Biochemical Genetics

, Volume 17, Issue 7–8, pp 599–619 | Cite as

Genetic variation, inheritance, and quaternary structure of malic enzyme in brook trout (Salvelinus fontinalis)

  • Mark Stoneking
  • Bernie May
  • James E. WrightJr.


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.

Key words

malic enzyme inheritance and joint segregation brook trout quaternary structure interspecies hybrids 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 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.Google Scholar
  2. 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.Google Scholar
  3. 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.Google Scholar
  4. Allendorf, F. W., and Utter, F. M. (1979). Population genetics of fish. In Fish Physiology, Vol. 8, Academic Press, New York, p. 407.Google Scholar
  5. 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.Google Scholar
  6. Aspinwall, N. (1974). Genetic analysis of duplicate malate dehydrogenase loci in the pink salmon, Oncorhynchus gorbuscha. Genetics 7665.Google Scholar
  7. Baker, W. W., and Mintz, B. (1969) Subunit structure and gene control of mouse NADP-malate dehydrogenase. Biochem. Genet. 2351.Google Scholar
  8. Buro, N. C., and Weller, D. L. (1974). Purification and characterization of malic enzyme of Entamoeba invadens: Evidence for isoenzymes. J. Protozool. 21796.Google Scholar
  9. Cazzulo, J. J., Juan, S. M., and Segura, E. L. (1977). The malic enzyme from Trypanosoma cruzi. J. Gen. Microbiol. 99237.Google Scholar
  10. Clayton, J. W., and Tretiak, D. N. (1972). Amine-citrate buffers for pH control in starch gel electrophoresis. J. Fish. Res. Board Can. 291169.Google Scholar
  11. 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.Google Scholar
  12. 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.Google Scholar
  13. 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.Google Scholar
  14. 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.Google Scholar
  15. Goodridge, A. G. (1968). Citrate-cleavage enzyme, “malic” enzyme and certain dehydrogenases in embryonic and growing chicks. Biochem. J. 108663.Google Scholar
  16. 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.Google Scholar
  17. 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.Google Scholar
  18. 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.Google Scholar
  19. 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.Google Scholar
  20. Mather, K. (1951). The Measurement of Linkage in Heredity Methuen, London.Google Scholar
  21. 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.Google Scholar
  22. 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.Google Scholar
  23. 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.Google Scholar
  24. 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.Google Scholar
  25. Morrison, W. J. (1970). Nonrandom segregation of two lactate dehydrogenase subunit loci in trout. Tr. Am. Fish. Soc. 99193.Google Scholar
  26. Morton, N. E. (1955). Sequential tests for the detection of linkage. Am. J. Hum. Genet. 7277.Google Scholar
  27. Nevaldine, B. H., Bassel, A. R., and Hsu, R. Y. (1974). Mechanism of pigeon liver malic enzyme subunit structure. Biochim. Biophys. Acta 336283.Google Scholar
  28. 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.Google Scholar
  29. Ohno, S., Stenius, C., Faisst, E., and Zenzes, M. T. (1965). Postzygotic chromosomal rearrangements in rainbow trout (Salmo irrideus Gibbons). Cytogenetics 4117.Google Scholar
  30. 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.Google Scholar
  31. 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.Google Scholar
  32. Ridgway, G. J., Sherburne, S. W., and Lewis, R. D. (1970). Polymorphism in the esterases of Atlantic herring. Tr. Am. Fish. Soc. 99147.Google Scholar
  33. Roberts, F. L. (1968). Chromosome polymorphism in North American landlocked Salmo salar. Can. J. Genet. Cytol. 10865.Google Scholar
  34. Rutter, W. J., and Lardy, H. A. (1958). Purification and properties of pigeon liver malic enzyme. J. Biol. Chem. 233374.Google Scholar
  35. 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.Google Scholar
  36. 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.Google Scholar
  37. Silpananta, P., and Goodridge, A. G. (1971). Synthesis and degradation of malic enzyme in chick liver. J. Biol. Chem. 2465754.Google Scholar
  38. Spina, J., Bright, H. J., and Rosenbloom, J. (1970). Purification and properties of l-malic enzyme from Escherichia coli. Biochemistry 93794.Google Scholar
  39. Stark, M. J., Thompson, B., and Frenkel, R. (1975). Possible alternative functions of rat liver malic enzyme. Arch. Biochem. Biophys. 166174.Google Scholar
  40. Takahashi, S. Y., Kageyama, T., and Ohnishi, E. (1976). Malic enzyme from silkworm eggs—Purification and characteristics. Comp. Biochem. Physiol. 55B479.Google Scholar
  41. Thorgaard, G. H. (1976). Robertsonian polymorphism and constitutive heterochromatin distribution in chromosomes of rainbow trout (Salmo gairdneri). Cytogenet. Cell Genet. 17174.Google Scholar
  42. 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.Google Scholar
  43. 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.Google Scholar
  44. 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.Google Scholar
  45. 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.Google Scholar
  46. 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).Google Scholar
  47. Whitt, G. S. (1970). Developmental genetics of the lactate dehydrogenase isozymes of fish. J. Exp. Zool. 1751.Google Scholar
  48. 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.Google Scholar
  49. Wright, J. E., and Atherton, L. M. (1970). Polymorphism for LDH and transferrin loci in brook trout populations. Tr. Am. Fish. Soc. 99179.Google Scholar
  50. 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.Google Scholar
  51. Wright, J. E., May, B., and Stoneking, M. (1979). Pseudolinkage of two muscle aspartate aminotransferase loci in brook trout (Salvelinus fontinalis). (Manuscript in preparation.)Google Scholar

Copyright information

© Plenum Publishing Corporation 1979

Authors and Affiliations

  • Mark Stoneking
    • 1
  • Bernie May
    • 1
  • James E. WrightJr.
    • 1
  1. 1.Department of BiologyThe Pennsylvania State UniversityUniversity Park

Personalised recommendations