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Studies of esterase 6 in Drosophila melanogaster: XI. Modification of esterase 6 activity by unlinked genes

Published online by Cambridge University Press:  14 April 2009

Craig S. Tepper ,
Rollin C. Richmond ,
Anne L. Terry  and
Alayne Senior
Craig S. Tepper
Affiliation:
Department of Biology, Indiana University, Bloomington, IN 47405, U.S.A.
Rollin C. Richmond
Affiliation:
Department of Biology, Indiana University, Bloomington, IN 47405, U.S.A.
Anne L. Terry
Affiliation:
Department of Biology, Indiana University, Bloomington, IN 47405, U.S.A.
Alayne Senior
Affiliation:
Department of Biology, Indiana University, Bloomington, IN 47405, U.S.A.
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The often remarkable similarity in structural gene products among related species has led to the hypothesis that species differences may reside largely in changes at regulatory gene loci. This hypothesis assumes that groups capable of speciating have allelic variation at regulatory loci in their natural populations. We have undertaken an analysis of the mode of regulation of the esterase 6 (Est 6) locus in Drosophila melanogaster to determine the nature and extent of regulatory gene variation in natural populations. Analyses of esterase 6 (EST 6) activity among strains carrying the same thermostability variants reveal that significant, specific-activity differences are present. Reciprocal crosses between lines having high and low EST 6 activity show that loci other than the Est 6 structural gene influence EST 6 activity. Analyses of male hybrids from crosses between D. melanogaster and simulans indicate that the X chromosome of these flies affects the expression of the Est 6 locus, resulting in unequal levels of enzyme activity from the two alleles. The effect is sex and tissue specific. Female hybrids carrying the X chromosomes of both species exhibit equal expression of the two Est 6 alleles. We have determined whether natural populations are polymorphic for X chromosomes which affect EST 6 activity by extracting single X chromosomes from wild-collected males and placing these chromosomes in identical genetic backgrounds. Stocks which are otherwise genetically identical but carry independently derived X chromosomes show significant differences in the activity of EST 6. These data suggest that regulatory loci may be commonly polymorphic in natural populations.

Type
Research Article
Information
Genetics Research , Volume 40 , Issue 2 , October 1982 , pp. 109 - 125
Copyright
Copyright © Cambridge University Press 1982

