Abstract
A single genetically marked P element can be efficiently mobilized to insertionally mutagenize the Drosophila genome. We have investigated how the structure of the starting element and its location along the X chromosome influenced the rate and location of mutations recovered. The structure of two P[rosy(+)] elements strongly affected mobilization by the autonomous ``Jumpstarter-1'' element. Their average transposition rates differed more than 12-fold, while their initial chromosomal location had a smaller effect. The lethal and sterile mutations induced by mobilizing a P[rosy(+)] element from position 1F were compared with those identified previously using a P[neo(R)] element at position 9C. With one possible exception, insertion hotspots for one element were frequently also targets of the other transposon. These experiments suggested that the genomic location of a P element does not usually influence its target sites on nonhomologous chromosomes. During the course of these experiments, Y-linked insertions expressing rosy(+) were recovered, suggesting that marked P elements can sometimes insert and function at heterochromatic sites.
Full Text
The Full Text of this article is available as a PDF (2.2 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Bellen H. J., O'Kane C. J., Wilson C., Grossniklaus U., Pearson R. K., Gehring W. J. P-element-mediated enhancer detection: a versatile method to study development in Drosophila. Genes Dev. 1989 Sep;3(9):1288–1300. doi: 10.1101/gad.3.9.1288. [DOI] [PubMed] [Google Scholar]
- Bier E., Vaessin H., Shepherd S., Lee K., McCall K., Barbel S., Ackerman L., Carretto R., Uemura T., Grell E. Searching for pattern and mutation in the Drosophila genome with a P-lacZ vector. Genes Dev. 1989 Sep;3(9):1273–1287. doi: 10.1101/gad.3.9.1273. [DOI] [PubMed] [Google Scholar]
- Bourouis M., Richards G. Remote regulatory sequences of the Drosophila glue gene sgs3 as revealed by P-element transformation. Cell. 1985 Feb;40(2):349–357. doi: 10.1016/0092-8674(85)90149-7. [DOI] [PubMed] [Google Scholar]
- 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]
- Cooley L., Berg C., Spradling A. Controlling P element insertional mutagenesis. Trends Genet. 1988 Sep;4(9):254–258. doi: 10.1016/0168-9525(88)90032-7. [DOI] [PubMed] [Google Scholar]
- Cooley L., Kelley R., Spradling A. Insertional mutagenesis of the Drosophila genome with single P elements. Science. 1988 Mar 4;239(4844):1121–1128. doi: 10.1126/science.2830671. [DOI] [PubMed] [Google Scholar]
- Coté B., Bender W., Curtis D., Chovnick A. Molecular mapping of the rosy locus in Drosophila melanogaster. Genetics. 1986 Apr;112(4):769–783. doi: 10.1093/genetics/112.4.769. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Edgar B. A., O'Farrell P. H. Genetic control of cell division patterns in the Drosophila embryo. Cell. 1989 Apr 7;57(1):177–187. doi: 10.1016/0092-8674(89)90183-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Eeken J. C., Sobels F. H., Hyland V., Schalet A. P. Distribution of MR-induced sex-linked recessive lethal mutations in Drosophila melanogaster. Mutat Res. 1985 Jun-Jul;150(1-2):261–275. doi: 10.1016/0027-5107(85)90122-8. [DOI] [PubMed] [Google Scholar]
- Eggleston W. B., Johnson-Schlitz D. M., Engels W. R. P-M hybrid dysgenesis does not mobilize other transposable element families in D. melanogaster. Nature. 1988 Jan 28;331(6154):368–370. doi: 10.1038/331368a0. [DOI] [PubMed] [Google Scholar]
- Engels W. R. Extrachromosomal control of mutability in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1979 Aug;76(8):4011–4015. doi: 10.1073/pnas.76.8.4011. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Engels W. R., Preston C. R. Identifying P factors in Drosophila by means of chromosome breakage hotspots. Cell. 1981 Nov;26(3 Pt 1):421–428. doi: 10.1016/0092-8674(81)90211-7. [DOI] [PubMed] [Google Scholar]
- Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
- Finnegan D. J. Eukaryotic transposable elements and genome evolution. Trends Genet. 1989 Apr;5(4):103–107. doi: 10.1016/0168-9525(89)90039-5. [DOI] [PubMed] [Google Scholar]
- García-Bellido A. Genetic Analysis of the Achaete-Scute System of DROSOPHILA MELANOGASTER. Genetics. 1979 Mar;91(3):491–520. doi: 10.1093/genetics/91.3.491. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Hawley R. S., Steuber R. A., Marcus C. H., Sohn R., Baronas D. M., Cameron M. L., Zitron A. E., Chase J. W. Molecular analysis of an unstable P element insertion at the singed locus of Drosophila melanogaster: evidence for intracistronic transposition of a P element. Genetics. 1988 May;119(1):85–94. doi: 10.1093/genetics/119.1.85. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ingham P. W., Pinchin S. M., Howard K. R., Ish-Horowicz D. Genetic Analysis of the Hairy Locus in DROSOPHILA MELANOGASTER. Genetics. 1985 Nov;111(3):463–486. doi: 10.1093/genetics/111.3.463. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Keith T. P., Riley M. A., Kreitman M., Lewontin R. C., Curtis D., Chambers G. Sequence of the structural gene for xanthine dehydrogenase (rosy locus) in Drosophila melanogaster. Genetics. 1987 May;116(1):67–73. doi: 10.1093/genetics/116.1.67. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kelley M. R., Kidd S., Berg R. L., Young M. W. Restriction of P-element insertions at the Notch locus of Drosophila melanogaster. Mol Cell Biol. 1987 Apr;7(4):1545–1548. doi: 10.1128/mcb.7.4.1545. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Lee C. S., Curtis D., McCarron M., Love C., Gray M., Bender W., Chovnick A. Mutations affecting expression of the rosy locus in Drosophila melanogaster. Genetics. 1987 May;116(1):55–66. doi: 10.1093/genetics/116.1.55. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McKearin D. M., Spradling A. C. bag-of-marbles: a Drosophila gene required to initiate both male and female gametogenesis. Genes Dev. 1990 Dec;4(12B):2242–2251. doi: 10.1101/gad.4.12b.2242. [DOI] [PubMed] [Google Scholar]
- Mullins M. C., Rio D. C., Rubin G. M. cis-acting DNA sequence requirements for P-element transposition. Genes Dev. 1989 May;3(5):729–738. doi: 10.1101/gad.3.5.729. [DOI] [PubMed] [Google Scholar]
- 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]
- Patel N. H., Snow P. M., Goodman C. S. Characterization and cloning of fasciclin III: a glycoprotein expressed on a subset of neurons and axon pathways in Drosophila. Cell. 1987 Mar 27;48(6):975–988. doi: 10.1016/0092-8674(87)90706-9. [DOI] [PubMed] [Google Scholar]
- Preston C. R., Engels W. R. Spread of P transposable elements in inbred lines of Drosophila melanogaster. Prog Nucleic Acid Res Mol Biol. 1989;36:71–85. doi: 10.1016/s0079-6603(08)60162-2. [DOI] [PubMed] [Google Scholar]
- Raymond J. D., Simmons M. J. An increase in the X-linked lethal mutation rate associated with an unstable locus in Drosophila melanogaster. Genetics. 1981 Jun;98(2):291–302. doi: 10.1093/genetics/98.2.291. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- Rushlow C. A., Chovnick A. Heterochromatic position effect at the rosy locus of Drosophila melanogaster: cytological, genetic and biochemical characterization. Genetics. 1984 Nov;108(3):589–602. doi: 10.1093/genetics/108.3.589. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schüpbach T., Wieschaus E. Female sterile mutations on the second chromosome of Drosophila melanogaster. I. Maternal effect mutations. Genetics. 1989 Jan;121(1):101–117. doi: 10.1093/genetics/121.1.101. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Simmons M. J., Lim J. K. Site specificity of mutations arising in dysgenic hybrids of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1980 Oct;77(10):6042–6046. doi: 10.1073/pnas.77.10.6042. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Simmons M. J., Raymond J. D., Johnson N. A., Fahey T. M. A comparison of mutation rates for specific loci and chromosome regions in dysgenic hybrid males of Drosophila melanogaster. Genetics. 1984 Jan;106(1):85–94. doi: 10.1093/genetics/106.1.85. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Spradling A. C., Rubin G. M. The effect of chromosomal position on the expression of the Drosophila xanthine dehydrogenase gene. Cell. 1983 Aug;34(1):47–57. doi: 10.1016/0092-8674(83)90135-6. [DOI] [PubMed] [Google Scholar]
- 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]
- Voelker R. A., Greenleaf A. L., Gyurkovics H., Wisely G. B., Huang S. M., Searles L. L. Frequent Imprecise Excision among Reversions of a P Element-Caused Lethal Mutation in Drosophila. Genetics. 1984 Jun;107(2):279–294. doi: 10.1093/genetics/107.2.279. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yedvobnick B., Muskavitch M. A., Wharton K. A., Halpern M. E., Paul E., Grimwade B. G., Artavanis-Tsakonas S. Molecular genetics of Drosophila neurogenesis. Cold Spring Harb Symp Quant Biol. 1985;50:841–854. doi: 10.1101/sqb.1985.050.01.102. [DOI] [PubMed] [Google Scholar]
- Yedvobnick B., Smoller D., Young P., Mills D. Molecular analysis of the neurogenic locus mastermind of Drosophila melanogaster. Genetics. 1988 Mar;118(3):483–497. doi: 10.1093/genetics/118.3.483. [DOI] [PMC free article] [PubMed] [Google Scholar]