Genetica

, Volume 86, Issue 1–3, pp 275–286

Horizontal transfer of P elements and other short inverted repeat transposons

  • M. G. Kidwell
Article

Abstract

Evidence for horizontal transfer of the P family of transposable elements in the genus Drosophila is reviewed and evaluated, along with observations consistent with the recent invasion of Drosophila melanogaster by these elements. Some other examples of horizontal transfer involving other groups of transposable elements having short inverted terminal repeats are also briefly described. The sequential mechanistic steps likely to be involved in a horizontal transfer event are explored, including the requirement for suitable interspecific vectors or carriers. Finally, the frequency and significance of horizontal transfer of transposable elements are briefly discussed within an evolutionary framework.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Anxolabéhère, D., M. G. Kidwell & G. Périquet, 1988. Molecular characteristics of diverse populations are consistent with the hypothesis of a recent invasion of Drosophila melanogaster by mobile P elements. Mol. Biol. Evol. 5: 252–269.Google Scholar
  2. Anxolabéhère, D. & G. Périquet, 1987. P-homologous sequences in Diptera are not restricted to the Drosophilidae family. Genet. Ibér. 39: 211–222.Google Scholar
  3. Behrens, U., N. Federoff, A. Laird, M. Muller-Neumann, P. Starlinger & J. Yoder, 1984. Cloning of the Zea mays controlling element Ac from the wx-m7 allele. Mol. Gen. Genet. 194: 346–347.Google Scholar
  4. Beverly, S. M. & A. C. Wilson, 1984. Molecular evolution in Drosophila and the higher Diptera. II. A time scale for fly evolution. J. Mol. Evol. 21: 1–13.Google Scholar
  5. Bhattacharyya, M. K., A. M. Smith, T. H. N. Ellis, C. Hedley & C. Martin, 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: 115–122.Google Scholar
  6. Blackman, R., & W. Gelbart, 1989. The transposable element hobo of Drosophila melanogaster, pp. 523–530 in Mobile DNA, edited by D. E. Berg and M. Howe, American Society of Microbiology, Washington D.C.Google Scholar
  7. Bregliano, J. C. & M. G. Kidwell, 1983. Hybrid dysgenesis determinants, pp. 363–410, in Mobile Genetic Elements, edited by J. A. Shapiro, Academic Press, New York.Google Scholar
  8. Brezinsky, L., G. V. L. Wang, T. Humphreys & J. Hunt, 1990. The transposable element Uhu from Hawaiian Drosophila — member of the widely dispersed class of Tc1-like transposons. Nucl. Acids Res. 18: 2053–2059.Google Scholar
  9. Brierly, H. L. & S. S. Potter, 1985. Distinct characteristics of loop sequences of two Drosophila foldback transposable elements. Nucleic Acid Res. 13: 485–500.Google Scholar
  10. Brookfield, J. F. Y., E. Montgomery & C. Langley, 1984. Apparent absence of transposable elements related to the P elements of D. melanogaster in other species of Drosophila. Nature 310: 330–332.Google Scholar
  11. Bucheton, A., R. Paro, H. M. Sang, A. Pelisson, D. J. Finnegan, 1984. The molecular basis of I-R hybrid dysgenesis:identification, cloning and properties of the I factor. Cell 38: 153–163.Google Scholar
  12. Bucheton, A., M. Simonelig, C. Vaury & M. Crozatier, 1986. Sequences similar to the I transposable element involved in I-R hybrid dysgenesis in D. melanogaster occur in other Drosophila species. Nature 322: 650–652.Google Scholar
  13. Calvi, B. R., T. J. Hong, S. D. Findley & W. M. Gelbart, 1991. Evidence for a common evolutionary origin of inverted repeat transposons in Drosophila and plants: hobo, Activator and Tam3. Cell 66: 465–471.Google Scholar
  14. Capy, P., J. R. David & D. L. Hartl, 1992. Evolution of the transposable element mariner in the Drosophila melanogaster species subgroup. Genetica 86: 37–46.Google Scholar
  15. Davila-Aponte, J. A., V. A. R. Huss, M. L. Sogin & T. R. Cech, 1991. A self-splicing group I intron in the nuclear pre-rRNA of the green alga, Ankistrodesmus stipitatus. Nucleic Acids Res. 19: 4429–4436.Google Scholar
