Hostname: page-component-586b7cd67f-dlnhk Total loading time: 0 Render date: 2024-11-26T23:23:40.645Z Has data issue: false hasContentIssue false

The synergistic effect of X-rays and deficiencies in DNA repair in P-M hybrid dysgenesis in Drosophila melanogaster

Published online by Cambridge University Press:  14 April 2009

Lola Margulies*
Affiliation:
Department of Microbiology and Immunology, New York Medical College, Valhalla, NY 10595
Carole S. Griffith
Affiliation:
Biology Department, CUNY, New York, New York 10021, Department of Ornithology, American Museum of Natural History, N.Y., N.Y. 10024
*
* Corresponding author.
Rights & Permissions [Opens in a new window]

Summary

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

X-rays and deficiencies in DNA repair had a synergistic effect on genetic damage associated with P-element mobility in Drosophila melanogaster. These interactions, using sterility and fecundity as endpoints, were tested in dysgenic males deficient in either excision or post-replication DNA repair. Three sublines of the Harwich P strain were used for the construction of hybrid males. These sublines differ in P-induction ability based on gonadal dysgenesis sterility (GD) and snw mutability tests, in P-element insertion site pattern, and in the types of defective P-elements, such as KP elements, they possess. A lower degree of gonadal dysgenesis was correlated with the presence of KP elements. GD sterility and snw mutability were not always correlated. Dysgenic hybrids originating from the standard reference subline, Harwichwhite, were much more sensitive to the post-replication repair than the excision repair defect. In contrast, sterility of hybrids derived from the weak subline was least affected by, and that of hybrids of the strongest subline was most affected by either DNA repair deficiency. The exacerbation by X-rays of the effects of DNA repair deficiencies on genetic damage indicates that both repair mechanisms are required for processing DNA lesions induced by the combined effect of P activity and ionizing radiation.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1991

