Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-26T13:54:19.512Z Has data issue: false hasContentIssue false

Mapping and characterization of P-element-induced mutations at quantitative trait loci in Drosophila melanogaster

Published online by Cambridge University Press:  14 April 2009

Chaoqiang Lai*
Affiliation:
Departments of Genetics, University of Edinburgh and North Carolina State University
Trudy F. C. Mackay
Affiliation:
Departments of Genetics, University of Edinburgh and North Carolina State University
*
* 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 chromosomes derived from crosses of inbred P and M Drosophila melanogaster strains that had extreme effects on abdominal and/or sternopleural bristle number in males, were further analyzed to determine their effects in females and to map the loci at which the mutations occurred. Seven lines that had on average 3.9 fewer sternopleural bristles than wildtype in males had average homozygous sternopleural bristle effects of −2·2. The bristle effects were partially recessive, with an average degree of dominance of −0·60. Physical mapping of the sternopleural bristle effects of these lines placed them all at approximately 24·7 cM. These mutations are apparently allelic on the basis of a complementation test, and deficiency mapping indicates they occur within chromosomal bands 8A4; 8C6. In situ hybridization analysis of the sites of P element insertions of these lines suggests that mutations probably resulted from excision of P elements at 8C on the original inbred P strain chromosome. Two additional lines, NDC(19) and DP(146), had reduced numbers of sternopleural and abdominal bristles. NDC(19) males had 9·7 fewer abdominal and 8·6 fewer sternopleural bristles than wildtype. The corresponding homozygous abdominal and sternopleural bristle number effects were −5·8 and −3·8, respectively; with the abdominal bristle effect completely recessive and the sternopleural bristle effect nearly additive. DP(146) males had 6·2 fewer abdominal and 4·1 fewer sternopleural bristles than wildtype, with homozygous abdominal bristle effects of −4·3 and sternopleural bristle effects of −2·0. Abdominal bristle effects of this line were partially recessive whereas the sternopleural bristle effects were additive. Physical mapping showed effects on both bristle traits segregated jointly in these two lines, with the NDC(19) mutation closely linked to y and the DP(146) mutation 0·17 cM from it. Complementation tests and deficiency mapping also indicate the mutations in lines NDC(19) and DP(146) are at closely linked but separate loci within chromosomal bands 1B2; 1B4–6 and 1B4–6; 1B10 respectively, with some epistatic effects. In situ hybridization analysis of sites of P element insertion suggest that the NDC(19) mutation, which may be a scute allele, was probably caused by a P element insertion in the IB region; the DP(146) mutation is also associated with an insertion at IB.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1993

References

Baker, B. S. & Belote, J. M. (1983). Sex determination and dosage compensation in Drosophila melanogaster. Annual Review of Genetics 17, 345393.CrossRefGoogle ScholarPubMed
Bier, E., Vaessin, H., Shepherd, S., Lee, K., McCall, K., Barbel, S., Ackerman, L., Carretto, R., Uemura, T., Grell, E., Jan, L. Y. & Jan, Y. N. (1989). Searching for pattern and mutation in the Drosophila genome with a P-lacZ vector. Genes and Development 3, 12731287.CrossRefGoogle ScholarPubMed
Bingham, P. M., Levis, 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, 693704.CrossRefGoogle ScholarPubMed
Bridges, C. B. (1938). A revised map of the salivary gland X-chromosome of Drosophila melanogaster. Journal of Heredity 29, 11.CrossRefGoogle Scholar
Caballero, A., Toro, M. A. & Lopez-Fanjul, C. (1991). The response to artificial selection from new mutations in Drosophila melanogaster. Genetics 128, 89102.CrossRefGoogle ScholarPubMed
Campuzano, S., Carramolino, L., Cabrera, C. V., Ruiz-Gomez, M., Villares, R., Boronat, A. & Modolell, J. (1985). Molecular genetics of the achaete-scute gene complex of D. melanogaster. Cell 40, 327338.CrossRefGoogle ScholarPubMed
Campuzano, S. & Modolell, J. (1992). Patterning the Drosophila nervous system: the achaete-scute gene complex. Trends in Genetics 8, 202208.CrossRefGoogle ScholarPubMed
Clayton, G. A. & Robertson, A. (1955). Mutation and quantitative variation. American Naturalist 89, 151158.CrossRefGoogle Scholar
Clayton, G. A. & Robertson, A. (1964). The effects of Xrays on quantitative characters. Genetical Research 5, 410422.CrossRefGoogle Scholar
Cooley, L., Kelley, R. & Spradling, A. (1986). Insertion mutagenesis of the Drosophila genome with single P elements. Science 239, 11211128.CrossRefGoogle Scholar
Dietrich, W., Katz, H., Lincoln, S. E., Shin, H.-S., Friedman, J., Dracopoli, N. C. & Lander, E. S. (1992). A genetic map of the mouse suitable for typing intraspecific crosses. Genetics 131, 423447.CrossRefGoogle ScholarPubMed
Durrant, A. & Mather, K. (1954). Heritable variation in a long inbred line of Drosophila. Genetica 27, 97119.CrossRefGoogle Scholar
East, E. M. (1916). Studies on size inheritance in Nicotiana. Genetics 1, 164176.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 for Microbiology.Google Scholar
Falconer, D. S. (1989). Introduction to Quantitative Genetics. Essex: Longman Scientific and Technical, Harlow.Google Scholar
Federoff, N. V. (1989). Maize transposable elements. In Mobile DNA (ed. Berg, D. E. and Howe, M. M.), pp. 375411. Washington D.C.: American Society for Microbiology.Google Scholar
Hill, W. G. & Knott, S. (1990). Identification of genes with large effects. In Advances in Statistical Methods for Genetical Improvement of Livestock (ed. Gianola, D. and Hammond, K.), pp. 477494. Berlin: Springer Verlag.CrossRefGoogle Scholar
Hollingdale, B. & Barker, J. S. F. (1971). Selection for increased abdominal bristle number in Drosophila melanogaster with concurrent irradiation. I. Populations derived from an inbred line. Theoretical and Applied Genetics 41, 208215.CrossRefGoogle ScholarPubMed
Jaenisch, R. (1980). Retro viruses and embryogenesis: microinjection of Moloney leukemia virus into midgestation mouse embroys. Cell 19, 181188.CrossRefGoogle Scholar
Jan, Y. N. & Jan, L. Y. (1990). Genes required for specifying cell fates in Drosophila embryonic sensory nervous systems. Trends in Neuroscience 13, 493498.CrossRefGoogle Scholar
Jenkins, N. A. & Copeland, N. G. (1985). High frequency germ-line acquisition of ecotropic MuLV proviruses in SWR/J-RF/J mice. Cell 43, 811819.CrossRefGoogle Scholar
Kitagawa, O. (1967). The effects of X-ray irradiation on selection response in Drosophila melanogaster. Japanese Journal of Genetics 42, 121137.Google Scholar
Lai, C. (1990). Quantitative genetic variation induced by P transposable elements in Drosophila melanogaster. Ph.D. thesis, University of Edinburgh.Google Scholar
Lai, C. & Mackay, T. F. C. (1990). Hybrid dysgenesisinduced quantitative variation on the X chromosome of Drosophila melanogaster. Genetics Y2A, 627636.CrossRefGoogle ScholarPubMed
Lefevre, G. (1976). A photographic representation and interpretation of the polytene chromosome of Drosophila melanogaster salivary glands. In The Genetics and Biology of Drosophila, 1a. (ed. Ashburner, M. and Novitski, E.). pp. 3166. New York: Academic Press.Google Scholar
Leigh, Brown A. J. & Moss, J. E. (1987). Transposition of the / element and copia in a natural population of Drosophila melanogaster. Genetical Research 49, 121128.CrossRefGoogle Scholar
Lindsley, D. L. and Zimm, G. G. (1992). The genome of Drosophila melanogaster. San Diego: Academic Press.Google Scholar
Lynch, M. (1988). The rate of polygenic mutation. Genetical Research 51, 137148.CrossRefGoogle ScholarPubMed
Mackay, T. F. C. (1985). Transposable element-induced response to artificial selection in Drosophila melanogaster. Genetics 111, 351374.CrossRefGoogle ScholarPubMed
Mackay, T. F. C. (1986). Transposable element-induced fitness mutations in Drosophila melanogaster. Genetical Research 48, 7787.CrossRefGoogle Scholar
Mackay, T. F. C. & Langley, C. H. (1990). Molecular and phenotypic variation in the achaete-scute region of Drosophila melanogaster. Nature 348, 6466.CrossRefGoogle ScholarPubMed
Mackay, T. F. C., Lyman, R. F. & Jackson, M. S. (1992). Effects of P element insertions on quantitative traits in Drosophila melanogaster. Genetics 130, 315332.CrossRefGoogle ScholarPubMed
Mather, K. & Wigan, L. G. (1942). The selection of invisible mutations. Proceedings of the Royal Society of London B 131, 5064.Google Scholar
Mayo, O. (1989). Identification of genes which influence quantitative traits. In Evolution and Animal Breeding (ed. Hill, W. G. and Mackay, T. F. C.), pp. 141146. Slough: CAB International.Google Scholar
McMillan, I. & Robertson, A. (1974). The power of methods for the detection of major genes affecting quantitative characters. Heredity 32, 349356.CrossRefGoogle ScholarPubMed
Mukai, T. (1979). Polygenic mutation. In Quantitative Genetic Variation, (ed. Thompson, J. N., Jr. and Thoday, J. M.). pp. 177195. New York: Academic Press.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
Ohnishi, O. (1977). Spontaneous and ethyl methanesulfonate-induced mutations controlling viability in Drosophila melanogaster. II. Homozygous effect of polygenic mutations. Genetics 87, 529545.CrossRefGoogle ScholarPubMed
Palmiter, R. D. & Brinster, R. L. (1986). Germ-line transformation of mice. Annual Review of Genetics 20, 465499.CrossRefGoogle ScholarPubMed
Paterson, A. H., Lander, E. S., Hewitt, J. D., Peterson, S., Lincoln, S. E. & Tanksley, S. D. (1988). Resolution of quantitative traits into Mendelian factors by using a complete RFLP linkage map. Nature 335, 721726.CrossRefGoogle Scholar
Paxman, G. J. (1957). A study of spontaneous mutation in Drosophila melanogaster. Genetica 29, 3957.CrossRefGoogle Scholar
Robertson, D. S. (1985). A possible technique for isolating genie DNA for quantitative traits in plants. Journal of Theoretical Biology 117, 110.CrossRefGoogle Scholar
Robertson, E., Bradley, A., Kuehn, M. & Evans, M. (1986). Germ-line transmission of genes introduced into cultured pluri-potential cells by retroviral vector. Nature 323, 445448.CrossRefGoogle Scholar
Serikawa, T., Kuramoto, T., Hilbert, P., Mori, M., Yamada, J., Dubay, C. J., Landpainter, K., Ganten, D., Guenet, J.-L., Lathrop, G. M. & Beckmann, J. S. (1992). Rat gene mapping using PCR-analyzed microsatellites. Genetics 131, 701721.CrossRefGoogle ScholarPubMed
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, 803811.CrossRefGoogle ScholarPubMed
Shrimpton, A. E., Montgomery, E. A. & Langley, C. H. (1986). OM mutations in Drosophila ananassae are linked to insertions of a transposable element. Genetics 114, 125135.CrossRefGoogle ScholarPubMed
Shrimpton, A. E. & Robertson, A., (1988 a). The isolation of polygenic factors controlling bristle score in Drosophila melanogaster. 1. Allocation of the third chromosome sternopleural bristle effects to chromosome sections. Genetics 118, 437443.CrossRefGoogle Scholar
Shrimpton, A. E. & Robertson, A., (1988 b). The isolation of polygenic factors controlling bristle score in Drosophila melanogaster. 2. Distribution of third chromosome bristle effects within chromosome sections. Genetics 118, 445459.CrossRefGoogle Scholar
Snedecor, G. W. & Cochran, W. G. (1971). Statistical Methods. Sixth edition. Iowa: Iowa State University Press, Ames.Google Scholar
Soller, M. & Beckmann, J. S. (1987). Cloning quantitative trait loci by insertional mutagenesis. Theoretical and Applied Genetics 74, 369378.CrossRefGoogle ScholarPubMed
Stuber, C. W. (1989). Marker-based selection for quantitative traits. In Proceedings of EU CARPI A Congress on Science in Plant Breeding (ed. Robellen, G.), pp. 3147. West Berlin: Paul Parey.Google Scholar
Thoday, J. M. (1979). Polygene mapping: uses and limitations. In Quantitative Genetic Variation (ed. Thompson, J. N., Jr and Thoday, J. M.). pp. 219233. New York: Academic Press.CrossRefGoogle Scholar
White, K., DeCelles, N. L. & Enlow, T. C. (1983). Genetic and Cellularity analysis of the locus vnd in Drosophila melanogaster. Genetics 104, 433448.CrossRefGoogle Scholar
Wilson, C., Pearson, R. K., Bellen, H. J., O'Kane, C., Grossniklaus, U. and Gehring, W. (1989). P-elementmediated enhancer detection: an efficient method for isolating and characterizing Cellularityly regulated genes in Drosophila. Genes and Development 3, 13011313.CrossRefGoogle ScholarPubMed