Skip to main content
NCBI home page
Genetics logoLink to Genetics
. 1990 Feb;124(2):339–355. doi: 10.1093/genetics/124.2.339

Evidence for Horizontal Transmission of the P Transposable Element between Drosophila Species

S B Daniels 1, K R Peterson 1, L D Strausbaugh 1, M G Kidwell 1, A Chovnick 1
PMCID: PMC1203926  PMID: 2155157

Abstract

Several studies have suggested that P elements have rapidly spread through natural populations of Drosophila melanogaster within the last four decades. This observation, together with the observation that P elements are absent in the other species of the melanogaster subgroup, has lead to the suggestion that P elements may have entered the D. melanogaster genome by horizontal transmission from some more distantly related species. In an effort to identify the potential donor in the horizontal transfer event, we have undertaken an extensive survey of the genus Drosophila using Southern blot analysis. The results showed that P-homologous sequences are essentially confined to the subgenus Sophophora. The strongest P hybridization occurs in species from the closely related willistoni and saltans groups. The D. melanogaster P element is most similar to the elements from the willistoni group. A wild-derived strain of D. willistoni was subsequently selected for a more comprehensive molecular examination. As part of the analysis, a complete P element was cloned and sequenced from this line. Its nucleotide sequence was found to be identical to the D. melanogaster canonical P, with the exception of a single base substitution at position 32. When the cloned element was injected into D. melanogaster embryos, it was able to both promote transposition of a coinjected marked transposon and induce singed-weak mutability, thus demonstrating its ability to function as an autonomous element. The results of this study suggest that D. willistoni may have served as the donor species in the horizontal transfer of P elements to D. melanogaster.

Full Text

The Full Text of this article is available as a PDF (6.6 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anxolabéhère D., Kidwell M. G., Periquet G. Molecular characteristics of diverse populations are consistent with the hypothesis of a recent invasion of Drosophila melanogaster by mobile P elements. Mol Biol Evol. 1988 May;5(3):252–269. doi: 10.1093/oxfordjournals.molbev.a040491. [DOI] [PubMed] [Google Scholar]
  2. Aviv H., Leder P. Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose. Proc Natl Acad Sci U S A. 1972 Jun;69(6):1408–1412. doi: 10.1073/pnas.69.6.1408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Beverley S. M., Wilson A. C. Molecular evolution in Drosophila and the higher Diptera II. A time scale for fly evolution. J Mol Evol. 1984;21(1):1–13. doi: 10.1007/BF02100622. [DOI] [PubMed] [Google Scholar]
  4. Bingham P. M., Kidwell M. G., Rubin G. M. The molecular basis of P-M hybrid dysgenesis: the role of the P element, a P-strain-specific transposon family. Cell. 1982 Jul;29(3):995–1004. doi: 10.1016/0092-8674(82)90463-9. [DOI] [PubMed] [Google Scholar]
  5. Black D. M., Jackson M. S., Kidwell M. G., Dover G. A. KP elements repress P-induced hybrid dysgenesis in Drosophila melanogaster. EMBO J. 1987 Dec 20;6(13):4125–4135. doi: 10.1002/j.1460-2075.1987.tb02758.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brookfield J. F., Montgomery E., Langley C. H. Apparent absence of transposable elements related to the P elements of D. melanogaster in other species of Drosophila. 1984 Jul 26-Aug 1Nature. 310(5975):330–332. doi: 10.1038/310330a0. [DOI] [PubMed] [Google Scholar]
  7. Daniels S. B., Strausbaugh L. D., Ehrman L., Armstrong R. Sequences homologous to P elements occur in Drosophila paulistorum. Proc Natl Acad Sci U S A. 1984 Nov;81(21):6794–6797. doi: 10.1073/pnas.81.21.6794. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Daniels S. B., Strausbaugh L. D. The distribution of P-element sequences in Drosophila: the willistoni and saltans species groups. J Mol Evol. 1986;23(2):138–148. doi: 10.1007/BF02099908. [DOI] [PubMed] [Google Scholar]
  9. Dente L., Cesareni G., Cortese R. pEMBL: a new family of single stranded plasmids. Nucleic Acids Res. 1983 Mar 25;11(6):1645–1655. doi: 10.1093/nar/11.6.1645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Engels W. R. The P family of transposable elements in Drosophila. Annu Rev Genet. 1983;17:315–344. doi: 10.1146/annurev.ge.17.120183.001531. [DOI] [PubMed] [Google Scholar]
  11. KISSANE J. M., ROBINS E. The fluorometric measurement of deoxyribonucleic acid in animal tissues with special reference to the central nervous system. J Biol Chem. 1958 Jul;233(1):184–188. [PubMed] [Google Scholar]
  12. Kaplan N., Darden T., Langley C. H. Evolution and extinction of transposable elements in Mendelian populations. Genetics. 1985 Feb;109(2):459–480. doi: 10.1093/genetics/109.2.459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Krawetz S. A., States J. C., Dixon G. H. Isolation and fractionation of total nucleic acids from tissues and cells. J Biochem Biophys Methods. 1986 Jan;12(1-2):29–36. doi: 10.1016/0165-022x(86)90048-5. [DOI] [PubMed] [Google Scholar]
  14. Lansman R. A., Shade R. O., Grigliatti T. A., Brock H. W. Evolution of P transposable elements: sequences of Drosophila nebulosa P elements. Proc Natl Acad Sci U S A. 1987 Sep;84(18):6491–6495. doi: 10.1073/pnas.84.18.6491. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Laski F. A., Rio D. C., Rubin G. M. Tissue specificity of Drosophila P element transposition is regulated at the level of mRNA splicing. Cell. 1986 Jan 17;44(1):7–19. doi: 10.1016/0092-8674(86)90480-0. [DOI] [PubMed] [Google Scholar]
  16. Lewin R. Can genes jump between eukaryotic species? Science. 1982 Jul 2;217(4554):42–43. doi: 10.1126/science.7089540. [DOI] [PubMed] [Google Scholar]
  17. Lewin R. Fish to bacterium gene transfer. Science. 1985 Mar 1;227(4690):1020–1020. doi: 10.1126/science.227.4690.1020. [DOI] [PubMed] [Google Scholar]
  18. Miller D. W., Miller L. K. A virus mutant with an insertion of a copia-like transposable element. Nature. 1982 Oct 7;299(5883):562–564. doi: 10.1038/299562a0. [DOI] [PubMed] [Google Scholar]
  19. O'Hare K., Rubin G. M. Structures of P transposable elements and their sites of insertion and excision in the Drosophila melanogaster genome. Cell. 1983 Aug;34(1):25–35. doi: 10.1016/0092-8674(83)90133-2. [DOI] [PubMed] [Google Scholar]
  20. O'brochta D. A., Handler A. M. Mobility of P elements in drosophilids and nondrosophilids. Proc Natl Acad Sci U S A. 1988 Aug;85(16):6052–6056. doi: 10.1073/pnas.85.16.6052. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Rio D. C., Laski F. A., Rubin G. M. Identification and immunochemical analysis of biologically active Drosophila P element transposase. Cell. 1986 Jan 17;44(1):21–32. doi: 10.1016/0092-8674(86)90481-2. [DOI] [PubMed] [Google Scholar]
  22. Rio D. C., Rubin G. M. Identification and purification of a Drosophila protein that binds to the terminal 31-base-pair inverted repeats of the P transposable element. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8929–8933. doi: 10.1073/pnas.85.23.8929. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Robertson H. M., Preston C. R., Phillis R. W., Johnson-Schlitz D. M., Benz W. K., Engels W. R. A stable genomic source of P element transposase in Drosophila melanogaster. Genetics. 1988 Mar;118(3):461–470. doi: 10.1093/genetics/118.3.461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Roiha H., Rubin G. M., O'Hare K. P element insertions and rearrangements at the singed locus of Drosophila melanogaster. Genetics. 1988 May;119(1):75–83. doi: 10.1093/genetics/119.1.75. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Rubin G. M., Spradling A. C. Vectors for P element-mediated gene transfer in Drosophila. Nucleic Acids Res. 1983 Sep 24;11(18):6341–6351. doi: 10.1093/nar/11.18.6341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Rushlow C. A., Bender W., Chovnick A. Studies on the mechanism of heterochromatic position effect at the rosy locus of Drosophila melanogaster. Genetics. 1984 Nov;108(3):603–615. doi: 10.1093/genetics/108.3.603. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Scavarda N. J., Hartl D. L. Interspecific DNA transformation in Drosophila. Proc Natl Acad Sci U S A. 1984 Dec;81(23):7515–7519. doi: 10.1073/pnas.81.23.7515. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Spradling A. C., Rubin G. M. Transposition of cloned P elements into Drosophila germ line chromosomes. Science. 1982 Oct 22;218(4570):341–347. doi: 10.1126/science.6289435. [DOI] [PubMed] [Google Scholar]
  29. Stacey S. N., Lansman R. A., Brock H. W., Grigliatti T. A. Distribution and conservation of mobile elements in the genus Drosophila. Mol Biol Evol. 1986 Nov;3(6):522–534. doi: 10.1093/oxfordjournals.molbev.a040413. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES