Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Mammalian genome innovation through transposon domestication

Abstract

Since the discovery of transposons, their sheer abundance in host genomes has puzzled many. While historically viewed as largely harmless ‘parasitic’ DNAs during evolution, transposons are not a mere record of ancient genome invasion. Instead, nearly every element of transposon biology has been integrated into host biology. Here we review how host genome sequences introduced by transposon activities provide raw material for genome innovation and document the distinct evolutionary path of each species.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Transposon domestication contributes to host biology.
Fig. 2: Transposon-derived gene regulatory elements diversify host gene isoforms and enrich expression regulation modality.
Fig. 3: Transposons confer unique modes of cis-gene regulation in host genomes.
Fig. 4: Co-option of transposon-encoded proteins contributes to new host biology.

Similar content being viewed by others

References

  1. McClintock, B. The origin and behavior of mutable loci in maize. Proc. Natl Acad. Sci. USA 36, 344–355 (1950).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Britten, R. J. & Davidson, E. H. Gene regulation for higher cells: a theory. Science 165, 349–357 (1969).

    Article  CAS  PubMed  Google Scholar 

  3. Nurk, S. et al. The complete sequence of a human genome. Science 376, 44–53 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Lander, E. S. et al. Initial sequencing and analysis of the human genome. Nature 409, 860–921 (2001).

    Article  CAS  PubMed  Google Scholar 

  5. Craig Venter, J. et al. The sequence of the human genome. Science 291, 1304–1351 (2001).

    Article  Google Scholar 

  6. Waterston, R. H. et al. Initial sequencing and comparative analysis of the mouse genome. Nature 420, 520–562 (2002).

    Article  CAS  PubMed  Google Scholar 

  7. Wicker, T. et al. A unified classification system for eukaryotic transposable elements. Nat. Rev. Genet. 8, 973–982 (2007).

    Article  CAS  PubMed  Google Scholar 

  8. Jangam, D., Feschotte, C. & Betrán, E. Transposable element domestication as an adaptation to evolutionary conflicts. Trends Genet. 33, 817–831 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Feschotte, C. & Pritham, E. J. DNA transposons and the evolution of eukaryotic genomes. Annu Rev. Genet. 41, 331–368 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Levin, H. L. & Moran, J. V. Dynamic interactions between transposable elements and their hosts. Nat. Rev. Genet. 12, 615–627 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Doolittle, W. F. & Sapienza, C. Selfish genes, the phenotype paradigm and genome evolution. Nature 284, 601–603 (1980).

    Article  CAS  PubMed  Google Scholar 

  12. Capy, P. Taming, domestication and exaptation: trajectories of transposable elements in genomes. Cells 10, 3590 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Polak, P. & Domany, E. Alu elements contain many binding sites for transcription factors and may play a role in regulation of developmental processes. BMC Genomics 7, 133–148 (2006).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Gifford, W. D., Pfaff, S. L. & Macfarlan, T. S. Transposable elements as genetic regulatory substrates in early development. Trends Cell Biol. 23, 218–226 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Garcia-Perez, J. R., Widmann, T. J. & Adams, I. R. The impact of transposable elements on mammalian development. Development 143, 4101–4114 (2016).

    Article  CAS  PubMed  Google Scholar 

  16. van de Lagemaat, L. N., Landry, J.-R., Mager, D. L. & Medstrand, P. Transposable elements in mammals promote regulatory variation and diversification of genes with specialized functions. Trends Genet. 19, 530–536 (2003).

    Article  PubMed  CAS  Google Scholar 

  17. Simonti, C. N., Pavličev, M. & Capra, J. A. Transposable element exaptation into regulatory regions is rare, influenced by evolutionary age, and subject to pleiotropic constraints. Mol. Biol. Evol. 34, 2856–2869 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Miyawaki, S. et al. The mouse Sry locus harbors a cryptic exon that is essential for male sex determination. Science 370, 121–124 (2020).

    Article  CAS  PubMed  Google Scholar 

  19. Flemr, M. et al. A retrotransposon-driven dicer isoform directs endogenous small interfering RNA production in mouse oocytes. Cell 155, 807–816 (2013).

    Article  CAS  PubMed  Google Scholar 

  20. Sakashita, A. et al. Endogenous retroviruses drive species-specific germline transcriptomes in mammals. Nat. Struct. Mol. Biol. 27, 967–977 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Modzelewski, A. J. et al. A mouse-specific retrotransposon drives a conserved Cdk2ap1 isoform essential for development. Cell 184, 5541–5558.e22 (2021).