References

REFERENCES

Abraham, I. & Doane, W. (1978). Genetic regulation of tissue-specific expression of amylase structural genes in Drosophila melanogaster. Proceedings National Academy of Science (U.S.A.) 75, 4446–4450.CrossRefGoogle ScholarPubMed
Anderson, S. & McDonald, J. F. (1981). Effect of environmental alcohol on in vivo properties of Drosophila alcohol dehydrogenase. Biochemical Genetics 19, 421–430.Google Scholar
Aronshtam, A. A. & Kuzin, B. A. (1974). Investigation of the activity of esterase 6 in ontogenesis in Drosophila melanogaster and Drosophila simulans. Zhurnal Obshei Biologii (USSR) 35, 926–933 (in Russian).Google Scholar
Aronshtam, A. A. & Korochkin, L. I. (1975). Expression of allelomorphs of the locus Est 6 in hybrids between Drosophila melanogaster and Drosophila simulans. Genetika 11, 87–91.Google Scholar
Barnes, B. W. & Birley, A. J. (1978). Genetic variation for enzyme activity in a population of Drosophila melanogaster. IV. Analysis of alcohol dehydrogenase activity in chromosome substitution lines. Heredity 40, 51–57.Google Scholar
Bliss, C. I. (1970). Statistics in Biology, vol. 2, New York: McGraw-Hill.Google Scholar
Carson, H. L. (1975). The genetics of speciation at the diploid level. American Naturalist 109, 83–92.CrossRefGoogle Scholar
Cavener, D. R. & Clegg, M. T. (1981). Temporal stability of allozyme frequencies in a natural population of Drosophila melanogaster. Genetics (submitted).Google Scholar
Chovnick, A., Gelbart, W., McCarron, M., Osmond, B., Candido, E. P. M. & Ballie, D. L. (1976). Organization of the rosy locus in Drosophila melanogaster: Evidence for a control element adjacent to the xanthine dehydrogenase structural element. Genetics 84, 233–255.Google Scholar
Cochrane, B. & Richmond, R. C. (1979). Studies of esterase 6 in Drosophila melanogaster. I. The genetics of a posttranslational modification. Biochemical Genetics 17, 167–183.Google Scholar
Courtright, J. B. (1967). Polygenic control of aldehyde oxidase in Drosophila. Genetics 57, 25–38.Google Scholar
Davidson, E. H. (1976). Gene Activity in Early Development. New York: Academic Press.Google Scholar
Davis, B. J. (1964). Disc electrophoresis. II. Methods and applications to human serum proteins. Annual New York Academia of Science 121, 404–422.Google Scholar
Dickinson, W. J. (1975). A genetic locus affecting the developmental expression of an enzyme in Drosophila melanogaster. Developmental Biology 42, 131–140.Google Scholar
Dickinson, W. J. (1980). Tissue specificity of enzyme expression regulated by diffusable factors: Evidence in Drosophila hybrids. Science. 207, 995–997.CrossRefGoogle ScholarPubMed
Engels, W. R. (1980). Hybrid dysgenesis in Drosophila and the stochastic loss hypothesis. Cold Spring Harbor Symposia on Quantitative Biology 20, 561–565.Google Scholar
Finnerty, V. & Johnson, G. (1979). Post-translational modification as a potential explanation of high levels of enzyme polymorphism: Xanthine dehydrogenase and aldehyde oxidase in Drosophila melanogaster. Genetics 91, 695–722.Google Scholar
Finnerty, V., McCarron, M. & Johnson, G. (1979). Gene expression in Drosophila: post-translational modification of aldehyde oxidase and xanthine dehydrogenase. Molecular General Genetics 172, 37–43.Google Scholar
Gilbert, D. G. & Richmond, R. C. (1981). Esterase 6 in Drosophila melanogaster: reproductive function of active and null males at low temperature. Proceedings National Academy of Science (U.S.A.) (in the Press, May).Google Scholar
Gilbert, D. G., Richmond, R. C. & Sheehan, K. B. (1981). Studies of Esterase 6 in Drosophila melanogaster. VII. The timing of remating in females inseminated by males having active or null alleles. Behavioral Genetics 11, 195–208.Google Scholar
Girard, P., Palabost, L. & Petit, C. (1977). Enzyme variation at seven loci in nine natural populations of Drosophila melanogaster. Biochemical Genetics 15, 589–599.Google Scholar
Hedrick, P. W. & McDonald, J. F. (1980). Regulatory gene adaptation: An evolutionary model. Heredity 45, 83–97.Google Scholar
Korochkin, L. I., Evgeniev, M. & Matveeva, N. (1972). The influence of genotype on phenotype expression of esterase in Drosophila of the virilis group. Drosophila Information Service 49, 103.Google Scholar
Korochkin, L. I., Belyaeva, E. S., Matveeva, X. M., Kuzin, B. A., & Serov, O. L. (1976). Genetics of esterases in Drosophila. IV. Slow-migrating S-esterase in Drosophila of the virilis group. Biochemical Genetics 14, 161–182.Google Scholar
Laurie-Ahlberg, C. C., Maroni, G. P., Brawley, G. C., Lucchesi, J. C. & Weir, B. S. (1980). Quantitative genetic variation of enzyme activities in natural populations of Drosophila melanogaster. Proceedings National Academy of Science (U.S.A.) 77, 1073–1077.Google Scholar
Lewontin, R. C. (1974). Genetic Basis of Evolutionary Change. New York: Columbia Press.Google Scholar
Lindman, H. R. (1974). Analysis of Variance in Complex Experimental Designs. San Francisco: W. H. Freeman.Google Scholar
Lindsley, D. L. & Grell, E. H. (1968). The Genetic Variations of Drosophila melanogaster. Carnegie Institution, Washington, D.C.Google Scholar
Lowry, O. H., Rosebrough, N. J., Farr, A. L. & Randall, R. J. (1951). Protein measurement with the folin phenol reagent. Journal Biological Chemistry 193, 265–275.CrossRefGoogle ScholarPubMed
MacIntyre, R. (1966). The genetics of acid phosphatase in Drosophila melanogaster and Drosophila simulans. Genetics 53, 461–474.Google Scholar
McDonald, J. F., Chambers, G. K., David, J. & Ayala, F. J. (1977). Adaptive response due to changes in gene regulation: A study with Drosophila. Proceedings National Academy of Science (U.S.A.) 74, 4562–4566.Google Scholar
McDonald, J. F. & Ayala, F. J. (1978). Genetic and biochemical basis of enzyme activity in natural populations. I. Alcohol dehydrogenase in Drosophila melanogaster. Genetics, 89, 371–388.Google Scholar
Norman, R. A. & Prakash, S. (1980). Activity variants of acid phosphatase-3 among chromosome 3 inversions of Drosophila pseudoobscura. Genetics 96, 743–755.Google Scholar
Pipkin, S. B. & Hewitt, N. E. (1972). Variation of alcohol dehydrogenase levels in Drosophila species hybrids. Journal of Heredity 63, 267–270.Google Scholar
Richmond, R. C., Gilbert, D. G., Sheehan, K. S., Gromko, M. H. & Butterworth, F. W. (1980). Esterase 6 and reproduction in Drosophila melanogaster. Science 207, 1483–1485.Google Scholar
Sheehan, K., Richmond, R. C., & Cochrane, B. J. (1979). Studies of esterase 6 in Drosophila melanogaster. III. The developmental pattern and tissue distribution. Insect Biochemistry 9, 443–450.Google Scholar
Stebbins, G. L. (1969). The Basis of Progressive Evolution. Chapel Hill: University of North Carolina Press.Google Scholar
Steel, R. G. D. & Torrie, J. H. (1970). Principles and Procedures in Statistics. New York: McGraw-Hill.Google Scholar
Sturtevent, A. H. (1920). Genetic Studies on Drosophila simulans. I. Introduction. Hybrids with Drosophila melanogaster. Genetics 5, 488–500.Google Scholar
Templeton, A. (1980 a). The theory of speciation via the founder principle. Genetics 94, 1011–1038.Google Scholar
Templeton, A. (1980 b). Modes of speciation and inferences based on genetic distance. Evolution 34, 719–729.Google Scholar
Vallentine, J. W. & Campbell, C. A. (1975). Genetic regulation and the fossil record. American Scientist 63, 673–680.Google Scholar
Wallace, B. (1963). Genetic diversity, genetic uniformity and heterosis. Canadian Journal of Genetic Cytology, 5, 239–253.Google Scholar
Ward, R. (1975). Alcohol dehydrogenase activity in Drosophila melanogaster: A quantitative character. Genetical Research 26, 81–93.Google Scholar
Wilson, A. C. (1975). Evolutionary importance of gene regulation. Stadler Symposia 7, 117–133.Google Scholar
Wilson, P. G. & McDonald, J. F. (1981). A comparative study of enzyme activity variation between α glycerophosphate and alcohol dehydrogeneses in Drosophila melanogaster. Genetics 55, 75–79.Google Scholar
Wright, T. R. F. (1963). The genetics of an esterase in Drosophila melanogaster. Genetics 48, 787–801.CrossRefGoogle ScholarPubMed