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Russian Journal of Genetics

, Volume 38, Issue 6, pp 594–601 | Cite as

Acquisition/Loss of Modules: the Construction Set of Transposable Elements

  • P. Capy
  • C. Maisonhaute
Article

Abstract

Phylogenetic analysis of transposable elements (TEs) allows us to define the relationships between the domains or gene(s) that compose them. Moreover, modules of a few amino-acids can be detected within gag, pol, envgenes or within the integrase domain of retrotransposons and transposase of DNA elements. The combination of these observations clearly shows that the evolutionary history of TEs is the outcome of the acquisition and loss of modules with differing origins and histories. This raises the question of the origin of TEs: are they derived from viruses? Do the basic building bricks come from the prokaryotes, and can they be assembled in the eukaryotes? Are the TEs found in prokaryotes the result of the disintegration of complex elements such as retroelements? Do they evolve from the simplest to the more complex, or are they opportunistic sequences evolving by acquiring and/or losing modules which may be either important or superfluous to their fitness (i.e., their ability to transpose). These are some of the questions that are addressed and discussed in the light of the comparative structures of TEs.

Keywords

Phylogenetic Analysis Evolutionary History Transposable Element Comparative Structure Complex Element 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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REFERENCES

  1. 1.
    Capy, P. et al., Relationships between Transposable Elements Based upon the Integrase-Transposase Domains: Is There a Common Ancestor?, J. Mol. Evol., 1996, vol. 42, pp. 359-369.Google Scholar
  2. 2.
    Capy, P. et al., Does the Integrase of LTR-retrotransposons and Most of the Transposases of Class II Elements Share a Common Ancestor?, Genetica, 1997, vol. 100, pp. 63-72.Google Scholar
  3. 3.
    Lerat, E. and Capy, P., Retrotransposons and Retroviruses: Analysis of the Envelope Gene, Mol. Biol. Evol., 1999, vol. 16, pp. 1198-1207.Google Scholar
  4. 4.
    Lerat, E. et al., Is the Evolution of Transposable Elements Modular?, Genetica, 2000, vol. 107, pp. 15-25.Google Scholar
  5. 5.
    Malik, H.S. and Eickbush, T.H., Modular Evolution of the Integrase Domain in the Ty3/Gypsy Class of LTR Retrotransposons, Virol., 1999, vol. 73, no. 6, pp. 5186-5190.Google Scholar
  6. 6.
    McClure, M.A., Evolution of Retroposons by Acquisition or Deletion of Retrovirus-like Genes, Mol. Biol. Evol., 1991, vol. 8, pp. 835-856.Google Scholar
  7. 7.
    Xiong, Y. and Eickbush, T.H., Origin and Evolution of Retroelements Based upon Their Reverse Transcriptase Sequences, EMBO J., 1990, vol. 9, pp. 3353-3362.Google Scholar
  8. 8.
    Fayet, O. et al., Functional Similarities between Retroviruses and the IS3 Family of Bacterial Insertion Sequences?, Mol. Microbiol., 1990, vol. 4, pp. 1771-1777.Google Scholar
  9. 9.
    Doak, T.G. et al., A Proposed Superfamily of Transposase-related Genes: New Members in Transposon-like Elements of Cilliated Protozoa and a Common "D35E" Motif, Proc. Natl. Acad. Sci. USA, 1994, vol. 91, pp. 942-946.Google Scholar
  10. 10.
    Khan, E. et al., Retroviral Integrase Domains: DNA Binding and the Recognition of LTR Sequences, Nucleic Acids Res., 1991, vol. 19, pp. 851-860.Google Scholar
  11. 11.
    Lerat, E. et al., Is the Evolution of Transposable Element Modular?, Genetica, 1999, vol. 107, pp. 15-25.Google Scholar
  12. 12.
    Serre, M.C. et al., Mutagenesis of the IS1 Transposase: Importance of a His-Arg-Tyr Triad for Activity, J. Bacteriol., 1995, vol. 177, pp. 5070-5077.Google Scholar
  13. 13.
    Feschotte, C. and Wessler, S.R., Treasures in the Attic: Rolling Circle Transposons Discovered in Eukaryotic Genomes, Proc. Natl. Acad. Sci. USA, 2001, vol. 98, pp. 8923-8924.Google Scholar
  14. 14.
    Kapitonov, V.V. and Jurka, J., Rolling-circle Transposons in Eukaryotes, Proc. Natl. Acad. Sci. USA, 2001, vol. 98, pp. 8714-8719.Google Scholar
  15. 15.
    ICTV VIIth Report, Murphy, F.A., Ed., New York: Springer-Verlag, 1998.Google Scholar
  16. 16.
    Malik, H.S., Burke, W.D., and Eickbush, T.H., The Age and Evolution of Non-LTR Retrotransposable Elements, Mol. Biol. Evol., 1999, vol. 16, no. 6, pp. 793-805.Google Scholar
  17. 17.
    Malik, H.S. and Eickbush, T.H., Phylogenetic Analysis of Ribonuclease H Domains Suggests a Late, Chimeric Origin of LTR Retrotransposable Elements and Retroviruses, Genome Res., 2001, vol. 11, pp. 1187-1197.Google Scholar
  18. 18.
    Malik, H.S., Henikoff, S., and Eickbush, T.H., Poised for Contagion: Evolutionary Origins of the Infectious Abilities of Invertebrate Retroviruses, Genome Res., 2000, vol. 10, pp. 1307-1318.Google Scholar
  19. 19.
    Feschotte, C. and Mouches, C., 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., 2000, vol. 17, no. 5, pp. 730-737.Google Scholar
  20. 20.
    Feschotte, C. and Mouches, C., Recent Amplification of Miniature Inverted-repeat Transposable Elements in the Vector Mosquito Culex pipiens: Characterization of the Mimo Family, Gene, 2000, vol. 250, nos. 1–2, pp. 109-116.Google Scholar
  21. 21.
    Malik, H.S. and Eickbush, T.H., The RTE Class of Non-LTR Retrotransposons Is Widely Distributed in Animals and Is the Origin of Many SINEs, Mol. Biol. Evol., 1998, vol. 15, pp. 1123-1134.Google Scholar
  22. 22.
    Ohshima, K. et al., The 3′ End of tRNA-derived Short Interspersed Repetitive Elements Are Derived from the 3′ Ends of Long Interspersed Repetitive Elements, Mol. Cell. Biol., 1996, vol. 16, pp. 3756-3764.Google Scholar
  23. 23.
    Okada, N. et al., SINEs and LINEs Share Common 3' Sequences: a Review, Gene, 1997, vol. 205, pp. 229-243.Google Scholar
  24. 24.
    Okada, N. and Hamada, M., The 3' Ends of tRNA-derived SINEs Originated from the 3' Ends of LINEs: a New Example from the Bovine Genome, J. Mol. Evol., 1997, vol. 44, suppl. 1, pp. S52-S56.Google Scholar
  25. 25.
    Eickbush, T.H., Transposing without Ends: the Non-LTR Retrotransposable Elements, New Biol., 1992, vol. 4, pp. 430-440.Google Scholar
  26. 26.
    Luan, D.D. et al., Reverse Transcription of R2Bm RNA Is Primed by a Nick at the Chromosomal Target Site: a Mechanism for Non-LTR Retrotransposition, Cell, 1993, vol. 72, pp. 595-605.Google Scholar
  27. 27.
    Petrov, D.A., Lozovskaya, E.R., and Hartl, D.L., High Intrinsic Rate of DNA Loss in Drosophila, Nature, 1996, vol. 384, no. 6607, pp. 346-349.Google Scholar
  28. 28.
    Capy, P., Perspectives: Evolution. Is Bigger Better in Cricket? [comment], Science, 2000, vol. 287, no. 5455, pp. 985-986.Google Scholar
  29. 29.
    Petrov, D.A. et al., Evidence for DNA Loss as a Determinant of Genome Size, Science, 2000, vol. 287, pp. 1060-1062.Google Scholar
  30. 30.
    Champion, S. et al., Characterization of the Reverse Transcriptase of 1731, a Drosophila melanogaster Retrotransposon, Eur. J. Biochem., 1992, vol. 209, no. 2, pp. 523-531.Google Scholar
  31. 31.
    Shiba, T. and Saigo, K., Retrovirus-like Particles Containing RNA Homologous to the Transposable Element copia in Drosophila melanogaster, Nature, 1983, vol. 302, no. 5904, pp. 119-124.Google Scholar
  32. 32.
    McClure, M.A., Vasi, T.K., and Fitch, W.M., Comparative Analysis of Multiple Protein-sequence Alignment Methods, Mol. Biol. Evol., 1994, vol. 11, pp. 571-592.Google Scholar
  33. 33.
    Shigenobu, S. et al., Genome Sequence of the Endocellular Bacterial Symbiont of Aphids Buchnera sp. APS, Nature, 2000, vol. 407, no. 6800, pp. 81-86.Google Scholar
  34. 34.
    Kurland, C.G. and Andersson, S.G., Origin and Evolution of the Mitochondrial Proteome, Microbiol. Mol. Biol. Rev., 2000, vol. 64, no. 4, pp. 786-820.Google Scholar
  35. 35.
    Brennicke, A. et al., The Mitochondrial Genome on Its Way to the Nucleus: Different Stages of Gene Transfer in Higher Plants, FEBS Lett., 1993, vol. 325, no. 1–2, pp. 140-145.Google Scholar
  36. 36.
    Harington, A. and Thornley, A.L., Biochemical and Genetic Consequences of Gene Transfer from Endosymbiont to Host Genome, J. Mol. Evol., 1982, vol. 18, no. 5, pp. 287-292.Google Scholar
  37. 37.
    Jordan, I.K. and McDonald, J.F., Phylogenetic Perspective Reveals Abundant Ty1/Ty2 Hybrid Elements in the Saccharomyces cerevisiae Genome (Letter), Mol. Biol. Evol., 1999, vol. 16(3), pp. 419-422.Google Scholar
  38. 38.
    Arkhipova, I. and Meselson, M., Transposable Elements in Sexual and Ancient Asexual Taxa, Proc. Natl. Acad. Sci. USA, 2000, vol. 97, no. 26, pp. 14473-14477.Google Scholar
  39. 39.
    Wright, S. and Finnegan, D., Genome Evolution: Sex and the Transposable Element, Curr. Biol., 2001, vol. 11, no. 8, pp. R296-R299.Google Scholar
  40. 40.
    Zeyl, C., Bell, G., and Green, D.M., Sex and the Spread of Retrotransposon Ty3 in Experimental Populations of Saccharomyces cerevisiae, Genetics, 1996, vol. 143, no. 4, pp. 1567-1577.Google Scholar
  41. 41.
    Varmus, H. and Brown, P., Retroviruses, in Mobile DNA, Berg, D.E. and Howe, M.M., Eds., Washington, DC: American Society for Microbiology, 1989, pp. 53-108.Google Scholar
  42. 42.
    Brunet, F. et al., Do Deletions of the Mos1-like Elements Occur Randomly in the Drosophilidae Family?, J. Mol. Evol., 2002, vol. 54, pp. 227-234.Google Scholar
  43. 43.
    Rubin, E. and Levy, A.A., Abortive Gap Repair: Underlying Mechanism for Ds Element Formation, Mol. Cell. Biol., 1997, vol. 17, no. 11, pp. 6294-6302.Google Scholar
  44. 44.
    Mammano, F. et al., Role of the Major Homology Region of Human Immunodeficiency Virus Type 1 in Virion Morphogenesis, J. Virol., 1994, vol. 68, pp. 4927-4936.Google Scholar
  45. 45.
    Pardue, M.-L. et al., Evolutionary Links between Telomeres and Transposable Elements, Genetica, 1997, vol. 100, pp. 73-84.Google Scholar
  46. 46.
    Covey, S.N., Amino Acid Sequence Homology in gag Region of Reverse Transcribing Elements and the Coat Protein Gene of Cauliflower Mosaic Virus, Nucleic Acids Res., 1986, vol. 14, pp. 623-633.Google Scholar
  47. 47.
    Yang, J., Malik, H.S., and Eickbush, T.H., Identification of the Endonuclease Domain Encoded by R2 and Other Site-specific, Non-long Terminal Repeat Retrotransposable Elements, Proc. Natl. Acad. Sci. USA, 1999, vol. 96, no. 14, pp. 7847-7852.Google Scholar

Copyright information

© MAIK "Nauka/Interperiodica" 2002

Authors and Affiliations

  • P. Capy
    • 1
  • C. Maisonhaute
    • 1
  1. 1.Laboratoire Populations, Génétique et EvolutionGif-sur-Yvette, CedexFrance

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