    Article  CAS  PubMed  Google Scholar 

  22. Senft, A. D. & Macfarlan, T. S. Transposable elements shape the evolution of mammalian development. Nat. Rev. Genet. 22, 691–711 (2021).

    Article  CAS  PubMed  Google Scholar 

  23. Chuong, E. B., Elde, N. C. & Feschotte, C. Regulatory activities of transposable elements: from conflicts to benefits. Nat. Rev. Genet. 18, 71–86 (2017).

    Article  CAS  PubMed  Google Scholar 

  24. Ito, J. et al. Systematic identification and characterization of regulatory elements derived from human endogenous retroviruses. PLoS Genet. 13, e1006883 (2017).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Notwell, J. H., Chung, T., Heavner, W. & Bejerano, G. A family of transposable elements co-opted into developmental enhancers in the mouse neocortex. Nat. Commun. 6, 6644 (2015).

    Article  CAS  PubMed  Google Scholar 

  26. Chuong, E. B., Elde, N. C. & Feschotte, C. Regulatory evolution of innate immunity through co-option of endogenous retroviruses. Science 351, 1083–1087 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Ye, M. et al. Specific subfamilies of transposable elements contribute to different domains of T lymphocyte enhancers. Proc. Natl Acad. Sci. USA 117, 7905–7916 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Peaston, A. E. et al. Retrotransposons regulate host genes in mouse oocytes and preimplantation embryos. Dev. Cell 7, 597–606 (2004).

    Article  CAS  PubMed  Google Scholar 

  29. Macfarlan, T. S. et al. Embryonic stem cell potency fluctuates with endogenous retrovirus activity. Nature 487, 57–63 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Franke, V. et al. Long terminal repeats power evolution of genes and gene expression programs in mammalian oocytes and zygotes. Genome Res. 27, 1384–1394 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Hasuwa, H. et al. Production of functional oocytes requires maternally expressed PIWI genes and piRNAs in golden hamsters. Nat. Cell Biol. 23, 1002–1012 (2021).

    Article  CAS  PubMed  Google Scholar 

  32. Gerlo, S., Davis, J. R. E., Mager, D. L. & Kooijman, R. Prolactin in man: a tale of two promoters. BioEssays 28, 1051–1055 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Emera, D. et al. Convergent evolution of endometrial prolactin expression in primates, mice, and elephants through the independent recruitment of transposable elements. Mol. Biol. Evol. 29, 239–247 (2012).

    Article  CAS  PubMed  Google Scholar 

  34. Davis, M. P. et al. Transposon-driven transcription is a conserved feature of vertebrate spermatogenesis and transcript evolution. EMBO Rep. 18, 1231–1247 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Beyer, U., Moll-Rocek, J., Moll, U. M. & Dobbelstein, M. Endogenous retrovirus drives hitherto unknown proapoptotic p63 isoforms in the male germ line of humans and great apes. Proc. Natl Acad. Sci. USA 108, 3624–3629 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Pi, W. et al. The LTR enhancer of ERV-9 human endogenous retrovirus is active in oocytes and progenitor cells in transgenic zebrafish and humans. Proc. Natl Acad. Sci. USA 101, 805–810 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Hu, T. et al. Long non-coding RNAs transcribed by ERV-9 LTR retrotransposon act in cis to modulate long-range LTR enhancer function. Nucleic Acids Res. 45, 4479–4492 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Feschotte, C. Transposable elements and the evolution of regulatory networks. Nat. Rev. Genet. 9, 397–405 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Sundaram, V. & Wysocka, J. Transposable elements as a potent source of diverse cis-regulatory sequences in mammalian genomes. Philos. Trans. R. Soc. Lond. B 375, 20190347 (2020).

    Article  CAS  Google Scholar 

  40. Xie, M. et al. DNA hypomethylation within specific transposable element families associates with tissue-specific enhancer landscape. Nat. Genet. 45, 836–841 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Pehrsson, E. C., Choudhary, M. N. K., Sundaram, V. & Wang, T. The epigenomic landscape of transposable elements across normal human development and anatomy. Nat. Commun. 10, 5640 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Miao, B. et al. Tissue-specific usage of transposable element-derived promoters in mouse development. Genome Biol. 21, 255–280 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Bourque, G. et al. Evolution of the mammalian transcription factor binding repertoire via transposable elements. Genome Res. 18, 1752–1762 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Wang, T. et al. Species-specific endogenous retroviruses shape the transcriptional network of the human tumor suppressor protein p53. Proc. Natl Acad. Sci. USA 104, 18613–18618 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Kunarso, G. et al. Transposable elements have rewired the core regulatory network of human embryonic stem cells. Nat. Genet. 42, 631–634 (2010).

    Article  CAS  PubMed  Google Scholar 

  46. Schmidt, D. et al. Waves of retrotransposon expansion remodel genome organization and CTCF binding in multiple mammalian lineages. Cell 148, 335–348 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Sundaram, V. et al. Widespread contribution of transposable elements to the innovation of gene regulatory networks. Genome Res 24, 1963–1976 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Sundaram, V. et al. Functional cis-regulatory modules encoded by mouse-specific endogenous retrovirus. Nat. Commun. 8, 14550 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Choudhary, M. N. K. et al. Co-opted transposons help perpetuate conserved higher-order chromosomal structures. Genome Biol. 21, 16 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Xia, B. et al. The genetic basis of tail-loss evolution in humans and apes. Preprint at bioRxiv https://doi.org/10.1101/2021.09.14.460388 (2021).

  51. Mayr, C. Regulation by 3′-untranslated regions. Annu. Rev. Genet. 51, 171–194 (2017).

    Article  CAS  PubMed  Google Scholar 

  52. Kelley, D. & Rinn, J. Transposable elements reveal a stem cell-specific class of long noncoding RNAs. Genome Biol. 13, R107 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  53. Jachowicz, J. W. et al. LINE-1 activation after fertilization regulates global chromatin accessibility in the early mouse embryo. Nat. Genet. 49, 1502–1510 (2017).

    Article  CAS  PubMed  Google Scholar 

  54. Lu, X. et al. The retrovirus HERVH is a long noncoding RNA required for human embryonic stem cell identity. Nat. Struct. Mol. Biol. 21, 423–425 (2014).

    Article  CAS  PubMed  Google Scholar 

  55. Percharde, M. et al. A LINE1–nucleolin partnership regulates early development and ESC identity. Cell 174, 391–405.e19 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Zhao, Y. et al. Transposon-triggered innate immune response confers cancer resistance to the blind mole rat. Nat. Immunol. 22, 1219–1230 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Chiappinelli, K. B. et al. Inhibiting DNA methylation causes an interferon response in cancer via dsRNA including endogenous retroviruses. Cell 162, 974–986 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Ueda, M. T. et al. Comprehensive genomic analysis reveals dynamic evolution of endogenous retroviruses that code for retroviral-like protein domains. Mob. DNA 11, 29–46 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Campillos, M., Doerks, T., Shah, P. K. & Bork, P. Computational characterization of multiple Gag-like human proteins. Trends Genet. 22, 585–589 (2006).

    Article  CAS  PubMed  Google Scholar 

  60. Zhang, W. et al. Structural basis of Arc binding to synaptic proteins: implications for cognitive disease. Neuron 86, 490–500 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Pastuzyn, E. D. et al. The neuronal gene Arc encodes a repurposed retrotransposon Gag protein that mediates intercellular RNA transfer. Cell 172, 275–288.e18 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Ashley, J. et al. Retrovirus-like Gag protein Arc1 binds RNA and traffics across synaptic boutons. Cell 172, 262–274.e11 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Kedrov, A. V., Durymanov, M. & Anokhin, K. V. The Arc gene: retroviral heritage in cognitive functions. Neurosci. Biobehav Rev. 99, 275–281 (2019).

    Article  CAS  PubMed  Google Scholar 

  64. Okuno, H. et al. Inverse synaptic tagging of inactive synapses via dynamic interaction of Arc/Arg3.1 with CaMKIIβ. Cell 149, 886–898 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Ono, R. et al. Deletion of Peg10, an imprinted gene acquired from a retrotransposon, causes early embryonic lethality. Nat. Genet. 38, 101–106 (2005).

    Article  PubMed  CAS  Google Scholar 

  66. Clark, M. B. et al. Mammalian gene PEG10 expresses two reading frames by high efficiency –1 frameshifting in embryonic-associated tissues. J. Biol. Chem. 282, 37359–37369 (2007).

    Article  CAS  PubMed  Google Scholar 

  67. Abed, M. et al. The Gag protein PEG10 binds to RNA and regulates trophoblast stem cell lineage specification. PLoS ONE 14, e0214110 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Segel, M. et al. Mammalian retrovirus-like protein PEG10 packages its own mRNA and can be pseudotyped for mRNA delivery. Science 373, 882–889 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Sha, M. et al. Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature 403, 785–789 (2000).

    Article  CAS  Google Scholar 

  70. Esnault, C., Cornelis, G., Heidmann, O. & Heidmann, T. Differential evolutionary fate of an ancestral primate endogenous retrovirus envelope gene, the EnvV syncytin, captured for a function in placentation. PLoS Genet. 9, e1003400 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Dupressoir, A. et al. Syncytin-A knockout mice demonstrate the critical role in placentation of a fusogenic, endogenous retrovirus-derived, envelope gene. Proc. Natl Acad. Sci. USA 106, 12127–12132 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Dupressoir, A. et al. A pair of co-opted retroviral envelope syncytin genes is required for formation of the two-layered murine placental syncytiotrophoblast. Proc. Natl Acad. Sci. USA 108, E1164–E1173 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Mangeney, M. et al. Placental syncytins: genetic disjunction between the fusogenic and immunosuppressive activity of retroviral envelope proteins. Proc. Natl Acad. Sci. USA 104, 20534–20539 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Marco, A. & Marín, I. CGIN1: a retroviral contribution to mammalian genomes. Mol. Biol. Evol. 26, 2167–2170 (2009).

    Article  CAS  PubMed  Google Scholar 

  75. Lloréns, C. & Marín, I. A mammalian gene evolved from the integrase domain of an LTR retrotransposon. Mol. Biol. Evol. 18, 1597–1600 (2001).

    Article  PubMed  Google Scholar 

  76. Shiura, H. et al. PEG10 viral aspartic protease domain is essential for the maintenance of fetal capillary structure in the mouse placenta. Development 148, dev199564 (2021).

    CAS  PubMed  PubMed Central  Google Scholar 

  77. Kitazawa, M., Tamura, M., Kaneko-Ishino, T. & Ishino, F. Severe damage to the placental fetal capillary network causes mid- to late fetal lethality and reduction in placental size in Peg11/Rtl1 KO mice. Genes Cells 22, 174–188 (2017).

    Article  CAS  PubMed  Google Scholar 

  78. McLaughlin, R. N. et al. Positive selection and multiple losses of the LINE-1-derived L1TD1 gene in mammals suggest a dual role in genome defense and pluripotency. PLoS Genet. 10, e1004531 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  79. Huang, S. et al. Discovery of an active RAG transposon illuminates the origins of V(D)J recombination. Cell 166, 102–114 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Ruiz, M. et al. Abnormalities of motor function, transcription and cerebellar structure in mouse models of THAP1 dystonia. Hum. Mol. Genet. 24, 7159–7170 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Dejosez, M. et al. Ronin is essential for embryogenesis and the pluripotency of mouse embryonic stem cells. Cell 133, 1162–1174 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Majumdar, S., Singh, A. & Rio, D. C. The human THAP9 gene encodes an active P-element DNA transposase. Science 339, 446–448 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Cosby, R. L. et al. Recurrent evolution of vertebrate transcription factors by transposase capture. Science 371, eabc6405 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Koonin, E. V. & Krupovic, M. Evolution of adaptive immunity from transposable elements combined with innate immune systems. Nat. Rev. Genet.16, 184–192 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  85. Kapitonov, V. V., Makarova, K. S. & Koonin, E. V. ISC, a novel group of bacterial and archaeal DNA transposons that encode Cas9 homologs. J. Bacteriol. 198, 797–807 (2015).

    Article  PubMed  CAS  Google Scholar 

  86. Altae-Tran, H. et al. The widespread IS200/IS605 transposon family encodes diverse programmable RNA-guided endonucleases. Science 374, 57–65 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Malfavon-Borja, R. & Feschotte, C. Fighting fire with fire: endogenous retrovirus envelopes as restriction factors. J. Virol. 89, 4047–4050 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Blanco-Melo, D., Gifford, R. J. & Bieniasz, P. D. Co-option of an endogenous retrovirus envelope for host defense in hominid ancestors. eLife 6, e22519 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  89. Grow, E. J. et al. Intrinsic retroviral reactivation in human preimplantation embryos and pluripotent cells. Nature 522, 221–225 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Frank, J. A. et al. Antiviral activity of a human placental protein of retroviral origin. Preprint at bioRxiv https://doi.org/10.1101/2020.08.23.263665 (2020).

  91. Yap, M. W., Colbeck, E., Ellis, S. A. & Stoye, J. P. Evolution of the retroviral restriction gene Fv1: inhibition of non-MLV retroviruses. PLoS Pathog. 10, e1003968 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  92. Horikoshi, M. et al. Positional cloning of the mouse retrovirus restriction gene Fvl. Nature 382, 826–829 (1996).

    Article  Google Scholar 

  93. Jin, Y., Tam, O. H., Paniagua, E. & Hammell, M. TEtranscripts: a package for including transposable elements in differential expression analysis of RNA-seq datasets. Bioinformatics 31, 3593–3599 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Yang, W. R., Ardeljan, D., Pacyna, C. N., Payer, L. M. & Burns, K. H. SQuIRE reveals locus-specific regulation of interspersed repeat expression. Nucleic Acids Res. 47, e27 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Bendall, M. L. et al. Telescope: characterization of the retrotranscriptome by accurate estimation of transposable element expression. PLoS Comput. Biol. 15, e1006453 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Miga, K. H. et al. Telomere-to-telomere assembly of a complete human X chromosome. Nature 585, 79–84 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Miga, K. H. & Wang, T. The need for a human pangenome reference sequence. Annu Rev. Genomics Hum. Genet 22, 81–102 (2021).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  98. Rhie, A. et al. Towards complete and error-free genome assemblies of all vertebrate species. Nature 592, 737–746 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Stoye, J. P. Koala retrovirus: a genome invasion in real time. Genome Biol. 7, 241 (2006).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  100. Dupuy, A. J., Akagi, K., Largaespada, D. A., Copeland, N. G. & Jenkins, N. A. Mammalian mutagenesis using a highly mobile somatic Sleeping Beauty transposon system. Nature 436, 221–226 (2005).

    Article  CAS  PubMed  Google Scholar 

  101. Ding, S. et al. Efficient transposition of the piggyBac (PB) transposon in mammalian cells and mice. Cell 122, 473–483 (2005).

    Article  CAS  PubMed  Google Scholar 

  102. Zamore, P. D., Tuschl, T., Sharp, P. A. & Bartel, D. P. RNAi: double-stranded RNA directs the ATP-dependent cleavage of mRNA at 21 to 23 nucleotide intervals. Cell 101, 25–33 (2000).

    Article  CAS  PubMed  Google Scholar 

  103. Jinek, M. et al. RNA-programmed genome editing in human cells. eLife 2013, e00471 (2013).

    Article  CAS  Google Scholar 

  104. Mali, P. et al. RNA-guided human genome engineering via Cas9. Science 339, 823–826 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Cong, L. et al. Multiplex genome engineering using CRISPR/Cas systems. Science 339, 819–823 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Casacuberta, E. Drosophila: retrotransposons making up telomeres. Viruses 9, 192–208 (2017).

    Article  PubMed Central  CAS  Google Scholar 

  107. Abad, J. P. et al. TAHRE, a novel telomeric retrotransposon from Drosophila melanogaster, reveals the origin of Drosophila telomeres. Mol. Biol. Evol. 21, 1620–1624 (2004).

    Article  CAS  PubMed  Google Scholar 

  108. Levis, R. W., Ganesan, R., Houtchens, K., Tolar, L. A. & Sheen, F. Miin Transposons in place of telomeric repeats at a Drosophila telomere. Cell 75, 1083–1093 (1993).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We are grateful to L. B. King for editing and proofreading this review. A.J.M. is supported by NIH (R00HD096108) and the Siebel Stem Cell Institute. T.W. is supported by NIH (R01HG007175, U24ES026699, U01CA200060, U01HG009391, U41HG010972 and U24HG012070). L.H. is a Thomas and Stacey Siebel Distinguished Chair Professor, and a Chan-Zuckerberg Biohub Investigator, supported by an HHMI Faculty Scholar award, a Bakar Fellow award and NIH grants (1R01GM114414, R01CA139067, 1R21OD027053, GRANT12095758, 1R01HD106809 and R01NS120287).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lin He.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Cell Biology thanks Todd Macfarlan and William Theurkauf for their contribution to the peer review of this work.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Modzelewski, A.J., Gan Chong, J., Wang, T. et al. Mammalian genome innovation through transposon domestication. Nat Cell Biol 24, 1332–1340 (2022). https://doi.org/10.1038/s41556-022-00970-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41556-022-00970-4

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing