Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1989 Nov;86(22):8887–8891. doi: 10.1073/pnas.86.22.8887

A long interspersed repetitive element--the I factor of Drosophila teissieri--is able to transpose in different Drosophila species.

P Abad 1, C Vaury 1, A Pélisson 1, M C Chaboissier 1, I Busseau 1, A Bucheton 1
PMCID: PMC298395  PMID: 2554335

Abstract

Long interspersed repetitive elements (LINEs) are transposable elements present in many species. In mammals they are difficult to study because most of them are defective and their transposition frequency is low. The I factor of Drosophila melanogaster is a LINE element that is particularly interesting because its transposition occurs at high frequency during I-R hybrid dysgenesis. This phenomenon occurs when males from the class of inducer strains are crossed with females from the class of reactive strains. Inducer strains contain several complete 5.4-kilobase I factors at various sites on the chromosomal arms. Reactive strains are devoid of complete I factors. Many results indicate that active I factors have invaded the D. melanogaster genome recently. To study the evolutionary history of I elements, we have cloned and sequenced a potentially active I factor from Drosophila teissieri. It is flanked by a target-site duplication and terminates at the 3' end by tandem repeats of the sequence TAA. When introduced into the germ line of a reactive strain of D. melanogaster by P element-mediated transformation, it is able to transpose and induces hybrid dysgenesis. This strengthens the hypothesis of a recent reinvasion of the D. melanogaster genome by active I factors giving rise to the inducer strains. They could have originated by horizontal transfer from another species. Such events also could occur for other LINE elements and might explain the spread of new variants in mammalian genomes. Moreover, the results give a further insight into I factor functional organization.

