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Mutability, sterility and suppression in P—M hybrid dysgenesis: the influence of P subline, cross, chromosome, sex and P-element structure

Published online by Cambridge University Press:  14 April 2009

Yuan Wang ,
Howard Balter ,
Max Levitan  and
Lola Margulies
Yuan Wang
Affiliation:
Department of Microbiology and Immunology, New York Medical College, Valhalla, NY 10595
Howard Balter
Affiliation:
Biology Department, Bronx Community College, Bronx, NY 10453
Max Levitan
Affiliation:
Department of Cell Biology and Anatomy, Mount Sinai School of Medicine, CUNY, NY 10029
Lola Margulies*
Affiliation:
Department of Microbiology and Immunology, New York Medical College, Valhalla, NY 10595
*
* Corresponding author.
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Three Harwich P sublines with different P-element activity potential were used to investigate the influence of P-derived chromosomes on snω mutability and vg suppression and to relate the induction of these dysgenic traits to the number and structure of P elements. Destabilization of the snω allele, a measure of P transposase activity, was differentially influenced by the major autosomes. Chromosome 2 of the standard Harwich subline, Hw, induced only 60% of the level of mutability relative to chromosome 3, whereas chromosome 3 of the weakest Harwich subline, Hf, induced only 50% of the mutability relative to chromosome 2. In somatic suppression of the vg21–3 allele, chromosome 3 of the Hf subline produced a lower level of complete suppression as compared to chromosome 3 of the Hw or the Hs subline (the high hybrid-dysgenesis-inducing subline). The level of these dysgenic traits and GD sterility, was not correlated with the number of P elements per individual (67–68) or per chromosome arm which was very similar among the sublines. The number of complete P elements per genome, based on Southern blot analysis of the X and major autosomes, ranged from 15 to 19. Destabilization of the snω allele and vg suppression by chromosome 3 was correlated with a greater number of complete P elements. Two novel unexpected observations emerged from these studies: both snω mutability and vg suppression data demonstrated high P-element activity in hybrids derived from non-dysgenic crosses irrespective of Harwich subline, indicating a lack of P-cytotype regulation. Mutability in non-dysgenic males ranged from 40 to 60% of the level found in dysgenic males. The high snω mutability and low GD sterility in non-dysgenic hybrids suggests that these traits may arise by a different mechanism.

Type
Research Article
Information
Genetics Research , Volume 62 , Issue 2 , October 1993 , pp. 111 - 123
Copyright
Copyright © Cambridge University Press 1993

References

Baiter, H., Griffith, C. S. & Margulies, L. (1992). Radiation and transposon-induced genetic damage in Drosophila melanogaster: X-ray dose-response and synergism with DNA-repair deficiency. Mutation Research 267, 31–42.Google Scholar
Biemont, C., Ronsseray, S., Anxolabehere, D., Izaabel, H. & Gautier, C. (1990). Localization of P elements, copy number regulation and cytotype determination in Drosophila melanogaster. Genetical Research 56, 3–14.CrossRefGoogle ScholarPubMed
Bingham, P. M., Lewis, R. & Rubin, G. M. (1981). The cloning of the DNA sequences from the white locus of Drosophila melanogaster using a novel and general method. Cell 25, 693–704.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 P strain specific transposon family. Cell 29, 995–1004.CrossRefGoogle 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, 4125–4135.CrossRefGoogle Scholar
Daniels, S. B., Clark, S. H., Kidwell, M. G. & Chovnick, A. (1987). Genetic transformation of Drosophila melanogaster with an autonomous P element: Pnenotypic and molecular analysis of long-established transformed lines. Genetics 115, 711–723.CrossRefGoogle Scholar
Engels, W. R. (1979 a). Hybrid dysgenesis in Drosophila melanogaster: rules of inheritance of female sterility. Genetical Research 33, 219–236.CrossRefGoogle Scholar
Engels, W. R. (1979 b). Extrachromosomal control of mutability in Drosophila melanogaster. Proceedings of the National Academy of Sciences, USA 76, 4011–4015.CrossRefGoogle ScholarPubMed
Engels, W. R. (1979 c). The estimation of mutation rates when premeiotic events are involved. Environmental Mutagenesis 1, 37–43.CrossRefGoogle ScholarPubMed
Engels, W. R. (1981). Germline mutability in Drosophila and its relation to hybrid dysgenesis and cytotype. Genetics 98, 565–587.CrossRefGoogle ScholarPubMed
Engels, W. R. (1984). A trans-acting product needed for P factor transposition. Science 226, 1194–1196.CrossRefGoogle ScholarPubMed
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., Engels, W. R. & Preston, C. R. (1979). Hybrid dysgenesis in Drosophila melanogaster: The biology of female and male sterility. Genetics 92, 161–174.CrossRefGoogle ScholarPubMed
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, 1003–1013.CrossRefGoogle ScholarPubMed
Kidwell, M. G. (1983). Hybrid dysgenesis in Drosophila melanogaster.: factors affecting_chromosomal contamination in the P—M system. Genetics 104, 317–341.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 86, 813–833.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, 1127–1140.CrossRefGoogle ScholarPubMed
Kokur, 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, 1147–1163.CrossRefGoogle Scholar
Lai, C. & Mackay, T. F. C. (1990). Hybrid dysgenesis-induced quantitative variation on the X chromosome of Drosophila melanogaster. Genetics 124, 627–636.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, 7–19.CrossRefGoogle ScholarPubMed
Lindsley, D. & Zimm, G. (1992). The Genome of Drosophila melanogaster. New York: Academic Press.Google Scholar
Mackay, T. F. C. (1986). Transposable element induced fitness mutations in Drosophila melanogaster. Genetical Research 48, 77–87.CrossRefGoogle Scholar
Mackay, T. F. C. (1987). Transposable element-induced polygenic mutations in Drosophila melanogaster. Genetical Research 49, 225–233.CrossRefGoogle 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., 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, 1–14.CrossRefGoogle 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, 448–455.CrossRefGoogle ScholarPubMed
Margulies, L. & Griffith, C. S. (1991). The synergistic effect of X-rays and deficiencies in DNA repair in P—M hybrid dysgenesis in Drosophila melanogaster. Genetical Research 58, 15–26.CrossRefGoogle Scholar
Misra, S. & Rio, D. C. (1990). Cytotype control of Drosophila P element transposition: The 66 kd protein is a repressor of transposase activity. Cell 62, 269–284.CrossRefGoogle ScholarPubMed
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, USA 84, 7605–7608.CrossRefGoogle 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, 25–35.CrossRefGoogle ScholarPubMed
Rio, D. C. (1990). Molecular mechanisms regulating Drosophila P element transposition. Annual Review in Genetics 24, 543–578.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, 21–32.CrossRefGoogle ScholarPubMed
Robertson, H. M., Preston, C. R., Phillis, R. W., Johnson-Schlitz, D. M., Benz, W. K. & Engels, W. R. (1988). A stable genomic source of P element transposase in Drosophila melanogaster. Genetics 118, 461–470.CrossRefGoogle ScholarPubMed
Rockwell, R. F., Findlay, C. S. & Cooke, F. (1987). Is there an optimum clutch size in snow geese? American Naturalist 130, 836–863.CrossRefGoogle Scholar
Roiha, H., Rubin, G. M. & O'Hare, K. (1988). P element insertions and rearrangements at the singed locus of Drosophila melanogaster. Genetics 119, 75–83.CrossRefGoogle ScholarPubMed
Rubin, G. M. (1984). Analysis of P transposable element functions in Drosophila. Cell 38, 135–146.Google Scholar
Schaeffer, R., Kidwell, M. G. & Faysto-Sterling, A. (1979). Hybrid dysgenesis in Drosophila melanogaster: morphological and cytological studies of ovarian dysgenesis. Genetics 92, 1141–1152.CrossRefGoogle Scholar
Shrimpton, A. E., Mackay, T. F. C. & Brown, A. J. Leigh (1990). Transposable element-induced response to artificial selection in Drosophila melanogaster: molecular analysis of selection lines. Genetics 125, 803–811.CrossRefGoogle ScholarPubMed
Simmons, G. M. (1987). Sterility—mutability correlation. On the correlation between sterility and mutability during P—M hybrid dysgenesis in Drosophila melanogaster. Genetical Research 50, 73–76.CrossRefGoogle Scholar
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, 663–676.CrossRefGoogle ScholarPubMed
Torkamanzehi, A., Moran, C. & Nicholas, F. W. (1988). P element induced mutation and quantitative variation in Drosophila melanogaster: Lack of enhanced response to selection in lines derived from dysgenic crosses. Genetical Research 51, 231–238.CrossRefGoogle Scholar
Williams, J. A., Pappu, S. S. & Bell, J. B. (1988 a). Sup-pressible P-element alleles of the vestigial locus in Drosophila melanogaster. Molecular and General Genetics 212, 370–374.CrossRefGoogle Scholar
Williams, J. A., Pappu, S. S. & Bell, J. B. (1988 b). Molecular analysis of hybrid dysgenesis-induced derivatives of a P-element allele at the vg locus. Molecular and Cellular Biology 8, 1489–1497.Google ScholarPubMed