Skip to main content
NCBI home page
Genetics logoLink to Genetics
. 1990 Mar;124(3):647–662. doi: 10.1093/genetics/124.3.647

Quantitative Effects of P Elements on Hybrid Dysgenesis in Drosophila Melanogaster

K E Rasmusson 1, M J Simmons 1, J D Raymond 1, C F McLarnon 1
PMCID: PMC1203958  PMID: 2155853

Abstract

Genetic analyses involving chromosomes from seven inbred lines derived from a single M' strain were used to study the quantitative relationships between the incidence and severity of P-M hybrid dysgenesis and the number of genomic P elements. In four separate analyses, the mutability of sn(w), a P element-insertion mutation of the X-linked singed locus, was found to be inversely related to the number of autosomal P elements. Since sn(w) mutability is caused by the action of the P transposase, this finding supports the hypothesis that genomic P elements titrate the transposase present within a cell. Other analyses demonstrated that autosomal transmission ratios were distorted by P element action. In these analyses, the amount of distortion against an autosome increased more or less linearly with the number of P elements carried by the autosome. Additional analyses showed that the magnitude of this distortion was reduced when a second P element-containing autosome was present in the genome. This reduction could adequately be explained by transposase titration; there was no evidence that it was due to repressor molecules binding to P elements and inhibiting their movement. The influence of genomic P elements on the incidence of gonadal dysgenesis was also investigated. Although no simple relationship between the number of P elements and the incidence of the trait could be discerned, it was clear that even a small number of elements could increase the incidence markedly. The failure to find a quantitative relationship between P element number and the incidence of gonadal dysgenesis probably reflects the complex etiology of this trait.

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.

  1. Anxolabéhère D., Nouaud D., Périquet G., Tchen P. P-element distribution in Eurasian populations of Drosophila melanogaster: A genetic and molecular analysis. Proc Natl Acad Sci U S A. 1985 Aug;82(16):5418–5422. doi: 10.1073/pnas.82.16.5418. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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]
  3. 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]
  4. 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]
  5. Daniels S. B., Clark S. H., Kidwell M. G., Chovnick A. Genetic transformation of Drosophila melanogaster with an autonomous P element: phenotypic and molecular analyses of long-established transformed lines. Genetics. 1987 Apr;115(4):711–723. doi: 10.1093/genetics/115.4.711. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Engels W. R. A trans-acting product needed for P factor transposition in Drosophila. Science. 1984 Dec 7;226(4679):1194–1196. doi: 10.1126/science.6095450. [DOI] [PubMed] [Google Scholar]
  7. Engels W. R., Benz W. K., Preston C. R., Graham P. L., Phillis R. W., Robertson H. M. Somatic effects of P element activity in Drosophila melanogaster: pupal lethality. Genetics. 1987 Dec;117(4):745–757. doi: 10.1093/genetics/117.4.745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Engels W. R. Germline hypermutability in Drosophila and its relation to hybrid dysgenesis and cytotype. Genetics. 1981 Jul;98(3):565–587. doi: 10.1093/genetics/98.3.565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. Greenberg R, Crow J F. A Comparison of the Effect of Lethal and Detrimental Chromosomes from Drosophila Populations. Genetics. 1960 Aug;45(8):1153–1168. doi: 10.1093/genetics/45.8.1153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Johnson-Schlitz D., Lim J. K. Cytogenetics of Notch mutations arising in the unstable X chromosome Uc of Drosophila melanogaster. Genetics. 1987 Apr;115(4):701–709. doi: 10.1093/genetics/115.4.701. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Kidwell M. G. Hybrid dysgenesis in Drosophila melanogaster: nature and inheritance of P element regulation. Genetics. 1985 Oct;111(2):337–350. doi: 10.1093/genetics/111.2.337. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Kidwell M. G., Novy J. B. Hybrid Dysgenesis in DROSOPHILA MELANOGASTER: Sterility Resulting from Gonadal Dysgenesis in the P-M System. Genetics. 1979 Aug;92(4):1127–1140. doi: 10.1093/genetics/92.4.1127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kocur G. J., Drier E. A., Simmons M. J. Sterility and hypermutability in the P-M system of hybrid dysgenesis in Drosophila melanogaster. Genetics. 1986 Dec;114(4):1147–1163. doi: 10.1093/genetics/114.4.1147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. 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]
  19. 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]
  20. 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]
  21. Simmons M. J., Raymond J. D., Boedigheimer M. J., Zunt J. R. The influence of nonautonomous P elements on hybrid dysgenesis in Drosophila melanogaster. Genetics. 1987 Dec;117(4):671–685. doi: 10.1093/genetics/117.4.671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Simmons M. J., Raymond J. D., Culbert T. P., Laverty T. R. Analysis of dysgenesis-induced lethal mutations on the X chromosome of a Q strain of Drosophila melanogaster. Genetics. 1984 May;107(1):49–63. doi: 10.1093/genetics/107.1.49. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Simmons M. J., Raymond J. D., Rasmusson K. E., Miller L. M., McLarnon C. F., Zunt J. R. Repression of P element-mediated hybrid dysgenesis in Drosophila melanogaster. Genetics. 1990 Mar;124(3):663–676. doi: 10.1093/genetics/124.3.663. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES