Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-22T23:54:36.189Z Has data issue: false hasContentIssue false

IR hybrid dysgenesis increases the frequency of recombination in Drosophila melanogaster

Published online by Cambridge University Press:  14 April 2009

Marie-Christine Chaboissier
Affiliation:
Centre de Génétique Moléculaire, CNRS, 91 198 Gif-sur-Yvette, France
Françoise Lemeunier
Affiliation:
Populations, Génétique et Evolution, CNRS, 91 198 Gif-sur- Yvette, France
Alain Bucheton*
Affiliation:
Centre de Génétique Moléculaire, CNRS, 91 198 Gif-sur-Yvette, France
*
Alain Bucheton, Centre de Génétique Moléculaire, CNRS, 91198 Gif-sur-Y vette, France, Phone: 33 1 69 82 32 77; Fax: 33 1 69 82 43 86; E-mail: [email protected].
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.

The I factor is a LINE-like transposable element responsible for the I-R system of hybrid dysgenesis in Drosophila melanogaster. Inducer strains of this species contain several I factors whereas reactive strains do not. I factors are stable in inducer strains, but transpose at high frequency in the germ-line of females, known as SF females, produced by crossing reactive females and inducer males. Various abnormalities occur in SF females, most of which result from this high rate of transposition. We report here that recombination is increased in the germ-line of these females. This is a new characteristic of the I-R system of hybrid dysgenesis that might also be associated with transposition of the I factor.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1995

References

Abad, P., Vaury, C., Pélisson, A., Chaboissier, M. C, Busseau, I., & Bucheton, A., (1989). A long interspersed repetitive element — the I factor of Drosophila teissieri — is able to transpose in different Drosophila species. Proceedings of the National Academy of Sciences, USA 86, 88878891.CrossRefGoogle ScholarPubMed
Ashburner, M., (1989). Drosophila. A Laboratory Manual. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.Google Scholar
Biessman, H., Champion, L. E., O'Hair, M., Ikenaga, K., Kasravi, B., & Mason, J., (1992). Frequent transpositions of Drosophila melanogaster HeT-A transposable elements to receding chromosome ends. EMBO Journal 11, 44594469.CrossRefGoogle Scholar
Bratthauer, G. L., & Fanning, T. G., (1992). Active LINE-1 retrotransposons in human testicular cancer. Oncogene 7, 507510.Google ScholarPubMed
Bucheton, A., (1990). I transposable elements and I-R hybrid dysgenesis in Drosophila. Trends in Genetics 6, 1621.CrossRefGoogle ScholarPubMed
Bucheton, A., Lavige, J. M., Picard, G., & L'Heritier, P., (1976). Non-mendelian female sterility in Drosophila melanogaster: quantitative variations in the efficiency of inducer and reactive strains. Heredity 36, 305314.CrossRefGoogle ScholarPubMed
Bucheton, A., Paro, R., Sang, H. M., Pélisson, A., & Finnegan, D. J., (1984). The molecular basis of I-R hybrid dysgenesis in Drosophila melanogaster: identification, cloning and the properties of the I factor. Cell 38, 153163.CrossRefGoogle ScholarPubMed
Bucheton, A., & Picard, G., (1978). Non-mendelian female sterility in Drosophila melanogaster: hereditary transmission of the reactive levels. Heredity 40, 207223.CrossRefGoogle Scholar
Busseau, I., Pélisson, A., & Bucheton, A., (1989 a). Characterization of 5' truncated copies of the I factor in Drosophila melanogaster. Nucleic Acids Research 17, 69396945.CrossRefGoogle ScholarPubMed
Busseau, I., Pélisson, A., & Bucheton, A. (1989 b). I elements of Drosophila melanogaster generate specific chromosomal rearrangements during transposition. Molecular and General Genetics 218, 222228.CrossRefGoogle ScholarPubMed
Chaboissier, M. C, Busseau, I., Prosser, J., Finnegan, D. J., & Bucheton, A., (1990). Identification of a potential RNA intermediate for transposition of the LINE-like element I factor of Drosophila melanogaster. EMBO Journal 9, 35573563.CrossRefGoogle ScholarPubMed
Crozatier, M., Vaury, C., Busseau, I., Pélisson, A., & Bucheton, A., (1988). Structure and genomic organization of I elements involved in I-R hybrid dysgenesis in Drosophila melanogaster. Nucleic Acids Research 16, 91999213.CrossRefGoogle ScholarPubMed
Dombroski, B. A., Mathias, S. L., Nanthakumar, E., Scott, A. F., & Kazazian, H. H., (1991). Isolation of an active human transposable element. Science 254, 18051808.CrossRefGoogle ScholarPubMed
Dombroski, B. A., Scott, A. F., & Kazazian, H. H., (1993). Two additional potential retrotransposons isolated from a human L1 subfamily that contains an active retrotransposable element. Proceedings of the National Academy of Sciences, USA 90, 65136517.CrossRefGoogle ScholarPubMed
Engels, W. R., (1989). P elements in Drosophila. In Mobile DNA (ed. Berg, D. E. and Howe, M. M.), pp. 437484. Washington D.C.: American Society of Microbiology.Google Scholar
Fawcett, D. H., Lister, C. K., Kellett, E., & Finnegan, D. J., (1986). Transposable elements controlling I-R hybrid dysgenesis in D. melanogaster are similar to mammalian LINEs. Cell 47, 10071015.CrossRefGoogle Scholar
Finnegan, D. J., (1989). The I factor and IR hybrid dysgenesis in Drosophila. In Mobile DNA (ed. Berg, D. E. and Howe, M. M.), pp. 503518. Washington D.C.: American Society of Microbiology.Google Scholar
Gans, M., Audit, C., & Masson, M., (1975). Isolation and characterization of sex-linked female sterile mutants in Drosophila melanogaster. Genetics 81, 683704.CrossRefGoogle ScholarPubMed
Geyer, P. K., & Corces, V. G., (1987). Separate regulatory elements are responsible for the complex pattern of tissue specific and developmental transcription of the yellow locus in Drosophila melanogaster. Genes and Development 1, 9961004.CrossRefGoogle ScholarPubMed
Hiraizumi, Y., (1981). Heterochromatic recombination in germ cells of Drosophila melanogaster females. Genetics 98, 105114.CrossRefGoogle ScholarPubMed
Jensen, S., Cavarec, L., Dhellin, O. & Heidmann, T., (1994). Retrotransposition of a marked Drosophila line-like I element in cells in culture. Nucleic Acids Research 22, 14841488.CrossRefGoogle ScholarPubMed
Jensen, S., & Heidmann, T., (1991). An indicator gene of germline retrotransposition in transgenic Drosophila demonstrates RNA-mediated transposition of the LINE I element. EMBO Journal 10, 19271937.CrossRefGoogle ScholarPubMed
Kazazian, H. H., Wong, C, Youssoufian, H., Scott, A. F., Philipp, D. G., & Antonarakis, S. E., (1988). Haemophilia A resulting from de novo insertion of LI sequences represents a novel mechanism for mutation in man. Nature 332, 164166.CrossRefGoogle Scholar
Lavige, J. M., (1986). I-R system of hybrid dysgenesis in Drosophila melanogaster: further data on the arrest of development of the embryos from SF females. Biology of the Cell 56, 207216.Google Scholar
Levis, R. W., Ganesan, R., Houtchens, K., Tolar, L. A., & Sheen, F., (1993). Transposons in place of telomeric repeats at a Drosophila telomere. Cell 75, 10831093.CrossRefGoogle Scholar
Lindsley, D. L., & Zimm, G. G., (1992). The Genome of Drosophila melanogaster. San Diego: Academic Press.Google Scholar
Maniatis, T., Fritsch, E. F., & Sambrook, J., (1989). Molecular Cloning: A Laboratory Manual 2nd edn.Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.Google Scholar
McLean, C., Bucheton, A., & Finnegan, D. J., (1993). The 5′ untranslated region of the I factor, a Long Interspersed Nuclear Element-like retrotransposon of Drosophila melanogaster, contains an internal promoter and sequences that regulate expression. Molecular and Cellular Biology 13, 10421050.Google ScholarPubMed
Miki, Y., Nishisho, I., Horii, A., Miyoshi, Y., Utsunomiya, J., Kinzler, K. W., Vogelstem, B., & Nakamura, Y., (1992). Disruption of the APCgene by a retrotransposal insertion of LI sequence in a colon cancer. Cancer Research 52, 643645.Google Scholar
Morse, B., Rotherg, P. G., South, V. J., Spandorfer, J. M., & Astrin, S. M., (1988). Insertional mutagenesis of the c-myc locus by a LINE-1 sequence of a human breast carcinoma. Nature 333, 8790.CrossRefGoogle ScholarPubMed
Narita, N., Nishio, H., Kitoh, Y., Ishikawa, Y., Minami, R., Kanamura, H., & Matsuo, M., (1993). Insertion of the 5′ truncated LI element into the 3' end of exon 44 of the dystrophin gene resulted in skipping of the exon during splicing in a case of Duchenne muscular dystrophy. Journal of Clinical Investigation 91, 18621867.CrossRefGoogle Scholar
Pearlman, R. E., Tsao, N., & Moens, P. B., (1992). Synaptonemal complexes from DNase-treated rat pachytene politicals contain (GT)n and LINE/SINE sequences. Genetics 130, 865872.CrossRefGoogle Scholar
Pélisson, A., (1981). The I-R system of hybrid dysgenesis in Drosophila melanogaster: are I factor insertions responsible for the mutator effect of the I-R interaction? Molecular and General Genetics 183, 123129.CrossRefGoogle ScholarPubMed
Pélisson, A., & Bregliano, J. C., (1981). The I-R system of hybrid dysgenesis in Drosophila melanogaster: construction and characterization of a non-inducer stock. Biology of the Cell 40, 159164.Google Scholar
Pélisson, A., Finnegan, D. J., & Bucheton, A., (1991). Evidence for retrotransposition of the I factor, a LINE element of Drosophila melanogaster. Proceedings of the National Academy of Sciences, USA 88, 49074910.CrossRefGoogle ScholarPubMed
Picard, G., (1976). Non-mendelian female sterility in Drosophila melanogaster: hereditary transmission of I factor. Genetics 83, 107123.CrossRefGoogle ScholarPubMed
Picard, G., (1978). Non-mendelian female sterility in Drosophila melanogaster: further data on chromosomal contamination. Molecular and General Genetics 164, 235247.CrossRefGoogle Scholar
Picard, G., Bregliano, J. C, Bucheton, A., Lavige, J. M., Pelisson, A., & Kidwell, M. G., (1978). Non-mendelian female sterility and hybrid dysgenesis in Drosophila melanogaster. Genetical Research 32, 275287.CrossRefGoogle ScholarPubMed
Picard, G., & L'Heritier, P. H., (1971). A maternally inherited factor inducing sterility in D. melanogaster. Drosophila Information Service 46, 54.Google Scholar
Proust, J., & Prudhommeau, C., (1982). Hybrid dysgenesis in Drosophila melanogaster. I. Further evidence for, and characterization of, the mutator effect of the inducerreactive interaction. Mutation Research 95, 225235.CrossRefGoogle ScholarPubMed
Proust, J., Prudhommeau, C., Ladevèze, V., Gotteland, M., & Fontyne-Blanchard, M. C., (1992). I-R hybrid dysgenesis in Drosophila melanogaster. Use of in situ hybridization to show the association of the I factor DNA with induced sex-linked recessive lethals. Mutation Research 268, 265285.CrossRefGoogle ScholarPubMed
Prudhommeau, C., & Proust, J., (1990). Hybrid dysgenesis in Drosophila melanogaster: nature and site specificity of induced recessive lethals. Mutation Research 230, 135157.CrossRefGoogle ScholarPubMed
Rubin, G. M., & Spradling, A. C., (1983). Vectors for P element-mediated gene transfer in Drosophila genome. Nucleic Acids Research 11, 63416351.CrossRefGoogle Scholar
Sang, H. M., Pelisson, A., Bucheton, A., & Finnegan, D. J., (1984). Molecular lesions associated with white gene mutations induced by I-R hybrid dysgenesis in Drosophila melanogaster. EMBO Journal 3, 30793085.CrossRefGoogle Scholar
Spradling, A. C., & Rubin, G. M., (1982). Genetic transformation of Drosophila with transposable element vectors. Science 218, 348353.Google Scholar
Tatout, C., Docquier, M., Lachaume, P., Mesure, M., Lecher, P., & Pinon, H., (1994). Germ-line expression of a functional LINE from Drosophila melanogaster: fine characterization allows for potential investigations of trans-regulators. International Journal of Developmental Biology 38, 2733.Google ScholarPubMed
Vaury, C., Abad, P., Pélisson, A., Lenoir, A., & Bucheton, A., (1990). Molecular characteristics of the heterochromatic I elements from a reactive strain of Drosophila melanogaster. Journal of Molecular Evolution 31, 424431.CrossRefGoogle ScholarPubMed