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. 1995 Jul;140(3):1047–1060. doi: 10.1093/genetics/140.3.1047

Nucleotide Sequence and Gene Organization of the Starfish Asterina Pectinifera Mitochondrial Genome

S Asakawa 1, H Himeno 1, K I Miura 1, K Watanabe 1
PMCID: PMC1206660  PMID: 7672576

Abstract

The 16,260-bp mitochondrial DNA (mtDNA) from the starfish Asterina pectinifera has been sequenced. The genes for 13 proteins, two rRNAs and 22 tRNAs are organized in an extremely economical fashion, similar to those of other animal mtDNAs, with some of the genes overlapping each other. The gene organization is the same as that for another echinoderm, sea urchin, except for the inversion of a 4.6-kb segment that contains genes for two proteins, 13 tRNAs and the 16S rRNA. Judging from the organization of the protein coding genes, mammalian mtDNAs resemble the sea urchin mtDNA more than that of the starfish. The region around the 3' end of the 12S rRNA gene of the starfish shows a high similarity with those for vertebrates. This region encodes a possible stem and loop structure; similar potential structures occur in this region of vertebrate mtDNAs and also in nonmitochondrial small subunit rRNA. A similar stem and loop structure is also found at the 3' end of the 16S rRNA genes in A. pectinifera, in another starfish Pisaster ochraceus, in vertebrates and in Drosophila, but not in sea urchins. The full sequence data confirm the presumption that AGA/AGG, AUA and AAA codons, respectively, code for serine, isoleucine, and asparagine in the starfish mitochondria, and that AGA/AGG codons are read by tRNA(GCU)(Ser), which possesses a truncated dihydrouridine arm, that was previously suggested from a partial mtDNA sequence. The structural characteristics of tRNAs and possible mechanisms for the change in the mitochondrial genetic code are also discussed.

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Selected References

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  1. Anderson S., Bankier A. T., Barrell B. G., de Bruijn M. H., Coulson A. R., Drouin J., Eperon I. C., Nierlich D. P., Roe B. A., Sanger F. Sequence and organization of the human mitochondrial genome. Nature. 1981 Apr 9;290(5806):457–465. doi: 10.1038/290457a0. [DOI] [PubMed] [Google Scholar]
  2. Anderson S., de Bruijn M. H., Coulson A. R., Eperon I. C., Sanger F., Young I. G. Complete sequence of bovine mitochondrial DNA. Conserved features of the mammalian mitochondrial genome. J Mol Biol. 1982 Apr 25;156(4):683–717. doi: 10.1016/0022-2836(82)90137-1. [DOI] [PubMed] [Google Scholar]
  3. Arcari P., Brownlee G. G. The nucleotide sequence of a small (3S) seryl-tRNA (anticodon GCU) from beef heart mitochondria. Nucleic Acids Res. 1980 Nov 25;8(22):5207–5212. doi: 10.1093/nar/8.22.5207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Arnason U., Gullberg A., Widegren B. The complete nucleotide sequence of the mitochondrial DNA of the fin whale, Balaenoptera physalus. J Mol Evol. 1991 Dec;33(6):556–568. doi: 10.1007/BF02102808. [DOI] [PubMed] [Google Scholar]
  5. Asakawa S., Kumazawa Y., Araki T., Himeno H., Miura K., Watanabe K. Strand-specific nucleotide composition bias in echinoderm and vertebrate mitochondrial genomes. J Mol Evol. 1991 Jun;32(6):511–520. doi: 10.1007/BF02102653. [DOI] [PubMed] [Google Scholar]
  6. Baer R. J., Dubin D. T. The sequence of a possible 5S RNA-equivalent in hamster mitochondria. Nucleic Acids Res. 1980 Aug 25;8(16):3603–3610. doi: 10.1093/nar/8.16.3603. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Barrell B. G., Bankier A. T., Drouin J. A different genetic code in human mitochondria. Nature. 1979 Nov 8;282(5735):189–194. doi: 10.1038/282189a0. [DOI] [PubMed] [Google Scholar]
  8. Beier H., Barciszewska M., Sickinger H. D. The molecular basis for the differential translation of TMV RNA in tobacco protoplasts and wheat germ extracts. EMBO J. 1984 May;3(5):1091–1096. doi: 10.1002/j.1460-2075.1984.tb01934.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Bibb M. J., Van Etten R. A., Wright C. T., Walberg M. W., Clayton D. A. Sequence and gene organization of mouse mitochondrial DNA. Cell. 1981 Oct;26(2 Pt 2):167–180. doi: 10.1016/0092-8674(81)90300-7. [DOI] [PubMed] [Google Scholar]
  10. Björk G. R., Ericson J. U., Gustafsson C. E., Hagervall T. G., Jönsson Y. H., Wikström P. M. Transfer RNA modification. Annu Rev Biochem. 1987;56:263–287. doi: 10.1146/annurev.bi.56.070187.001403. [DOI] [PubMed] [Google Scholar]
  11. Brown W. M., Prager E. M., Wang A., Wilson A. C. Mitochondrial DNA sequences of primates: tempo and mode of evolution. J Mol Evol. 1982;18(4):225–239. doi: 10.1007/BF01734101. [DOI] [PubMed] [Google Scholar]
  12. Cantatore P., Gadaleta M. N., Roberti M., Saccone C., Wilson A. C. Duplication and remoulding of tRNA genes during the evolutionary rearrangement of mitochondrial genomes. 1987 Oct 29-Nov 4Nature. 329(6142):853–855. doi: 10.1038/329853a0. [DOI] [PubMed] [Google Scholar]
  13. Cantatore P., Roberti M., Loguercio Polosa P., Mustich A., Gadaleta M. N. Mapping and characterization of Paracentrotus lividus mitochondrial transcripts: multiple and overlapping transcription units. Curr Genet. 1990 Mar;17(3):235–245. doi: 10.1007/BF00312615. [DOI] [PubMed] [Google Scholar]
  14. Cantatore P., Roberti M., Rainaldi G., Gadaleta M. N., Saccone C. The complete nucleotide sequence, gene organization, and genetic code of the mitochondrial genome of Paracentrotus lividus. J Biol Chem. 1989 Jul 5;264(19):10965–10975. [PubMed] [Google Scholar]
  15. Cantatore P., Roberti M., Rainaldi G., Saccone C., Gadaleta M. N. Clustering of tRNA genes in Paracentrotus lividus mitochondrial DNA. Curr Genet. 1988;13(1):91–96. doi: 10.1007/BF00365762. [DOI] [PubMed] [Google Scholar]
  16. Clary D. O., Wolstenholme D. R. The mitochondrial DNA molecular of Drosophila yakuba: nucleotide sequence, gene organization, and genetic code. J Mol Evol. 1985;22(3):252–271. doi: 10.1007/BF02099755. [DOI] [PubMed] [Google Scholar]
  17. Clayton D. A. Replication and transcription of vertebrate mitochondrial DNA. Annu Rev Cell Biol. 1991;7:453–478. doi: 10.1146/annurev.cb.07.110191.002321. [DOI] [PubMed] [Google Scholar]
  18. Clayton D. A. Transcription of the mammalian mitochondrial genome. Annu Rev Biochem. 1984;53:573–594. doi: 10.1146/annurev.bi.53.070184.003041. [DOI] [PubMed] [Google Scholar]
  19. Crozier R. H., Crozier Y. C. The mitochondrial genome of the honeybee Apis mellifera: complete sequence and genome organization. Genetics. 1993 Jan;133(1):97–117. doi: 10.1093/genetics/133.1.97. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Dahlberg A. E. The functional role of ribosomal RNA in protein synthesis. Cell. 1989 May 19;57(4):525–529. doi: 10.1016/0092-8674(89)90122-0. [DOI] [PubMed] [Google Scholar]
  21. Desjardins P., Morais R. Sequence and gene organization of the chicken mitochondrial genome. A novel gene order in higher vertebrates. J Mol Biol. 1990 Apr 20;212(4):599–634. doi: 10.1016/0022-2836(90)90225-B. [DOI] [PubMed] [Google Scholar]
  22. Dubin D. T., HsuChen C. C., Cleaves G. R., Timko K. D. Sequence and structure of a serine transfer RNA with GCU anticodon from mosquito mitochondria. J Mol Biol. 1984 Jun 25;176(2):251–260. doi: 10.1016/0022-2836(84)90423-6. [DOI] [PubMed] [Google Scholar]
  23. Dubin D. T., HsuChen C. C. Sequence and structure of a methionine transfer RNA from mosquito mitochondria. Nucleic Acids Res. 1984 May 25;12(10):4185–4189. doi: 10.1093/nar/12.10.4185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Dubin D. T., Montoya J., Timko K. D., Attardi G. Sequence analysis and precise mapping of the 3' ends of HeLa cell mitochondrial ribosomal RNAs. J Mol Biol. 1982 May 5;157(1):1–19. doi: 10.1016/0022-2836(82)90510-1. [DOI] [PubMed] [Google Scholar]
  25. Elliott D. J., Jacobs H. T. Mutually exclusive synthetic pathways for sea urchin mitochondrial rRNA and mRNA. Mol Cell Biol. 1989 Mar;9(3):1069–1082. doi: 10.1128/mcb.9.3.1069. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Gadaleta G., Pepe G., De Candia G., Quagliariello C., Sbisà E., Saccone C. The complete nucleotide sequence of the Rattus norvegicus mitochondrial genome: cryptic signals revealed by comparative analysis between vertebrates. J Mol Evol. 1989 Jun;28(6):497–516. doi: 10.1007/BF02602930. [DOI] [PubMed] [Google Scholar]
  27. Gray M. W., Sankoff D., 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. Nucleic Acids Res. 1984 Jul 25;12(14):5837–5852. doi: 10.1093/nar/12.14.5837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Gutell R. R., Weiser B., Woese C. R., Noller H. F. Comparative anatomy of 16-S-like ribosomal RNA. Prog Nucleic Acid Res Mol Biol. 1985;32:155–216. doi: 10.1016/s0079-6603(08)60348-7. [DOI] [PubMed] [Google Scholar]
  29. Haucke H. R., Gellissen G. Different mitochondrial gene orders among insects: exchanged tRNA gene positions in the COII/COIII region between an orthopteran and a dipteran species. Curr Genet. 1988 Nov;14(5):471–476. doi: 10.1007/BF00521271. [DOI] [PubMed] [Google Scholar]
  30. Henikoff S. Unidirectional digestion with exonuclease III in DNA sequence analysis. Methods Enzymol. 1987;155:156–165. doi: 10.1016/0076-6879(87)55014-5. [DOI] [PubMed] [Google Scholar]
  31. Himeno H., Masaki H., Kawai T., Ohta T., Kumagai I., Miura K., Watanabe K. Unusual genetic codes and a novel gene structure for tRNA(AGYSer) in starfish mitochondrial DNA. Gene. 1987;56(2-3):219–230. doi: 10.1016/0378-1119(87)90139-9. [DOI] [PubMed] [Google Scholar]
  32. Hoffmann R. J., Boore J. L., Brown W. M. A novel mitochondrial genome organization for the blue mussel, Mytilus edulis. Genetics. 1992 Jun;131(2):397–412. doi: 10.1093/genetics/131.2.397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. HsuChen C. C., Cleaves G. R., Dubin D. T. A major lysine tRNA with a CUU anticodon in insect mitochondria. Nucleic Acids Res. 1983 Dec 20;11(24):8659–8662. doi: 10.1093/nar/11.24.8659. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Jacobs H. T., Asakawa S., Araki T., Miura K., Smith M. J., Watanabe K. Conserved tRNA gene cluster in starfish mitochondrial DNA. Curr Genet. 1989 Mar;15(3):193–206. doi: 10.1007/BF00435506. [DOI] [PubMed] [Google Scholar]
  35. Jacobs H. T. Do ribosomes regulate mitochondrial RNA synthesis? Bioessays. 1989 Jul;11(1):27–34. doi: 10.1002/bies.950110108. [DOI] [PubMed] [Google Scholar]
  36. Jacobs H. T., Elliott D. J., Math V. B., Farquharson A. Nucleotide sequence and gene organization of sea urchin mitochondrial DNA. J Mol Biol. 1988 Jul 20;202(2):185–217. doi: 10.1016/0022-2836(88)90452-4. [DOI] [PubMed] [Google Scholar]
  37. Janke A., Päbo S. Editing of a tRNA anticodon in marsupial mitochondria changes its codon recognition. Nucleic Acids Res. 1993 Apr 11;21(7):1523–1525. doi: 10.1093/nar/21.7.1523. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Jukes T. H., Osawa S. The genetic code in mitochondria and chloroplasts. Experientia. 1990 Dec 1;46(11-12):1117–1126. doi: 10.1007/BF01936921. [DOI] [PubMed] [Google Scholar]
  39. Kim S. H., Sussman J. L. pi turn is a conformational pattern in RNA loops and bends. Nature. 1976 Apr 15;260(5552):645–646. doi: 10.1038/260645a0. [DOI] [PubMed] [Google Scholar]
  40. Kumazawa Y., Yokogawa T., Hasegawa E., Miura K., Watanabe K. The aminoacylation of structurally variant phenylalanine tRNAs from mitochondria and various nonmitochondrial sources by bovine mitochondrial phenylalanyl-tRNA synthetase. J Biol Chem. 1989 Aug 5;264(22):13005–13011. [PubMed] [Google Scholar]
  41. Messing J. New M13 vectors for cloning. Methods Enzymol. 1983;101:20–78. doi: 10.1016/0076-6879(83)01005-8. [DOI] [PubMed] [Google Scholar]
  42. Montoya J., Gaines G. L., Attardi G. The pattern of transcription of the human mitochondrial rRNA genes reveals two overlapping transcription units. Cell. 1983 Aug;34(1):151–159. doi: 10.1016/0092-8674(83)90145-9. [DOI] [PubMed] [Google Scholar]
  43. Montoya J., Ojala D., Attardi G. Distinctive features of the 5'-terminal sequences of the human mitochondrial mRNAs. Nature. 1981 Apr 9;290(5806):465–470. doi: 10.1038/290465a0. [DOI] [PubMed] [Google Scholar]
  44. Moritz C., Brown W. M. Tandem duplication of D-loop and ribosomal RNA sequences in lizard mitochondrial DNA. Science. 1986 Sep 26;233(4771):1425–1427. doi: 10.1126/science.3018925. [DOI] [PubMed] [Google Scholar]
  45. Moritz C., Brown W. M. Tandem duplications in animal mitochondrial DNAs: variation in incidence and gene content among lizards. Proc Natl Acad Sci U S A. 1987 Oct;84(20):7183–7187. doi: 10.1073/pnas.84.20.7183. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Muramatsu T., Yokoyama S., Horie N., Matsuda A., Ueda T., Yamaizumi Z., Kuchino Y., Nishimura S., Miyazawa T. A novel lysine-substituted nucleoside in the first position of the anticodon of minor isoleucine tRNA from Escherichia coli. J Biol Chem. 1988 Jul 5;263(19):9261–9267. doi: 10.1351/pac198961030573. [DOI] [PubMed] [Google Scholar]
  47. Murgola E. J. Suppression and the code: beyond codons and anticodons. Experientia. 1990 Dec 1;46(11-12):1134–1141. doi: 10.1007/BF01936923. [DOI] [PubMed] [Google Scholar]
  48. Okimoto R., Macfarlane J. L., Clary D. O., Wolstenholme D. R. The mitochondrial genomes of two nematodes, Caenorhabditis elegans and Ascaris suum. Genetics. 1992 Mar;130(3):471–498. doi: 10.1093/genetics/130.3.471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Okimoto R., Macfarlane J. L., Wolstenholme D. R. Evidence for the frequent use of TTG as the translation initiation codon of mitochondrial protein genes in the nematodes, Ascaris suum and Caenorhabditis elegans. Nucleic Acids Res. 1990 Oct 25;18(20):6113–6118. doi: 10.1093/nar/18.20.6113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Okimoto R., Wolstenholme D. R. A set of tRNAs that lack either the T psi C arm or the dihydrouridine arm: towards a minimal tRNA adaptor. EMBO J. 1990 Oct;9(10):3405–3411. doi: 10.1002/j.1460-2075.1990.tb07542.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Osawa S., Jukes T. H. Codon reassignment (codon capture) in evolution. J Mol Evol. 1989 Apr;28(4):271–278. doi: 10.1007/BF02103422. [DOI] [PubMed] [Google Scholar]
  52. Pont-Kingdon G. A., Beagley C. T., Okimoto R., Wolstenholme D. R. Mitochondrial DNA of the sea anemone, Metridium senile (Cnidaria): prokaryote-like genes for tRNA(f-Met) and small-subunit ribosomal RNA, and standard genetic code specificities for AGR and ATA codons. J Mol Evol. 1994 Oct;39(4):387–399. doi: 10.1007/BF00160271. [DOI] [PubMed] [Google Scholar]
  53. Päbo S., Thomas W. K., Whitfield K. M., Kumazawa Y., Wilson A. C. Rearrangements of mitochondrial transfer RNA genes in marsupials. J Mol Evol. 1991 Nov;33(5):426–430. doi: 10.1007/BF02103134. [DOI] [PubMed] [Google Scholar]
  54. Qureshi S. A., Jacobs H. T. Characterization of a high-affinity binding site for a DNA-binding protein from sea urchin embryo mitochondria. Nucleic Acids Res. 1993 Feb 25;21(4):811–816. doi: 10.1093/nar/21.4.811. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Ramón Valverde J., Batuecas B., Moratilla C., Marco R., Garesse R. The complete mitochondrial DNA sequence of the crustacean Artemia franciscana. J Mol Evol. 1994 Oct;39(4):400–408. doi: 10.1007/BF00160272. [DOI] [PubMed] [Google Scholar]
