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Horizontal transfer of P elements and other short inverted repeat transposons

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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.

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References

  • 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 

  • Anxolabéhère, D. & G. Périquet, 1987. P-homologous sequences in Diptera are not restricted to the Drosophilidae family. Genet. Ibér. 39: 211–222.

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • Emmons, S. W., L. Yesner, K. S. Ruan & D. Katzenberg, 1983. Evidence for a transposon in Caenorhabditis elegans. Cell 32: 55–65.

    Google Scholar 

  • 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 

  • Fedoroff, N., S. Wessler & M. Shure, 1983. Isolation of the transposable maize controlling elements Ac and Ds. Cell 35: 235–242.

    Google Scholar 

  • Finnegan, D. J., 1989. Eukaryotic transposable elements and genome evolution. Trends in Genetics 5: 103–107.

    Google Scholar 

  • Flavell, A. J., 1992. Ty1-copia group retrotransposons and the evolution of retroelements in the eukaryotes. Genetica 86: 203–214.

    Google Scholar 

  • Fontdevila, A., 1992. Genetic instability and rapid speciation: are they coupled? Genetica 86: 247–258.

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • Grandbastien, M.-A., 1992. Retroelements in higher plants. Trends in Genetics 8: 103–108.

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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 

  • Hickey, D. A., 1992. Evolutionary dynamics of transposable elements in prokaryotes and eukaryotes. Genetica 86: 269–274.

    Google Scholar 

  • 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 

  • 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 

  • Kaplan, N., T. Darden & C. Langley, 1985. Evolution and extinction of transposable elements in Mendelian populations. Genetics 109: 459–480.

    Google Scholar 

  • 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 

  • 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 

  • Kidwell, M. G., 1983. Evolution of hybrid dysgenesis determinants in Drosophila melanogaster. Proc. Natl. Acad. Sci. U.S.A. 80: 1655–1659.

    Google Scholar 

  • Kidwell, M. G. & J. F. Kidwell, 1975. Cytoplasm-chromosome interactions in Drosophila melanogaster. Nature 253: 755–759.

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • Maruyama, K. & D. L. Hartl, 1991a. Evolution of the transposable element mariner in Drosophila species. Genetics 128: 319–329.

    Google Scholar 

  • 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 

  • McClintock, B., 1948. Mutable loci in maize. Carnegie Inst. Wash. Yrbk. 47: 155–169.

    Google Scholar 

  • McClintock, B., 1984. The significance of responses of the genome to challenge. Science 226: 792–801.

    Google Scholar 

  • McDonald, J. F., 1990. Macroevolution and retroviral elements. BioScience 40: 183–191.

    Google Scholar 

  • 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).

  • Miller, D. W. & L. K. Miller, 1982. A virus mutant with an insertion of a copia-like element. Nature 299: 562–564.

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • Pohlman, R. F., N. V. Federoff & J. Messing, 1984. The nucleotide sequence of the maize controlling element Activator. Cell 37: 635–643.

    Google Scholar 

  • 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 

  • Rio, D. C., 1990. Molecular mechanisms regulating Drosophila P element transposition. Ann. Rev. Genet. 24: 543–578.

    Google Scholar 

  • 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 

  • 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 

  • Rozenzweig, B., L. W. Liao & D. Hirsh, 1983. Sequence of the C. elegans transposable element Tc1. Nucl. Acids Res. 11: 4201–4209.

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • Sved, J. A., 1973. Short term heritable changes affecting viability in Drosophila melanogaster. Nature 241: 453–454.

    Google Scholar 

  • Syvanen, M. 1984. The evolutionary implications of mobile genetic elements. Ann. Rev. Genet. 18: 271–293.

    Google Scholar 

  • 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 

  • 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 

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Kidwell, M.G. Horizontal transfer of P elements and other short inverted repeat transposons. Genetica 86, 275–286 (1992). https://doi.org/10.1007/BF00133726

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