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. 1996 Dec;144(4):1623–1638. doi: 10.1093/genetics/144.4.1623

Flanking Duplications and Deletions Associated with P-Induced Male Recombination in Drosophila

C R Preston 1, J A Sved 1, W R Engels 1
PMCID: PMC1207714  PMID: 8978050

Abstract

We studied P element-induced recombination in germline mitotic cells by examining the structure of the recombinant chromosomes. We found that most recombinants retain a mobile P element at the site of the recombination, usually with either a deletion or a duplication immediately adjacent to the P end at which the crossover occurred. The sizes of these deletions and duplications ranged from a few base pairs to well over 100 kb. These structures fit the ``hybrid element insertion'' (HEI) model of male recombination in which the two P-element copies on sister chromatids combine to form a ``hybrid element'' whose termini insert into a nearby position on the homologue. The data suggest that P-induced recombination can be used as an efficient means of generating flanking deletions in the vicinity of existing P elements. These deletions are easily screened using distant flanking markers, and they can be chosen to extend in a given direction depending on which reciprocal recombinant type is selected. Furthermore, the retention of a mobile P element allows one to extend the deletion or generate additional variability at the site by subsequent rounds of recombination.

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Selected References

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  1. 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]
  2. Castrillon D. H., Gönczy P., Alexander S., Rawson R., Eberhart C. G., Viswanathan S., DiNardo S., Wasserman S. A. Toward a molecular genetic analysis of spermatogenesis in Drosophila melanogaster: characterization of male-sterile mutants generated by single P element mutagenesis. Genetics. 1993 Oct;135(2):489–505. doi: 10.1093/genetics/135.2.489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. Duttaroy A., McCarron M., Sitaraman K., Doughty G., Chovnick A. The relationship between P elements and male recombination in Drosophila melanogaster. Genetics. 1990 Feb;124(2):317–329. doi: 10.1093/genetics/124.2.317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Engels W. R., Johnson-Schlitz D. M., Eggleston W. B., Sved J. High-frequency P element loss in Drosophila is homolog dependent. Cell. 1990 Aug 10;62(3):515–525. doi: 10.1016/0092-8674(90)90016-8. [DOI] [PubMed] [Google Scholar]
  6. Engels W. R. P elements in Drosophila. Curr Top Microbiol Immunol. 1996;204:103–123. doi: 10.1007/978-3-642-79795-8_5. [DOI] [PubMed] [Google Scholar]
  7. Gloor G. B., Nassif N. A., Johnson-Schlitz D. M., Preston C. R., Engels W. R. Targeted gene replacement in Drosophila via P element-induced gap repair. Science. 1991 Sep 6;253(5024):1110–1117. doi: 10.1126/science.1653452. [DOI] [PubMed] [Google Scholar]
  8. Gray Y. H., Tanaka M. M., Sved J. A. P-element-induced recombination in Drosophila melanogaster: hybrid element insertion. Genetics. 1996 Dec;144(4):1601–1610. doi: 10.1093/genetics/144.4.1601. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. Howe M., Dimitri P., Berloco M., Wakimoto B. T. Cis-effects of heterochromatin on heterochromatic and euchromatic gene activity in Drosophila melanogaster. Genetics. 1995 Jul;140(3):1033–1045. doi: 10.1093/genetics/140.3.1033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Isackson D. R., Johnson T. K., Denell R. E. Hybrid dysgenesis in Drosophila: the mechanism of T-007-induced male recombination. Mol Gen Genet. 1981;184(3):539–543. doi: 10.1007/BF00352536. [DOI] [PubMed] [Google Scholar]
  12. Johnson-Schlitz D. M., Engels W. R. P-element-induced interallelic gene conversion of insertions and deletions in Drosophila melanogaster. Mol Cell Biol. 1993 Nov;13(11):7006–7018. doi: 10.1128/mcb.13.11.7006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Karpen G. H., Spradling A. C. Analysis of subtelomeric heterochromatin in the Drosophila minichromosome Dp1187 by single P element insertional mutagenesis. Genetics. 1992 Nov;132(3):737–753. doi: 10.1093/genetics/132.3.737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Kidwell M. G., Kidwell J. F. Selection for male recombination in Drosophila melanogaster. Genetics. 1976 Oct;84(2):333–351. doi: 10.1093/genetics/84.2.333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kidwell M. G., Kidwell J. F., Sved J. A. Hybrid Dysgenesis in DROSOPHILA MELANOGASTER: A Syndrome of Aberrant Traits Including Mutation, Sterility and Male Recombination. Genetics. 1977 Aug;86(4):813–833. doi: 10.1093/genetics/86.4.813. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lee L. G., Connell C. R., Woo S. L., Cheng R. D., McArdle B. F., Fuller C. W., Halloran N. D., Wilson R. K. DNA sequencing with dye-labeled terminators and T7 DNA polymerase: effect of dyes and dNTPs on incorporation of dye-terminators and probability analysis of termination fragments. Nucleic Acids Res. 1992 May 25;20(10):2471–2483. doi: 10.1093/nar/20.10.2471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lee M. P., Brown S. D., Chen A., Hsieh T. S. DNA topoisomerase I is essential in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1993 Jul 15;90(14):6656–6660. doi: 10.1073/pnas.90.14.6656. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. McCarron M. Y., Duttaroy A., Doughty G. A., Chovnick A. P-element transposase induces male recombination in Drosophila melanogaster. Genet Res. 1989 Oct;54(2):137–141. doi: 10.1017/s0016672300028500. [DOI] [PubMed] [Google Scholar]
