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Genetic and molecular analysis of repression in the P–M system of hybrid dysgenesis in Drosophila melanogaster

Published online by Cambridge University Press:  14 April 2009

Ellen M. Heath
Affiliation:
Department of Genetics and Cell Biology, University of Minnesota, St Paul, Minnesota 55108–1095, U.S.A.
Michael J. Simmons*
Affiliation:
Department of Genetics and Cell Biology, University of Minnesota, St Paul, Minnesota 55108–1095, U.S.A.
*
* Corresponding author.
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Twelve inbred lines derived from an M′ strain of Drosophila melanogaster were used to study the repression of P-element-mediated hybrid dysgenesis. Initial assessments indicated that the lines differed in the ability to repress gonadal dysgenesis, and that this ability was highly correlated with the ability to repress snw hypermutability. Later assessments indicated that most of the lines with low or intermediate repression potential evolved to a state of higher repression potential; however, Southern analyses failed to reveal significant changes in the array of genomic P elements that could account for this evolution. In addition, none of the lines possessed the incomplete P element known as KP, which has been proposed to explain repression in some D. melanogaster strains. One of the lines maintained intermediate repression potential throughout the period of study (52 generations), indicating that the intermediate condition was not intrinsically unstable. Genetic analyses demonstrated that in some of the lines, repression potential was influenced by factors that were inherited maternally through at least two generations; however, these factors were not as influential as those in a classic P cytotype strain. Additional tests with a dysgenesis-inducing X chromosome called T-5 indicated that repression itself was mediated by a combination of maternal effects and paternally inherited factors that were expressed after fertilization. These tests also suggested that in some circumstances, the P transposase, or its message, might be transmitted through the maternal cytoplasm.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1991

