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. 1988 Nov;85(22):8593–8597. doi: 10.1073/pnas.85.22.8593

Mutant gene phenotypes mediated by a Drosophila melanogaster retrotransposon require sequences homologous to mammalian enhancers.

P K Geyer 1, M M Green 1, V G Corces 1
PMCID: PMC282505  PMID: 2847167

Abstract

We have analyzed the molecular structure of phenotypic revertants of gypsy-induced mutations to understand the molecular mechanisms by which this retrotransposon causes mutant phenotypes in Drosophila melanogaster. The independent partial revertants analyzed are caused by the insertion of different transposons into the same region of gypsy. One partial revertant of the yellow allele y2 arose as a consequence of the insertion of the jockey mobile element into gypsy sequences, whereas a second incomplete revertant is due to the insertion of the hobo transposon. In addition, a previously isolated partial revertant of the Hairy-wing allele Hw1 resulted from the integration of the BS transposable element into the same gypsy sequences. The region affected by the insertion of the three transposons contains 12 copies of a repeated motif that shows striking homology to mammalian transcriptional enhancers. Our results suggest that these sequences, which might be involved in the transcriptional control of the gypsy element, are also responsible for the induction of mutant phenotypes by this retrotransposon.

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Selected References

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

  1. Biessmann H. Molecular analysis of the yellow gene (y) region of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1985 Nov;82(21):7369–7373. doi: 10.1073/pnas.82.21.7369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bohmann D., Keller W., Dale T., Schöler H. R., Tebb G., Mattaj I. W. A transcription factor which binds to the enhancers of SV40, immunoglobulin heavy chain and U2 snRNA genes. Nature. 1987 Jan 15;325(6101):268–272. doi: 10.1038/325268a0. [DOI] [PubMed] [Google Scholar]
  3. Campuzano S., Balcells L., Villares R., Carramolino L., García-Alonso L., Modolell J. Excess function hairy-wing mutations caused by gypsy and copia insertions within structural genes of the achaete-scute locus of Drosophila. Cell. 1986 Jan 31;44(2):303–312. doi: 10.1016/0092-8674(86)90764-6. [DOI] [PubMed] [Google Scholar]
  4. Chia W., Howes G., Martin M., Meng Y. B., Moses K., Tsubota S. Molecular analysis of the yellow locus of Drosophila. EMBO J. 1986 Dec 20;5(13):3597–3605. doi: 10.1002/j.1460-2075.1986.tb04688.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Frischauf A. M., Lehrach H., Poustka A., Murray N. Lambda replacement vectors carrying polylinker sequences. J Mol Biol. 1983 Nov 15;170(4):827–842. doi: 10.1016/s0022-2836(83)80190-9. [DOI] [PubMed] [Google Scholar]
  6. Gerasimova T. I., Matjunina L. V., Mizrokhi L. J., Georgiev G. P. Successive transposition explosions in Drosophila melanogaster and reverse transpositions of mobile dispersed genetic elements. EMBO J. 1985 Dec 30;4(13B):3773–3779. doi: 10.1002/j.1460-2075.1985.tb04147.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Geyer P. K., Corces V. G. Separate regulatory elements are responsible for the complex pattern of tissue-specific and developmental transcription of the yellow locus in Drosophila melanogaster. Genes Dev. 1987 Nov;1(9):996–1004. doi: 10.1101/gad.1.9.996. [DOI] [PubMed] [Google Scholar]
  8. Geyer P. K., Green M. M., Corces V. G. Reversion of a gypsy-induced mutation at the yellow (y) locus of Drosophila melanogaster is associated with the insertion of a newly defined transposable element. Proc Natl Acad Sci U S A. 1988 Jun;85(11):3938–3942. doi: 10.1073/pnas.85.11.3938. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Geyer P. K., Richardson K. L., Corces V. G., Green M. M. Genetic instability in Drosophila melanogaster: P-element mutagenesis by gene conversion. Proc Natl Acad Sci U S A. 1988 Sep;85(17):6455–6459. doi: 10.1073/pnas.85.17.6455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Geyer P. K., Spana C., Corces V. G. On the molecular mechanism of gypsy-induced mutations at the yellow locus of Drosophila melanogaster. EMBO J. 1986 Oct;5(10):2657–2662. doi: 10.1002/j.1460-2075.1986.tb04548.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Green M. M., Lefevre G., Jr The cytogenetics of mutator gene-induced X-linked lethals in Drosophila melanogaster. Mutat Res. 1972 Sep;16(7):59–64. doi: 10.1016/0027-5107(72)90064-4. [DOI] [PubMed] [Google Scholar]
