Direct evidence that genetic variation in glycerol-3-phosphate and malate dehydrogenase genes (Gpdh and Mdh1) affects adult ethanol tolerance in Drosophila melanogaster

Genetics

Volumn 181, Issue 2, 2009, Pages 607-614

  Eanes, Walter F ^a   Merritt, Thomas J S ^a,b   Flowers, Jonathan M ^a,c   Kumagai, Seiji ^a,d   Zhu, Chen Tseh ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b LAURENTIAN UNIVERSITY   (Canada)

^c NEW YORK UNIVERSITY   (United States)

^d DUKE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCEROL 3 PHOSPHATE DEHYDROGENASE; MALATE DEHYDROGENASE;

ALCOHOL TOLERANCE; ARTICLE; CONTROLLED STUDY; DNA POLYMORPHISM; DROSOPHILA MELANOGASTER; ENZYME ACTIVITY; GENE DELETION; GENE INTERACTION; GENE LOCUS; GENETIC RECOMBINATION; GENETIC VARIABILITY; GENOTYPE; NONHUMAN; PRIORITY JOURNAL;

ALCOHOL DEHYDROGENASE; ALLELES; ANIMALS; CROSSES, GENETIC; DROSOPHILA MELANOGASTER; DRUG TOLERANCE; ETHANOL; EVOLUTION; FEMALE; GENE DELETION; GENE DUPLICATION; GENES, INSECT; GENETIC VARIATION; GLYCEROLPHOSPHATE DEHYDROGENASE; MALATE DEHYDROGENASE; MALE; SELECTION (GENETICS);

DROSOPHILA MELANOGASTER;

EID: 62449196667     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.108.089383     Document Type: Article

References (44)

1. BEGUN, D. J., A. J. BETANCOURT, C. H. LANGLEY and W. STEPHAN, 1999 Is the fast/slow allozyme variation at the Adh locus of Drosophila melanogaster an ancient balanced polymorphism? Mol. Biol. Evol. 16: 1816-1819.
2. BERRY, M. N., R. B. GREGORY, A. R. GRIVELL, J. W. PHILLIPS and A. SCHON, 1994 The capacity of reducing-equivalent shuttles limits glycolysis during ethanol oxidation. Eur. J. Biochem. 225: 557-564.
3. BEWLEY, G. C., D. W. NIESEL and J. R. WILKINS, 1984 Purification and characterization of the naturally occurring allelic variants of sn-glycerol-3-phosphate dehydrogenase in Drosophila melanogaster. Comp. Biochem. Physiol. B 79: 23-32.
4. CAVENER, D. R., and M. T. CLEGG, 1978 Dynamics of correlated genetic systems. IV. Multilocus effects of ethanol stress environments. Genetics 90: 629-644.
5. COHAN, F. M., and J.-D. GRAF, 1985 Latitudinal cline in Drosophila melanogaster for knockdown resistance to ethanol fumes and for rates of response to selection for further resistance. Evolution 39: 278-293.
6. COHAN, F. M., and A. A. HOFFMANN, 1986 Genetic divergence under uniform selection. II. Different responses to selection for knockdown resistance to ethanol among Drosophila melanogaster populations and their replicate lines. Genetics 114: 145-164.
7. DAVID, J. R., and C. BOCQUET, 1975 Similarities and differences in latitudinal adaptation of two Drosophila sibling species. Nature 257: 588-590.
8. DYKHUIZEN, D. E., A. M. DEAN and D. L. HARTL, 1987 Metabolic flux and fitness. Genetics 115: 25-31.
9. FARFARI, S., V. SCHULZ, B. CORKEY and M. PRENTKI, 2000 Glucose-regulated anaplerosis and cataplerosis in pancreatic beta-cells: possible implication of a pyruvate/citrate shuttle in insulin secretion. Diabetes 49: 718-726.
10. FREEMAN, S., and J. C. HERRON, 2004 Evolutionary Analysis, Ed. 3. Pearson-Prentice Hall, Upper Saddle River, NJ.
11. FRERIKSEN, A., D. SEYKENS and P. W. H. HEINSTRA, 1994 Differences between larval and adult Drosophila in metabolic degradation of ethanol. Evolution 48: 504-508.
12. FRY, J. D., and M. SAWEIKIS, 2006 Aldehyde dehydrogenase is essential for both adult and larval ethanol resistance in Drosophila melanogaster. Genet. Res. 87: 87-92.
13. FRY, J. D., K. DONLON and M. SAWEIKIS, 2008 A worldwide polymorphism in aldehyde dehydrogenase in Drosophila melanogaster: evidence for selection mediated by dietary ethanol. Evolution 62: 66-75.
14. FUTUYMA, D. J., 2005 Evolution. Sinauer, Sunderland, MA.
15. GEER, B. W., S. W. MCKECHNIE and M. L. LANGEVIN, 1983 Regulation of sn-glycerol-3-phosphate dehydrogenase in Drosophila melanogaster larvae by dietary ethanol and sucrose. J. Nutr. 113: 1632-1642.
16. GEER, B. W., P. W. HEINSTRA and S. W. MCKECHNIE, 1993 The biological basis of ethanol tolerance in Drosophila. Comp. Biochem. Physiol. 105B: 203-229.
17. GUAY, C., S. R. M. MADIRAJU, A. AUMAIS, E. JOLY and M. PRENTKI, 2007 A role for ATP-citrate lyase, malic enzyme, and pyruvate/citrate cycling in glucose-induced insulin secretion. J. Biol. Chem. 282: 35657-35665.
18. HARTL, D. L., D. E. DYKHUIZEN and A. M. DEAN, 1985 Limits of adaptation: the evolution of selective neutrality. Genetics 111: 655-674.
19. HAY, R. E., and F. B. ARMSTRONG, 1976 Biochemical characterization of allelic forms of soluble malate dehydrogenase of Drosophila melanogaster. Insect Biochem. 6: 367-376.
20. HUDSON, R. R., M. KREITMAN and M. AGUADÉ , 1987 A test of neutral molecular evolution based on nucleotide data. Genetics 116: 153-159.
21. JOHNSON, F. M., and C. DENNISTON, 1964 Genetic variation of alcohol dehydrogenase in Drosophila melanogaster. Nature 204: 906.
22. KANG, S. J., S. H. LEE and K. S. PARK, 1998 DNA polymorphisms at alpha-Gpdh locus of Drosophila melanogaster in Korean population. Genes Genet. Syst. 73: 227-235.
23. KREITMAN, M., 1983 Nuleotide polymorphism at the alcohol dehydrogenase locus of Drosophila melanogaster. Nature 304: 412-417.
24. KREITMAN, M., and H. AKASHI, 1995 Molecular evidence for natural selection. Annu. Rev. Ecol. Syst. 26: 403-422.
25. LAURIE-AHLBERG, C. C., and G. C. BEWLEY, 1983 Naturally occurring genetic variation affecting the expression of sn-glycerol-3-phosphate dehydrogenase in Drosophila melanogaster. Biochem. Genet. 21: 943-961.
26. LISSEMORE, J. L., C. A. BAUMGARDNER, B. W. GEER and D. T. SULLIVAN, 1990 Effect of dietary carbohydrates and ethanol on expression of genes encoding sn-glycerol-3-phosphate dehydrogenase, aldolase, and phosphoglycerate kinase in Drosophila larvae. Biochem. Genet. 28: 615-630.
27. MCELFRESH, K. C., and J. F. MCDONALD, 1983 The effect of alcohol stress on nicotinamide adenine dinucleotide (NAD+) levels in Drosophila. Biochem. Genet. 21: 365-374.
28. MCKENZIE, J. A., and P. A. PARSONS, 1972 Alcohol tolerance: an ecological parameter in the relative success of Drosophila melanogaster and D. simulans. Oecologia 10: 373-388.
29. MERRITT, T. J., D. DUVERNELL and W. F. EANES, 2005 Natural and synthetic alleles provide complementary insights into the nature of selection acting on the Men polymorphism of Drosophila melanogaster. Genetics 171: 1707-1718.
30. MERRITT, T. J., E. SEZGIN, C. T. ZHU and W. F. EANES, 2006 Triglyceride pools, flight and activity variation at the Gpdh locus in Drosophila melanogaster. Genetics 172: 293-304.
31. MILLER, S., R. W. PEARCY and E. BERGER, 1975 Polymorphism at the alpha-glycerophosphatedehy drogenase locus in Drosophila melanogaster. I. Properties of adult allozymes. Biochem. Genet. 13: 175-188.
32. MONTOOTH, K. L., K. T. SIEBENTHALL and A. G. CLARK, 2006 Membrane lipid physiology and toxin catabolism underlie ethanol and acetic acid tolerance in Drosophila melanogaster. J. Exp. Biol. 209: 3837-3850.
33. MOROZOVA, T. V., R. R. ANHOLT and T. F. MACKAY, 2006 Transcriptional response to alcohol exposure in Drosophila melanogaster. Genome Biol. 7: R95.
34. MOROZOVA, T. V., R. R. ANHOLT and T. F. MACKAY, 2007 Phenotypic and transcriptional response to selection for alcohol sensitivity in Drosophila melanogaster. Genome Biol. 8: R231.
35. OAKESHOTT, J. G., J. B. GIBSON, P. R. ANDERSON, W. R. KNIBB, D. G. ANDERSON et al., 1982 Alcohol dehydrogenase and glycerol-3-phosphate dehydrogenase clines in Drosophila melanogaster on different continents. Evolution 36: 86-96.
36. OAKESHOTT, J. G., S. W. MCKECHNIE and G. K. CHAMBERS, 1984 Population genetics of the metabolically related Adh, Gpdh, and Tpi polymorphisms in Drosophila melanogaster. I. Geographic variation in Gpdh and Tpi allele frequencies in different continents. Genetica 63: 21-29.
37. PARKS, A. L., K. R. COOK, M. BELVIN, N. A. DOMPE, R. FAWCETT et al., 2004 Systematic generation of high-resolution deletion coverage of the Drosophila melanogaster genome. Nat. Genet. 36: 288-292.
38. PECSENYE, K., and A. SAURA, 1998 Interaction between the Adh and Odh loci in response to ethanol in Drosophila melanogaster. Biochem. Genet. 36: 147-170.
39. RUBI, B., A. DEL ARCO, C. BARTLEY, J. SATRUSTEGUI and P. MAECHLER, 2004 The malate-aspartate NADH shuttle member Aralar1 determines glucose metabolic fate, mitochondrial activity, and insulin secretion in beta cells. J. Biol. Chem. 279: 55659-55666.
40. SCHOLZ, H., J. RAMOND, C. M. SINGH and U. HEBERLEIN, 2000 Functional ethanol tolerance in Drosophila. Neuron 28: 261-271.
41. SCHOLZ, H., M. FRANZ and U. HEBERLEIN, 2005 The hangover gene defines a stress pathway required for ethanol tolerance development. Nature 436: 845-847.
42. SEZGIN, E., D. D. DUVERNELL, L. M. MATZKIN, Y. DUAN, C. T. ZHU et al., 2004 Single-locus latitudinal clines and their relationship to temperate adaptation in metabolic genes and derived alleles in Drosophila melanogaster. Genetics 168: 923-931.
43. TAKANO, T. S., S. KUSAKABE and T. MUKAI, 1993 DNA polymorphism and the origin of protein polymorphism at the Gpdh locus of Drosophila melanogaster, pp. 179-190 in Mechanisms of Molecular Evolution, edited by N. TAKAHATA and A. G. CLARK. Japan Scientific Societies Press and Sinauer Associates, Tokyo/New York.
44. VAN DER ZEL, A., R. DADOO, B. W. GEER and P. W. H. HEINSTRA, 1991 The involvement of catalase in alcohol metabolism in Drosophila melanogaster larvae. Arch. Biochem. Biophys. 287: 121-127.