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Genome Defense Against Transposable Elements and the Origins of Regulatory RNA

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Transposons and the Dynamic Genome

Part of the book series: Genome Dynamics and Stability ((GENOME,volume 4))

Abstract

Under selective pressure to contain the harmful effects of transposition, genomes have evolved multiple RNA-based mechanisms for regulating transposable elements (TEs). In this chapter, we describe a number of examples of RNA-based TE defense mechanisms. Once established, these RNA-mediated TE silencing mechanisms, such as RNA interference by miRNAs, may come to be used to regulate host genes. It is becoming possible to reconstruct evolutionary transitions demonstrating how specific TE defense mechanisms were co-opted to provide additional regulatory complexity for host genes. For instance, we have recently shown how miRNAs may have evolved from siRNA encoding TEs. Here we propose another specific model, the transcript infection model, whereby TE insertion dynamics can couple RNA-mediated repression mechanisms to the regulation of host genes.

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References

  1. Ambros V (2004) The functions of animal microRNAs. Nature 431:350–355

    Article  PubMed  CAS  Google Scholar 

  2. Aravin A, Gaidatzis D, Pfeffer S, Lagos -Quintana M, Landgraf P, Iovino N et al. (2006) A novel class of small RNAs bind to MILI protein in mouse testes. Nature 442:203–207

    PubMed  CAS  Google Scholar 

  3. Aravin AA, Hannon GJ, Brennecke J (2007) The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 318:761–764

    Article  PubMed  CAS  Google Scholar 

  4. Aravin AA, Lagos-Quintana M, Yalcin A, Zavolan M, Marks D, Snyder B et al. (2003) The small RNA profile during Drosophila melanogaster development. Dev Cell 5:337–350

    Article  PubMed  CAS  Google Scholar 

  5. Aravin AA, Naumova NM, Tulin AV, Vagin VV, Rozovsky YM, Gvozdev VA (2001) Double-stranded RNA-mediated silencing of genomic tandem repeats and transposable elements in the D. melanogaster germline. Curr Biol 11:1017–1027

    Article  PubMed  CAS  Google Scholar 

  6. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297

    Article  PubMed  CAS  Google Scholar 

  7. Boivin A, Gally C, Netter S, Anxolabehere D, Ronsseray S (2003) Telomeric associated sequences of Drosophila recruit polycomb-group proteins in vivo and can induce pairing-sensitive repression. Genetics 164:195–208

    PubMed  CAS  Google Scholar 

  8. Borchert GM, Lanier W, Davidson BL (2006) RNA polymerase III transcribes human microRNAs. Nat Struct Mol Biol 13:1097–1101

    Article  PubMed  CAS  Google Scholar 

  9. Brennecke J, Aravin AA, Stark A, Dus M, Kellis M, Sachidanandam R et al. (2007) Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128:1089–1103

    Article  PubMed  CAS  Google Scholar 

  10. Brennecke J, Hipfner DR, Stark A, Russell RB, Cohen SM (2003) Bantam encodes a developmentally regulated microRNA that controls cell proliferation and regulates the proapoptotic gene hid in Drosophila. Cell 113:25–36

    Article  PubMed  CAS  Google Scholar 

  11. Britten RJ, Davidson EH (1969) Gene regulation for higher cells: a theory. Science 165:349–357

    Article  PubMed  CAS  Google Scholar 

  12. Bucheton A (1995) The relationship between the flamenco gene and gypsy in Drosophila: how to tame a retrovirus. Trends Genet 11:349–353

    Article  PubMed  CAS  Google Scholar 

  13. Bureau TE, Wessler SR (1992) Tourist: a large family of small inverted repeat elements frequently associated with maize genes. Plant Cell 4:1283–1294

    Article  PubMed  CAS  Google Scholar 

  14. Bureau TE, Wessler SR (1994) Stowaway: a new family of inverted repeat elements associated with the genes of both monocotyledonous and dicotyledonous plants. Plant Cell 6:907–916

    Article  PubMed  CAS  Google Scholar 

  15. Carmell MA, Girard A, Van de Kant HJ, Bourc'his D, Bestor TH, De Rooij DG et al. (2007) MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Dev Cell 12:503–514

    Article  PubMed  CAS  Google Scholar 

  16. Cerutti H, Casas-Mollano JA (2006) On the origin and functions of RNA-mediated silencing: from protists to man. Curr Genet 50:81–99

    Article  PubMed  CAS  Google Scholar 

  17. Chen CZ, Li L, Lodish HF, Bartel DP (2004) MicroRNAs modulate hematopoietic lineage differentiation. Science 303:83–86