  56. Roberti M., Mustich A., Gadaleta M. N., Cantatore P. Identification of two homologous mitochondrial DNA sequences, which bind strongly and specifically to a mitochondrial protein of Paracentrotus lividus. Nucleic Acids Res. 1991 Nov 25;19(22):6249–6254. doi: 10.1093/nar/19.22.6249. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Roe B. A., Ma D. P., Wilson R. K., Wong J. F. The complete nucleotide sequence of the Xenopus laevis mitochondrial genome. J Biol Chem. 1985 Aug 15;260(17):9759–9774. [PubMed] [Google Scholar]
  58. Roels H., Sarhan M. J., Hanotiau I., de Fays M., Genet P., Bernard A., Buchet J. P., Lauwerys R. Preclinical toxic effects of manganese in workers from a Mn salts and oxides producing plant. Sci Total Environ. 1985 Mar 15;42(1-2):201–206. doi: 10.1016/0048-9697(85)90022-1. [DOI] [PubMed] [Google Scholar]
  59. Saiki R. K., Gelfand D. H., Stoffel S., Scharf S. J., Higuchi R., Horn G. T., Mullis K. B., Erlich H. A. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science. 1988 Jan 29;239(4839):487–491. doi: 10.1126/science.2448875. [DOI] [PubMed] [Google Scholar]
  60. Shibutani S., Takeshita M., Grollman A. P. Insertion of specific bases during DNA synthesis past the oxidation-damaged base 8-oxodG. Nature. 1991 Jan 31;349(6308):431–434. doi: 10.1038/349431a0. [DOI] [PubMed] [Google Scholar]
  61. Silverman S., Heckman J., Cowling G. J., Delaney A. D., Dunn R. J., Gillam I. C., Tener G. M., Söll D., RajBhandary U. L. The nucleotide sequence of the initiator tRNA from Drosophila melanogaster. Nucleic Acids Res. 1979 Feb;6(2):421–433. doi: 10.1093/nar/6.2.421. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Smith M. J., Arndt A., Gorski S., Fajber E. The phylogeny of echinoderm classes based on mitochondrial gene arrangements. J Mol Evol. 1993 Jun;36(6):545–554. doi: 10.1007/BF00556359. [DOI] [PubMed] [Google Scholar]
  63. Smith M. J., Banfield D. K., Doteval K., Gorski S., Kowbel D. J. Gene arrangement in sea star mitochondrial DNA demonstrates a major inversion event during echinoderm evolution. Gene. 1989 Mar 15;76(1):181–185. doi: 10.1016/0378-1119(89)90022-x. [DOI] [PubMed] [Google Scholar]
  64. Sundaralingam M., Mizuno H., Stout C. D., Rao S. T., Liedman M., Yathindra N. Mechanisms of chain folding in nucleic acids. The (omega, omega) plot and its correlation to the nucleotide geometry in yeast tRNAPhe1. Nucleic Acids Res. 1976 Oct;3(10):2471–2484. doi: 10.1093/nar/3.10.2471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Suzuki T., Ueda T., Ohama T., Osawa S., Watanabe K. The gene for serine tRNA having anticodon sequence CAG in a pathogenic yeast, Candida albicans. Nucleic Acids Res. 1993 Jan 25;21(2):356–356. doi: 10.1093/nar/21.2.356. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Tzeng C. S., Hui C. F., Shen S. C., Huang P. C. The complete nucleotide sequence of the Crossostoma lacustre mitochondrial genome: conservation and variations among vertebrates. Nucleic Acids Res. 1992 Sep 25;20(18):4853–4858. doi: 10.1093/nar/20.18.4853. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Ueda T., Ohta T., Watanabe K. Large scale isolation and some properties of AGY-specific serine tRNA from bovine heart mitochondria. J Biochem. 1985 Nov;98(5):1275–1284. doi: 10.1093/oxfordjournals.jbchem.a135394. [DOI] [PubMed] [Google Scholar]
