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.
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References
Ainley WM, Macreadie IG, Butov RA (1985) Var 1 gene on the mitochondrial genome ofTorulopsis glabrata. J Mol Biol 184:565–576
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-r402
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 77:3167–3170
Browning KS, RajBhandary UL (1982) Cytochrome oxidase subunit III gene inNeurospora crassa mitochondria: location and sequence. J Biol Chem 257:5253–5296
Clark-Walker GD, McArthur CR, Sriprakash K (1985) Location of transcriptional control signals and transfer RNA sequence inTorulopsis glabrata mitochondrial DNA. EMBO J 4:465–473
Coruzzi G, Tzagoloff A (1979) Assembly of the mitochondrial membrane system: DNA sequence of subunit 2 of yeast cytochrome oxidase. J Biol Chem 254:9324–9330
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 77:3159–3163
Hori H, Osawa S (1987) Origin and evolution of organisms as deduced from 5S ribosomal RNA sequences. Mol Biol Evol 4:445–472
Jacobs HT, Elliot D, Math VB, Farquharson A (1988) Nucleotide sequence and gene organization of sea urchin mitochondrial DNA. J Mol Biol 202:185–217
Jukes TH (1981) Amino acid codes in mitochondria as possible clues to primitive codes. J Mol Evol 18:15–17
Jukes TH (1985) A change in the genetic code inMycoplasma capricolum. J Mol Evol 22:361–362
Jukes TH, Bhushan V (1986) Silent nucleotide substitutions and G+C content of some mitochondrial and bacterial genes. J Mol Evol 24:39–44
Jukes TH, Osawa S, Muto A (1987) Divergence and directional mutation pressures. Nature 325:668
Kawaguchi Y, Honda H, Taniguchi-Moriimura J, Iwasaki S (1989) The codon CUG is read as serine in an asporogenic yeastCandida cylindracea. Nature 341:164–166
Köchel HG, Lazarus CM, Basak N, Küntzel H (1981) Mitochondrial tRNA gene clusters inAspergillus nidulans: organization and nucleotide sequence. Cell 23:625–633
Lewin B (1987) Genes III. John Wiley & Sons, New York
Li M, Tzagoloff A (1979) Assembly of the mitochondrial membrane system: sequence of yeast mitochondrial valine and an unusual threonine tRNA gene. Cell 18:47–53
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 20:507–517
Macino G, Morelli G (1983) Cytochrome oxidase subunit z gene inNeurospora crassa mitochondria. J Biol Chem 258: 13230–13235
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 178:491–507
Muto A, Osawa S (1987) The guanine and cytosine content of genomic DNA and bacterial evolution. Proc Natl Acad Sci USA 84:1166–1169
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 10:4783–4794
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 255:9828–9837
Osawa S, Jukes TH (1989) Codon reassignment (codon capture) in evolution. J Mol Evol 28:271–278
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: 202–207
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 29:373–380
Pape LK, Tzagoloff A (1985) Cloning and characterization of the gene for the yeast cytoplasmic threonyl-tRNA synthetase. Nucleic Acids Res 13:6171–6183
Pape LK, Koerner TJ, Tzagoloff A (1985) Characterization of a yeast nuclear gene (MST1) coding for the mitochondrial threonyl-tRNA1 synthetase. J Biol Chem 260:15362–15370
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 132:344–348
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-r188
Sueoka N (1962) On the genetic basis of variation and heterogeneity of DNA base composition. Proc Natl Acad Sci USA 48:582–592
Sueoka N (1988) Directional mutation pressure and neutral molecular evolution. Proc Natl Acad Sci USA 85:2653–2657
Thalenfeld BE, Tzagoloff A (1980) Assembly of mitochondrial membrane syystem: sequence of theOxi 2 gene of yeast mitochondrial DNA. J Biol Chem 255:6173–6180
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 27:4–11
Zamaroczy M, Bernardi G (1986) The GC clusters of the mitochondrial genome and their evolutionary origin. Gene 41: 1–22
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Osawa, S., Collins, D., Ohama, T. et al. Evolution of the mitochondrial genetic code III. Reassignment of CUN codons from leucine to threonine during evolution of yeast mitochondria. J Mol Evol 30, 322–328 (1990). https://doi.org/10.1007/BF02101886
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DOI: https://doi.org/10.1007/BF02101886