References

Bingham, P. M., Kidwell, M. G. & Rubin, G. M. (1982). The molecular basis of P-M hybrid dysgenesis: the role of the P element, P strain specific transposon family. Cell 29, 9951004.Google Scholar
Bishop, Y. M., Fienberg, S. E. & Holland, P. W. (1975). Discrete Multivariate Analysis: Theory and Practice. MIT Press, Cambridge, MA.Google Scholar
Black, D. M., Jackson, M. S., Kidwell, G. M. & Dover, G. A. (1987). KP elements repress P-induced hybrid dysgenesis in D. melanogaster. EMBO Journal 6, 41254135.CrossRefGoogle Scholar
Boyd, J. B., Golino, M. & Setlow, R. (1976). The mei-9 mutant of Drosophila melanogaster increases mutagen sensitivity and decreases excision repair. Genetics 84, 527544.Google Scholar
Boyd, J. B. & Setlow, R. (1976). Characterization of postreplication repair in mutagen-sensitive strains of Drosophila melanogaster. Genetics 84, 507526.CrossRefGoogle ScholarPubMed
Bregliano, J. C. & Kidwell, M. G. (1983). Hybrid dysgenesis determinants. In Mobile Genetic Elements (ed. Shapiro, J. A.). London and New York, Academic Press.Google 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 analysis of long-established transformed lines. Genetics 115, 711723.Google Scholar
Daniels, S. B., Peterson, K. R., Strausbaugh, L. D., Kidwell, M. G. & Chovnick, A. (1990). Evidence for horizontal transmission of the P transposable element between Drosophila species. Genetics 124, 339355.CrossRefGoogle Scholar
Eeken, J. C. J. & Sobels, F. H. (1981). Modification of MR activity in repair deficient strains of Drosophila melanogaster. Mutation Research 83, 191200.Google Scholar
Eeken, J. C. J. & Sobels, F. H. (1983). The influence of deficiences in DNA repair on MR-mediated reversion of an insertion-sequence mutation in Drosophila melanogaster. Mutation Research 110, 287295.Google Scholar
Engels, W. R. (1979 a). Hybrid dysgenesis in Drosophila melanogaster: rules of inheritance of female sterility. Genetical Research 33, 219236.CrossRefGoogle Scholar
Engels, W. R. (1979 b). Extrachromosomal control of mutability in Drosophila melanogaster. Proceedings of the National Academy of Sciences, USA 76, 40114015.CrossRefGoogle ScholarPubMed
Engels, W. R. (1979 c). The estimation of mutation rates when premeiotic events are involved. Environmental Mutagenesis 1, 3743.CrossRefGoogle ScholarPubMed
Engels, W. R. (1981). Germline mutability in Drosophila and its relation to hybrid dysgenesis and cytotype. Genetics 98, 565587.Google Scholar
Engels, W. R. (1983). The P family of transposable elements in Drosophila. Annual Review of Genetics 17, 315344.CrossRefGoogle Scholar
Engels, W. R. (1984). A trans-acting product needed for P factor transposition. Science 226, 11941196.Google Scholar
Engels, W. R. (1989). P elements in Drosophila melanogaster. in Mobile DNA (ed. Berg, D. E. and Howe, M.). Washington, D.C.: ASM Publications.Google Scholar
Engels, W. R. & Preston, C. R. (1979). Hybrid dysgenesis in Drosophila melanogaster: the biology of female and male sterility. Genetics 92, 161174.Google Scholar
Engels, W. R. & Preston, C. R. (1984). Formation of chromosome rearrangements by P factors in Drosophila. Genetics 107, 657678.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
Karess, R. E. & Rubin, G. M. (1984). Analysis of P transposable element function in Drosophila. Cell 38, 135146.CrossRefGoogle ScholarPubMed
Kidwell, M. G. (1983). Hybrid dysgenesis in Drosophila melanogaster: factors affecting chromosomal contamination in the P-M system. Genetics 104, 317341.CrossRefGoogle ScholarPubMed
Kidwell, M. G. (1985). Hybrid dysgenesis in Drosophila melanogaster: nature and inheritance of P element regulation. Genetics 111, 337350.Google Scholar
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 86, 813833.CrossRefGoogle ScholarPubMed
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
Kocur, G. J., Drier, E. A. & Simmons, M. J. (1986). Sterility and hypermutability in the P-M system of hybrid dysgenesis in Drosophila melanogaster. Genetics 114, 11471163.Google Scholar
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.Google Scholar
Lindsley, D. & Grell, R. (1968). Genetic Variations of Drosophila melanogaster. Carnegie Institute of Washington, Publication no. 627.Google Scholar
Maniatis, T., Fritsch, E. F. & Sanbrook, J. (1982). Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, New York, Cold Spring Harbor laboratory.Google Scholar
Marcus, C. M. (1985). Single fly DNA extraction procedure. Drosophila Information Service 61, 193.Google Scholar
Margulies, L., Briscoe, D. J. & Wallace, S. S. (1986). The relationship between radiation-induced and transposon-induced genetic damage during Drosophila oogenesis. Mutation Research 162, 5568.CrossRefGoogle ScholarPubMed
Margulies, L., Briscoe, J. D. & Wallace, S. S. (1987). The relationship between radiation-induced and transposon-induced genetic damage during Drosophila spermatogenesis. Mutation Research 179, 183195.CrossRefGoogle ScholarPubMed
Margulies, L., Griffith, C. S., Dooley, J. C. & Wallace, S. S. (1989). The interaction between transposon mobility and X rays in Drosophila: hybrid sterility and chromosome loss. Mutation Research 215, 114.Google Scholar
Margulies, L. (1990). A high level of hybrid dysgenesis in Drosophila: high thermosensitivity, dependence on DNA repair and incomplete cytotype regulation. Molecular General Genetics 220, 448455.CrossRefGoogle ScholarPubMed
Maw, H., Wallace, S. S. & Margulies, L. (1988). Radiation-induced and transposon-induced chromosome damage in Drosophila: translocations and transmission distortion. Radiation Research 115, 503515.Google Scholar
Misra, S. & Rio, D. C. (1990). Cytotype control of Drosophila P-element transposition: The 66 kDa protein is a repressor of transposase activity. Cell 62, 269284.CrossRefGoogle Scholar
Nitasaka, E., Mukai, T. & Yamazaki, T. (1987). Represser of P elements in Drosophila melanogaster: cycotype determination by a defective P element carrying only open reading frames 0 through 2. Proceedings of the National Academy of Sciences USA 84, 76057608.Google Scholar
O'Hare, K. & Rubin, G. M. (1983). Structure of P transposable elements in Drosophila melanogaster and their sites of insertion and excision. Cell 34, 2535.CrossRefGoogle ScholarPubMed
Rockwell, R. F., Findlay, C. S. & Cooke, F. (1987). Is there an optimum clutch size in snow geese? American naturalist 130, 836863.CrossRefGoogle Scholar
Rio, D. C., Laski, F. A. & Rubin, G. M. (1986). Identification and immunochemical analysis of biologically active Drosophila P element transposase. Cell 44, 2132.Google Scholar
Roiha, H., Rubin, G. M. & O'Hare, K. (1988). P element insertions and rearrangements at the singed locus of Drosophila melanogaster. Genetics 119, 7583.CrossRefGoogle ScholarPubMed
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
Rubin, G. M. & Spradling, A. C. (1982). Genetic trans-formation of Drosophila with transposable element vectors. Science 218, 348353.CrossRefGoogle Scholar
Schaeffer, R., Kidwell, M. G. & Faysto-Sterling, A. (1979). Hybrid dysgenesis in Drosophila melanogaster: morphological and cytological studies of ovarian dysgenesis. Genetics 92, 11411152.CrossRefGoogle Scholar
Sehested, K. (1970). The Fricke dosimeter. In Manual on Radiation Dosimetry (ed. Holm, N. W. and Berry, R. J.). New York, Marcel Dekker, Inc.Google Scholar
Shrimpton, A. E., MacKay, T. F. C. & Leigh, Brown A. J. (1990). Transposable element-induced response to artificial selection in Drosophila melanogaster: molecular analysis of selection lines. Genetics 125, 803811.Google Scholar
Simmoms, G. M. (1987). Sterility-mutability correlation. On the correlation between sterility and mutability during P-M hybrid dysgenesis in Drosophila melanogaster. Genetical Research 50, 7376.Google Scholar
Simmons, M. J. & Lim, J. K. (1980). Site specificity of mutations arising in dysgenic hybrids of Drosophila melanogaster. Proceedings of the National Academy of Science, USA 77, 60426046.Google Scholar
Simmons, M. J., Johnson, N. A., Fahey, T. M., Nellett, S. M. & Raymond, J. D. (1980). Analysis of dysgenesis-induced lethal mutations on the chromosome of a Q strain of Drosophila melanogaster. Genetics 107, 4963.Google Scholar
Simmons, M. J. & Bucholz, L. M. (1985). Transposase titration in Drosophila melanogaster: a model of cytotype in the P–M system of hybrid dysgenesis. Proceedings of the National Academy of Sciences, USA 82, 81198123.Google Scholar
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
Slatko, B. E., Mason, J. M. & Woodruff, R. C. (1984). The DNA transposition system of hybrid dysgenesis in Drosophila melanogaster can function despite defects in host DNA repair. Genetical Research 43, 159171.Google Scholar
Sokal, R. R. & Rohlf, J. F. (1981). Biometry. W. H. Freeman & Co., New York.Google Scholar
Spradling, A. C. & Rubin, G. M. (1982). Transposition of cloned P elements into Drosophila germline chromosomes. Science 218, 341347.CrossRefGoogle Scholar
Voelker, R. A., Greenleaf, A. L., Gyurkovics, H., Wisely, G. B., Huang, S. M. & Searles, L. L. (1984). Frequent imprecise excision among reversions of a P-element caused lethal mutation in Drosophila. Genetics 107, 279294.CrossRefGoogle ScholarPubMed