  16. Daniels, S. B., A. Chovnick & I. A. Boussy, 1990a. Distribution of hobo transposable elements in the genus Drosophila. Mol. Biol. Evol. 7: 589–606.Google Scholar
  17. Daniels, S. B., K. R. Peterson, L. D. Strausbaugh, M. G. Kidwell & A. Chovnick, 1990b. Evidence for horizontal transmission of the P transposable element between Drosophila species. Genetics 124: 339–355.Google Scholar
  18. Daniels, S. B. & L. D. Strausbaugh, 1986. The distribution of P element sequences in Drosophila: the willistoni and saltans species groups. J. Mol. Evol. 23: 138–148.Google Scholar
  19. Doolittle, R. F., D. F. Feng, M. S. Johnson & M. A. McClure, 1989. Origins and evolutionary relationships of retroviruses. Quarterly Rev. Biol. 64: 1–29.Google Scholar
  20. Doolittle, R. F., D. F. Feng, K. L. Anderson & M. R. Alberro, 1990. A naturally occurring horizontal gene transfer from a eukaryote to a prokaryote. J. Mol. Evol. 31: 383–388.Google Scholar
  21. Emmons, S. W., L. Yesner, K. S. Ruan & D. Katzenberg, 1983. Evidence for a transposon in Caenorhabditis elegans. Cell 32: 55–65.Google Scholar
  22. Engels, W. R., 1989. P elements in Drosophila, pp. 437–484 in Mobile DNA, edited by D. E. Berg and M. Howe, American Society of Microbiology, Washington D.C.Google Scholar
  23. Fedoroff, N., S. Wessler & M. Shure, 1983. Isolation of the transposable maize controlling elements Ac and Ds. Cell 35: 235–242.Google Scholar
  24. Finnegan, D. J., 1989. Eukaryotic transposable elements and genome evolution. Trends in Genetics 5: 103–107.Google Scholar
  25. Flavell, A. J., 1992. Ty1-copia group retrotransposons and the evolution of retroelements in the eukaryotes. Genetica 86: 203–214.Google Scholar
  26. Fontdevila, A., 1992. Genetic instability and rapid speciation: are they coupled? Genetica 86: 247–258.Google Scholar
  27. Fraser, M. J., 1986. Transposon-mediated mutagenesis of baculoviruses: transposon shuttling and implications for speciation. Symposium: Genetics in Entomology. Ann. Entomol. Soc. Amer. 79: 773–783.Google Scholar
  28. Gloor, G. B., N. A. Nassif, D. M. Johnson Schlitz, C. R. Preston & W. R. Engels, 1991. Targeted gene replacement in Drosophila via P element-induced gap repair. Science 253: 1110–1117.Google Scholar
  29. Good, A. G., G. Meister, H. Brock, T. A. Grigliatti, D. Hickey, 1989. Rapid spread of transposable P elements in experimental populations of Drosophila melanogaster. Genetics 122: 387–396.Google Scholar
  30. Grandbastien, M.-A., 1992. Retroelements in higher plants. Trends in Genetics 8: 103–108.Google Scholar
  31. Hagemann, S., W. J. Miller & W. Pinsker, 1990. P-related sequences in Drosophila bifasciata: a molecular clue to the understanding of P-element evolution in the genus Drosophila. J. Mol. Evol. 31: 478–484.Google Scholar
  32. Harris, L. J., D. L. Baille & A. M. Rose, 1988. Sequence identity between an inverted repeat family of transposable elements in Drosophila and Caenorhabditis. Nucl. Acids Res. 16: 5991–5999.Google Scholar
  33. Hehl, R., W. K. F. Nacken, A. Krause, H. Saedler & H. Sommer, 1991. Structural analysis of Tam3, a transposable element from Antirrhinum majus reveals homologies to the Ac element from maize. Plant Mol. Biol. 16: 369–371.Google Scholar
  34. Herrmann, A., W. Schultz & K. Hahlbrock, 1988. Two alleles of the single copy chalcone synthetase gene in parsley differ by a transposon-like element. Mol. Gen. Genet. 212: 93–98.Google Scholar
  35. Hickey, D. A., 1992. Evolutionary dynamics of transposable elements in prokaryotes and eukaryotes. Genetica 86: 269–274.Google Scholar
  36. Houck, M. A., J. B. Clark, K. R. Peterson & M. G. Kidwell, 1991. Possible horizontal transfer of Drosophila genes by the mite Proctolaelaps regalis. Science 253: 1125–1129.Google Scholar
