Summary
In the 50 million years since the polyploidization event that gave rise to the catostomid family of fishes the duplicate genes encoding isozymes have undergone different fates. Ample opportunity has been available for regulatory evolution of these duplicate genes. Approximately half the duplicate genes have lost their expressions during this time. Of the duplicate genes remaining, the majority have diverged to different extents in their expression within and among adult tissues. The pattern of divergence of duplicate gene expression is consistent with the accumulation of mutations at regulatory genes. The absence of a correlation of extent of divergence of gene expression with the level of genetic variability for isozymes at these loci is consistent with the view that the rates of regulatory gene and structural gene evolution are uncoupled. The magnitude of divergence of duplicate gene expressions varies among tissues, enzymes, and species. Little correlation was found with the extent of divergence of duplicate gene expression within a species and its degree of morphological “conservatism”, although species pairs which are increasingly taxonomically distant are less likely to share specific patterns of differential gene expression. Probable phylogenetic times of origin of several patterns of differential gene expression have been proposed. Some patterns of differential gene expression have evolved in recent evolutionary times and are specific to one or a few species, whereas at least one pattern of differential gene expression is present in nearly all species and probably arose soon after the polyploidization event. Multilocus isozymes, formed by polyploidization, provide a useful model system for studying the forces responsible for the maintenance of duplicate genes and the evolution of these once identical genes to new spatially and temporally specific patterns of regulation.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Allendorf, F.W., Utter, F.M., May, B.P. (1975). Gene duplication within the family Salmonidae: II. Detection and determination of the genetic control of duplicate loci through inheritance studies and the examination of populations. In: Isozymes IV. Genetics and Evolution, C.L. Markert, ed., pp. 415–432, New York: Academic Press
Armstrong, P.B., Child, J.S. (1965). Stages in the normal development ofFundulus heteroclitus. Biol. Bull.128, 143–168
Avise, J.C., Kitto, B.G. (1973). Phosphoglucose isomerase gene duplication in the bony fishes, an evolutionary history. Biochem. Genet.8, 113–132
Bailey, G.S., Poulter, R.T.M., Stockwell, P.A. (1978). Gene duplication in tetraploid fish: a model for silencing at unlinked duplicated loci. Proc. Nat. Acad. Sci.75, 5575–5579
Britten, R.J., Davidson, E.H. (1969). Gene regulation for higher cells: A theory. Science165, 349–357
Britten, R.J., Davidson, E.H. (1971). Repetitive and non-repetitive DNA sequences and a speculation on the origins of evolutionary novelty. Quart. Rev. of Biol.46, 111–138
Bullough, W.S. (1965). Mitotic and functional homeostasis. Cancer Res.25, 1683–1727
Cherry, L.M., Case, S.M., Wilson, A.C. (1978). Frog perspective on the morphological difference between humans and chimpanzees. Science200, 209–211
Dayhoff, M. (1972). Atlas of protein sequence and structure. Volume 5. Washington, D.C.: National Biomedical Research Foundation
Dice, J.F., Goldberg, A.L. (1975). Relationship between in vivo degradative rates and isoelectric points of proteins. Proc. Natl. Acad. Sci.72, 3893–3897
Don, M., Masters, C.J. (1976). On the comparative turnover rates of the lactate dehydrogenase isozymes in rat tissues. Eur. J. Biochem.7, 215–220
Engel, W., Schmidtke, J., Vogel, W., Wolf, U. (1973). Genetic polymorphism of lactate dehydrogenase isoenzymes in the carp (Cyprinus carpio) apparently due to a “null allele.” Biochem. Genet.8, 281–289
Engle, W., Schmidtke, J., Wolf, U. (1975). Diploid-tetraploid relationships in teleostean fishes. In: Isozymes IV. Genetics and Evolution, C.L. Markert, ed., pp. 449–476. New York: Academic Press
Eppenberger, H.M., Scholl, A., Ursprung, H. (1971). Tissue specific isoenzyme patterns of creatine kinase (2.7.3.2) in trout. FEBS Letters14, 317–319
Ferris, S.D., Whitt, G.S. (1977a). Loss of duplicate gene expression after polyploidization. Nature265, 258–260
Ferris, S.D., Whitt, G.S. (1977b). Duplicate gene expression in diploid and tetraploid loaches (Cypriniformes, Cobitidae). Biochem. Genet.15, 1097–1111
Ferris, S.D., Whitt, G.S. (1977c). The evolution of duplicate gene expression in the carp (Cyprinus carpio). Experientia33, 1299–1301
Ferris, S.D., Whitt, G.S. (1978a). Phylogeny of tetraploid catostomid fishes based on the loss of duplicate gene expression. Syst. Zool.27, 189–206
Ferris, S.D., Whitt, G.S. (1978b). Genetic and molecular analysis of nonrandom dimer assembly of creatine kinase isozymes of fishes. Biochem. Genet.16, 811–830
Ferris, S.D., Portnoy, S., Whitt, G.S. (1979). The roles of speciation and divergence time in the loss of duplicate gene expression. Theoret. Pop. Biol. (in press)
Fisher, S.E., Whitt, G.S. (1978). Evolution of isozyme loci and their differential tissue expression: Creatine kinase as a model system. J. Mol. Evol.12, 25–55
Fisher, S.E., Shaklee, J.B., Ferris, S.D., Whitt, G.S. (1979). Evolution of five multilocus isozyme systems in the chordates. In: Animal Genetics and Evolution (in press)
Flickinger, R. (1975). Relation of an evolutionary mechanism to differentiation. Differentiation3, 155–159
Garcia-Olmedo, F., Carbonero, P., Aragoncillo, C., Salcedo, G. (1978). Loss of redundant gene expression after polyploidization in plants. Experientia34, 332–333
Gilbert, B.E., Johnson, T.C. (1972). Protein turnover during maturation of mouse brain tissue. J. Cell. Biol.53, 143–147
Goldberg, E. (1977). Isozymes in testes and spermatozoa. In: Isozymes, Current Topics in Biological and Medical Research, M. Rattazzi, J.G. Scandalios, G.S. Whitt, eds.,1, 80–125. New York: Alan R. Liss, Inc.
Goodman, M., Moore, G.W., Matsuda, G. (1975). Evolution of vertebrate hemoglobin amino acid sequences. In: Isozymes IV. Genetics and Evolution, C.L. Markert, ed., pp. 181–206. New York: Academic Press
Gottlieb, L.D. (1976). Biochemical consequences of speciation in plants. In: Molecular Evolution, F.J. Ayala, ed., pp. 123–140. Sinauer Associates, Inc., Sunderland, Mass.
Gottlieb, L.D. (1977). Evidence for duplication and divergence of the structural gene for phosphogluco-isomerase in diploid species ofClarkia. Genetics86, 289–307
Hart, G.E., Langston, P.J. (1977). Chromosomal location and evolution of isozyme structural genes in hexaploid wheat. Heredity39, 263–277
Holmes, R.S., Markert, C.L. (1969). Immunochemical homologies among subunits of trout lactate dehydrogenase isozymes. Proc. Natl. Acad. Sci. U.S.A.64, 205–210
Hopkinson, D.A., Edwards, Y.H., Harris, H. (1976). The distributions of subunit numbers and subunit sizes of enzymes: a study of the products of 100 human gene loci. Ann. Hum. Genet., Lond.39, 383–411
Ingram, V.M. (1961). Gene evolution and the haemoglubins. Nature189, 704–708
Jones, G.L., Masters, C.J. (1974). On the synthesis and degradation of the multiple forms of catalase in mouse liver. Arch. Biochem. Biophys.161, 601–609
King, M., Wilson, A.C. (1975). Evolution at two levels in humans and chimpanzees. Science188, 107–116
Klebe, R.J. (1975). A simple method for the quantitation of isozyme patterns. Biochem. Genet.13, 805–812
Lim, S.T., Kay, R.M., Bailey, G.S. (1975). Lactate dehydrogenase isozymes in salmonid fish. Evidence for unique and rapid functional divergence of duplicated H4 lactate dehydrogenases. J. Biol. Chem.250, 1790–1800
Lim, S.T., Bailey, G.S. (1977). Gene duplication in salmonid fishes: Evidence for duplicated but catalytically equivalent A4 lactate dehydrogenases. Biochem. Genet.15, 707–721
Lebherz, H.G. (1975). Evidence for lack of subunit exchange between aldolase tetramers in vivo. J. Biol. Chem.250, 7388–7391
Lewis, N., Gibson, J. (1978). Variation in amount of enzyme protein in natural populations. Biochem. Genet.16, 159–170
Long, W.L., Ballard, W.W. (1976). Normal embryonic stages of the white sucker,Catostomus commersoni. Copeia 1976, 342–351
Majerus, P.W., Kilburn, E. (1969). Acetyl coenzyme A carboxylase. The roles of synthesis and degradation in regulation of enzyme levels in rat liver. J. Biol. Chem.244, 6254–6262
Markert, C.L., Masui, Y. (1969). Lactate dehydrogenase isozymes of the penguinPygoscelis adeliae. J. Exp. Zool.172, 121–146
Markert, C.L., Ursprung, H. (1971). Developmental Genetics. New Jersey: Prentice Hall
Markert. C.L., Shaklee, J.B., Whitt, G.S. (1975). Evolution of a gene. Science189, 102–114
Nadal-Ginard, B. (1978). Regulation of lactate dehydrogenase levels in the mouse. J. Biol. Chem.253, 170–177
Ohno, S. (1970). Evolution by Gene Duplication. New York: Springer-Verlag
Perutz, M.F., Kendrew, J.C., Watson, H.C. (1965). Structure and function of haemoglobin. II. Some relations between polypeptide chain configuration and amino acid sequence. J. Mol. Biol.13, 669–678
Pesce, A., Fondy, T.P. Stolzenbach, F., Castillo, F., Kaplan, N.O. (1967). The comparative enzymology of lactic dehydrogenases. J. Biol. Chem.242, 2151–2167
Petit, C., Zuckerkandl, E. (1976). Evolution Genetique des Populations, Evolution Moleculaire. Paris: Herman Press
Scandalios, J.G. (1975). Differential gene expression and biochemical properties of catalase isozymes in maize. In: Isozymes III: Developmental Biology, C.L. Markert, ed., pp. 213–238. New York: Academic Press
Shaklee, J.B., Kepes, K.L., Whitt, G.S. (1973). Specialized lactate dehydrogenase isozymes: The molecular and genetic basis for the unique eye and liver LDHs of teleost fishes. J. Exp. Zool.185, 217–240
Shaklee, J.B., Champion, M.J., Whitt, G.S. (1974). Developmental genetics of teleosts: A biochemical analysis of lake chubsucker ontogeny. Devel. Biol.38, 356–382
Shaklee, J.B. (1975). The role of subunit interactions in the genesis of non-binomial lactate dehydrogenase isozyme distributions. In: Isozymes I: Molecular Structure, C.L. Markert, ed., pp. 101–118. New York: Academic Press
Shaw, C.R., Prasad, R. (1970). Starch gel electrophoresis of enzymes—A compilation of recipes. Biochem. Genet.4, 297–320
Shows, T.B., Massaro, E.J., Ruddle, F.H. (1969). Evolutionary evidence for a regulator gene controlling the lactate dehydrogenase B gene in rodent erythrocytes. Biochem. Genet.3, 525–536
Shultze, B., Oehlert, W. (1960). Autoradiographic investigation of incorporation of3H-thymidine into cells of rat and mouse. Science131, 737–738
Sparrow, A.H., Nauman, A.F. (1976). Evolution of genome size by DNA doublings. Science192, 524–529
Uyeno, T., Smith, G.R. (1972). Tetraploid origin of the karyotype of catostomid fishes. Science175, 644–646
Wallace, B., Kass, T.L. (1974). On the structure of gene control regions. Genetics77, 541–558
Watts, D.C. (1975). Evolution of phosphagen kinases in the chordate line. Symp. Zool. Soc., London36, 105–127
Whitt, G.S., Miller, E.T., Shaklee, J.B. (1973). Developmental and biochemical genetics of lactate dehydrogenase isozymes in fishes. In: Genetics and Mutagenesis of Fish, J.H. Schroder, ed., pp. 243–276. New York: Springer-Verlag
Whitt, G.S., Childers, W.F., Shaklee, J.B., Matsumoto, J. (1976). Linkage analysis of the multilocus glucosephosphate isomerase isozyme system in sunfish (Centrarchidae, Teleostii). Genetics82, 35–42
Whitt, G.S., Philipp, D.P., Childers, W.F. (1977). Aberrant gene expression during development of hybrid sunfishes (Perciformes, Teleostei). Differentiation9, 97–109
Wilson, A.C., Sarich, V.M., Maxson, L.R., (1974). The importance of gene rearrangement in evolution: evidence from studies on rates of chromosomal, protein, and anatomical evolution. Proc. Nat. Acad. Sci. U.S.A.71, 3028–3030
Zuckerkandl, E. (1965). The evolution of hemoglobin. Sci. Amer.212, 110–118
Zuckerkandl, E. (1968). Hemoglobins, Haeckel's “Biogenetic Law.” and Molecular Aspects of Development, In: Structural Chemistry and Molecular Biology. A. Rich, N. Davidson, eds., pp. 256–274. San Francisco: W.H. Freeman and Co.
Zuckerkandl, E. (1978). Multilocus enzymes, gene regulation, and genetic sufficiency. J. Mol. Evol.12, 57–89
Zuckerkandl, E., Pauling, L. (1965). In: Evolving Genes and Proteins. V. Bryson, H.J. Vogel, eds., p. 97. New York: Academic Press
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Ferris, S.D., Whitt, G.S. Evolution of the differential regulation of duplicate genes after polyploidization. J Mol Evol 12, 267–317 (1979). https://doi.org/10.1007/BF01732026
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF01732026