Advertisement

Journal of Molecular Evolution

, Volume 28, Issue 4, pp 271–278 | Cite as

Codon reassignment (codon capture) in evolution

  • Syozo Osawa
  • Thomas H. Jukes
Article

Summary

The genetic code, once thought to be “frozen”, show variations from the universal code. Variations are found in mitochondria,Mycoplasma, and ciliated protozoa. The variations results from reassignment of codons, especially stop codons. The ressignments take place by disappearance of a codon from coding sequences, followed by its reappearance in a new role. Simultaneously, a changed anticodon must appear. We discuss the role of directional mutation pressure in the pressure in the events, and we also describe the possibility that such events have taken place during early evolution of the genetic code and can occur during its present evolution.

Key words

Genetic code Codon reassignment Codon capture Directional mutation pressure AT/GC pressure Wobble rules Mitochondria Mycoplasma Ciliated protozoa 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Andachi Y, Yamao F, Iwami M, Muto A, Osawa S (1987a) Occurrence of unmodified adenine and uracil at the first position of anticodon in threonine tRNAs inMycoplasma capricolum. Proc Natl Acad Sci USA 84:7398–7402PubMedGoogle Scholar
  2. Andachi Y, Muto A, Yamao F, Osawa S (1987b) Novel codonanticodon recognition patterns inMycoplasma capricolum. proc Jpn Acad 63(B):353–356Google Scholar
  3. Anderson S, Bankier AT, Barrell BG de Bruijn MHL, Coulson AR, Drouin J, Eperon IC, Nierlich DP, Roe BA, Sanger F, Schreier PH, Smith AJH, Staden R, Young IG (1981) Sequence and organization of the human mitochondrial genome. Nature 290:457–465PubMedGoogle Scholar
  4. Barrell G, Bankier AT, Drouin J (1979) A different genetic code in human mitochondria. Nature 282:189–194PubMedGoogle Scholar
  5. Bartnik E, Borsuk P (1986) A glycine tRNA gene from lupine mitochondria. Nucleic acids Res 14:2407PubMedGoogle Scholar
  6. Bonitz SG, Berlani R, Coruzzi G, Li M, Macino G, Nobrega FG, Nobrega MP, Thalenfeld BE, Tzagoloff A (1980) Codon recognition rules in yeast mitochondria. Proc Natl Acad Sci USA 77:3167–3170PubMedGoogle Scholar
  7. Cantatore P, Roberti M, Rainaldi G, Saccone C, Gadaleta MN (1988) Clustering of tRNA genes inParacentrotus lividus mitochondrial DNA. Curr Genet 13:91–96PubMedGoogle Scholar
  8. Caron F, Meyer E (1985) DoesParamecium primaurelia use a different genetic code in its macronucleus. Nature 314:185–188PubMedGoogle Scholar
  9. Clary DO, Wolstenholme DR (1985) The mitochondrial DNA molecule ofDrosophila yakuba: nucleotide sequence, gene organization, and genetic code. J Mol Evol 22:252–271PubMedGoogle Scholar
  10. Crick FHC (1966) Codon-anticodon pairing: the wobble hypothesis. J Mol Biol 19:548–555PubMedGoogle Scholar
  11. Fasman GD (ed) (1976) Handbook of biochemistry and molecular biology, ed 2. Nucleic acids, vol 2. CRC Press, Cleveland OHGoogle Scholar
  12. Fox TD (1987) Natural variation in the genetic code. Annu Rev Genet 21:67–91PubMedGoogle Scholar
  13. Fox TD, Leaver CJ (1981) TheZea mays mitochondrial gene coding cytochrome oxidase subunit II has an intervening sequence and does not contain TGA codons. Cell 26:315–323PubMedGoogle Scholar
  14. Gray MW, Spencer DF (1983) Wheat mitochondrial DNA encodes a eubacteria-like initiator methionine transfer RNA. FEBS Lett 161:323–327Google Scholar
  15. Hanyu N, Kuchino Y, Nishimura S, Beier H (1986) Dramatic events in ciliate evolution: alteration of UAA and UAG termination codons to glutamine codons due to anticodon mutations in twoTetrahymena tRNAs Gln. EMBO J 5:1307–1311Google Scholar
  16. Heckman JE, Sarnoff J, Alzner-de Weerd B, Yin S, RajBhandary UL (1980) Novel features in the genetic code and codon reading patterns inNeurospora crassa mitochondria based on sequences of six mitochondrial tRNAs. Proc Natl Acad Sci USA 77:3159–3163PubMedGoogle Scholar
  17. Helftenbein E (1985) Nucleotide sequence of a macronuclear DNA molecule coding for alpha-tubulin from the ciliateStylonychia lemnae. Special codon usage: TAA is not a translation termination codon. Nucleic Acids Res 13:415–433PubMedGoogle Scholar
  18. Hiesel R, Brennicke A (1983) Cytochrome oxidase subunit II gene in mitochondria ofOenothera has no intron. EMBO J 2:2173–2178Google Scholar
  19. Himeno H, Masaki H, Kawai T, Ohta T, Kumagai I, Miura K Watanabe K (1987) Unusual genetic code and a novel gene structure for tRNA Ser AGY in starfish mitochondrial DNA. Gene 56:219–230PubMedGoogle Scholar
  20. Hori H, Osawa S (1987) Origin and evolution of organisms as deduced from 5S ribosomal RNA sequences. Mol Biol Evol 4:445–472PubMedGoogle Scholar
  21. Horowitz S, Gorovsky MA (1985) An unusual genetic code in nuclear genes ofTetrahymena. Proc Natl Acad Sci USA 82: 2452–2455PubMedGoogle Scholar
  22. Joyce PBM, Gray MW (1988) Nucleotide sequence of a wheat mitochondrial glutamine tRNA gene. Nucleic Acids Res 16: 1210PubMedGoogle Scholar
  23. Jukes TH (1981) Amino acid codes in mitochondria as possible clues to primitive codes. J Mol Evol 18:15–17PubMedGoogle Scholar
  24. Jukes TH (1983) Evolution of the amino acid code: inferences from mitochondrial codes. J Mol Evol 19:219–225PubMedGoogle Scholar
  25. Jukes TH (1985) A change in the genetic code inMycoplasma capricolum. J Mol Evol 22:361–362PubMedGoogle Scholar
  26. Jukes TH, Bhushan V (1986) Silent nucleotide substitutions and G+C content of some mitochondrial and bacterial genes. J Mol Evol 24:39–44PubMedGoogle Scholar
  27. Jukes TH, Osawa S, Muto A (1987a) Divergence and directional mutation pressures. Nature 325:668Google Scholar
  28. Jukes TH, Osawa S, Muto A, Lehman N (1987b) Evolution of anticodons: variations in the genetic code. Cold Spring Harbor Symp Quant Biol 52:769–776PubMedGoogle Scholar
  29. Macreadie IG, Novitski CE, Maxwell RJ, John U, Ooi B-G, McMullen GLL, Lukins HB, Linnane AW, Nagley P (1983) Biogenesis of mitochondria: the mitochondrial gene (appl) coding for mitochondrial ATPase subunit 8 inSaccharomyces cerevisiae. Nucleic Acids Res 11:4435–4451PubMedGoogle Scholar
  30. Marechal L, Gullemau P, Grieneberger J-M, Jeannin G, Weil J-H (1985) Sequence and codon recognition of bean mitochondria ad chloroplast tRNAs Trp: evidence for a high degree of homology. Nucleic Acids Res 13:4411–4416PubMedGoogle Scholar
  31. Maruyama S, Gojobori T, Aota S, Ikemura T (1986) Codon usage tabulaged from the GenBank genetic sequence data. Nucleic Acids Res 14(Suppl):r151–197PubMedGoogle Scholar
  32. Muramatsu T, Yokoyama S, Hirose N, Matsuda A, Ueda T, Yamaizumi Z, uchino Y, Nishimura S, Miyazawa T (1988a) A novel lysine-substituted nucleoside in the first position of the anticodon of minor isoleucine tRNA fromEscherichia coli. J Biol Chem 263:9261–9267PubMedGoogle Scholar
  33. Muramatsu T, Nishikawa K, Nemoto F, Kuchino Y, Nishimura A, Miyazawa T, Yokoyama S (1988b) Codon and aminoacid specificities of a transfer RNA are both converted by a single post-transcriptional modification. Nature 336:179–181PubMedGoogle Scholar
  34. Muto A, Osawa S (1987) The guanine and cytosine content of genomic DNA and bacterial evolution. Proc Natl Acad Sci USA 84:1166–1169Google Scholar
  35. Ohama T, Yamao F, Muto A, Osawa S (1987) Organization and codon usage of the streptomycin operon inMicrococcus luteus, a bacterium with a high genomic G+C content. J Bacteriol 169:4770–4777PubMedGoogle Scholar
  36. Ohkubo S, Muto A, Kawauchi Y, Yamao F, Osawa S (1987) The ribosomal protein gene cluster ofMycoplasma capricolum. Mol Gen Genet 210:314–322PubMedGoogle Scholar
  37. Osawa S, Jukes TH, Muto A, Yamao F, Ohama T, Andachi Y (1987) Role of directional mutation pressure in the evolution of the eubacterial genetic code. Cold Spring Harbor Symp Quant Biol 55:777–789Google Scholar
  38. Osawa S, Jukes TH (1988) Evolution of the genetic code as affected by anticodon content. Trends in Genet 4:191–198Google Scholar
  39. Preer JR Jr, Preer LB, Rudman BM, Barnett AJ (1985) Deviation from the universal code shown by the gene for surface protein 51A inParamecium. Nature 314:188–190PubMedGoogle Scholar
  40. Shuster A, Brennicke A (1985) TGA-termination codon in the apocytochrome b gene fromOenothera mitochondria. Curr Genet 9:157–163Google Scholar
  41. Sibler AP, Dirheimer G, Martin RP (1985) Yeast mitochondrial tRNA Ile and tRNA Met: nucleotide sequence and codon recognition patterns. Nucleic Acids Res 13:1341–1345PubMedGoogle Scholar
  42. Sibler AP, Dirheimer G, Martin RP (1986) Codon reading patterns inSaccharomyces cerevisiae mitochondria based on sequences of mitochondrial tRNAs. FEBS Lett 194:131–138PubMedGoogle Scholar
  43. Sprinzl M, Hartmann T, Meissner F, Moll J, Vorderwulbecke T (1987) Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res 15(Suppl):r53-r188PubMedGoogle Scholar
  44. Stern DB, Bang AG, Thompson WF (1986) The watermelon mitochondrial URF-1 gene: evidence for a complex structure. Curr Genet 10:857–869PubMedGoogle Scholar
  45. Sueoka N (1962) On the genetic basis of variation and heterogeneity of DNA base composition. Proc Natl Acad Sci USA 48:166–169Google Scholar
  46. Sueoka N (1988) Directional mutaton pressure and neutral molecular evolution. Proc Natl Acad Sci USA 85:2653–2657PubMedGoogle Scholar
  47. Wallace DC (1982) Structure and evolution of organelle genomes. Microbiol Rev 46:208–240PubMedGoogle Scholar
  48. Watanabe K (1986) Mitochondrial tRNAs. Cell Technol 5:103–113 [in Japanese]Google Scholar
  49. Wintz H, Grieneberger J-M, Weil J-H, Lonsdale DM (1988) Localization and nucleotides sequence of two tRNA genes and a tRNA pseudo-gene in the maize mitochondrial genome: evidence for the transcription of a chloroplast gene in mitochondria. Crr Genet 13:247–254Google Scholar
  50. Wolstenholme DR, Macfarlane JL, Okimoto R, Clary DO, Wahleithner JA (1987) Bizarre tRNAs inferred from DNA sequences of mitochondrial genomes of nematode worms. Proc Natl Acad Sci USA 84:1324–1328PubMedGoogle Scholar
  51. Yamao F, Muto A, Kawauchi Y, Iwami M, Iwagami S, Azumi Y, Osawa S (1985) UGA is read as tryptophan inMycoplasma capricolum. Proc Natl Acad Sci USA 82:2306–2309PubMedGoogle Scholar
  52. Yamao F, Iwagami S, Azumi Y, Muto A, Osawa S (1988) Evolutionary dynamics of tryptophan tRNAs inMycoplasma capricolum. Mol Gen Genet 212:364–369PubMedGoogle Scholar
  53. Yokoyama S, Watanabe T, Murao K, Ishikura H, Yamaizumi Z, Nishimura S, Miyazawa T (1985) Molecular mechanism of codon recognition by tRNAs with modified uridine in the first position of the anticodon. Proc Natl Acad Sci USA 82: 4905–4909PubMedGoogle Scholar

Copyright information

© Springer-Verlag New York Inc 1989

Authors and Affiliations

  • Syozo Osawa
    • 1
  • Thomas H. Jukes
    • 2
  1. 1.Laboratory of Molecular Genetics, Department of BiologyNagoya UniversityNagoyaJapan
  2. 2.Space Sciences LaboratoryUniversity of CaliforniaBerkeleyUSA

Personalised recommendations