieh Y-C, Klein H-U, Bennett DA et al. 2018. Tau activates transposable elements in Alzheimer's disease. Cell Rep 23:102874–80
    [Google Scholar]
  48. 48.
    Guo W, Wang D, Lisch D. 2021. RNA-directed DNA methylation prevents rapid and heritable reversal of transposon silencing under heat stress in Zea mays. PLOS Genet 17:6e1009326
    [Google Scholar]
  49. 49.
    Heard E, Martienssen RA. 2014. Transgenerational epigenetic inheritance: myths and mechanisms. Cell 157:195–109
    [Google Scholar]
  50. 50.
    Hirochika H, Sugimoto K, Otsuki Y, Tsugawa H, Kanda M. 1996. Retrotransposons of rice involved in mutations induced by tissue culture. PNAS 93:157783–88
    [Google Scholar]
  51. 51.
    Holoch D, Moazed D. 2015. RNA-mediated epigenetic regulation of gene expression. Nat. Rev. Genet. 16:271–84
    [Google Scholar]
  52. 52.
    Hosaka A, Saito R, Takashima K, Sasaki T, Fu Y et al. 2017. Evolution of sequence-specific anti-silencing systems in Arabidopsis. Nat. Commun. 8:12161
    [Google Scholar]
  53. 53.
    Hsieh T-F, Ibarra CA, Silva P, Zemach A, Eshed-Williams L et al. 2009. Genome-wide demethylation of Arabidopsis endosperm. Science 324:59331451–54
    [Google Scholar]
  54. 54.
    Ikeda Y, Pélissier T, Bourguet P, Becker C, Pouch-Pélissier M-N et al. 2017. Arabidopsis proteins with a transposon-related domain act in gene silencing. Nat. Commun. 8:15122
    [Google Scholar]
  55. 55.
    Ito H, Gaubert H, Bucher E, Mirouze M, Vaillant I, Paszkowski J. 2011. An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress. Nature 472:7341115–19
    [Google Scholar]
  56. 56.
    Ito H, Kakutani T. 2014. Control of transposable elements in Arabidopsis thaliana. Chromosome Res 22:2217–23
    [Google Scholar]
  57. 57.
    Ito H, Kim J-M, Matsunaga W, Saze H, Matsui A et al. 2016. A stress-activated transposon in Arabidopsis induces transgenerational abscisic acid insensitivity. Sci. Rep. 6:23181
    [Google Scholar]
  58. 58.
    Ivancevic AM, Kortschak RD, Bertozzi T, Adelson DL. 2018. Horizontal transfer of BovB and L1 retrotransposons in eukaryotes. Genome Biol 19:185
    [Google Scholar]
  59. 59.
    Ivics Z, Hackett PB, Plasterk RH, Izsvák Z. 1997. Molecular reconstruction of Sleeping Beauty, a Tc1-like transposon from fish, and its transposition in human cells. Cell 91:4501–10
    [Google Scholar]
  60. 60.
    Jacobs FMJ, Greenberg D, Nguyen N, Haeussler M, Ewing AD et al. 2014. An evolutionary arms race between KRAB zinc-finger genes ZNF91/93 and SVA/L1 retrotransposons. Nature 516:7530242–45
    [Google Scholar]
  61. 61.
    Jansz N, Faulkner GJ. 2021. Endogenous retroviruses in the origins and treatment of cancer. Genome Biol 22:1147
    [Google Scholar]
  62. 62.
    Jiang J, Liu J, Sanders D, Qian S, Ren W et al. 2021. UVR8 interacts with de novo DNA methyltransferase and suppresses DNA methylation in Arabidopsis. Nat. Plants 7:2184–97
    [Google Scholar]
  63. 63.
    Jiang N, Bao Z, Zhang X, Eddy SR, Wessler SR. 2004. Pack-MULE transposable elements mediate gene evolution in plants. Nature 431:7008569–73
    [Google Scholar]
  64. 64.
    Josefsson C, Dilkes B, Comai L. 2006. Parent-dependent loss of gene silencing during interspecies hybridization. Curr. Biol. 16:131322–28
    [Google Scholar]
  65. 65.
    Judd J, Sanderson H, Feschotte C. 2021. Evolution of mouse circadian enhancers from transposable elements. Genome Biol 22:1193
    [Google Scholar]
  66. 66.