    Article  PubMed  CAS  Google Scholar 

  18. Cogoni C, Macino G (1997) Isolation of quelling-defective (qde) mutants impaired in posttranscriptional transgene-induced gene silencing in Neurospora crassa. Proc Natl Acad Sci USA 94:10233–10238

    Article  PubMed  CAS  Google Scholar 

  19. Cogoni C, Macino G (1999) Gene silencing in Neurospora crassa requires a protein homologous to RNA-dependent RNA polymerase. Nature 399:166–169

    Article  PubMed  CAS  Google Scholar 

  20. Conley AB, Miller WJ, Jordan IK (2008) Human cis natural antisense transcripts initiated by transposable elements. Trends Genet 24:53–56

    Article  PubMed  CAS  Google Scholar 

  21. Covey SN, Al-Kaff NS, Lángara A, Turner DS (1997) Plants combat infection by gene silencing. Nature 385:781–782

    Article  CAS  Google Scholar 

  22. Cox DN, Chao A, Baker J, Chang L, Qiao D, Lin H (1998) A novel class of evolutionarily conserved genes defined by piwi are essential for stem cell self-renewal. Genes Dev 12:3715–3727

    Article  PubMed  CAS  Google Scholar 

  23. Dalmay T, Hamilton A, Rudd S, Angell S, Baulcombe DC (2000) An RNA-dependent RNA polymerase gene in Arabidopsis is required for posttranscriptional gene silencing mediated by a transgene but not by a virus. Cell 101:543–553

    Article  PubMed  CAS  Google Scholar 

  24. De Carvalho F, Gheysen G, Kushnir S, Van Montagu M, Inze D, Castresana C (1992) Suppression of beta-1,3-glucanase transgene expression in homozygous plants. EMBO J 11:2595–2602

    PubMed  Google Scholar 

  25. Deng W, Lin H (2002) Miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev Cell 2:819–830

    Article  PubMed  CAS  Google Scholar 

  26. Desset S, Meignin C, Dastugue B, Vaury C (2003) COM, a heterochromatic locus governing the control of independent endogenous retroviruses from Drosophila melanogaster. Genetics 164:501–509

    PubMed  CAS  Google Scholar 

  27. Feschotte C, Mouches C (2000) Evidence that a family of miniature inverted-repeat transposable elements (MITEs) from the Arabidopsis thaliana genome has arisen from a pogo-like DNA transposon. Mol Biol Evol 17:730–737

    PubMed  CAS  Google Scholar 

  28. Feschotte C, Zhang X, Wessler SR (2002) Miniature inverted-repeat transposable elements and their relationships to established DNA transposons. In: Craig N, Craigie R, Gellert M, Lambowitz A (eds) Mobile DNA II. ASM Press, Washington, DC, pp 1147–1158

    Google Scholar 

  29. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806–811

    Article  PubMed  CAS  Google Scholar 

  30. Girard A, Hannon GJ (2008) Conserved themes in small-RNA-mediated transposon control. Trends Cell Biol 18:136–148

    Article  PubMed  CAS  Google Scholar 

  31. Girard A, Sachidanandam R, Hannon GJ, Carmell MA (2006) A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature 442:199–202

    PubMed  Google Scholar 

  32. Gunawardane LS, Saito K, Nishida KM, Miyoshi K, Kawamura Y, Nagami T et al. (2007) A slicer-mediated mechanism for repeat-associated siRNA 5′ end formation in Drosophila. Science 315:1587–1590

    Article  PubMed  CAS  Google Scholar 

  33. Hartig JV, Tomari Y, Forstemann K (2007) piRNAs – the ancient hunters of genome invaders. Genes Dev 21:1707–1713

    Article  PubMed  CAS  Google Scholar 

  34. Henikoff S, Ahmad K, Malik HS (2001) The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293:1098–1102

    Article  PubMed  CAS  Google Scholar 

  35. Hoskins RA, Carlson JW, Kennedy C, Acevedo D, Evans-Holm M, Frise E et al. (2007) Sequence finishing and mapping of Drosophila melanogaster heterochromatin. Science 316:1625–1628

    Article  PubMed  CAS  Google Scholar 

  36. Houwing S, Kamminga LM, Berezikov E, Cronembold D, Girard A, Van den Elst H et al. (2007) A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in Zebrafish. Cell 129:69–82

    Article  PubMed  CAS  Google Scholar 

  37. Josse T, Teysset L, Todeschini AL, Sidor CM, Anxolabehere D, Ronsseray S (2007) Telomeric trans-silencing: an epigenetic repression combining RNA silencing and heterochromatin formation. PLoS Genet 3:1633–1643