  12. Green M. M. The genetics of a mutator gene in Drosophila melanogaster. Mutat Res. 1970 Oct;10(4):353–363. doi: 10.1016/0027-5107(70)90048-5. [DOI] [PubMed] [Google Scholar]
  13. Hiraizumi Y. Spontaneous recombination in Drosophila melanogaster males. Proc Natl Acad Sci U S A. 1971 Feb;68(2):268–270. doi: 10.1073/pnas.68.2.268. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Marlor R. L., Parkhurst S. M., Corces V. G. The Drosophila melanogaster gypsy transposable element encodes putative gene products homologous to retroviral proteins. Mol Cell Biol. 1986 Apr;6(4):1129–1134. doi: 10.1128/mcb.6.4.1129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. Mizrokhi L. J., Obolenkova L. A., Priimägi A. F., Ilyin Y. V., Gerasimova T. I., Georgiev G. P. The nature of unstable insertion mutations and reversions in the locus cut of Drosophila melanogaster: molecular mechanism of transposition memory. EMBO J. 1985 Dec 30;4(13B):3781–3787. doi: 10.1002/j.1460-2075.1985.tb04148.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Modolell J., Bender W., Meselson M. Drosophila melanogaster mutations suppressible by the suppressor of Hairy-wing are insertions of a 7.3-kilobase mobile element. Proc Natl Acad Sci U S A. 1983 Mar;80(6):1678–1682. doi: 10.1073/pnas.80.6.1678. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Mount S. M., Green M. M., Rubin G. M. Partial revertants of the transposable element-associated suppressible allele white-apricot in Drosophila melanogaster: structures and responsiveness to genetic modifiers. Genetics. 1988 Feb;118(2):221–234. doi: 10.1093/genetics/118.2.221. [DOI] [PMC free article] [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. Parkhurst S. M., Corces V. G. Forked, gypsys, and suppressors in Drosophila. Cell. 1985 Jun;41(2):429–437. doi: 10.1016/s0092-8674(85)80016-7. [DOI] [PubMed] [Google Scholar]
  21. Parkhurst S. M., Corces V. G. Interactions among the gypsy transposable element and the yellow and the suppressor of hairy-wing loci in Drosophila melanogaster. Mol Cell Biol. 1986 Jan;6(1):47–53. doi: 10.1128/mcb.6.1.47. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Parkhurst S. M., Corces V. G. Retroviral elements and suppressor genes in Drosophila. Bioessays. 1986 Aug;5(2):52–57. doi: 10.1002/bies.950050203. [DOI] [PubMed] [Google Scholar]
  23. Parkhurst S. M., Harrison D. A., Remington M. P., Spana C., Kelley R. L., Coyne R. S., Corces V. G. The Drosophila su(Hw) gene, which controls the phenotypic effect of the gypsy transposable element, encodes a putative DNA-binding protein. Genes Dev. 1988 Oct;2(10):1205–1215. doi: 10.1101/gad.2.10.1205. [DOI] [PubMed] [Google Scholar]
  24. Peifer M., Bender W. The anterobithorax and bithorax mutations of the bithorax complex. EMBO J. 1986 Sep;5(9):2293–2303. doi: 10.1002/j.1460-2075.1986.tb04497.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Rosales R., Vigneron M., Macchi M., Davidson I., Xiao J. H., Chambon P. In vitro binding of cell-specific and ubiquitous nuclear proteins to the octamer motif of the SV40 enhancer and related motifs present in other promoters and enhancers. EMBO J. 1987 Oct;6(10):3015–3025. doi: 10.1002/j.1460-2075.1987.tb02607.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Rutledge B. J., Mortin M. A., Schwarz E., Thierry-Mieg D., Meselson M. Genetic interactions of modifier genes and modifiable alleles in Drosophila melanogaster. Genetics. 1988 Jun;119(2):391–397. doi: 10.1093/genetics/119.2.391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Streck R. D., Macgaffey J. E., Beckendorf S. K. The structure of hobo transposable elements and their insertion sites. EMBO J. 1986 Dec 20;5(13):3615–3623. doi: 10.1002/j.1460-2075.1986.tb04690.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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