    Kabelitz T, Kappel C, Henneberger K, Benke E, Nöh C, Bäurle I. 2014. eQTL mapping of transposon silencing reveals a position-dependent stable escape from epigenetic silencing and transposition of AtMu1 in the Arabidopsis lineage. Plant Cell 26:83261–71
    [Google Scholar]
  67. 67.
    Kaeppler SM, Kaeppler HF, Rhee Y. 2000. Epigenetic aspects of somaclonal variation in plants. Plant Mol. Biol. 43:2–3179–88
    [Google Scholar]
  68. 68.
    Kapitonov VV, Koonin EV. 2015. Evolution of the RAG1-RAG2 locus: both proteins came from the same transposon. Biol. Direct. 10:20
    [Google Scholar]
  69. 69.
    Kapusta A, Kronenberg Z, Lynch VJ, Zhuo X, Ramsay L et al. 2013. Transposable elements are major contributors to the origin, diversification, and regulation of vertebrate long noncoding RNAs. PLOS Genet 9:4e1003470
    [Google Scholar]
  70. 70.
    Kawakatsu T, Huang S-SC, Jupe F, Sasaki E, Schmitz RJ et al. 2016. Epigenomic diversity in a global collection of Arabidopsis thaliana accessions. Cell 166:2492–505
    [Google Scholar]
  71. 71.
    Khan H, Smit A, Boissinot S. 2006. Molecular evolution and tempo of amplification of human LINE-1 retrotransposons since the origin of primates. Genome Res 16:178–87
    [Google Scholar]
  72. 72.
    Kim EY, Wang L, Lei Z, Li H, Fan W, Cho J 2021. Ribosome stalling and SGS3 phase separation prime the epigenetic silencing of transposons. Nat. Plants 7:3303–9
    [Google Scholar]
  73. 73.
    Konkel MK, Batzer MA. 2010. A mobile threat to genome stability: The impact of non-LTR retrotransposons upon the human genome. Semin. Cancer Biol. 20:4211–21
    [Google Scholar]
  74. 74.
    Krasileva KV. 2019. The role of transposable elements and DNA damage repair mechanisms in gene duplications and gene fusions in plant genomes. Curr. Opin. Plant Biol. 48:18–25
    [Google Scholar]
  75. 75.
    Krupovic M, Makarova KS, Forterre P, Prangishvili D, Koonin EV. 2014. Casposons: a new superfamily of self-synthesizing DNA transposons at the origin of prokaryotic CRISPR-Cas immunity. BMC Biol 12:36
    [Google Scholar]
  76. 76.
    Kumar S, Stecher G, Suleski M, Hedges SB. 2017. TimeTree: a resource for timelines, timetrees, and divergence times. Mol. Biol. Evol. 34:71812–19
    [Google Scholar]
  77. 77.
    Kunarso G, Chia N-Y, Jeyakani J, Hwang C, Lu X et al. 2010. Transposable elements have rewired the core regulatory network of human embryonic stem cells. Nat. Genet. 42:7631–34
    [Google Scholar]
  78. 78.
    Kuromori T, Hirayama T, Kiyosue Y, Takabe H, Mizukado S et al. 2004. A collection of 11 800 single-copy Ds transposon insertion lines in Arabidopsis. Plant J 37:6897–905
    [Google Scholar]
  79. 79.
    Lai Y, Lu XM, Daron J, Pan S, Wang J et al. 2020. The Arabidopsis PHD-finger protein EDM2 has multiple roles in balancing NLR immune receptor gene expression. PLOS Genet 16:9e1008993
    [Google Scholar]
  80. 80.
    Lavialle C, Cornelis G, Dupressoir A, Esnault C, Heidmann O et al. 2013. Paleovirology of ‘syncytins’, retroviral env genes exapted for a role in placentation. Philos. Trans. R. Soc. B 368:162620120507
    [Google Scholar]
  81. 81.
    Li W, Prazak L, Chatterjee N, Grüninger S, Krug L et al. 2013. Activation of transposable elements during aging and neuronal decline in Drosophila. Nat. Neurosci. 16:5529–31
    [Google Scholar]
  82. 82.
    Lin R, Ding L, Casola C, Ripoll DR, Feschotte C, Wang H. 2007. Transposase-derived transcription factors regulate light signaling in Arabidopsis. Science 318:58541302–5
    [Google Scholar]
  83. 83.
    Lin X, Faridi N, Casola C. 2016. An ancient transkingdom horizontal transfer of Penelope-like retroelements from arthropods to conifers. Genome Biol. Evol. 8:41252–66
    [Google Scholar]
  84. 84.
    Lisch D, Slotkin RK. 2011. Strategies for silencing and escape: the ancient struggle between transposable elements and their hosts. Int. Rev. Cell Mol. Biol. 292:119–52
    [Google Scholar]
  85. 85.
    Liu GE, Alkan C, Jiang L, Zhao S, Eichler EE. 2009. Comparative analysis of Alu repeats in primate genomes. Genome Res 19:5876–85
    [Google Scholar]
  86. 86.
    Liu S, de Jonge J, Trejo-Arellano MS, Santos-González J, Köhler C, Hennig L. 2021. Role of H1 and DNA methylation in selective regulation of transposable elements during heat stress. New Phytol 229:42238–50
    [Google Scholar]
  87. 87.
    Lv Y, Hu F, Zhou Y, Wu F, Gaut BS. 2019. Maize transposable elements contribute to long non-coding RNAs that are regulatory hubs for abiotic stress response. BMC Genom 20:1864
    [Google Scholar]
  88. 88.
    Lynch VJ, Leclerc RD, May G, Wagner GP 2011. Transposon-mediated rewiring of gene regulatory networks contributed to the evolution of pregnancy in mammals. Nat. Genet. 43:111154–59
    [Google Scholar]
  89. 89.
    Ma J, Bennetzen JL. 2004. Rapid recent growth and divergence of rice nuclear genomes. PNAS 101:3412404–10
    [Google Scholar]
  90. 90.
    Malone CD, Brennecke J, Dus M, Stark A, McCombie WR et al. 2009. Specialized piRNA pathways act in germline and somatic tissues of the Drosophila ovary. Cell 137:3522–35
    [Google Scholar]
  91. 91.
    Malone CD, Hannon GJ. 2009. Small RNAs as guardians of the genome. Cell 136:4656–68
    [Google Scholar]
  92. 92.
    Mason JM, Randall TA, Capkova Frydrychova R. 2016. Telomerase lost?. Chromosoma 125:165–73
    [Google Scholar]
  93. 93.
    Mateo L, González J. 2014. Pogo-like transposases have been repeatedly domesticated into CENP-B-related proteins. Genome Biol. Evol. 6:82008–16
    [Google Scholar]
  94. 94.
    McCarty DR, Liu P, Koch KE 2018. The UniformMu resource: construction, applications, and opportunities. The Maize Genome J Bennetzen, S Flint-Garcia, C Hirsch, R Tuberosa 131–42 Cham, Switz.: Springer
    [Google Scholar]
  95. 95.
    McClintock B. 1950. The origin and behavior of mutable loci in maize. PNAS 36:6344–55
    [Google Scholar]
  96. 96.
    McClintock B. 1964. Aspects of gene regulation in maize. Carnegie Inst. Wash. Yearb. 63:592–601
    [Google Scholar]
  97. 97.
    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 8:2e1002474
    [Google Scholar]
  98. 98.
    McCue AD, Slotkin RK. 2012. Transposable element small RNAs as regulators of gene expression. Trends Genet 28:12616–23
    [Google Scholar]
  99. 99.
    Michalak P. 2009. Epigenetic, transposon and small RNA determinants of hybrid dysfunctions. Heredity 102:145–50
    [Google Scholar]
  100. 100.
    Mirouze M, Reinders J, Bucher E, Nishimura T, Schneeberger K et al. 2009. Selective epigenetic control of retrotransposition in Arabidopsis. Nature 461:7262427–30
    [Google Scholar]
  101. 101.
    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 411:6834212–14
    [Google Scholar]
  102. 102.
    Morata J, Marín F, Payet J, Casacuberta JM. 2018. Plant lineage-specific amplification of transcription factor binding motifs by miniature inverted-repeat transposable elements (MITEs). Genome Biol. Evol. 10:51210–20
    [Google Scholar]
  103. 103.
    Naito K, Zhang F, Tsukiyama T, Saito H, Hancock CN et al. 2009. Unexpected consequences of a sudden and massive transposon amplification on rice gene expression. Nature 461:72671130–34
    [Google Scholar]
  104. 104.
    Ninova M, Chen Y-CA, Godneeva B, Rogers AK, Luo Y et al. 2020. Su(var)2-10 and the SUMO pathway link piRNA-guided target recognition to chromatin silencing. Mol. Cell 77:3556–70.e6
    [Google Scholar]
  105. 105.
    Notwell JH, Chung T, Heavner W, Bejerano G. 2015. A family of transposable elements co-opted into developmental enhancers in the mouse neocortex. Nat. Commun. 6:6644
    [Google Scholar]
  106. 106.
    Nuthikattu S, McCue AD, Panda K, 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 162:1116–31
    [Google Scholar]
  107. 107.
    Ong-Abdullah M, Ordway JM, Jiang N, Ooi S-E, Kok S-Y et al. 2015. Loss of Karma transposon methylation underlies the mantled somaclonal variant of oil palm. Nature 525:7570533–37
    [Google Scholar]
  108. 108.
    Ozata DM, Gainetdinov I, Zoch A, O'Carroll D, Zamore PD 2019. PIWI-interacting RNAs: small RNAs with big functions. Nat. Rev. Genet. 20:289–108
    [Google Scholar]
  109. 109.
    Pace JK, Gilbert C, Clark MS, Feschotte C. 2008. Repeated horizontal transfer of a DNA transposon in mammals and other tetrapods. PNAS 105:4417023–28
    [Google Scholar]
  110. 110.
    Partridge SR, Kwong SM, Firth N, Jensen SO. 2018. Mobile genetic elements associated with antimicrobial resistance. Clin. Microbiol. Rev. 31:4e00088–17
    [Google Scholar]
  111. 111.
    Pastuzyn ED, Day CE, Kearns RB, Kyrke-Smith M, Taibi AV et al. 2018. The neuronal gene Arc encodes a repurposed retrotransposon gag protein that mediates intercellular RNA transfer. Cell 172:1–2275–88.e18
    [Google Scholar]
  112. 112.
    Peng Y, Zhang Y, Gui Y, An D, Liu J et al. 2019. Elimination of a retrotransposon for quenching genome instability in modern rice. Mol. Plant. 12:101395–407
    [Google Scholar]
  113. 113.
    Pereira JF, Ryan PR. 2019. The role of transposable elements in the evolution of aluminium resistance in plants. J. Exp. Bot. 70:141–54
    [Google Scholar]
  114. 114.
    Peschke VM, Phillips RL. 1991. Activation of the maize transposable element Suppressor-mutator (Spm) in tissue culture. Theor. Appl. Genet. 81:190–97
    [Google Scholar]
  115. 115.
    Pezic D, Manakov SA, Sachidanandam R, Aravin AA. 2014. piRNA pathway targets active LINE1 elements to establish the repressive H3K9me3 mark in germ cells. Genes Dev 28:131410–28
    [Google Scholar]
  116. 116.
    Picelli S, Björklund AK, Reinius B, Sagasser S, Winberg G, Sandberg R. 2014. Tn5 transposase and tagmentation procedures for massively scaled sequencing projects. Genome Res 24:122033–40
    [Google Scholar]
  117. 117.
    Pinzón N, Bertrand S, Subirana L, Busseau I, Escrivá H, Seitz H. 2019. Functional lability of RNA-dependent RNA polymerases in animals. PLOS Genet 15:2e1007915
    [Google Scholar]
  118. 118.
    Piriyapongsa J, Jordan IK. 2008. Dual coding of siRNAs and miRNAs by plant transposable elements. RNA 14:5814–21
    [Google Scholar]
  119. 119.
    Piriyapongsa J, Mariño-Ramírez L, Jordan IK 2007. Origin and evolution of human microRNAs from transposable elements. Genetics 176:21323–37
    [Google Scholar]
  120. 120.
    Pollan M. 2001. The Botany of Desire New York: Random House
    [Google Scholar]
  121. 121.
    Poretti M, Praz CR, Meile L, Kälin C, Schaefer LK et al. 2020. Domestication of high-copy transposons underlays the wheat small RNA response to an obligate pathogen. Mol. Biol. Evol. 37:3839–48
    [Google Scholar]
  122. 122.
    Qiu Y, Köhler C. 2020. Mobility connects: transposable elements wire new transcriptional networks by transferring transcription factor binding motifs. Biochem. Soc. Trans. 48:31005–17
    [Google Scholar]
  123. 123.
    Ramsay L, Marchetto MC, Caron M, Chen S-H, Busche S et al. 2017. Conserved expression of transposon-derived non-coding transcripts in primate stem cells. BMC Genom 18:1214
    [Google Scholar]
  124. 124.
    Ropars J, Rodríguez de la Vega RC, López-Villavicencio M, Gouzy J, Sallet E et al. 2015. Adaptive horizontal gene transfers between multiple cheese-associated fungi. Curr. Biol. 25:192562–69
    [Google Scholar]
  125. 125.
    Roquis D, Robertson M, Yu L, Thieme M, Julkowska M, Bucher E. 2021. Genomic impact of stress-induced transposable element mobility in Arabidopsis. Nucleic Acids Res 49:1810431–47
    [Google Scholar]
  126. 126.
    Sarot E, Payen-Groschêne G, Bucheton A, Pélisson A. 2004. Evidence for a piwi-dependent RNA silencing of the gypsy endogenous retrovirus by the Drosophila melanogaster flamenco gene. Genetics 166:31313–21
    [Google Scholar]
  127. 127.
    Schrevens S, Sanglard D. 2021. Hijacking transposable elements for saturation mutagenesis in fungi. Front. Fungal Biol. 2:633876
    [Google Scholar]
  128. 128.
    Schultz DC, Ayyanathan K, Negorev D, Maul GG, Rauscher FJ III 2002. 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 16:8919–32
    [Google Scholar]
  129. 129.
    Shan X, Liu Z, Dong Z, Wang Y, Chen Y et al. 2005. Mobilization of the active MITE transposons mPing and Pong in rice by introgression from wild rice (Zizania latifolia Griseb.). Mol. Biol. Evol. 22:4976–90
    [Google Scholar]
  130. 130.
    Sigman MJ, Panda K, Kirchner R, McLain LL, Payne H et al. 2021. An siRNA-guided ARGONAUTE protein directs RNA polymerase V to initiate DNA methylation. Nat. Plants 7:111461–74
    [Google Scholar]
  131. 131.
    Sigman MJ, Slotkin RK. 2016. The first rule of plant transposable element silencing: location, location, location. Plant Cell 28:2304–13
    [Google Scholar]
  132. 132.
    Singh J, Freeling M, Lisch D. 2008. A position effect on the heritability of epigenetic silencing. PLOS Genet 4:10e1000216
    [Google Scholar]
  133. 133.
    Slotkin RK, Freeling M, Lisch D. 2003. Mu killer causes the heritable inactivation of the Mutator family of transposable elements in Zea mays. Genetics 165:2781–97
    [Google Scholar]
  134. 134.
    Slotkin RK, Freeling M, Lisch D. 2005. Heritable transposon silencing initiated by a naturally occurring transposon inverted duplication. Nat. Genet. 37:6641–44
    [Google Scholar]
  135. 135.
    Slotkin RK, Martienssen R. 2007. Transposable elements and the epigenetic regulation of the genome. Nat. Rev. Genet. 8:4272–85
    [Google Scholar]
  136. 136.
    Slotkin RK, Vaughn M, Borges F, Tanurdzić M, Becker JD et al. 2009. Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136:3461–72
    [Google Scholar]
  137. 137.
    Suh A, Witt CC, Menger J, Sadanandan KR, Podsiadlowski L et al. 2016. Ancient horizontal transfers of retrotransposons between birds and ancestors of human pathogenic nematodes. Nat. Commun. 7:11396
    [Google Scholar]
  138. 138.
    Van't Hof AE, Campagne P, Rigden DJ, Yung CJ, Lingley J et al. 2016. The industrial melanism mutation in British peppered moths is a transposable element. Nature 534:7605102–5
    [Google Scholar]
  139. 139.
    Wang D, Zhang J, Zuo T, Zhao M, Lisch D, Peterson T. 2020. Small RNA-mediated de novo silencing of Ac/Ds transposons is initiated by alternative transposition in maize. Genetics 215:2393–406
    [Google Scholar]
  140. 140.