    Article  PubMed  CAS  Google Scholar 

  38. Karpen GH, Spradling AC (1992) Analysis of subtelomeric heterochromatin in the Drosophila minichromosome Dp1187 by single P element insertional mutagenesis. Genetics 132:737–753

    PubMed  CAS  Google Scholar 

  39. Ketting RF, Haverkamp TH, Van Luenen HG, Plasterk RH (1999) Mut-7 of C. elegans, required for transposon silencing and RNA interference, is a homolog of Werner syndrome helicase and RNaseD. Cell 99:133–141

    Article  PubMed  CAS  Google Scholar 

  40. Kidwell MG (1983) Evolution of hybrid dysgenesis determinants in Drosophila melanogaster. Proc Natl Acad Sci USA 80:1655–1659

    Article  PubMed  CAS  Google Scholar 

  41. Kim VN (2006) Small RNAs just got bigger: Piwi-interacting RNAs (piRNAs) in mammalian testes. Genes Dev 20:1993–1997

    Article  PubMed  CAS  Google Scholar 

  42. Kuhn TS (1962) The Structure of Scientific Revolutions. University of Chicago Press, Chicago

    Google Scholar 

  43. Kuramochi-Miyagawa S, Kimura T, Ijiri TW, Isobe T, Asada N, Fujita Y et al. (2004) Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development 131:839–849

    Article  PubMed  CAS  Google Scholar 

  44. Kuramochi-Miyagawa S, Kimura T, Yomogida K, Kuroiwa A, Tadokoro Y, Fujita Y et al. (2001) Two mouse piwi-related genes: miwi and mili. Mech Dev 108:121–133

    Article  PubMed  CAS  Google Scholar 

  45. Lankenau S, Corces VG, Lankenau D-H (1994) The Drosophila micropia retrotransposon encodes a testis-specific antisense RNA complementary to reverse transcriptase. Mol Cell Biol 14:1764–1775

    PubMed  CAS  Google Scholar 

  46. Lau NC, Seto AG, Kim J, Kuramochi-Miyagawa S, Nakano T, Bartel DP et al. (2006) Characterization of the piRNA complex from rat testes. Science 313:363–367

    Article  PubMed  CAS  Google Scholar 

  47. Lee RC, Feinbaum RL, Ambros V (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75:843–854

    Article  PubMed  CAS  Google Scholar 

  48. Lindbo JA, Silva-Rosales L, Proebsting WM, Dougherty WG (1993) Induction of a Highly Specific Antiviral State in Transgenic Plants: Implications for Regulation of Gene Expression and Virus Resistance. Plant Cell 5:1749–1759

    Article  PubMed  CAS  Google Scholar 

  49. Malik HS, Vermaak D, Henikoff S (2002) Recurrent evolution of DNA-binding motifs in the Drosophila centromeric histone. Proc Natl Acad Sci USA 99:1449–1454

    Article  PubMed  CAS  Google Scholar 

  50. Marin L, Lehmann M, Nouaud D, Izaabel H, Anxolabehere D, Ronsseray S (2000) P-Element repression in Drosophila melanogaster by a naturally occurring defective telomeric P copy. Genetics 155:1841–1854

    PubMed  CAS  Google Scholar 

  51. Matzke MA, Matzke AJ (2004) Planting the seeds of a new paradigm. PLoS Biol 2:E133

    Article  PubMed  CAS  Google Scholar 

  52. Matzke MA, Mette MF, Matzke AJ (2000) Transgene silencing by the host genome defense: implications for the evolution of epigenetic control mechanisms in plants and vertebrates. Plant Mol Biol 43:401–415

    Article  PubMed  CAS  Google Scholar 

  53. Meignin C, Dastugue B, Vaury C (2004) Intercellular communication between germ line and somatic line is utilized to control the transcription of ZAM, an endogenous retrovirus from Drosophila melanogaster. Nucleic Acids Res 32:3799–3806

    Article  PubMed  CAS  Google Scholar 

  54. Mette MF, Van der Winden J, Matzke M, Matzke AJ (2002) Short RNAs can identify new candidate transposable element families in Arabidopsis. Plant Physiol 130:6–9

    Article  PubMed  CAS  Google Scholar 

  55. Metzlaff M, O'Dell M, Cluster PD, Flavell RB (1997) RNA-mediated RNA degradation and chalcone synthase A silencing in petunia. Cell 88:845–854