  68. Wakita K., Watanabe Y., Yokogawa T., Kumazawa Y., Nakamura S., Ueda T., Watanabe K., Nishikawa K. Higher-order structure of bovine mitochondrial tRNA(Phe) lacking the 'conserved' GG and T psi CG sequences as inferred by enzymatic and chemical probing. Nucleic Acids Res. 1994 Feb 11;22(3):347–353. doi: 10.1093/nar/22.3.347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Wolstenholme D. R. Animal mitochondrial DNA: structure and evolution. Int Rev Cytol. 1992;141:173–216. doi: 10.1016/s0074-7696(08)62066-5. [DOI] [PubMed] [Google Scholar]
  70. Wolstenholme D. R., Macfarlane J. L., Okimoto R., Clary D. O., Wahleithner J. A. Bizarre tRNAs inferred from DNA sequences of mitochondrial genomes of nematode worms. Proc Natl Acad Sci U S A. 1987 Mar;84(5):1324–1328. doi: 10.1073/pnas.84.5.1324. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Woo N. H., Roe B. A., Rich A. Three-dimensional structure of Escherichia coli initiator tRNAfMet. Nature. 1980 Jul 24;286(5771):346–351. doi: 10.1038/286346a0. [DOI] [PubMed] [Google Scholar]
  72. Yanisch-Perron C., Vieira J., Messing J. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene. 1985;33(1):103–119. doi: 10.1016/0378-1119(85)90120-9. [DOI] [PubMed] [Google Scholar]
  73. Yarus M., Cline S. W., Wier P., Breeden L., Thompson R. C. Actions of the anticodon arm in translation on the phenotypes of RNA mutants. J Mol Biol. 1986 Nov 20;192(2):235–255. doi: 10.1016/0022-2836(86)90362-1. [DOI] [PubMed] [Google Scholar]
  74. Yarus M. Translational efficiency of transfer RNA's: uses of an extended anticodon. Science. 1982 Nov 12;218(4573):646–652. doi: 10.1126/science.6753149. [DOI] [PubMed] [Google Scholar]
  75. Yokogawa T., Kumazawa Y., Miura K., Watanabe K. Purification and characterization of two serine isoacceptor tRNAs from bovine mitochondria by using a hybridization assay method. Nucleic Acids Res. 1989 Apr 11;17(7):2623–2638. doi: 10.1093/nar/17.7.2623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Yokogawa T., Suzuki T., Ueda T., Mori M., Ohama T., Kuchino Y., Yoshinari S., Motoki I., Nishikawa K., Osawa S. Serine tRNA complementary to the nonuniversal serine codon CUG in Candida cylindracea: evolutionary implications. Proc Natl Acad Sci U S A. 1992 Aug 15;89(16):7408–7411. doi: 10.1073/pnas.89.16.7408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Yokogawa T., Watanabe Y., Kumazawa Y., Ueda T., Hirao I., Miura K., Watanabe K. A novel cloverleaf structure found in mammalian mitochondrial tRNA(Ser) (UCN). Nucleic Acids Res. 1991 Nov 25;19(22):6101–6105. doi: 10.1093/nar/19.22.6101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Yoneyama Y. [The nucleotide sequences of the heavy and light strand replication origins of the Rana catesbeiana mitochondrial genome]. Nihon Ika Daigaku Zasshi. 1987 Aug;54(4):429–440. doi: 10.1272/jnms1923.54.429. [DOI] [PubMed] [Google Scholar]
  79. Zwieb C., Glotz C., Brimacombe R. Secondary structure comparisons between small subunit ribosomal RNA molecules from six different species. Nucleic Acids Res. 1981 Aug 11;9(15):3621–3640. doi: 10.1093/nar/9.15.3621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. de Bruijn M. H. Drosophila melanogaster mitochondrial DNA, a novel organization and genetic code. Nature. 1983 Jul 21;304(5923):234–241. doi: 10.1038/304234a0. [DOI] [PubMed] [Google Scholar]
  81. de Bruijn M. H., Klug A. A model for the tertiary structure of mammalian mitochondrial transfer RNAs lacking the entire 'dihydrouridine' loop and stem. EMBO J. 1983;2(8):1309–1321. doi: 10.1002/j.1460-2075.1983.tb01586.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. de Bruijn M. H., Schreier P. H., Eperon I. C., Barrell B. G., Chen E. Y., Armstrong P. W., Wong J. F., Roe B. A. A mammalian mitochondrial serine transfer RNA lacking the "dihydrouridine" loop and stem. Nucleic Acids Res. 1980 Nov 25;8(22):5213–5222. doi: 10.1093/nar/8.22.5213. [DOI] [PMC free article] [PubMed] [Google Scholar]

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