Skip to main content
SpringerLink
Log in

Essential factors determining codon usage in ubiquitin genes

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Summary

Ubiquitin is ubiquitous in all eukaryotes and its amino acid sequence shows extreme conservation. Ubiquitin genes comprise direct repeats of the ubiquitin coding unit with no spacers. The nucleotide sequences coding for 13 ubiquitin genes from 11 species reported so far have been compiled and analyzed. The G+C content of codon third base reveals a positive linear correlation with the genome G+C content of the corresponding species. The slope strongly suggests that the overall G+C content of codons of polyubiquitin genes clearly reflects the genome G+C content by AT/GC substitutions at the codon third position. The G+C content of ubiquitin codon third base also shows a positive linear correlation with the overall G+C content of coding regions of compiled genes, indicating the codon choices among synonymous codons reflect the average codon usage pattern of corresponding species. On the other hand, the monoubiquitin gene, which is different from the polyubiquitin gene in gene organization, gene expression, and function of the encoding protein, shows a different codon usage pattern compared with that of the polyubiquitin gene. From comparisons of the levels of synonymous substitutions among ubiquitin repeats and the homology of the amino acid sequence of the tail of monomeric ubiquitin genes, we propose that the molecular evolution of ubiquitin genes occurred as follows: Plural primitive ubiquitin sequences were dispersed on genome in ancestral eukaryotes. Some of them situated in a particular environment fused with the tail sequence to produce monomeric ubiquitin genes that were maintained across species. After divergence of species, polyubiquitin genes were formed by duplication of the other primitive ubiquitin sequences on different chromosomes. Differences in the environments in which ubiquitin genes are embedded reflect the differences in codon choice and in gene expression pattern between poly- and monomeric ubiquitin genes.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Aota S, Ikemura T (1986) Diversity in G+C content at the third position of codons in vertebrate genes and its causes. Nucleic Acids Res 14:6345–6355

    PubMed  Google Scholar 

  • Baker RT, Board PG (1987) The human ubiquitin gene family: structure of a gene and pseudogene from the Ub B subfamily. Nucleic Acids Res 15:443–463

    PubMed  Google Scholar 

  • Bernardi G, Bernardi G (1986) Compositional constraints and genome evolution. J Mol Evol 24:1–11

    PubMed  Google Scholar 

  • Bernardi G, Olofsson B, Filipski J, Zerial M, Salinas J, Cuny G, Mennier-Rotival M, Rodier F (1985) The mosaic genome of warm-blooded vertebrates. Science 228:953–958

    PubMed  Google Scholar 

  • Bond U, Schlesinger MJ (1985) Ubiquitin is a heat shock protein in chicken embryo fibroblasts. Mol Cell Biol 5:949–956

    PubMed  Google Scholar 

  • Bond U, Schlesinger MJ (1986) The chicken ubiquitin gene contains a heat shock promoter and expresses an unstable mRNA in heat-shocked cells. Mol Cell Biol 6:4602–4610

    PubMed  Google Scholar 

  • Callis J, Pollmann L, Shanklin J, Wettern M, Vierstra RD (1989) Sequence of a cDNA fromChlamydomonas reinhardii encoding a ubiquitin 52 amino acid extension protein. Nucleic Acids Res 17:8377

    PubMed  Google Scholar 

  • Comings DE (1978) Mechanisms of chromosome banding and implications for chromosome structure. Annu Rev Genet 12: 25–46

    Article  PubMed  Google Scholar 

  • CRC Handbook of Biochemistry and Molecular Biology (1976) ed 3. Nucleic acids, vol II. CRC Press, Cleveland OH

  • Dworkin-Rastl E, Shrutkowski A, Dworkin MB (1984) Multiple ubiquitin mRNAs duringXenopus laevis development contain tandem repeats of the 76 amino acid coding sequence. Cell 39:321–325

    Article  PubMed  Google Scholar 

  • Einspanier R, Sharma HS, Scheit KH (1987) An mRNA encoding poly-ubiquitin in porcine corpus luteum: identification by cDNA. DNA 6:395–400

    PubMed  Google Scholar 

  • Finley D, Özkaynak E, Varshavsky A (1987) The yeast polyubiquitin gene is essential for resistance to high temperatures, starvation, and other stresses. Cell 48:1035–1046

    Article  PubMed  Google Scholar 

  • Gausing K, Barkardottir R (1986) Structure and expression of ubiquitin genes in higher plants. Eur J Biochem 158:57–62

    Article  PubMed  Google Scholar 

  • Giorda R, Ennis HL (1987) Structure of two developmentally regulatedDictyostelium discoideum ubiquitin genes. Mol Cell Biol 7:2097–2103

    PubMed  Google Scholar 

  • Goldknopf IL, Busch H (1977) Isopeptide linkage between non-histone and histone 2A polypeptides of chromosomal conjugate-protein A24. Proc Natl Acad Sci USA 74:864–868

    PubMed  Google Scholar 

  • Goldstein G, Scheid M, Hammerling U, Boyse EA, Schlesinger DH, Niall HD (1975) Isolation of a polypeptide that has lymphocyte-differentiating properties and is probably represented universally in living cells. Proc Natl Acad Sci USA 72: 11–15

    PubMed  Google Scholar 

  • Graham RW, Jones D, Candido PM (1989) UbiA, the major polyubiquitin locus inCaenorhabditis elegans, has unusual structural features and is constitutively expressed. Mol Cell Biol 9:268–277

    PubMed  Google Scholar 

  • Grosjean H, Sankoff D, Min Jou W, Fiers W, Cedergren RJ (1978) Bacteriophage MS2 RNA: a correlation between the stability of codon-anticodon interaction and the choice of codon words. J Mol Evol 12:113–119

    Article  PubMed  Google Scholar 

  • Hasegawa M, Yasunaga T, Miyata T (1979) Secondary structure of MS2 phage RNA and bias in code word usage. Nucleic Acids Res 7:2073–2079

    PubMed  Google Scholar 

  • Hershko A, Ciechanover A (1986) The ubiquitin pathway for the degradation of intracellular proteins. Prog Nucleic Acids Res Mol Biol 33:19–56

    Google Scholar 

  • Ikemura T (1981a) Correlation between the abundance ofEscherichia coli transfer RNAs and the occurrence of the repetitive codon in protein genes. J Mol Biol 146:1–21

    Article  PubMed  Google Scholar 

  • Ikemura T (1981b) Correlation between the abundance ofEscherichia coli transfer RNAs and the occurrence of the repetitive codon in protein genes: a proposal for a synonymous codon choice that is optimal for theE. coli translational system. J Mol Biol 151:389–409

    Article  PubMed  Google Scholar 

  • Ikemura T (1982) Correlation between the abundance of yeast transfer RNAs and the occurrence of the repetitive codon in protein genes: differences in synonymous codon choice patterns of yeast andEscherichia coli with references to the abundance of isoacceptor transfer RNAs. J Mol Biol 158:573–579

    Article  PubMed  Google Scholar 

  • Ikemura T (1985) Codon usage and tRNA content in unicellular and multicellular organisms. Mol Biol Evol 2:13–34

    PubMed  Google Scholar 

  • Ikemura T, Aota S (1988) Global variation in G+C content along vertebrate genome DNA—possible correlation with chromosome band structure. J Mol Biol 203:1–13

    Article  PubMed  Google Scholar 

  • Kirchhoff LV, Kimm KS, Engman DM, Donelson JE (1988) Ubiquitin genes in Trypanosomatidae. J Biol Chem 263: 12698–12704

    PubMed  Google Scholar 

  • Klug A, Rhodes D (1987) ‘Zinc fingers’: a novel protein motif for nucleic acid recognition. Trends Biol Sci 12:464–469

    Article  Google Scholar 

  • Lamb BC (1984) The properties of meiotic gene conversion important in its effects on evolution. Heredity 53:113–138

    PubMed  Google Scholar 

  • Lee H, Simon JA, Lis JT (1988) Structure and expression of ubiquitin genes ofDrosophila melanogaster. Mol Cell Biol 8: 4727–4735

    PubMed  Google Scholar 

  • Leung DW, Spencer SA, Cachianes G, Hammonds RG, Collins C, Henzel WJ, Barnard R, Waters MJ, Wood WI (1987) Growth hormone receptor and serum binding proteins: purification, cloning and expression. Nature 330:537–543

    Article  PubMed  Google Scholar 

  • Levinger L, Varshavsky A (1982) Selective arrangement of ubiquitinated and D1 protein-containing nucleosomes within theDrosphila genome. Cell 28:375–385

    Article  PubMed  Google Scholar 

  • Lund PK, Moats-Staats BM, Simmons JG, Hoyt E, D'Ercole AJ, Martin F, Van Wyck JJ (1985) Nucleotide sequence analysis of a cDNA encoding human ubiquitin reveals that ubiquitin is synthesized as a precursor. J Biol Chem 260:7609–7613

    PubMed  Google Scholar 

  • Maruyama T, Gojobori T, Aota S, Ikemura T (1986) Codon usage tabulated from the GenBank genetic sequence data. Nucleic Acids Res 14:r151-r197

    PubMed  Google Scholar 

  • McKenna MG (1975) In: Luckett WP, Szalay FS (eds) Phylogeny of the primates. Plenum, New York, p 21

    Google Scholar 

  • Mita K, Ichimura S, Zama M, James TC (1988) Specific codon usage pattern and its implications on the secondary structure of silk fibroin mRNA. J Mol Biol 203:917–925

    Article  PubMed  Google Scholar 

  • Müller-Taubenberger A, Hagman J, Noegel A, Gerisch G (1988) Ubiquitin gene expression inDictyostelium is induced by heat and cold shock, cadmium, and inhibitors of protein synthesis. J Cell Sci 90:51–58

    PubMed  Google Scholar 

  • Muto A, Osawa S (1987) The guanine and cytosine content of genomic DNA and bacterial evolution. Proc Natl Acad Sci USA 84:166–169

    PubMed  Google Scholar 

  • Nichols BP, Miozzari GF, van Cleemput M, Bennett GM, Yanofsky C (1980) Nucleotide sequences of the trpG regions ofEscherichia coli, Shigella dysenteriae, Salmonella typhimurium andSerratia marcescens. J Mol Biol 142:503–517

    Article  PubMed  Google Scholar 

  • Özkaynak E, Finley D, Solomon MJ, Varshavsky A (1987) The yeast ubiquitin genes: a family of natural gene fusions. EMBO J 6:1429–1439

    PubMed  Google Scholar 

  • Rechsteiner M (1987) Ubiquitin-mediated pathways for intracellular proteolysis. Annu Rev Cell Biol 3:1–30

    Article  PubMed  Google Scholar 

  • Romero-Herrera AE, Lehman H, Joysey KA, Friday AE (1973) Molecular evolution of myoglobin and the fossil record: a phylogenetic synthesis. Nature 246:389–395

    Article  PubMed  Google Scholar 

  • Salvesen G, Lloyd C, Farley D (1987) cDNA encoding a human homolog of yeast ubiquitin 1. Nucleic Acids Res 15:5485

    PubMed  Google Scholar 

  • Sharp PM, Li WH (1987a) Ubiquitin genes as a paradigm of concerted evolution of tandem repeats. J Mol Evol 25:58–64

    Article  PubMed  Google Scholar 

  • Sharp PM, Li WH (1987b) The codon adaptation index—a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 15:1281–1294

    PubMed  Google Scholar 

  • Siegelman M, Bond MW, Gallatin WM, St John T, Smith HT, Fried VA, Weissman IL (1986) Cell surface molecule associated with lymphocyte homing is a ubiquitinated branchedchain glycoprotein. Science 231:823–829

    PubMed  Google Scholar 

  • St John T, Gallatin WM, Siegelman M, Smith HT, Fried VA, Weissman IL (1986) Expression cloning of a lymphocyte homing receptor cDNA: ubiquitin is a reactive species. Science 231:845–850

    PubMed  Google Scholar 

  • Wada A, Suyama A (1986) Local stability of DNA and RNA secondary structure and its relation to biological function. Prog Biophys Mol Biol 47:113–157

    Article  PubMed  Google Scholar 

  • Warrick H, Spudich J (1988) Codon preference inDictyostelium discoideum. Nucleic Acids Res 16:6617–6635

    PubMed  Google Scholar 

  • Wells D, Bains W, Kedes L (1986) Codon usage in histone gene families of higher eukaryotes reflects functional rather than phylogenetic relationships. J Mol Evol 23:224–241

    PubMed  Google Scholar 

  • Westphal M, Müller-Taubenberger A, Noegel A, Gerisch G (1986) Transcript regulation and carboxyterminal extension of ubiquitin inDictyostelium discoideum. FEBS Lett 209:92–96

    Article  Google Scholar 

  • Wiborg O, Pedersen MS, Wind A, Berglund LE, Marcker KA, Vuust J (1985) The human ubiquitin multigene family: some genes contain multiple directly repeated ubiquitin coding sequences. EMBO J 4:755–759

    PubMed  Google Scholar 

  • Wu RS, Tsai S, Bonner WM (1983) Changes in histone H3 composition and synthesis pattern during lymphocyte activation. Biochemistry 22:2868–3872

    Google Scholar 

  • Yanofsky C, van Cleemput M (1982) Nucleotide sequence of trpE ofSalmonella typhimurium and its homology with the corresponding sequence ofEscherichia coli. J Mol Biol 155: 235–246

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Division of Biology, National Institute of Radiological Sciences, 260, Chiba, Chiba, Japan

    Kazuei Mita & Sachiko Ichimura

  2. Training School, National Institute of Radiological Sciences, 260, Chiba, Chiba, Japan

    Mitsuru Nenoi

Authors
  1. Kazuei Mita
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sachiko Ichimura
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mitsuru Nenoi
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mita, K., Ichimura, S. & Nenoi, M. Essential factors determining codon usage in ubiquitin genes. J Mol Evol 33, 216–225 (1991). https://doi.org/10.1007/BF02100672

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02100672

Key words

Search

Navigation