Skip to main content
Log in

Phosphoglucose isomerase gene duplication in the bony fishes: An evolutionary history

  • Published:
Biochemical Genetics Aims and scope Submit manuscript

Abstract

Electrophoretic patterns of phosphoglucose isomerase (PGI) in bony fishes provide strong evidence for a model of genetic control by two independent structural gene loci, most likely resulting from a gene duplication. This model is confirmed by a comparison of certain kinetic and molecular properties of the PGI homodimers (PGI-1 and PGI-2) isolated from extracts of the teleost Astyanax mexicanus. In addition, in most higher teleosts examined, the PGI enzymes show a regular pattern of tissue distribution, with PGI-2 predominant in muscle, the heterodimer often strongest in the heart, and PGI-1 predominant in liver and other organs. An examination of 53 species of bony fishes belonging to 38 families indicates a widespread occurrence of duplicate PGI loci and an early origin of the gene duplication, perhaps in the Leptolepiformes. The apparent presence of three PGI loci in trout and goldfish exemplifies how new loci can be incorporated into the genome through polyploidization.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Avise, J. C., and Selander, R. K. (1972). Evolutionary genetics of cave-dwelling fishes of the genus Astyanax. Evolution 261.

    Google Scholar 

  • Bailey, G. S., Cock, G. T., and Wilson, A. C. (1969). Gene duplication in fishes: Malate dehydrogenase of salmon and trout. Biochem. Biophys. Res. Commun. 34605.

    Google Scholar 

  • Bailey, G. S., Wilson, A. C., Halver, J. E., and Johnson, C. L. (1970). Multiple forms of supernatant malate dehydrogenase in salmonid fishes. J. Biol. Chem. 2455927.

    Google Scholar 

  • Bailey, R. M., Fitch, J. E., Herald, E. S., Lachner, E. A., Lindsey, C. C., Robins, C. R., and Scott, W. B. (1970). A list of common and scientific names of fishes from the United States and Canada. Am. Fish. Soc. Serial. Publ., No. 6.

  • Bender, K., and Ohno, S. (1968). Duplication of the autosomally inherited 6-phosphogluconate dehydrogenase gene locus in tetraploid species of cyprinid fish. Biochem. Genet. 2101.

    Google Scholar 

  • Carter, N. D., and Parr, C. W. (1967). Isoenzymes of phosphoglucose isomerase in mice. Nature 216511.

    Google Scholar 

  • DeLorenzo, R. J., and Ruddle, F. H. (1969). Genetic control of two electrophoretic variants of glucose phosphate isomerase in the mouse (Mus musculus). Biochem. Genet. 3151.

    Google Scholar 

  • Detter, J. C., Ways, P. O., Giblett, E. R., Baughman, M. A., Hopkinson, D. A., Povey, S., and Harris, H. (1968). Inherited variations in human phosphohexose isomerase. Ann. Hum. Genet. 31329.

    Google Scholar 

  • Fondy, T. P., and Kaplan, N. O. (1965). Structural and functional properties of the H and M subunits of lactic dehydrogenases. Ann. N. Y. Acad. Sci. 119888.

    Google Scholar 

  • Hines, M. C., and Wolfe, R. G. (1963). Phosphoglucose isomerase. II. Influence of pH on kinetic parameters. Biochemistry 2770.

    Google Scholar 

  • Huxley, J. (1942). Evolution: The Modern Synthesis, Allen and Unwin, London.

    Google Scholar 

  • Ingram, V. M. (1961). Gene evolution and the haemoglobins. Nature 189704.

    Google Scholar 

  • Johnson, W. E., and Selander, R. K. (1971). Protein variation and systematics in kangaroo rats (genus Dipodomys). Syst. Zool. 20 377.

    Google Scholar 

  • Johnson, W. E., Selander, R. K., Smith, M. H., and Kim, Y. J. (1972). Biochemical genetics of sibling species of the cotton rat (Sigmodon). Stud. Genet. (Univ. Texas Publ.) 7 (7213):297.

    Google Scholar 

  • Kahana, S. E., Lowry, O. H., Schulz, D. W., Passonneau, J. V., and Crawford, E. J. (1960). The kinetics of phosphoglucoisomerase. J. Biol. Chem. 235 2178.

    Google Scholar 

  • Kaplan, N. O. (1965). Evolution of dehydrogenases. In Bryson, V., and Vogel, H. J. (eds.), Evolving Genes and Proteins, Academic Press, New York, p.243.

    Google Scholar 

  • Kitto, G. B., and Kaplan, N. O. (1966). Purification and properties of chicken heart mitochondrial and supernatant malic dehydrogenases. Biochemistry 53966.

    Google Scholar 

  • Klose, J., Wolf, U., Hitzeroth, H., Ritter, H., Atkin, N. B., and Ohno, S. (1968). Duplication of LDH gene loci by polyploidization in the fish order Clupeiformes. Humangenetik 5190.

    Google Scholar 

  • Klose, J., Wolf, U., Hitzeroth, H., Ritter, H., and Ohno, S. (1969). Polyploidization in the fish family Cyprinidae, order Cypriniformes. II. Duplication of the gene loci coding for lactate dehydrogenase (E.C.:1.1.1.27) and 6-phosphogluconate dehydrogenase (E.C.:1.1.1.44) in various species of Cyprinidae. Humangenetik 7245.

    Google Scholar 

  • Lagler, K. F., Bardach, J. E., and Miller, R. R. (1962). Ichthyology, Wiley, New York.

    Google Scholar 

  • Lewis, E. B. (1951). Pseudoallelism and gene evolution. Cold Spring Harbor Symp. Quant. Biol. 16159.

    Google Scholar 

  • Massaro, E. J., and Markert, C. L. (1968). Isozyme patterns of salmonoid fishes: Evidences for multiple cistrons for lactate dehydrogenase polypeptides. J. Exptl. Zool. 168223.

    Google Scholar 

  • Morrison, W. J., and Wright, J. E. (1966). Genetic analysis of three lactate dehydrogenase isozyme system in trout: Evidence for linkage for genes coding subunits A and B. J. Exptl. Zool. 163259.

    Google Scholar 

  • Nakagawa, Y., and Noltmann, E. A. (1967). Multiple forms of yeast phosphoglucose isomerase. I. Resolution of the crystalline enzyme into three isoenzymes. J. Biol. Chem. 204782.

    Google Scholar 

  • Nelson, G. J. (1969). Gill arches and the phylogeny of fishes, with notes on the classification of vertebrates. Bull. Am. Mus. Nat. Hist. 141475.

    Google Scholar 

  • Noltmann, E. A. (1964). Isolation of crystalline phosphoglucose isomerase from rabbit muscle. J. Biol. Chem. 2391545.

    Google Scholar 

  • Nottebohm, F., and Selander, R. K. (1972). Vocal dialects and gene frequencies in the Chingolo sparrow (Zonotrichia capensis). Condor 74137.

    Google Scholar 

  • Ohno, S. (1970). Evolution by Gene Duplication, Springer-Verlag, New York.

    Google Scholar 

  • Ohno, S., and Morrison, M. (1966). Multiple gene loci for the monomeric hemoglobin of the hagfish (Eptatretus stoutii). Science 1541034.

    Google Scholar 

  • Ohno, S., Muramoto, J., Christian, L., and Atkin, N. B. (1967). Diploid-tetraploid relationship among Old-World members of the fish family Cyprinidae. Chromosoma 231.

    Google Scholar 

  • Ohno, S., Wolf, U., and Atkin, N. B. (1968). Evolution from fish to mammals by gene duplication. Hereditas 59169.

    Google Scholar 

  • Prasad, R., and Wright, D. A. (1971). Sponge method of preparative electrophoresis. Isozyme Bull. 412.

    Google Scholar 

  • Quiroz-Gutierrez, A., and Ohno, S. (1970). The evidence of gene duplication for S-form NADP-linked isocitrate dehydrogenase in carp and goldfish. Biochem. Genet. 493.

    Google Scholar 

  • Ralin, D. B., Selander, R. K., and Yang, S. Y. (1972). Protein variation and systematics in the genus Hyla. In preparation.

  • Ramsey, P. R., Avise, J. C., Smith, M. H., and Urbston, D. F. (1972). Protein variation and genic heterozygosity in white-tailed deer (Odocoileus virginianus). In preparation.

  • Romer, A. S. (1966). Vertebrate Paleontology, 3rd ed., University of Chicago Press, Chicago.

    Google Scholar 

  • Rosen, D. E., and Patterson, C. (1969). The structure and relationships of the paracanthopterygian fishes. Bull. Am. Mus. Nat. Hist. 141 357.

    Google Scholar 

  • Selander, R. K., Hunt, W. G., and Yang, S. Y. (1969). Protein polymorphism and genic heterozygosity in two European subspecies of the house mouse. Evolution 23379.

    Google Scholar 

  • Selander, R. K., Yang, S. R., Lewontin, R. C., and Johnson, W. E. (1970). Genetic variation in the horseshoe crab (Limulus polyphemus), a phylogenetic “relic.” Evolution 24402.

    Google Scholar 

  • Selander, R. K., Smith, M. H., Yang, S. Y., Johnson, W. E., and Gentry, J. B. (1971). Biochemical polymorphism and systematics in the genus Peromyscus. I. Variation in the old-field mouse (Peromyscus polionotus). Stud. Genet. (Univ. Texas Publ.) 6 (710349.

    Google Scholar 

  • Selander, R. K., Johnson, W. E., and Avise, J. C. (1972). Biochemical population genetics of fiddler crabs (Uca). In preparation.

  • Stephens, S. G. (1951). Possible significance of duplication in evolution. Advan. Genet. 4247.

    Google Scholar 

  • Tsuyuki, H., and Gadd, R. E. A. (1963). The multiple hemoglobins of some members of the Salmonidae family. Biochim. Biophys. Acta 71219.

    Google Scholar 

  • Watts, R. L., and Watts, D. C. (1968a). Gene duplication and the evolution of enzymes. Nature 2171125.

    Google Scholar 

  • Watts, R. L., and Watts, D. C. (1968b). The implications for molecular evolution of possible mechanisms of primary gene duplication. J. Theoret. Biol. 20227.

    Google Scholar 

  • Webster, T. P., Selander, R. K., and Yang, S. Y. (1972). Genetic variability and similarity in the Anolis lizards of Bimini. Evolution (submitted).

  • Whitt, G. S. (1970). Genetic variation of supernatant and mitochondrial malate dehydrogenase isozymes in the teleost Fundulus heteroclitus. Experientia 26734.

    Google Scholar 

  • Yoshida, A., and Carter, N. D. (1969). Nature of rabbit phosphoglucose isomerase isozymes. Biochim. Biophys. Acta 194151.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

This research was supported in part by a NSF graduate traineeship to J.C.A., by the Clayton Foundation for Research in Biochemistry (G.B.K.), by NSF Grant GB-15644 and NIH Grant GM-15769 to Robert K. Selander, and by contract AT(38-1)-310 between the University of Georgia and the U.S. Atomic Energy Commission.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Avise, J.C., Kitto, G.B. Phosphoglucose isomerase gene duplication in the bony fishes: An evolutionary history. Biochem Genet 8, 113–132 (1973). https://doi.org/10.1007/BF00485540

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00485540

Keywords

Navigation