    Article  PubMed  CAS  Google Scholar 

  56. Morgan GT (1995) Identification in the human genome of mobile elements spread by DNA-mediated transposition. J Mol Biol 254:1–5

    Article  PubMed  CAS  Google Scholar 

  57. Napoli C, Lemieux C, Jorgensen R (1990) Introduction of a chimeric chalcone synthase gene into Petunia results in reversible co-suppression of homologous genes in trans. Plant Cell 2:279–289

    Article  PubMed  CAS  Google Scholar 

  58. O'Donnell KA, Boeke JD (2007) Mighty Piwis defend the germline against genome intruders. Cell 129:37–44

    Article  PubMed  CAS  Google Scholar 

  59. Oosumi T, Belknap WR, Garlick B (1995) Mariner transposons in humans. Nature 378:672

    Article  PubMed  CAS  Google Scholar 

  60. Pelisson A, Song SU, Prud'homme N, Smith PA, Bucheton A, Corces VG (1994) Gypsy transposition correlates with the production of a retroviral envelope-like protein under the tissue-specific control of the Drosophila flamenco gene. EMBO J 13:4401–4411

    PubMed  CAS  Google Scholar 

  61. Piriyapongsa J, Jordan IK (2007) A Family of Human MicroRNA Genes from Miniature Inverted-Repeat Transposable Elements. PLoS ONE 2:e203

    Article  PubMed  CAS  Google Scholar 

  62. Piriyapongsa J, Jordan IK (2008) Dual coding of siRNAs and miRNAs by plant transposable elements. RNA 14:814–821

    Article  PubMed  CAS  Google Scholar 

  63. Piriyapongsa J, Marino-Ramirez L, Jordan IK (2007) Origin and evolution of human microRNAs from transposable elements. Genetics 176:1323–1337

    Article  PubMed  CAS  Google Scholar 

  64. Plasterk RH (2002) RNA silencing: the genome's immune system. Science 296:1263–1265

    Article  PubMed  CAS  Google Scholar 

  65. Popper KR (1959) The Logic of Scientific Discovery. Hutchinson, London

    Google Scholar 

  66. Prud'homme N, Gans M, Masson M, Terzian C, Bucheton A (1995) Flamenco, a gene controlling the gypsy retrovirus of Drosophila melanogaster. Genetics 139:697–711

    PubMed  Google Scholar 

  67. Ratcliff F, Harrison BD, Baulcombe DC (1997) A similarity between viral defense and gene silencing in plants. Science 276:1558–1560

    Article  PubMed  CAS  Google Scholar 

  68. Reinhart BJ, Slack FJ, Basson M, Pasquinelli AE, Bettinger JC, Rougvie AE et al. (2000) The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403:901–906

    Article  PubMed  CAS  Google Scholar 

  69. Reiss D, Josse T, Anxolabehere D, Ronsseray S (2004) Aubergine mutations in Drosophila melanogaster impair P cytotype determination by telomeric P elements inserted in heterochromatin. Mol Genet Genomics 272:336–343

    Article  PubMed  CAS  Google Scholar 

  70. Romano N, Macino G (1992) Quelling: transient inactivation of gene expression in Neurospora crassa by transformation with homologous sequences. Mol Microbiol 6:3343–3353

    Article  PubMed  CAS  Google Scholar 

  71. Ronsseray S, Lehmann M, Anxolabehere D (1991) The maternally inherited regulation of P elements in Drosophila melanogaster can be elicited by two P copies at cytological site 1A on the X chromosome. Genetics 129:501–512

    PubMed  CAS  Google Scholar 

  72. Ronsseray S, Lehmann M, Nouaud D, Anxolabehere D (1997) P element regulation and X-chromosome subtelomeric heterochromatin in Drosophila melanogaster. Genetica 100:95–107

    Article  PubMed  CAS  Google Scholar 

  73. Ruby JG, Jan C, Player C, Axtell MJ, Lee W, Nusbaum C et al. (2006) Large-scale sequencing reveals 21U-RNAs and additional microRNAs and endogenous siRNAs in C. elegans. Cell 127:1193–1207

    Article  PubMed  CAS  Google Scholar 

  74. Ruby JG, Jan CH, Bartel DP (2007) Intronic microRNA precursors that bypass Drosha processing. Nature 448:83–86

    Article  PubMed  CAS  Google Scholar 

  75. Saito K, Nishida KM, Mori T, Kawamura Y, Miyoshi K, Nagami T et al. (2006) Specific association of Piwi with rasiRNAs derived from retrotransposon and heterochromatic regions in the Drosophila genome. Genes Dev 20:2214–2222