    Wang S, Liang H, Xu Y, Li L, Wang H et al. 2021. Genome-wide analyses across Viridiplantae reveal the origin and diversification of small RNA pathway-related genes. Commun. Biol. 4:1412
    [Google Scholar]
  141. 141.
    Weiser NE, Kim JK. 2019. Multigenerational regulation of the Caenorhabditis elegans chromatin landscape by germline small RNAs. Annu. Rev. Genet. 53:289–311
    [Google Scholar]
  142. 142.
    Wells JN, Feschotte C. 2020. A field guide to eukaryotic transposable elements. Annu. Rev. Genet. 54:539–61
    [Google Scholar]
  143. 143.
    Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P et al. 2007. A unified classification system for eukaryotic transposable elements. Nat. Rev. Genet. 8:12973–82
    [Google Scholar]
  144. 144.
    Wood JG, Jones BC, Jiang N, Chang C, Hosier S et al. 2016. Chromatin-modifying genetic interventions suppress age-associated transposable element activation and extend life span in Drosophila. PNAS 113:4011277–82
    [Google Scholar]
  145. 145.
    Wu J, Xu J, Liu B, Yao G, Wang P et al. 2018. Chromatin analysis in human early development reveals epigenetic transition during ZGA. Nature 557:7704256–60
    [Google Scholar]
  146. 146.
    Xia B, Zhang W, Wudzinska A, Huang E, Brosh R et al. 2021. The genetic basis of tail-loss evolution in humans and apes. bioRxiv 2021.09.14.460388. https://doi.org/10.1101/2021.09.14.460388
    [Crossref]
  147. 147.
    Yang Y, Xu J, Ge S, Lai L. 2021. CRISPR/Cas: advances, limitations, and applications for precision cancer research. Front. Med. 8:649896
    [Google Scholar]
  148. 148.
    Zanni V, Eymery A, Coiffet M, Zytnicki M, Luyten I et al. 2013. Distribution, evolution, and diversity of retrotransposons at the flamenco locus reflect the regulatory properties of piRNA clusters. PNAS 110:4919842–47
    [Google Scholar]
  149. 149.
    Zhang H, Lang Z, Zhu J-K. 2018. Dynamics and function of DNA methylation in plants. Nat. Rev. Mol. Cell Biol. 19:8489–506
    [Google Scholar]
  150. 150.
    Zhang H-H, Peccoud J, Xu M-R-X, Zhang X-G, Gilbert C 2020. Horizontal transfer and evolution of transposable elements in vertebrates. Nat. Commun. 11:11362
    [Google Scholar]
  151. 151.
    Zhang J, Yu C, Pulletikurti V, Lamb J, Danilova T et al. 2009. Alternative Ac/Ds transposition induces major chromosomal rearrangements in maize. Genes Dev 23:6755–65
    [Google Scholar]
  152. 152.
    Zhang X, Qi Y. 2019. The landscape of Copia and Gypsy retrotransposon during maize domestication and improvement. Front. Plant Sci. 10:1533
    [Google Scholar]
  153. 153.
    Zhang Y, Wendte JM, Ji L, Schmitz RJ 2020. Natural variation in DNA methylation homeostasis and the emergence of epialleles. PNAS 117:94874–84
    [Google Scholar]
  154. 154.
    Zhu H, Li C, Gao C. 2020. Applications of CRISPR-Cas in agriculture and plant biotechnology. Nat. Rev. Mol. Cell Biol. 21:11661–77
    [Google Scholar]
  155. 155.
    Zilberman D, Cao X, Jacobsen SE. 2003. ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science 299:5607716–19
    [Google Scholar]
  156. 156.
    Zoch A, Auchynnikava T, Berrens RV, Kabayama Y, Schöpp T et al. 2020. SPOCD1 is an essential executor of piRNA-directed de novo DNA methylation. Nature 584:7822635–39
    [Google Scholar]
  157. 157.
    Zong J, Yao X, Yin J, Zhang D, Ma H. 2009. Evolution of the RNA-dependent RNA polymerase (RdRP) genes: duplications and possible losses before and after the divergence of major eukaryotic groups. Gene 447:129–39
    [Google Scholar]
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