References

Anxolabéhère, D., Nouaud, D., Périquet, G. & Ronsseray, S. (1986). Evolution des potentialités dysgénésiques du système P–M dans des populations expérimentales mixtes P, Q, M et M′ de Drosophila melanogaster. Genetica 69, 8195.CrossRefGoogle Scholar
Berg, R. L., Engels, W. R. & Kreber, R. A. (1980). Site-specific X-chromosome rearrangements from hybrid dysgenesis in Drosophila melanogaster. Science 210, 427429.CrossRefGoogle ScholarPubMed
Bingham, P. M., Kidwell, M. G. & Rubin, G. M. (1982). The molecular basis of P–M hybrid dysgenesis: the role of the P element, a strain-specific transposon family. Cell 29, 693704.CrossRefGoogle Scholar
Black, D. M., Jackson, M. S., Kidwell, M. G. & Dover, G. A. (1987). KP elements repress P-induced hybrid dysgenesis in D. melanogaster. EMBO Journal 6, 41254135.CrossRefGoogle Scholar
Curtsinger, J. W. (1984). Components of selection in X chromosome lines of Drosophila melanogaster: Sex ratio modification by meiotic drive and viability selection. Genetics 108, 941952.CrossRefGoogle Scholar
Daniels, S. B., Clark, S. H., Kidwell, M. G. & Chovnick, A. (1987). Genetic transformation of Drosophila melanogaster with an autonomous P element: phenotypic and molecular analyses of long-established transformed lines. Genetics 115, 711723.CrossRefGoogle ScholarPubMed
Engels, W. R. (1979 a). Germline aberrations associated with a case of hybrid dysgenesis in Drosophila melanogaster males. Genetical Research 33, 137146.CrossRefGoogle Scholar
Engels, W. R. (1979 b). Extrachromosomal control of mutability in Drosophila melanogaster. Proceedings of the National Academy of Sciences, U.S.A. 76, 40114015.CrossRefGoogle ScholarPubMed
Engels, W. R. (1979 c). Hybrid dysgenesis in Drosophila melanogaster: rules of inheritance of female sterility. Genetical Research 33, 137146.CrossRefGoogle Scholar
Engels, W. R. (1979 d). The estimation of mutation rates when premeiotic events are involved. Environmental Mutagenesis 1, 3743.CrossRefGoogle ScholarPubMed
Engels, W. R. (1981). Germline hypermutability in Drosophila and its relationship to hybrid dysgenesis and cytotype. Genetics 98, 565587.CrossRefGoogle Scholar
Engels, W. R. (1984). A trans-acting product needed for P factor transposition in Drosophila. Science 226, 11941196.CrossRefGoogle ScholarPubMed
Engels, W. R. & Preston, C. R. (1979). Hybrid dysgenesis in Drosophila melanogaster: the biology of male and female sterility. Genetics 95, 161175.CrossRefGoogle Scholar
Engels, W. R. & Preston, C. R. (1981). Identifying P factors in Drosophila by means of chromosome breakage hot-spots. Cell 26, 421428.CrossRefGoogle Scholar
Hirara, R., Hisamatsu, N. & Hirota, T. (1985). Hybrid dysgenesis in Drosophila melanogaster; Type conversions observed in the recently established isofemale lines and hybrid lines originated from M × P crosses. Japanese Journal of Genetics 60, 199214.Google Scholar
Jackson, M. S., Black, D. M. & Dover, G. A. (1988). Amplification of KP elements associated with the repression of hybrid dysgenesis in Drosophila melanogaster. Genetics 120, 10031013.CrossRefGoogle ScholarPubMed
Jongeward, G., Simmons, M. & Heath, E. (1987). The instability of a P element insertion mutation is affected by chromosomes derived paternally from a pseudo-M strain of Drosophila melanogaster. Drosophila Information Service 66, 7780.Google Scholar
Karess, R. E. & Rubin, G. M. (1984). Analysis of P transposable element functions in Drosophila. Cell 38, 135146.CrossRefGoogle ScholarPubMed
Kiyasu, P. K. & Kidwell, M. G. (1984). Hybrid dysgenesis in Drosophila melanogaster: the evolution of mixed P and M populations maintained at high temperature. Genetical Research, Cambridge 44, 251259.CrossRefGoogle Scholar
Kidwell, M. G. (1981). Hybrid dysgenesis in Drosophila melanogaster: the genetics of cytotype determination in a neutral strain. Genetics 98, 275290.CrossRefGoogle Scholar
Kidwell, M. G. (1983). Evolution of hybrid dysgenesis determinants in Drosophila melanogaster. Proceedings of the National Academy of Sciences, U.S.A. 80, 16551659.CrossRefGoogle ScholarPubMed
Kidwell, M. G. (1985). Hybrid dysgenesis in Drosophila melanogaster: Nature and inheritance of P element regulation. Genetics 111, 337350.CrossRefGoogle ScholarPubMed
Kidwell, M. G. & Kidwell, J. F. (1976). Selection for male recombination in Drosophila melanogaster. Genetics, 84, 333351.CrossRefGoogle ScholarPubMed
Kidwell, M. G., Kidwell, J. F. & Sved, J. A. (1977). Hybrid dysgenesis in Drosophila melanogaster: a syndrome of aberrant traits including mutation, sterility, and male recombination. Genetics 36, 813833.CrossRefGoogle Scholar
Kidwell, M. G. & Novy, J. B. (1979). Hybrid dysgenesis in Drosophila melanogaster: sterility resulting from gonadal dysgenesis in the P–M system. Genetics 92, 11271140.CrossRefGoogle ScholarPubMed
Kidwell, M. G., Kimura, K. & Black, D.M. (1988). Evolution of hybrid dysgenesis potential following P element contamination in Drosophila melanogaster. Genetics 119, 815828.CrossRefGoogle ScholarPubMed
Laski, F. A., Rio, D. C. & Rubin, G. M. (1986). The tissue specificity of Drosophila P element transposition is regulated, at the level of mRNA splicing. Cell 44, 719.CrossRefGoogle ScholarPubMed
Lindsley, D. L. & Grell, E. H. (1968). Genetic Variations of Drosophila melanogaster. Carnegie Institute of Washington, Publication no. 627.Google Scholar
Nitasaka, E., Mukai, T. & Yamazaki, T. (1987). Repressor of P elements in, Drosophila melanogaster: cytotype determination by a defective P element carrying only open reading frames 0 through 2. Proceedings of the National Academy of Sciences, U.S.A. 84, 76057608.CrossRefGoogle Scholar
O'Hare, K. & Rubin, G. M. (1983). Structure of P transposable elements and their sites of insertion and excision in the Drosophila melanogaster genome. Cell 34, 2535.CrossRefGoogle ScholarPubMed
Rasmusson, K. E., Simmons, M. J., Raymond, J. D. & McLarnon, C. F. (1990). Quantitative effects of P elements on hybrid dysgenesis in Drosophila melanogaster. Genetics 124, 647662.CrossRefGoogle ScholarPubMed
Rio, D. C, Laski, F. A. & Rubin, G. M. (1986). Identification and immunochemical analysis of biologically active Drosophila P element transposase. Cell 44, 2132.CrossRefGoogle ScholarPubMed
Robertson, H. M. & Engels, W. R. (1989). Modified P elements that mimic the P cytotype in Drosophila melanogaster. Genetics 123, 815824.CrossRefGoogle Scholar
Rubin, G. M., Kidwell, M.G. & Bingham, P. M. (1982). The molecular basis of P–M hybrid dysgenesis: the nature of induced mutations. Cell 29, 987994.CrossRefGoogle ScholarPubMed
Sakoyama, Y., Todo, T., Ishiwa-Chigusa, S., Honjo, T. & Kondo, S. (1985). Structures of defective P transposable elements prevalent in natural Q and Q-derived M strains of Drosophila melanogaster. Proceedings of the National Academy of Sciences, U.S.A. 82, 62366239.CrossRefGoogle ScholarPubMed
Simmons, M. J. & Lim, J. K. (1980). Site specificity of mutations arising in dysgenic hybrids of Drosophila melanogaster. Proceedings of the National Academy of Sciences, U.S.A. 77, 60426046.CrossRefGoogle ScholarPubMed
Simmons, M. J. & Bucholz, L. M. (1985). Transposase titration in Drosophila melanogaster: a model for cytotype in the P–M system of hybrid dysgenesis. Proceedings of the National Academy of Sciences, U.S.A. 82, 81198123.CrossRefGoogle Scholar
Simmons, M. J., Johnson, N. A., Fahey, T. M., Nellett, S. M. & Raymond, J. D. (1980). High mutability in male hybrids of Drosophila melanogaster. Genetics 96, 479490.CrossRefGoogle ScholarPubMed
Simmons, M. J., Raymond, J. D., Boedigheimer, M. J. & Zunt, J. R. (1987). The influence of nonautonomous P elements on hybrid dysgenesis in Drosophila melanogaster. Genetics 117, 671685.CrossRefGoogle ScholarPubMed
Simmons, M. J., Raymond, J. D., Rasmusson, K. E., Miller, L. M., McLarnon, C. F. & Zunt, J. R. (1990). Repression of P element-mediated hybrid dysgenesis in Drosophila melanogaster. Genetics 124, 663676.CrossRefGoogle ScholarPubMed
Spradling, A. C. & Rubin, G. M. (1982). Transposition of cloned P elements into Drosophila germ line chromosomes. Science 218, 341347.CrossRefGoogle ScholarPubMed