Full text

PDF
8889

Images in this article

Selected References

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

  1. Appleyard R K. Segregation of New Lysogenic Types during Growth of a Doubly Lysogenic Strain Derived from Escherichia Coli K12. Genetics. 1954 Jul;39(4):440–452. doi: 10.1093/genetics/39.4.440. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bucheton A., Lavige J. M., Picard G., L'Heritier P. Non-mendelian female sterility in Drosophila melanogaster: quantitative variations in the efficiency of inducer and reactive strains. Heredity (Edinb) 1976 Jun;36(3):305–314. doi: 10.1038/hdy.1976.38. [DOI] [PubMed] [Google Scholar]
  3. Bucheton A., Paro R., Sang H. M., Pelisson A., Finnegan D. J. The molecular basis of I-R hybrid dysgenesis in Drosophila melanogaster: identification, cloning, and properties of the I factor. Cell. 1984 Aug;38(1):153–163. doi: 10.1016/0092-8674(84)90536-1. [DOI] [PubMed] [Google Scholar]
  4. Caccone A., Amato G. D., Powell J. R. Rates and patterns of scnDNA and mtDNA divergence within the Drosophila melanogaster subgroup. Genetics. 1988 Apr;118(4):671–683. doi: 10.1093/genetics/118.4.671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Crozatier M., Vaury C., Busseau I., Pelisson A., Bucheton A. Structure and genomic organization of I elements involved in I-R hybrid dysgenesis in Drosophila melanogaster. Nucleic Acids Res. 1988 Oct 11;16(19):9199–9213. doi: 10.1093/nar/16.19.9199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. D'Ambrosio E., Waitzkin S. D., Witney F. R., Salemme A., Furano A. V. Structure of the highly repeated, long interspersed DNA family (LINE or L1Rn) of the rat. Mol Cell Biol. 1986 Feb;6(2):411–424. doi: 10.1128/mcb.6.2.411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Di Nocera P. P., Casari G. Related polypeptides are encoded by Drosophila F elements, I factors, and mammalian L1 sequences. Proc Natl Acad Sci U S A. 1987 Aug;84(16):5843–5847. doi: 10.1073/pnas.84.16.5843. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Di Nocera P. P. Close relationship between non-viral retroposons in Drosophila melanogaster. Nucleic Acids Res. 1988 May 11;16(9):4041–4052. doi: 10.1093/nar/16.9.4041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fanning T. G., Singer M. F. LINE-1: a mammalian transposable element. Biochim Biophys Acta. 1987 Dec 8;910(3):203–212. doi: 10.1016/0167-4781(87)90112-6. [DOI] [PubMed] [Google Scholar]
  10. Fawcett D. H., Lister C. K., Kellett E., Finnegan D. J. Transposable elements controlling I-R hybrid dysgenesis in D. melanogaster are similar to mammalian LINEs. Cell. 1986 Dec 26;47(6):1007–1015. doi: 10.1016/0092-8674(86)90815-9. [DOI] [PubMed] [Google Scholar]
  11. Johnson M. S., McClure M. A., Feng D. F., Gray J., Doolittle R. F. Computer analysis of retroviral pol genes: assignment of enzymatic functions to specific sequences and homologies with nonviral enzymes. Proc Natl Acad Sci U S A. 1986 Oct;83(20):7648–7652. doi: 10.1073/pnas.83.20.7648. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Jubier-Maurin V., Wincker P., Cuny G., Roizès G. The relationships between the 5' end repeats and the largest members of the L1 interspersed repeated family in the mouse genome. Nucleic Acids Res. 1987 Sep 25;15(18):7395–7410. doi: 10.1093/nar/15.18.7395. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Karess R. E., Rubin G. M. Analysis of P transposable element functions in Drosophila. Cell. 1984 Aug;38(1):135–146. doi: 10.1016/0092-8674(84)90534-8. [DOI] [PubMed] [Google Scholar]
  14. Kazazian H. H., Jr, Wong C., Youssoufian H., Scott A. F., Phillips D. G., Antonarakis S. E. Haemophilia A resulting from de novo insertion of L1 sequences represents a novel mechanism for mutation in man. Nature. 1988 Mar 10;332(6160):164–166. doi: 10.1038/332164a0. [DOI] [PubMed] [Google Scholar]
  15. Kimmel B. E., ole-MoiYoi O. K., Young J. R. Ingi, a 5.2-kb dispersed sequence element from Trypanosoma brucei that carries half of a smaller mobile element at either end and has homology with mammalian LINEs. Mol Cell Biol. 1987 Apr;7(4):1465–1475. doi: 10.1128/mcb.7.4.1465. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Mizrokhi L. J., Georgieva S. G., Ilyin Y. V. jockey, a mobile Drosophila element similar to mammalian LINEs, is transcribed from the internal promoter by RNA polymerase II. Cell. 1988 Aug 26;54(5):685–691. doi: 10.1016/s0092-8674(88)80013-8. [DOI] [PubMed] [Google Scholar]
  17. Morse B., Rotherg P. G., South V. J., Spandorfer J. M., Astrin S. M. Insertional mutagenesis of the myc locus by a LINE-1 sequence in a human breast carcinoma. Nature. 1988 May 5;333(6168):87–90. doi: 10.1038/333087a0. [DOI] [PubMed] [Google Scholar]
  18. Picard G., Bregliano J. C., Bucheton A., Lavige J. M., Pelisson A., Kidwell M. G. Non-mendelian female sterility and hybrid dysgenesis in Drosophila melanogaster. Genet Res. 1978 Nov;32(3):275–287. doi: 10.1017/s0016672300018772. [DOI] [PubMed] [Google Scholar]
  19. Picard G. Non-mendelian female sterility in Drosophila melanogaster: hereditary transmission of I factor. Genetics. 1976 May;83(1):107–123. doi: 10.1093/genetics/83.1.107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Pritchard M. A., Dura J. M., Pélisson A., Bucheton A., Finnegan D. J. A cloned I-factor is fully functional in Drosophila melanogaster. Mol Gen Genet. 1988 Nov;214(3):533–540. doi: 10.1007/BF00330491. [DOI] [PubMed] [Google Scholar]
  21. Rubin G. M., Spradling A. C. Genetic transformation of Drosophila with transposable element vectors. Science. 1982 Oct 22;218(4570):348–353. doi: 10.1126/science.6289436. [DOI] [PubMed] [Google Scholar]
  22. Samson M. L., Wegnez M. The 5S ribosomal genes in the Drosophila melanogaster species subgroup. Nucleotide sequence of a 5S unit from Drosophila simulans and Drosophila teissieri. Nucleic Acids Res. 1984 Jan 25;12(2):1003–1014. doi: 10.1093/nar/12.2.1003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Scherer G., Telford J., Baldari C., Pirrotta V. Isolation of cloned genes differentially expressed at early and late stages of Drosophila embryonic development. Dev Biol. 1981 Sep;86(2):438–447. doi: 10.1016/0012-1606(81)90202-5. [DOI] [PubMed] [Google Scholar]
  24. Schwarz-Sommer Z., Leclercq L., Göbel E., Saedler H. Cin4, an insert altering the structure of the A1 gene in Zea mays, exhibits properties of nonviral retrotransposons. EMBO J. 1987 Dec 20;6(13):3873–3880. doi: 10.1002/j.1460-2075.1987.tb02727.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Simonelig M., Bazin C., Pelisson A., Bucheton A. Transposable and nontransposable elements similar to the I factor involved in inducer-reactive (IR) hybrid dysgenesis in Drosophila melanogaster coexist in various Drosophila species. Proc Natl Acad Sci U S A. 1988 Feb;85(4):1141–1145. doi: 10.1073/pnas.85.4.1141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Steller H., Pirrotta V. A transposable P vector that confers selectable G418 resistance to Drosophila larvae. EMBO J. 1985 Jan;4(1):167–171. doi: 10.1002/j.1460-2075.1985.tb02332.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES