Journal of Molecular Evolution

, Volume 30, Issue 4, pp 322–328 | Cite as

Evolution of the mitochondrial genetic code III. Reassignment of CUN codons from leucine to threonine during evolution of yeast mitochondria

  • Syozo Osawa
  • David Collins
  • Takeshi Ohama
  • Thomas H. Jukes
  • Kimitsuna Watanabe
Article

Summary

Yeast mitochondria use UUR as the sole leucine codons. CUN, universal leucine codons, are read as threonine by aberrant threonine tRNA with anticodon sequence (UAG).

The reassignment of CUN codons to threonine during yeast mitochondrial evolution could have proceeded by the disappearance of CUN codons from the reading frames of messenger RNA, through mutation mainly to UUR leucine codons as a result of AT pressure. We suggest that this was accompanied by a loss of leucine-accepting ability of tRNA Leu(UAG). This tRNA could have then acquired threonine-accepting activity through the appearance of an additional threonyl-tRNA synthetase. CUN codons that subsequently appeared from mutations of various other codons would have been translated as threonine. This change in the yeast mitochondrial genetic code is likely to have evolved through a series of nondisruptive nucleotide substitutions that produced no widespread replacement of leucine by threonine in proteins as a consequence.

Key words

Genetic code Codon reassignment (capture) CUN leucine codons CUN threonine codons tRNA Yeast mitochondria tRNA synthetases 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ainley WM, Macreadie IG, Butov RA (1985) Var 1 gene on the mitochondrial genome ofTorulopsis glabrata. J Mol Biol 184:565–576CrossRefPubMedGoogle Scholar
  2. Aota S, Gojobori T, Ishibashi F, Maruyama T, Ikemura T (1988) Codon usage tabulated from the GenBank genetic sequence data. Nucleic Acids Res 16(Suppl):r315-r402PubMedGoogle Scholar
  3. 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
  4. Browning KS, RajBhandary UL (1982) Cytochrome oxidase subunit III gene inNeurospora crassa mitochondria: location and sequence. J Biol Chem 257:5253–5296PubMedGoogle Scholar
  5. Clark-Walker GD, McArthur CR, Sriprakash K (1985) Location of transcriptional control signals and transfer RNA sequence inTorulopsis glabrata mitochondrial DNA. EMBO J 4:465–473PubMedGoogle Scholar
  6. Coruzzi G, Tzagoloff A (1979) Assembly of the mitochondrial membrane system: DNA sequence of subunit 2 of yeast cytochrome oxidase. J Biol Chem 254:9324–9330PubMedGoogle Scholar
  7. Heckman JE, Sarnoff J, Alzner-deWeerd 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
  8. Hori H, Osawa S (1987) Origin and evolution of organisms as deduced from 5S ribosomal RNA sequences. Mol Biol Evol 4:445–472PubMedGoogle Scholar
  9. Jacobs HT, Elliot D, Math VB, Farquharson A (1988) Nucleotide sequence and gene organization of sea urchin mitochondrial DNA. J Mol Biol 202:185–217CrossRefPubMedGoogle Scholar
  10. Jukes TH (1981) Amino acid codes in mitochondria as possible clues to primitive codes. J Mol Evol 18:15–17CrossRefPubMedGoogle Scholar
  11. Jukes TH (1985) A change in the genetic code inMycoplasma capricolum. J Mol Evol 22:361–362PubMedGoogle Scholar
  12. Jukes TH, Bhushan V (1986) Silent nucleotide substitutions and G+C content of some mitochondrial and bacterial genes. J Mol Evol 24:39–44CrossRefPubMedGoogle Scholar
  13. Jukes TH, Osawa S, Muto A (1987) Divergence and directional mutation pressures. Nature 325:668CrossRefGoogle Scholar
  14. Kawaguchi Y, Honda H, Taniguchi-Moriimura J, Iwasaki S (1989) The codon CUG is read as serine in an asporogenic yeastCandida cylindracea. Nature 341:164–166CrossRefPubMedGoogle Scholar
  15. Köchel HG, Lazarus CM, Basak N, Küntzel H (1981) Mitochondrial tRNA gene clusters inAspergillus nidulans: organization and nucleotide sequence. Cell 23:625–633CrossRefPubMedGoogle Scholar
  16. Lewin B (1987) Genes III. John Wiley & Sons, New YorkGoogle Scholar
  17. Li M, Tzagoloff A (1979) Assembly of the mitochondrial membrane system: sequence of yeast mitochondrial valine and an unusual threonine tRNA gene. Cell 18:47–53CrossRefPubMedGoogle Scholar
  18. Macino G, Tzagoloff A (1980) Assembly of the mitochondrial membrane system: sequence analysis of a yeast mitochondrial ATPase gene containing theoli-2 andoli-4 loci. Cell 20:507–517CrossRefPubMedGoogle Scholar
  19. Macino G, Morelli G (1983) Cytochrome oxidase subunit z gene inNeurospora crassa mitochondria. J Biol Chem 258: 13230–13235PubMedGoogle Scholar
  20. Morelli G, Macino G (1984) Two intervening sequences in the ATPase subunit 6 gene ofNeurospora crassa: a short intron (93 base-pairs) and a long intron that is stable after excision. J Mol Biol 178:491–507CrossRefPubMedGoogle Scholar
  21. 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
  22. Netzker R, Kochel HG, Basak N, Kuntzel H (1982) Nucleotide sequence ofAspergillus nidulans mitochondrial genes coding for ATPase subunit 6, cytochrome oxidase subunit 3, seven unidentified proteins, four tRNAs and L-rRNA. Nucleic Acids Res 10:4783–4794PubMedGoogle Scholar
  23. Nobrega FG, Tzagoloff A (1980) Assembly of the mitochondrial membrane system: DNA sequence and organization of the cytochrome b gene inSaccharomyces cerevisiae D273-10B. J Biol Chem 255:9828–9837PubMedGoogle Scholar
  24. Osawa S, Jukes TH (1989) Codon reassignment (codon capture) in evolution. J Mol Evol 28:271–278PubMedGoogle Scholar
  25. Osawa S, Ohama T, Jukes TH, Watanabe K (1989a) Evolution of the mitochondrial genetic code I. Origin of AGR serine and stop codons in metazoan mitochondria. J Mol Evol 29: 202–207PubMedGoogle Scholar
  26. Osawa S, Ohama T, Jukes TH, Watanabe K, Yokoyama S (1989b) Evolution of the mitochondrial genetic code II. Reassignment of codon AUA from isoleucine to methionine. J Mol Evol 29:373–380PubMedGoogle Scholar
  27. Pape LK, Tzagoloff A (1985) Cloning and characterization of the gene for the yeast cytoplasmic threonyl-tRNA synthetase. Nucleic Acids Res 13:6171–6183PubMedGoogle Scholar
  28. Pape LK, Koerner TJ, Tzagoloff A (1985) Characterization of a yeast nuclear gene (MST1) coding for the mitochondrial threonyl-tRNA1 synthetase. J Biol Chem 260:15362–15370PubMedGoogle Scholar
  29. Sibler AP, Dirheimer G, Martin RP (1981) Nucleotide sequence of a yeast mitochondrial threonine tRNA able to decode the C-U-N leucine codons. FEBS Lett 132:344–348CrossRefPubMedGoogle Scholar
  30. Sprinzl M, Hartmann T, Meissner F, Moll J, Vordewulbecke T (1987) Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res 15(Suppl):r53-r188PubMedGoogle Scholar
  31. Sueoka N (1962) On the genetic basis of variation and heterogeneity of DNA base composition. Proc Natl Acad Sci USA 48:582–592PubMedGoogle Scholar
  32. Sueoka N (1988) Directional mutation pressure and neutral molecular evolution. Proc Natl Acad Sci USA 85:2653–2657PubMedGoogle Scholar
  33. Thalenfeld BE, Tzagoloff A (1980) Assembly of mitochondrial membrane syystem: sequence of theOxi 2 gene of yeast mitochondrial DNA. J Biol Chem 255:6173–6180PubMedGoogle Scholar
  34. Waring RB, Davies RW, Lee S, Grisi E, Berks MM, Scazzocchio C (1981) The mosaic organization of the apocytochrome b gene ofAspergillus nidulans revealed by DNA sequencing. Cell 27:4–11CrossRefPubMedGoogle Scholar
  35. Zamaroczy M, Bernardi G (1986) The GC clusters of the mitochondrial genome and their evolutionary origin. Gene 41: 1–22CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag New York Inc. 1990

Authors and Affiliations

  • Syozo Osawa
    • 1
  • David Collins
    • 2
  • Takeshi Ohama
    • 1
  • Thomas H. Jukes
    • 2
  • Kimitsuna Watanabe
    • 3
  1. 1.Laboratory of Molecular BiologyNagoya UniversityNagoyaJapan
  2. 2.Space Sciences LaboratoryUniversity of CaliforniaBerkeleyUSA
  3. 3.Department of Life ChemistryTokyo Institute of TechnologyYokohamaJapan

Personalised recommendations