Abstract
There are five G6P-specific G6PD isozymes in both brook and lake trout. The most anodal isozyme in each species has the same electrophoretic mobility; however, the five lake trout isozymes are more widely spaced on polyacrylamide gels than are those from brook trout. In hybrids, i.e., splake trout, nine forms of G6PD can be resolved. These results can be explained by a model in which we assume that each isozyme is a tetramer and that two different subunit types are produced. In splake trout, three electrophoretically distinct subunits yield 15 tetramers. That only nine are detected is a consequence of coincident electrophoretic mobility of some of the possible subunit combinations. Our results indicate that the G6PD isozymes in these trout are the products of two codominant autosomal gene loci. The hypothesis that G6PD and H6PD arose from a common ancestral type G6PD is supported by microcomplement fixation data which show an immunochemical relatedness between these enzymes. The relationship of G6PD and H6PD in trout is discussed from an evolutionary standpoint.
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Bailey, G. S., and Wilson, A. C. (1970). Multiple forms of supernatant malate dehydrogenase in salmonid fishes. J. Biol. Chem. 2455927.
Beutler, E., and Collins, Z. (1965). Hybridization of glucose-6-phosphate dehydrogenase from rat and human erythrocytes. Science 1501306.
Beutler, E., and Morrison, M. (1967). Localization and characteristics of hexose 6-phosphate dehydrogenase (glucose dehydrogenase). J. Biol. Chem. 2425289.
Bhatnagar, M. K. (1969). Autosomal determination of erythrocyte glucose-6-phosphate dehydrogenase in domestic chickens and ring-necked pheasants. Biochem. Genet. 385.
Bonsignore, A., Lorenzoni, I., Cancedda, R., Morelli, A. Giuliano, F., and De Flora, A. (1969). Metabolism of human erythrocyte glucose-6-phosphate dehydrogenase. V. Exchange between free and apoenzyme-bound NADP. Ital. J. Biochem. 18439.
Bonsignore, A., Lorenzoni, I., Cancedda, R., and De Flora, A. (1970). Distinctive patterns of NADP binding to dimeric and tetrameric glucose-6-phosphate dehydrogenase from human red cells. Biochem. Biophys. Res. Commun. 39142.
Chrambach, A., Reisfeld, R. A., Wyckoff, M., and Zaccari, J. (1967). A procedure for rapid and sensitive staining of protein fractionated by polyacrylamide gel electrophoresis. Anal. Biochem. 20150.
Cooper, D. W., and Irwin, M. R. (1968). Glucose-6-phosphate dehydrogenase: Evidence for tetrameric structure in doves (Streptopelia). Proc. Natl. Acad. Sci. 61979.
Cooper, D. W., Irwin, M. R., and Stone, W. H. (1969). Inherited variation in the dehydrogenases of doves (Streptopelia). II. Autosomal inheritance of glucose-6-phosphate dehydrogenase. Genetics 62607.
Criss, W. E., and McKerns, K. W. (1968). Purification and partial characterization of glucose-6-phosphate dehydrogenase from cow adrenal cortex. Biochemistry 7125.
Engel, W., Op't Hof, J., and Wolf, U. (1970). Sorbitol dehydrogenase isozymes in clupeoid fish: A further example of gene duplication through polyploid evolution. Humangenetik 9157.
Gaunce, A. O., and D'Iorio, A. (1970). Microdetermination of protein by an automated Lowry method. Anal. Biochem. 37204.
Glock, G. E., and McLean, P. (1953). Further studies on the properties and assay of glucose-6-phosphate dehydrogenase of rat liver. Biochem. J. 55400.
Goldberg, E. (1966). Lactate dehydrogenase of trout: Hybridication in vivo and in vitro. Science 1511091
Jones, M. L. (1970). The presence of certain dehydrogenases among polychaetous annelids as shown by disc electrophoresis. Comp. Biochem. Physiol. 36605.
Kamada, T., and Hori, S. H. (1970). A phylogenic study of animal glucose-6-phosphate dehydrogenases. Japan. J. Genet. 45319.
Kirkman, H. N., and Hendrickson, E. M. (1962). Glucose-6-phosphate dehydrogenase from human erythrocytes. II. Subactive states of the enzyme from normal persons. J. Biol. Chem. 2372371.
Klose, J., Wolf, U., Hitzeroth, H., and Ritter, H. (1968). Duplication of the lactate dehydrogenase gene loci by polyploidization in the fish order Clupeiformes. Humangenetik 5190.
Kornberg, A., and Horecker, B. L. (1955). Glucose-6-phosphate dehydrogenase. Meth. Enzymol. 1323.
Levine, L., and Van Vunakis, H. (1967). Micro complement fixation. Meth. Enzymol. 11928.
Lowry, O. H., Rosebrough, N. J., Farr, A. L., and Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193265.
Luzzatto, L. (1967). Regulation of the activity of glucose-6-phosphate dehydrogenase by NADP+ and NADPH. Biochim. Biophys. Acta 14618.
Mandula, B., Srivastava, S. K., and Beutler, E. (1970). Hexose-6-phosphate dehydrogenase: Distribution in rat tissues and effect of diet, age, and steroids. Arch. Biochem. Biophys. 141155.
Manwell, C., and Baker, C. M. A. (1969). Hybrid proteins, heterosis, and the origin of species. I. Unusual variation of polychaete Hyalinoecia “nothing dehydrogenases” and of quail Coturnix erythrocyte enzymes. Comp. Biochem. Physiol. 281007.
McKerns, K. W., and Kaleita, E. (1960). Inhibition of glucose-6-phosphate dehydrogenase by hormones. Biochem. Biophys. Res. Commun. 2344.
Newburgh, R. W., and Cheldelin, V. H. (1956). The intracellular distribution of pentose cycle activity in rabbit kidney and liver. J. Biol. Chem. 21889.
Ohno, S., Payne, H. W., Morrison, M., and Beutler, E. (1966). Hexose-6-phosphate dehydrogenase found in human liver. Science 1531015.
Ohno, S., Muramoto, J., Klein, J., and Atkin, N. B. (1967). Diploid-tetraploid relationship in clupeoid and salmonoid fish. Chromosomes Today 2139.
Ohno, S., Wolf, U., and Atkin, N. B. (1968). Evolution from fish to mammals by gene duplication. Hereditas 59169.
Powers, D. A., Lenhoff, H. M., and Leone, C. A. (1968). Glucose-6-phosphate dehydrogenase and 6-phosphogluconate dehydrogenase activities in coelenterates. Comp. Biochem. Physiol. 27139.
Sarich, V. M., and Wilson, A. C. (1966). Quantitative immunochemistry and the evolution of primate albumins: Microcomplement fixation. Science 1541563.
Shatton, J. B., Halver, J. E., and Weinhouse, S. (1971). Glucose (hexose-6-phosphate) dehydrogenase in liver of rainbow trout. J. Biol. Chem. 2464878.
Shaw, C. R. (1966). Glucose-6-phosphate dehydrogenase: Homologous molecules in deer, mouse, and man. Science 1531013.
Shaw, C. R., and Barto, E. (1965). Autosomally determined polymorphism of glucose-6-phosphate dehydrogenase in Peromyscus. Science 1481099.
Shaw, C. R., and Koen, A. L. (1968). Glucose-6-phosphate dehydrogenase and hexose 6-phosphate dehydrogenase of mammalian tissues. Ann. N. Y. Acad. Sci. 151149.
Srivastava, S. K., Blume, K. G., Beutler, E., and Yoshida, A. (1972). Immunological difference between glucose-6-P dehydrogenase and hexose-6-P dehydrogenase from human liver. Nature New Biol. 238240.
Stegeman, J. J. (1972). The occurrence, characterization and biological significance of hexose-6-phosphate dehydrogenase in trout. Ph.D. dissertation, Northwestern University, Evanston, Ill.
Stegeman, J. J., and Goldberg, E. (1971). Distribution and characterization of hexose 6-phosphate dehydrogenase in trout. Biochem. Genet. 5579.
Stegeman, J. J., and Goldberg, E. (1972). Inheritance of hexose 6-phosphate dehydrogenase polymorphism in brook trout. Biochem. Genet. 7279.
Stollar, D., and Levine, L. (1963). Two-dimensional immunodiffusion. Meth. Enzymol. 6848.
Trujillo, J. M., Walden, B., O'Neill, P., and Anstall, H. (1965). Sex-linkage of glucose-6-phosphate dehydrogenase in the horse and donkey. Science 1481603.
Wasserman, E., and Levine, L. (1961). Quantitative micro-complement fixation and its use in the study of antigenic structure by specific antigen-antibody inhibition. J. Immunol. 87290.
Wolf, U., Klose, J., and Oser, G. (1969). Zur Gen-lokalisierung der Glucose-6-phosphat-dehydrogenase bei Vogeln. Humangenetik 8137.
Wolf, U., Engel, W., and Faust, J. (1970). The mechanism of diploidization in vertebrate evolution: Coexistence of tetrasomic and disomic gene loci for the isocitrate dehydrogenase in trout (Salmo irideus). Humangenetik 9150.
Yamauchi, T. (1972). Studies of glucose-6-phosphate dehydrogenase in brook, lake, and splake trout. Ph.D. dissertation, Northwestern University, Evanston, Ill.
Yoshida, A., and Hoagland, V. D., Jr. (1970). Active molecular unit and NADP content of human glucose-6-phosphate dehydrogenase. Biochem. Biophys. Res. Commun. 401167.
Young, W. J., Porter, J. E., and Childs, B. (1964). Glucose-6-phosphate dehydrogenase in Drosophila: X-linked electrophoretic variants. Science 143140.
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This research was supported in part by National Science Foundation Grant GB-7271 and by United States Public Health Predoctoral Fellowship 4 FO1 GM 43657-03.
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Yamauchi, T., Goldberg, E. Glucose 6-phosphate dehydrogenase from brook, lake, and splake trout: An isozymic and immunological study. Biochem Genet 10, 121–134 (1973). https://doi.org/10.1007/BF00485760
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DOI: https://doi.org/10.1007/BF00485760