  20. McCarron M., Duttaroy A., Doughty G., Chovnick A. Drosophila P element transposase induces male recombination additively and without a requirement for P element excision or insertion. Genetics. 1994 Mar;136(3):1013–1023. doi: 10.1093/genetics/136.3.1013. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Mellerick D. M., Kassis J. A., Zhang S. D., Odenwald W. F. castor encodes a novel zinc finger protein required for the development of a subset of CNS neurons in Drosophila. Neuron. 1992 Nov;9(5):789–803. doi: 10.1016/0896-6273(92)90234-5. [DOI] [PubMed] [Google Scholar]
  22. Nassif N., Penney J., Pal S., Engels W. R., Gloor G. B. Efficient copying of nonhomologous sequences from ectopic sites via P-element-induced gap repair. Mol Cell Biol. 1994 Mar;14(3):1613–1625. doi: 10.1128/mcb.14.3.1613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. O'Hare K., Driver A., McGrath S., Johnson-Schiltz D. M. Distribution and structure of cloned P elements from the Drosophila melanogaster P strain pi 2. Genet Res. 1992 Aug;60(1):33–41. doi: 10.1017/s0016672300030640. [DOI] [PubMed] [Google Scholar]
  24. Preston C. R., Engels W. R. P-element-induced male recombination and gene conversion in Drosophila. Genetics. 1996 Dec;144(4):1611–1622. doi: 10.1093/genetics/144.4.1611. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. 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]
  26. Rosenthal A., Charnock-Jones D. S. New protocols for DNA sequencing with dye terminators. DNA Seq. 1992;3(1):61–64. doi: 10.3109/10425179209039697. [DOI] [PubMed] [Google Scholar]
  27. Rubin G. M., Kidwell M. G., Bingham P. M. The molecular basis of P-M hybrid dysgenesis: the nature of induced mutations. Cell. 1982 Jul;29(3):987–994. doi: 10.1016/0092-8674(82)90462-7. [DOI] [PubMed] [Google Scholar]
  28. Sentry J. W., Kaiser K. P element transposition and targeted manipulation of the Drosophila genome. Trends Genet. 1992 Oct;8(10):329–331. doi: 10.1016/0168-9525(92)90267-8. [DOI] [PubMed] [Google Scholar]
  29. Sinclair D. A., Grigliatti T. A. Investigation of the nature of P-induced male recombination in Drosophila melanogaster. Genetics. 1985 Jun;110(2):257–279. doi: 10.1093/genetics/110.2.257. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Smoller D., Friedel C., Schmid A., Bettler D., Lam L., Yedvobnick B. The Drosophila neurogenic locus mastermind encodes a nuclear protein unusually rich in amino acid homopolymers. Genes Dev. 1990 Oct;4(10):1688–1700. doi: 10.1101/gad.4.10.1688. [DOI] [PubMed] [Google Scholar]
  31. Staveley B. E., Heslip T. R., Hodgetts R. B., Bell J. B. Protected P-element termini suggest a role for inverted-repeat-binding protein in transposase-induced gap repair in Drosophila melanogaster. Genetics. 1995 Mar;139(3):1321–1329. doi: 10.1093/genetics/139.3.1321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Sved J. A., Eggleston W. B., Engels W. R. Germ-line and somatic recombination induced by in vitro modified P elements in Drosophila melanogaster. Genetics. 1990 Feb;124(2):331–337. doi: 10.1093/genetics/124.2.331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Svoboda Y. H., Robson M. K., Sved J. A. P-element-induced male recombination can be produced in Drosophila melanogaster by combining end-deficient elements in trans. Genetics. 1995 Apr;139(4):1601–1610. doi: 10.1093/genetics/139.4.1601. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Takasu-Ishikawa E., Yoshihara M., Hotta Y. Extra sequences found at P element excision sites in Drosophila melanogaster. Mol Gen Genet. 1992 Mar;232(1):17–23. doi: 10.1007/BF00299132. [DOI] [PubMed] [Google Scholar]
  35. Whiteley M., Noguchi P. D., Sensabaugh S. M., Odenwald W. F., Kassis J. A. The Drosophila gene escargot encodes a zinc finger motif found in snail-related genes. Mech Dev. 1992 Feb;36(3):117–127. doi: 10.1016/0925-4773(92)90063-p. [DOI] [PubMed] [Google Scholar]
  36. 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]
  37. Zhang P., Spradling A. C. Efficient and dispersed local P element transposition from Drosophila females. Genetics. 1993 Feb;133(2):361–373. doi: 10.1093/genetics/133.2.361. [DOI] [PMC free article] [PubMed] [Google Scholar]

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