Abstract
Electrophoretic variation is described for malic enzyme (ME) for the first time in brook trout (Salvelinus fontinalis). Since the quaternary structure of ME was not clear from examination of banding patterns in brook trout alone, ME phenotypes in rainbow trout (Salmo gairdneri) × brook trout hybrids as well as in esocid species demonstrated that ME is tetrameric. A model of two duplicated loci is proposed to account for the observed variation. One locus (ME-2) is fixed and one locus (ME-1) is variable with three electrophoretically distinct alleles; the protein products of ME-1 are reduced in activity relative to the protein products of ME-2. Joint segregation was examined between ME-1 and ten other biochemical loci in brook trout, and between ME-1, ME-2, and nine other biochemical loci in a splake—lake trout (Salvelinus namaycush) × brook trout hybrid—backcross. All pairwise examinations showed random assortment except ME-2 with an isocitrate dehydrogenase locus (IDH-3), which showed complete linkage in the splake backcross. This may be due to a chromosomal aberration.
Similar content being viewed by others
References
Allendorf, F. W. (1975). Genetic variability in a species possessing extensive gene duplication: Genetic interpretation of duplicate loci and examination of genetic variation in populations of rainbow trout. Ph.D. thesis, University of Washington, 98 pp.
Allendorf, F. W., and Utter, F. M. (1973). Gene duplication within the family Salmonidae: disomic inheritance of two loci reported to be tetrasomic in rainbow trout. Genetics 74647.
Allendorf, F. W., and Utter, F. M. (1976). Gene duplication in the family Salmonidae. III. Linkage between two duplicated loci coding for aspartate aminotransferase in the cutthroat trout (Salmo clarki). Hereditas 8219.
Allendorf, F. W., and Utter, F. M. (1979). Population genetics of fish. In Fish Physiology, Vol. 8, Academic Press, New York, p. 407.
Allendorf, F. W., Mitchell, N., Ryman, N., and Stahl, G. (1977). Isozyme loci in brown trout (Salmo trutta L.): Detection and interpretation from population data. Hereditas 86179.
Aspinwall, N. (1974). Genetic analysis of duplicate malate dehydrogenase loci in the pink salmon, Oncorhynchus gorbuscha. Genetics 7665.
Baker, W. W., and Mintz, B. (1969) Subunit structure and gene control of mouse NADP-malate dehydrogenase. Biochem. Genet. 2351.
Buro, N. C., and Weller, D. L. (1974). Purification and characterization of malic enzyme of Entamoeba invadens: Evidence for isoenzymes. J. Protozool. 21796.
Cazzulo, J. J., Juan, S. M., and Segura, E. L. (1977). The malic enzyme from Trypanosoma cruzi. J. Gen. Microbiol. 99237.
Clayton, J. W., and Tretiak, D. N. (1972). Amine-citrate buffers for pH control in starch gel electrophoresis. J. Fish. Res. Board Can. 291169.
Cohen, P. T. W., and Omenn, G. S. (1972). Genetic variation of the cytoplasmic and mitochondrial malic enzymes in the monkey Macaca nemestrina. Biochem. Genet. 7289.
Davisson, M. T., Wright, J. E., and Atherton, L. M. (1973). Cytogenetic analysis of pseudolinkage of LDH loci in the teleost genus Salvelinus. Genetics 73645.
Donnelly, R. F., Johnson, K. R., Hershberger, W. K., and Bevan, D. E. (1978). Identification of Kodiak Island pink salmon populations based on biochemical genetic variation. Final Report, Fisheries Research Institute, College of Fisheries, University of Washington, Contract No. 3813.
Gold, J. R., and Gall, G. A. E. (1975). Chromosome cytology and polymorphism in the California High Sierra golden trout (Salmo aguabonita). Can. J. Genet. Cytol. 1741.
Goodridge, A. G. (1968). Citrate-cleavage enzyme, “malic” enzyme and certain dehydrogenases in embryonic and growing chicks. Biochem. J. 108663.
Korkes, S., Del Campillo, A., and Ochoa, S. (1950). Biosynthesis of dicarboxylic acids by carbon dioxide fixation. IV. Isolation and properties of an adaptive “malic” enzyme from Lactobacillus arabinosus. J. Biol. Chem. 187891.
Li, J. J. (1972). NADP-malic enzyme. In vitro interspecies hybridization of rat and hamster liver enzymes: Evidence for an isologous tetrameric structure. Arch. Biochem. Biophys. 150812.
Li, J. J., Ross, C. R., Tepperman, H. M., and Tepperman, J. (1975). Nicotinamide adenine dinucleotide phosphate-malic enzyme of rat liver: Purification, properties, and immunochemical studies. J. Biol. Chem. 250141.
Lin, R. C., and Davis, E. J. (1974). Malic enzymes of rabbit heart mitochondria. Separation and comparison of some characteristics of a nicotinamide adenine dinucleotide-preferring and a nicotinamide adenine dinucleotide phosphate-specific enzyme. J. Biol. Chem. 2493867.
Mather, K. (1951). The Measurement of Linkage in Heredity Methuen, London.
May, B. (1975). Electrophoretic variation in the genus Oncorhynchus: The methodology, genetic basis, and practical applications to fisheries research and management. M.S. thesis, University of Washington, 95 pp. University Microfilms No. 13-10,112. Ann Arbor, Mich.
May, B., and Holbrook, F. R. (1978). Absence of genetic variability in the green peach aphid, Myzus persicae (Hemiptera: Aphididae). Ann. Entomol. Soc. Am. 71809.
May, B., Utter, F. M., and Allendorf, F. W. (1975). Biochemical genetic variation in pink and chum salmon: Inheritance of intraspecies variation and apparent absence of interspecies introgression following massive hybridization of hatchery stocks. J. Hered. 66227.
May, B., Wright, J. E., and Stoneking, M. (1979). A survey of joint segregation of biochemical loci in Salmonidae. J. Fish. Res. Board Can. 361114.
Morrison, W. J. (1970). Nonrandom segregation of two lactate dehydrogenase subunit loci in trout. Tr. Am. Fish. Soc. 99193.
Morton, N. E. (1955). Sequential tests for the detection of linkage. Am. J. Hum. Genet. 7277.
Nevaldine, B. H., Bassel, A. R., and Hsu, R. Y. (1974). Mechanism of pigeon liver malic enzyme subunit structure. Biochim. Biophys. Acta 336283.
Ohno, S. (1970). The enormous diversity in genome sizes of fish as a reflection of nature's extensive experiments with gene duplication. Tr. Am. Fish. Soc. 99120.
Ohno, S., Stenius, C., Faisst, E., and Zenzes, M. T. (1965). Postzygotic chromosomal rearrangements in rainbow trout (Salmo irrideus Gibbons). Cytogenetics 4117.
Ohno, S., Muramoto, J., Klein, J., and Atkin, N.B. (1969). Diploid-tetraploid relationship in clupeoid and salmonoid fish. In Chromosomes Today, Vol. II, Oliver and Boyd, Edinburgh, p. 139.
Povey, S., Wilson, D. E., Harris, H., Gromley, I. P., Perry, P., and Buckton, K. E. (1975). Sub-unit structure of soluble and mitochondrial malic enzyme: Demonstration of human mitochondrial enzyme in human-mouse hybrids. Ann. Hum. Genet. 39203.
Ridgway, G. J., Sherburne, S. W., and Lewis, R. D. (1970). Polymorphism in the esterases of Atlantic herring. Tr. Am. Fish. Soc. 99147.
Roberts, F. L. (1968). Chromosome polymorphism in North American landlocked Salmo salar. Can. J. Genet. Cytol. 10865.
Rutter, W. J., and Lardy, H. A. (1958). Purification and properties of pigeon liver malic enzyme. J. Biol. Chem. 233374.
Sauer, L. A. (1973). An NAD- and NADP-dependent malic enzyme with regulatory properties in rat liver and adrenal cortex mitochondrial fractions. Biochem. Biophys. Res. Commun. 50524.
Shows, T. B., Chapman, V. M., and Ruddle, F. H. (1970). Mitochondrial malate dehydrogenase and malic enzyme: Mendelian inherited electrophoretic variants in the mouse. Biochem. Genet. 4707.
Silpananta, P., and Goodridge, A. G. (1971). Synthesis and degradation of malic enzyme in chick liver. J. Biol. Chem. 2465754.
Spina, J., Bright, H. J., and Rosenbloom, J. (1970). Purification and properties of l-malic enzyme from Escherichia coli. Biochemistry 93794.
Stark, M. J., Thompson, B., and Frenkel, R. (1975). Possible alternative functions of rat liver malic enzyme. Arch. Biochem. Biophys. 166174.
Takahashi, S. Y., Kageyama, T., and Ohnishi, E. (1976). Malic enzyme from silkworm eggs—Purification and characteristics. Comp. Biochem. Physiol. 55B479.
Thorgaard, G. H. (1976). Robertsonian polymorphism and constitutive heterochromatin distribution in chromosomes of rainbow trout (Salmo gairdneri). Cytogenet. Cell Genet. 17174.
Tracey, M. L., Nelson, K., Hedgecock, D., Shleser, R. A., and Pressick, M. L. (1975). Biochemical genetics of lobsters: Genetic variation and the structure of American lobster (Homarus americanus) populations. J. Fish. Res. Board Can. 322091.
Utter, F. M., Allendorf, F. W., and Hodgins, H. O. (1973). Genetic variability and relationships in Pacific salmon and related trout based on protein variations. Syst. Zool. 22257.
Utter, F. M., Hodgins, H. O., and Allendorf, F. W. (1974). Biochemical genetic studies of fishes: Potentialities and limitations. In Biochemical and Biophysical Perspectives in Marine Biology Vol. I, Academic Press, New York, p. 213.
Utter, F. M., Allendorf, F. W., and May, B. (1976). The use of protein variation in the management of salmonid populations. Trans. 41st N. Am. Wildlife Nat. Res. Conf. Wildlife Management Institute, Washington, D.C. pp. 373–384.
Utter, F. M., Allendorf, F. W., and May, B. (1979) The genetic basis of creatine kinase variation in skeletal muscle of salmonid fishes. Biochem. Genet. (in press).
Whitt, G. S. (1970). Developmental genetics of the lactate dehydrogenase isozymes of fish. J. Exp. Zool. 1751.
Whitt, G. S., Miller, E. T., and Shaklee, J. B. (1973). Developmental and biochemical genetics of lactate dehydrogenase isozymes in fishes. In Genetics and Mutagenesis of Fish Springer-Verlag, New York, p. 243.
Wright, J. E., and Atherton, L. M. (1970). Polymorphism for LDH and transferrin loci in brook trout populations. Tr. Am. Fish. Soc. 99179.
Wright, J. E., Heckman, R., and Atherton, L. M. (1975). Genetic and developmental analysis of LDH isozymes in trout. In Isozymes, Vol. III: Developmental Biology, Academic Press, New York, p. 375.
Wright, J. E., May, B., and Stoneking, M. (1979). Pseudolinkage of two muscle aspartate aminotransferase loci in brook trout (Salvelinus fontinalis). (Manuscript in preparation.)
Author information
Authors and Affiliations
Additional information
Authorized for publication as Paper No. 5599 in the Journal Series of The Pennsylvania Agricultural Experiment Station, University Park, Pennsylvania, in cooperation with the Benner Spring Fish Research Station, The Pennsylvania Fish Commission, Bellefonte, Pennsylvania. M.S. was supported by an NSF Graduate Fellowship.
Rights and permissions
About this article
Cite this article
Stoneking, M., May, B. & Wright, J.E. Genetic variation, inheritance, and quaternary structure of malic enzyme in brook trout (Salvelinus fontinalis) . Biochem Genet 17, 599–619 (1979). https://doi.org/10.1007/BF00502121
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF00502121