    Article  PubMed  CAS  Google Scholar 

  76. Sarot E, Payen-Groschene P, Bucheton A, Pelisson A (2004) Evidence for a piwi-dependent RNA silencing of the gypsy endogenous retrovirus by the Drosophila melanogaster flamenco gene. Genetics 166:1313–1321

    Article  PubMed  CAS  Google Scholar 

  77. Savitsky M, Kwon D, Georgiev P, Kalmykova A, Gvozdev V (2006) Telomere elongation is under the control of the RNAi-based mechanism in the Drosophila germline. Genes Dev 20:345–354

    Article  PubMed  CAS  Google Scholar 

  78. Sawyer SL, Emerman M, Malik HS (2004) Ancient adaptive evolution of the primate antiviral DNA-editing enzyme APOBEC3G. PLoS Biol 2:E275

    Article  PubMed  CAS  Google Scholar 

  79. Schwarz DS, Hutvagner G, Haley B, Zamore PD (2002) Evidence that siRNAs function as guides, not primers, in the Drosophila and human RNAi pathways. Mol Cell 10:537–548

    Article  PubMed  CAS  Google Scholar 

  80. Sijen T, Kooter JM (2000) Post-transcriptional gene-silencing: RNAs on the attack or on the defense? Bioessays 22:520–531

    Article  PubMed  CAS  Google Scholar 

  81. Sijen T, Plasterk RH (2003) Transposon silencing in the Caenorhabditis elegans germ line by natural RNAi. Nature 426:310–314

    Article  PubMed  CAS  Google Scholar 

  82. Slotkin RK, Freeling M, Lisch D (2005) Heritable transposon silencing initiated by a naturally occurring transposon inverted duplication. Nat Genet 37:641–644

    Article  PubMed  CAS  Google Scholar 

  83. Smalheiser NR, Torvik VI (2005) Mammalian microRNAs derived from genomic repeats. Trends Genet 21:322–326

    Article  PubMed  CAS  Google Scholar 

  84. Smit AF, Riggs AD (1996) Tiggers and DNA transposon fossils in the human genome. Proc Natl Acad Sci USA 93:1443–1448

    Article  PubMed  CAS  Google Scholar 

  85. Smith CD, Shu S, Mungall CJ, Karpen GH (2007) The Release 5.1 annotation of Drosophila melanogaster heterochromatin. Science 316:1586–1591

    Article  PubMed  CAS  Google Scholar 

  86. Stuart JR, Haley KJ, Swedzinski D, Lockner S, Kocian PE, Merriman PJ et al. (2002) Telomeric P elements associated with cytotype regulation of the P transposon family in Drosophila melanogaster. Genetics 162:1641–1654

    PubMed  CAS  Google Scholar 

  87. Tabara H, Sarkissian M, Kelly WG, Fleenor J, Grishok A, Timmons L et al. (1999) The rde-1 gene, RNA interference, and transposon silencing in C. elegans. Cell 99:123–132

    Article  PubMed  CAS  Google Scholar 

  88. Tolia NH, Joshua-Tor L (2007) Slicer and the argonautes. Nat Chem Biol 3:36–43

    Article  PubMed  CAS  Google Scholar 

  89. Vagin VV, Sigova A, Li C, Seitz H, Gvozdev V, Zamore PD (2006) A distinct small RNA pathway silences selfish genetic elements in the germline. Science 313:320–324

    Article  PubMed  CAS  Google Scholar 

  90. Van Blokland R, Van der Geest N, Mol JNM, Kooter JM (1994) Transgene-mediated suppression of chalcone synthase expression in Petunia hybrida results from an increase in RNA turnover. Plant J 6:861–877

    Article  CAS  Google Scholar 

  91. Van der Krol AR, Mur LA, Beld M, Mol JN, Stuitje AR (1990) Flavonoid genes in petunia: addition of a limited number of gene copies may lead to a suppression of gene expression. Plant Cell 2:291–299

    Article  PubMed  Google Scholar 

  92. Wang XH, Aliyari R, Li WX, Li HW, Kim K, Carthew R et al. (2006) RNA interference directs innate immunity against viruses in adult Drosophila. Science 312:452–454

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Wolfgang J. Miller .

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Dirk-Henner Lankenau Jean-Nicolas Volff

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Jordan, I.K., Miller, W.J. (2008). Genome Defense Against Transposable Elements and the Origins of Regulatory RNA. In: Lankenau, DH., Volff, JN. (eds) Transposons and the Dynamic Genome. Genome Dynamics and Stability, vol 4. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7050_2008_041

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