Experientia

, Volume 46, Issue 11–12, pp 1117–1126 | Cite as

The genetic code in mitochondria and chloroplasts

  • T. H. Jukes
  • S. Osawa

Summary

The universal genetic code is used without changes in chloroplasts and in mitochondria of green plants. Non-plant mitochondria use codes that include changes from the universal code. Chloroplasts use 31 anticodons in translating the code; a number smaller than that used by bacteria, because chloroplasts have eliminated 10 CNN anticodons that are found in bacteria. Green plant mitochondria (mt) obtain some tRNAs from the cytosol, and genes for some other tRNAs have been acquired from chloroplast DNA. The code in non-plant mt differs from the universal code in the following usages found in various organisms: UGA for Trp, AUA for Met, AGR for Ser and stop, AAA for Asn, CUN for Thr, and possibly UAA for Tyr. CGN codons are not used byTorulopsis yeast mt. Non-plant mt, e.g. in vertebrates, may use a minimum of 22 anticodons for complete translation of mRNA sequences. The following possible causes are regarded as contributing to changes in the non-plant mt: directional mutation pressure, genomic economization, changes in charging specificity of tRNAs, loss of release factor RF2, changes in RF1, changes in anticodons, loss of lysidine-forming enzyme system, and disappearance of codons from coding sequences.

Key words

Genetic code mitochondria evolution organelles 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Andachi, Y., Yamao, F., Muto, A., and Osawa, S., Codon recognition patterns as deduced from sequences of the complete set of transfer RNA species inMycoplasma capricolum: Resemblance to mitochondria. J. molec. Biol.209 (1989) 37–54.CrossRefPubMedGoogle Scholar
  2. 2.
    Barrell, G., Bankier, A. T., and Drouin, J., A different genetic code in human mitochondria. Nature282 (1979) 189–194.PubMedGoogle Scholar
  3. 3.
    Cantatore, P., Roberti, M., Morisco, R., Rainaldi, G., Gadaleta, M. N., and Saccone, C., A novel gene order in theParacentrotus lividus mitochondrial genome. Gene53 (1987) 41–54.CrossRefPubMedGoogle Scholar
  4. 4.
    Clark-Walker, G. D., McArthur, C. R., and Sriprakash, K., Location of transcriptional control signals and transfer RNA sequence inTorulopsis glabrata mitochondrial DNA. EMBO J.4 (1985) 465–473.PubMedGoogle Scholar
  5. 5.
    Gray, M. W., and Boer, P. H., Organization and expression of algal (Chlamydomonas reinhardtii) mitochondrial DNA. Phil. Trans. R. Soc. Lond. B319 (1988) 135–147.Google Scholar
  6. 6.
    Gray, M. W., and Doolittle, W. F., Has the endosymbiont hypothesis been proven? Microbiol. Rev.46 (1982) 1–42.PubMedGoogle Scholar
  7. 7.
    Gray, M. W., Sankoff, D., and Cedergren, R. J., On the evolutionary descent of organisms and organelles: A global phylogeny based on a highly conserved structural core in small subunit ribosomal RNA. Nucl. Acids Res.12 (1984) 5837–5852.PubMedGoogle Scholar
  8. 8.
    Gray, M. W., Cedergren, R., Abel, Y., and Sankoff, D., On the evolutionary origin of the plant mitochondrion and its genome. Proc. natl Acad. Sci. USA86 (1989) 2267–2271.Google Scholar
  9. 9.
    Green, A. G., Maréchal, L., Weil, J. H., and Guillemaut, P., APhaseolus vulgaris mitochondrial tDNALeu is identical to its cytoplasmic counterpart. Plant molec. Biol.10 (1987) 13–19.CrossRefGoogle Scholar
  10. 10.
    Himeno, H., Masaki, H., Ohta, T., Kumagai, I., Miura, K.-I., and Watanabe, K., Unusual genetic codes and a novel genome structure for tRNASer AGY in starfish mitochondrial DNA. Gene56 (1987) 219–230.CrossRefPubMedGoogle Scholar
  11. 11.
    Izuchi, S.-I., and Sugita, M., Nucleotide sequence of a tomato mitochondrial tRNACys (GCA) gene. Nucleic Acids Res.17 (1990) 1248.Google Scholar
  12. 12.
    Jacobs, H. T., Elliott, D. J., Math, V. B., and Farquharson, A., Nucleotide sequence and gene organization of sea-urchin mitochondrial DNA. J. molec. Biol.202 (1988) 185–217.CrossRefPubMedGoogle Scholar
  13. 13.
    Joyce, P. B., and Gray, M. W., Chloroplast-like transfer RNA genes expressed in wheat mitochondria. Nucleic Acids Res.17 (1989) 5461–5476.PubMedGoogle Scholar
  14. 14.
    Köchel, H. G., Lazarus, C. M., Basak, N., and Küntzel, H., Mitochondrial tRNA gene clusters inAspergillus nidulans: organizations and nucleotide sequence. Cell23 (1981) 625–633.CrossRefPubMedGoogle Scholar
  15. 15.
    Küntzel, H., and Köchel, H. G., Evolution of rRNA and origin of mitochondria. Nature293 (1981) 751–755.CrossRefPubMedGoogle Scholar
  16. 16.
    Lee, C. C., Timms, K. M., Trotman, C. N. A., and Tate, W. P., Isolation of a rat mitochondrial release factor: Accommodation of the changed genetic code for termination. J. biol. Chem.262 (1987) 3548–3552.PubMedGoogle Scholar
  17. 17.
    Maréchal-Drouard, L., and Guillemaut, P., Nucleotide sequence of bean mitochondrial tRNALeu4 and of its cytoplasmic counterpart. Re-examination of the modified nucleotide present at position 12 in bean mitochondrial and cytoplasmic tRNALeu1 sequences. Nucleic Acids Res.16 (1988) 11812.PubMedGoogle Scholar
  18. 18.
    Maréchal-Drouard, L., Weil, J. H., and Guillemaut, P., Import of several tRNAs from the cytoplasm into the mitochondria in beanPhaseolus vulgaris. Nucleic Acids Res.16 (1988) 4777–4788.PubMedGoogle Scholar
  19. 19.
    Maréchal-Drouard, L., Guillemaut, P., Cosset, A., Arbogast, M., Weber, F., Weil, J., and Dietrich, A., Transfer RNAs of potato (Solanum tuberosum) mitochondria have different genetic origins. Nucleic Acids Res.18 (1990) 3689–3696.PubMedGoogle Scholar
  20. 20.
    McCarroll, R., Olsen, G. J., Stahl, Y. D., Woese, C. R., and Sogin, M. L., Nucleotide sequence of theDictyostelium discoideum small-subunit ribosomal ribonucleic acid inferred from the gene sequence: Evolutionary implications. Biochemistry22 (1983) 5858–5868.CrossRefGoogle Scholar
  21. 21.
    Muramatsu, T., Nishikawa, K., Nemoto, F., Kuchino, Y., Nishimura, A., Miyazawa, T., and Yokoyama, S., Codon and amino acid specificities of a transfer RNA are both converted by a single post-transcriptional modification. Nature336 (1988) 179–181.CrossRefPubMedGoogle Scholar
  22. 22.
    Ohama, T., Osawa, S., Watanabe, K., and Jukes, T. H., Evolution of the mitochondrial genetic code IV. AAA as an asparagine codon in some animal mitochondria. J. molec. Evol.30 (1990) 329–332.PubMedGoogle Scholar
  23. 23.
    Osawa, S., Collins, D., Ohama, T., Jukes, T. H., and Watanabe, K., Evolution of the mitochondrial genetic code III. Reassignment of CUN codons from leucine to threonine during evolution of yeast mitochondria. J. molec. Evol.30 (1990) 322–328.PubMedGoogle Scholar
  24. 24.
    Osawa, S., and Jukes, T. H., Evolution of the genetic code by anticodon content. Trends Genet.4 (1988) 191–198.CrossRefPubMedGoogle Scholar
  25. 25.
    Osawa, S., and Jukes, T. H., Codon reassignment (codon capture) in evolution. J. molec. Evol.28 (1989) 271–278.PubMedGoogle Scholar
  26. 26.
    Osawa, S., Ohama, T., Jukes, T. H., and Watanabe, K., Evolution of the mitochondrial genetic code I. Origin of AGR serine and stop codons in metazoan mitochondria. J. molec. Evol.29 (1989) 202–207.PubMedGoogle Scholar
  27. 27.
    Osawa, S., Ohama, T., Jukes, T. H., Watanabe, K., and Yokoyama, S., Evolution of the mitochondrial genetic code II. Reassignment of codon AUA from isoleucine to methionine. J. molec. Evol.29 (1989) 373–380.PubMedGoogle Scholar
  28. 28.
    Osawa, S., Muto, A., Jukes, T. H., and Ohama, T., Evolutionary changes in the genetic code. Proc. Roy. Soc. Lond. B241 (1990) 19–28.Google Scholar
  29. 29.
    Ozeki, H., Ohyama, K., Inokuchi, H., Fukuzawa, H., Kiochi, T., Sano, T., Nakahigashi, K., and Umesono, K., Genetic system of chloroplasts. Cold Spring Harbor Symp. quant. Biol.52 (1987) 791–804.PubMedGoogle Scholar
  30. 30.
    Parks, T. D., Dougherty, W. G., Levings, C. S. III, and Timothy, D. H., Identification of two methoinine transfer RNA genes in the maize mitochondrial genome. Plant Physiol.76 (1984) 1079–1082.Google Scholar
  31. 30a.
    Schön, A., Kannangara, C. G., Gough, S., and Söll, D., Protein biosynthesis in organelles requires misaminoacylation of tRNA. Nature331 (1988) 187 ff.CrossRefPubMedGoogle Scholar
  32. 31.
    Seilhamer, J. J., and Cummings, D. J., Altered genetic code inParamecium mitochondria: Possible evolutionary trends. Med. gen. Genet.187 (1982) 236–239.CrossRefGoogle Scholar
  33. 32.
    Suyama, Y., Two-dimensional polyacrylamide gel electrophoresis analysis ofTetrahymena mitochondrial tRNA. Curr. Genet.10 (1986) 411–420.CrossRefPubMedGoogle Scholar
  34. 33.
    Wallace, D. C. W., Structure and evolution of organelle genomes. Microbiol. Rev.46 (1982) 208–240.PubMedGoogle Scholar
  35. 34.
    Weber, F., Dietrich, A., Weil, J.-H., and Maréchal-Drouard, L., A potato mitochondrial isoleucine tRNA is coded for by a mitochondrial gene possessing a methionine anticodon. Nucl. Acids Res.18 (1990) 5027–5030.PubMedGoogle Scholar
  36. 35.
    Wolstenholme, D. R., Okimoto, R., Macfarlane, J. L., Pont, G. A., Chamberlin, H. M., Garey, J. R., and Okada, N. A., Unusual features of lower invertebrate mitochondrial genomes, in: Structure, Function and Biogenesis of Energy Transfer Systems. Eds E. Quagriello, S. Papa, F. Palmieri and C. Saccone. Elsevier, Amsterdam 1990.Google Scholar
  37. 36.
    Wakasugi, T., Ohme, M., Shinozaki, K., and Sugiura, M., Structure of tobacco chloroplast genes of tRNA Ile (CAU), tRNA Leu (CAA), tRNA Cys (GCA), tRNA Ser (UGA) and tRNA Thr (GGU): a compilation of tRNA genes from tobacco chloroplasts. Plant molec. Biol.7 (1986) 385–392.CrossRefGoogle Scholar
  38. 37.
    Yang, D., Oyaizu, Y., Oyaizu, H., Olsen, G. J., and Woese, C. R., Mitochondrial origins. Proc. natl Acad. Sci. USA82 (1985) 4443–4447.PubMedGoogle Scholar

Copyright information

© Birkhäuser Verlag Basel 1990

Authors and Affiliations

  • T. H. Jukes
    • 1
    • 2
  • S. Osawa
    • 1
    • 2
  1. 1.Space Sciences LaboratoryUniversity of California/BerkeleyOaklandUSA
  2. 2.Laboratory of Molecular Genetics, Department of BiologyNagoya UniversityNagoyaJapan

Personalised recommendations