  37. Jacobson, J. W., M. M. Medhora, D. L. Hartl, 1986. Molecular structure of a somatically unstable transposable element. Proc. Natl. Acad. Sci. USA 83: 8684–8688.Google Scholar
  38. Kaplan, N., T. Darden & C. Langley, 1985. Evolution and extinction of transposable elements in Mendelian populations. Genetics 109: 459–480.Google Scholar
  39. Kay, B. K. & I. B. Dawid, 1983. The 1723 element: a long, homogeneous, highly repeated DNA unit interspersed in the genome of Xenopus laevis. J. Mol. Biol. 170: 583–596.Google Scholar
  40. Kidwell, M. G., 1979. Hybrid dysgenesis in Drosophila melanogaster: The relationship between the P-M and I-R interaction systems. Genet. Res. 33: 105–117.Google Scholar
  41. Kidwell, M. G., 1983. Evolution of hybrid dysgenesis determinants in Drosophila melanogaster. Proc. Natl. Acad. Sci. U.S.A. 80: 1655–1659.Google Scholar
  42. Kidwell, M. G. & J. F. Kidwell, 1975. Cytoplasm-chromosome interactions in Drosophila melanogaster. Nature 253: 755–759.Google Scholar
  43. Kidwell, M. G., J. F. Kidwell & J. A. Sved, 1977. Hybrid dysgenesis in Drosophila melanogaster: a syndrome of aberrant traits including mutation, sterility, and male recombination. Genetics 36: 813–833.Google Scholar
  44. Kidwell, M. G., K. Kimura & D. M. Black, 1988. Evolution of hybrid dysgenesis potential following P element contamination in Drosophila melanogaster. Genetics 119: 815–828.Google Scholar
  45. Kidwell, M. G., J. B. Novy & S. M. Feeley, 1981. Rapid unidirectional change of hybrid dysgenesis potential in Drosophila. J. Heredity 72: 32–38.Google Scholar
  46. Kidwell, M. G., T. Frydryk & J. B. Novy, 1983. The hybrid dysgenesis potential of Drosophila melanogaster strains of diverse temporal and geographical natural origins. 55: 97–100.Google Scholar
  47. Kiyasu, P. K. & M. G. Kidwell, 1984. Hybrid dysgenesis in Drosophila melanogaster: the evolution of mixed P and M populations maintained at high temperature. Genet. Res. 44: 251–259.Google Scholar
  48. Lansman, R. A., S. N. Stacy, T. A. Grigliatti & H. W. Brock, 1985. Sequences homologous to the P mobile element of Drosophila melanogaster are widely distributed in the subgenus Sophophora. Nature 318: 561–563.Google Scholar
  49. Lidholm, D.-A., G. H. Gudmundsson & H. G. Boman, 1991. A highly repetitive, mariner-like element in the genome of Hyalophora cecropia. J. Biol. Chem. 266: 11518–11521.Google Scholar
  50. Maruyama, K. & D. L. Hartl, 1991a. Evolution of the transposable element mariner in Drosophila species. Genetics 128: 319–329.Google Scholar
  51. Maryama, K. & D. L. Hartl, 1991b. Interspecific transfer of the transposable element mariner between Drosophila and Zaprionus. J. Mol. Evol. 33: 514–524.Google Scholar
  52. McClintock, B., 1948. Mutable loci in maize. Carnegie Inst. Wash. Yrbk. 47: 155–169.Google Scholar
  53. McClintock, B., 1984. The significance of responses of the genome to challenge. Science 226: 792–801.Google Scholar
  54. McDonald, J. F., 1990. Macroevolution and retroviral elements. BioScience 40: 183–191.Google Scholar
  55. Miller, W. J., S. Hagemann, E. Reiter & W. Pinsker, 1992. P element homologous sequences are tandemly repeated in the genome of Drosophila guanche. Proc. Natl. Acad. Sci. USA 89: (in press).Google Scholar
  56. Miller, D. W. & L. K. Miller, 1982. A virus mutant with an insertion of a copia-like element. Nature 299: 562–564.Google Scholar
  57. Mizrokhi, L. J. & A. M. Mazo, 1990. Evidence for horizontal transmission of the mobile element jockey between distant Drosophila species. Proc. Natl. Acad. Sci. U.S.A. 87: 9216–9220.Google Scholar
  58. Muller-Neumann, M., J. I. Yoder & P. Starlinger, 1984. The DNA sequence of the transposable element Ac of Zea mays L. Mol. Gen. Genet. 198: 19–24.Google Scholar
  59. O'Brochta, D. A. & A. M. Handler, 1988. Mobility of P elements in Drosophilids and nondrosophilids. Proc. Natl. Acad. Sci. U.S.A. 85: 6052–6056.Google Scholar
  60. O'Brochta, D. A., S. P. Gomez & A. M. Handler, 1991. P element excision in Drosophila melanogaster and related drosophilids. Mol. Gen. Genet. 225: 387–394.Google Scholar
  61. O'Hare, K. & G. M. Rubin, 1983. Structure of P transposable elements and their sites of insertion and excision in the Drosophila melanogaster genome. Cell 34: 25–35.Google Scholar
  62. Paricio, N., M. Pérez-Alonso, M. J. Martinez-Sebastian & R. deFrutos, 1991. P sequences of Drosophila subobscura lack exon 3 and may encode a 66 kd repressor-like protein. Nucleic Acids Res. 19: 6713–6718.Google Scholar
  63. Picard, G., 1971. Uh cas de sterilite femelle, chez Drosophila melanogaster, lie a un agent transmis maternellement. Comptes Rendues Acad. Sci. Paris 272; 2484–2487.Google Scholar
  64. Pohlman, R. F., N. V. Federoff & J. Messing, 1984. The nucleotide sequence of the maize controlling element Activator. Cell 37: 635–643.Google Scholar
  65. Preston, C. R. & W. R. Engels, 1989. Spread of P transposable elements in inbred lines of Drosophila melanogaster, pp. 71–85, in Progress in Nucleic Acid Research and Molecular Biology: Hollaender Symposium Proceedings, edited by W. Cohn and K. Moldave. Academic Press, New York.Google Scholar
  66. Rio, D. C., 1990. Molecular mechanisms regulating Drosophila P element transposition. Ann. Rev. Genet. 24: 543–578.Google Scholar
  67. Rio, D. C., G. Barnes, F. A. Laski, J. Rine & G. M. Rubin, 1988. Evidence for P element transposase activity in mammalian cells and yeast. J. Mol. Biol. 200: 411–415.Google Scholar
  68. Rio, D. C. & G. M. Rubin, 1988. Identification and purification of a Drosophila protein that binds to the terminal 31-basepair inverted repeats of the P transposable element. Proc. Natl. Acad. Sci. USA 85: 8925–8929.Google Scholar
  69. Rozenzweig, B., L. W. Liao & D. Hirsh, 1983. Sequence of the C. elegans transposable element Tc1. Nucl. Acids Res. 11: 4201–4209.Google Scholar
  70. Schwartz, D. and E. Dennis, 1986. Transposase activity of the Ac controlling element in maize is regulated by its degree of methylation. Mol. Gen. Genet. 205: 476–482.Google Scholar
  71. Simonelig, M. & A. Anxolabéhère, 1991. A P element of Scaptomyza pallida is active in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 88: 6102–6106.Google Scholar
  72. Sommer, H., R. Carpenter, B. J. Harrison & H. Saedler, 1985. The transposable element Tam3 of Antirrhinum majus generates a novel type of sequence alteration upon excision. Mol. Gen. Genet. 199: 225–231.Google Scholar
  73. Stacey, S. N., R. A. Lansman, H. W. Brock & T. A. Grigliatti, 1986. Distribution and conservation of mobile elements in the genus Drosophila. Mol. Biol. Evol. 3: 522–534.Google Scholar
  74. Streck, R. D., J. E. MacGaffey & S. K. Beckendorf, 1986. The structure of hobo transposable elements and their insertion sites. EMBO J. 5: 3615–3623.Google Scholar
  75. Sved, J. A., 1973. Short term heritable changes affecting viability in Drosophila melanogaster. Nature 241: 453–454.Google Scholar
  76. Syvanen, M. 1984. The evolutionary implications of mobile genetic elements. Ann. Rev. Genet. 18: 271–293.Google Scholar
  77. Throckmorton, L. H., 1975. The phylogeny, ecology and geography of Drosophila, pp. 421–469 in Handbook of Genetics, Vol. 3., edited by R. C. King Plenum Press, New York.Google Scholar
  78. Tsubota, S. I. & H. Dang-Vu, 1991. Capture of flanking DNA by a P element in Drosophila melanogaster: Creation of a transposable element. Proc. Natl. Acad. Sci. U.S.A. 88: 693–697.Google Scholar

Copyright information

© Kluwer Academic Publishers 1992

Authors and Affiliations

  • M. G. Kidwell
    • 1
  1. 1.Department of Ecology and Evolutionary BiologyUniversity of ArizonaTucsonUSA

Personalised recommendations