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Natural Repressors of P-induced hybrid dysgenesis in Drosophila melanogaster: a model for repressor evolution

Published online by Cambridge University Press:  14 April 2009

P. Corish ,
D. M. Black ,
D. W. Featherston ,
J. Merriam  and
G. A. Dover
P. Corish
Affiliation:
Department of Genetics, Adrian Building, University of Leicester, University Road, Leicester LEI 7RH, UK
D. M. Black
Affiliation:
Beatson Institute for Cancer Research, Garscube Estate, Switchback Road, Bearden, Glasgow, Scotland
D. W. Featherston
Affiliation:
Katholieke Universiteit, 6525 ED, Nijmegen, Netherlands
J. Merriam
Affiliation:
Department of Biology, University of California, Los Angeles, 405 Hilgard Avenue, CA 90024, USA
G. A. Dover
Affiliation:
Department of Genetics, Adrian Building, University of Leicester, University Road, Leicester LEI 7RH, UK
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Type I repressors control P element transposition and comprise full length elements and elements with small 3′ deletions in the final exon. Using a sensitive assay for measuring the strength of repression of P element transposition in somatic and germline tissues, we have isolated and characterized a naturally occurring type I repressor element from a Q population of Drosophila melanogaster. We demonstrate that the almost complete repression of transposition in this population is a mixture of KP elements with intermediate levels of repression, and the strong contribution of a single 2·6 kb P element deletion derivative, which we call SR (Strong Repressor). A deletion in the final intron of SR allows for the constitutive production of a putative 75 kDa repressor protein in germline tissues in addition to the production of the 66 kDa repressor in the soma, which would result in a biparental mode of inheritance of repression. Basedon the four observed classes of natural Q populations, we propose a model in which populations containing SR-like elements, capable of producing strong type I repressor constitutively, have a selective advantage over populations which rely either on maternally transmitted P cytotype or on KPinduced weak levels of repression. Such populations may subsequently spread and constitute an evolutionary stable strategy for the repression of hybrid dysgenesis in Drosophila melanogaster.

Type
Research Article
Information
Genetics Research , Volume 67 , Issue 2 , April 1996 , pp. 109 - 121
Copyright
Copyright © Cambridge University Press 1996

References

Andrews, J. D., & Gloor, G. B., (1995). A role for the KP leucine zipper in regulating P element transposition in Drosophila melanogaster. Genetics 141, 587–594.Google Scholar
Black, D. M., Jackson, M. S., Kidwell, M. G., & Dover, G. A., (1987). KP elements repress P-induced hybrid dysgenesis in Drosophila melanogaster. EM BO Journal 6, 4125–4135.Google Scholar
Boussy, I. A., Healy, M. J., Oakeshott, J. G., & Kidwell, M. G., (1988). Molecular analysis of the P, M gonadal dysgenesis cline in eastern Australian Drosophila melanogaster. Genetics 119, 889–902.CrossRefGoogle Scholar
Engels, W. R., (1984). A trans-acting product needed for P factor transposition in Drosophila. 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. M.). 437–484.Google Scholar
Engels, W. R., Johnsonschlitz, D. M., Eggleston, W. B., & Sved, J., (1990). High-frequency P element loss in Drosophila is homolog dependent. Cell 62, 515–525.CrossRefGoogle ScholarPubMed
Gloor, G. B., Preston, C. R., Johnsonschlitz, D. M. et al. , (1993). Type I repressors of P element mobility. Genetics 135, 81–95.CrossRefGoogle ScholarPubMed
Hazelrigg, T., Levis, R., & Rubin, G. M., (1984). Transformation of white locus DNA in Drosophila — dosage compensation, zeste interaction, and position effects. Cell 36, 469–481.Google Scholar
Jackson, M. S., Black, D. M. and Dover, G. A., (1988). Amplification of KP elements associated with the repression of hybrid dysgenesis in Drosophila melanogaster. Genetics 120, 1003–1013.Google Scholar
Karn, J., Matthes, H. W. D., Gait, M. J., & Brenner, S., (1984). A new selective phage cloning vector, lambda-2001, with sites for Xba I, Bam HI, Hind III, Eco RI, Sst 1 and Xho I. Gene 32, 217–224.CrossRefGoogle 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 36, 813–833.CrossRefGoogle Scholar
Kidwell, M. G., (1983). Evolution of hybrid dysgenesis determinants in Drosophila melanogaster. Proceedings of The National Academy of Sciences of The United States of America Biological Sciences 80, 1655–1659.CrossRefGoogle ScholarPubMed
Kidwell, M. G., Kimura, K., & Black, D. M., (1988). Evolution of hybrid dysgenesis potential following P element contamination in Drosophila melanogaster. Genetic 119, 815–828.CrossRefGoogle ScholarPubMed
Kidwell, M. G., (1992). Horizontal transfer of P-elements and other short inverted repeat transposons. Genetica 86, 275–286.CrossRefGoogle ScholarPubMed
Lansman, R. A., Shade, R. O., Grigliatti, T. A., & Brock, H. W., (1987). Evolution of P transposable elementssequences of Drosophila nebulosa P elements. Proceedings of The National Academy of Sciences of The United States of America 84, 6491–6495.CrossRefGoogle ScholarPubMed
Laski, F. A., Rio, D. C., & Rubin, G. M., (1986). Tissue specificity of Drosophila P element transposition is regulated at the level of mRNA splicing. Cell 44, 7–19.Google Scholar
Lemaitre, B., & Coen, D., (1991). P-regulatory products repress in vivo the P promoter activity in P-lacz fusion genes. Proceedings of The National Academy of Sciences of The United States of America 88, 4419–4423.CrossRefGoogle Scholar
Lemaitre, B., Ronsseray, S., & Coen, D., (1993). Maternal repression of the P element promoter in the germline of Drosophila melanogaster — a model for the P cytotype. Genetics 135, 149–160.Google Scholar
Lindsley, D. L., & Zimm, G. G., (1992). ‘The Genome of Drosophila melanogaster.’ Academic Press.Google Scholar
Smith, J. Maynard, (1982). ‘Evolution and the Theory of Games.’ Cambridge University Press.CrossRefGoogle Scholar
Mian, A., & Dover, G. A., (1990). Promoter variation in the ribosomal-RNA genes in Drosophila melanogaster. Nucleic Acids Research 18, 3795–3801.CrossRefGoogle ScholarPubMed
Miller, W. J., Hagemann, S., Reiter, E., & Pinsker, W., (1992). P element homologous sequences are tandemly repeated in the genome of Drosophila guanche. Proceedings of The National Academy of Sciences of The United States of America 89, 4018–4022.CrossRefGoogle ScholarPubMed
Misra, S., Buratowski, R. M., Ohkawa, T., & Rio, D. C., (1993). Cytotype control of Drosophila melanogaster P element transposition — genomic position determines maternal repression. Genetics 135, 785–800.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, 269–284.Google Scholar
Nitasaka, E., Mukai, T., & Yamazaki, T., (1987). Repressor of P elements in Drosophila melanogaster — cytotype determination by a defective element carrying only open reading frames 0 through 2. Proceedings of The National Academy of Sciences of The United States of America 84, 7605–7608.CrossRefGoogle Scholar
O'Hare, K., Driver, A., Mcgrath, S., & Johnsonschiltz, D. M., (1992). Distribution and structure of cloned P elements from the Drosophila melanogaster P strain PI. Genetical Research 60, 33–41.Google Scholar
O'Hare, K., & Rubin, G. M., (1983). Structures of P transposable elements and their sites of insertion and excision in the Drosophila melanogaster genome. Cell 34, 25–35.Google Scholar
Paricio, N., Perezalonso, M., Martinezsebastian, M. J., & Defrutos, R., (1991). P sequences of Drosophila subobscura lack exon-3 and may encode a 66-kDa repressor-like protein. Nucleic Acids Research 19, 6713–6718.CrossRefGoogle Scholar
Paricio, N., Martinezsebastian, M. J., & Defrutos, R., (1994). A heterochromatic P sequence in the D. subobscura genome. Genetica 92, 177–186.Google Scholar
Preston, C. R., & Engels, W. R., (1989). Spread of P transposable elements in inbred lines of Drosophila melanogaster. Progress in Nucleic Acid Research and Molecular Biology 36, 71–85.Google Scholar
Rasmusson, K. E., Raymond, J. D., & Simmons, M. J., (1993). Repression of hybrid dysgenesis in Drosophila melanogaster by individual naturally-occurring P elements. Genetics 133, 605–622.CrossRefGoogle ScholarPubMed
Rio, D. C., (1990). Molecular mechanisms regulating Drosophila P element transposition. Annual Review of Genetics 24, 543–578.CrossRefGoogle ScholarPubMed
Robertson, H. M., & Engels, W. R., (1989). Modified P elements that mimic the P cytotype in Drosophila melanogaster. Genetics 123, 815–824.Google Scholar
Robertson, H. M., Preston, C. R., Phillis, R. W. et al. , (1988). A stable genomic source of P element transposase in Drosophila melanogaster. Genetics 118, 461–470.Google Scholar
Roche, S. E., Schiff, M., & Rio, D. C., (1995). P-element repressor autoregulation involves germ-line transcriptional repression and reduction of third intron splicing. Genes & Development 9, 1278–1288.CrossRefGoogle ScholarPubMed
Ronserray, S., Lehmann, M., & Anxolabehere, D., (1991). The maternally inherited regulation of P elements in Drosophila melanogaster can be elicited by 2 P copies at cytological site 1A on the X-chromosome. Genetics 129, 501–512.Google Scholar
Sambrook, J., Fritsch, E. F., & Maniatis, T., (1989). ‘Molecular Cloning—A Laboratory Manual.’ Cold Spring Harbor Laboratory Press.Google Scholar
Sakoyama, Y., Tod, T., Isiwachigusa, S. et al. , (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 of The United States of America 82, 6236–6239.CrossRefGoogle ScholarPubMed
Siebel, C. W., Admon, A., & Rio, D. C., (1995). Somaspecific expression and cloning of PSI, a negative regulator of P element pre-messenger-RNA splicing. Genes & Development 9, 269–283.Google Scholar
Williams, J. A., Pappu, S. S., & Bell, J. B., (1988). Suppressible P element alleles of the vestigial locus in Drosophila melanogaster. Molecular and General Genetics 212, 370–374.Google Scholar