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Mitochondrial DNA of the sea anemone, Metridium senile (Cnidaria): Prokaryote-like genes for tRNAf-Met and small-subunit ribosomal RNA, and standard genetic code specificities for AGR and ATA codons

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Abstract

The nucleotide sequence of a segment of the mitochondrial DNA (mtDNA) molecule of the sea anemone Metridium senile (phylum Cnidaria, class Anthozoa, order Actiniaria) has been determined, within which have been identified the genes for respiratory chain NADH dehydrogenase subunit 2 (ND2), the small-subunit rRNA (s-rRNA), cytochrome c oxidase subunit II(COII), ND4, ND6, cytochrome b (Cyt b), tRNAf-Met, and the large-subunit rRNA (1-rRNA). The eight genes are arranged in the order given and are all transcribed from the same strand of the molecule. The overall order of the M. senile mt-genes differs from that of other metazoan mtDNAs. In M. senile mt-protein genes, AGA and AGG codons appear to have the standard genetic code specification of arginine, rather than serine as found for other invertebrate mt-genetic codes. Also, ATA has the standard genetic code specification of isoleucine. TGA occurs in three M. senile mt-protein genes and may specify tryptophan as in other metazoan, protozoan, and some fungal mt-genetic codes. The M. senile mt-rRNAf-Met gene has primary and secondary structure features closely resembling those of the Escherichia coli initiator tRNA, including standard dihydrouridine and TΨC loop sequences and a mismatch pair at the top of the aminoacyl stem. Determinations of the 5′ and 3′ end nucleotides of the M. senile mt-srRNAs indicated that these molecules have a homogenous size of 1,081 ntp, larger than any other known metazoan mt-s-rRNAs. Consistent with its larger size, the M. senile mt-s-rRNA can be folded into a secondary structure that more closely resembles that of the E. coli 16S rRNA than can any other metazoan mt-s-rRNA. These findings concerning M. senile mtDNA indicate that most of the unusual features regarding metazoan mt-genetic codes, rRNAs, and probably tRNAs developed after divergence of the Cnidarian line from the ancestral line common to other metazoa.

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References

  • 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 290:457–465

    Google Scholar 

  • Anderson S, de Bruijn MHL, Coulson AR, Eperon IC, Sanger F, Young IG (1982) The complete sequence of bovine mitochondrial DNA: conserved features of the mammalian mitochondrial genome. J Mol Biol 156:683–717

    Google Scholar 

  • Arnason U, Gulberg A, Widegren B (1991) The complete nucleotide sequence of the mitochondrial DNA of the fin whale, Balaenoptera physalus. J Mol Evol 55:231–249

    Google Scholar 

  • Arnason U, Johansson E (1992) The complete mitochondrial DNA sequence of the harbor seal, Phoca viluina. J Mol Evol 34:493–505

    Google Scholar 

  • Asakawa S, Kumazawa Y, Araki T, Himeno H, Miura K, Watanabe K (1991) Strand-specific nucleotide composition bias in echinoderm and vertebrate mitochondrial genomes. J Mol Evol 32:511–520

    Google Scholar 

  • Berk AJ, Sharp PA (1977) Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease digested hybrids. Cell 12:721–732

    Google Scholar 

  • Bessho Y, Ohama T, Osawa S (1992) Planarian mitochondria II. The unique genetic code as deduced from cytochrome c oxidase subunit I gene sequences. J Mol Evol 34:331–335

    Google Scholar 

  • Bibb MJ, van Etten RA, Wright CT, Walberg MW, Clayton DA (1981) Sequence and gene organization of mouse mitochondrial DNA. Cell 26:167–180

    Google Scholar 

  • Bridges D, Cunningham CW, Schierwater B, DeSalle R, Buss LW (1992) Class level relationships in the phylum Cnidaria: evidence from mitochondrial genome structure. Proc Natl Acad Sci USA 89:8750–8753

    Google Scholar 

  • Cantatore P, Roberti M, Rainaldi G, Gadaleta MN, Saccone C (1989) The complete nucleotide sequence, gene organization, and genetic code of the mitochondrial genome of Paracentrotus lividus. J Biol Chem 264:10965–10975

    Google Scholar 

  • Chomyn A, Attardi G (1987) Mitochondrial gene products. Curr Top Bioenergetics 15:295–329

    Google Scholar 

  • Clary DO, Wolstenholme DR (1985a) The mitochondrial DNA molecule of Drosophila yakuba: nucleotide sequence, gene organization, and genetic code. J Mol Evol 22:252–271

    Google Scholar 

  • Clary DO, Wolstenholme DR (1985b) The ribosomal RNA genes of Drosophila mitochondrial DNA. Nucleic Acids Res 13:4029–4045

    Google Scholar 

  • Crozier RH, Crozier YC (1993) The mitochondrial genome of the honey bee Apis melifera: complete sequence and genome organization. Genetics 133:97–117

    Google Scholar 

  • Dahlberg AE (1989) The functional role of ribosomal RNA in protein synthesis. Cell 57:525–529

    Google Scholar 

  • Dale RMK, McClure B, Houchins JP (1985) A rapid single-stranded cloning strategy for producing overlapping clones for use in DNA sequencing: application to sequencing the corn mitochondrial 18S rDNA. Plasmid 13:31–40

    Google Scholar 

  • Dams E, Henricks L, Van der Peer Y, Neef JM, Smits G, Vandenbempt I, Wachter R-De (1988) Compilation of small ribosomal subunit RNA sequences. Nucleic Acids Res 16:r87-r173

    Google Scholar 

  • Desjardins P, Morais R (1991) Sequence and organization of the chicken mitochondrial genome. A novel gene order in higher vertebrates. J Mol Evol 32:153–161

    Google Scholar 

  • Dirheimer G, Keith G, Sibler A-P, Martin RP (1979) The primary structure of tRNAs and their rare nucleosides. In: Schimmel PR, Soll D, Abelson JN (eds) Transfer RNA: structure, properties and recognition. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, pp 19–41

    Google Scholar 

  • Frohman MA (1990) RACE: rapid amplification of cDNA ends. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols, a guide to methods and applications. Academic Press Inc, San Diego, pp 28–38

    Google Scholar 

  • Gadaleta G, Pepe G, DeCandia G, Quagliariello C, Sbisa E, Saccone C (1989) The complete nucleotide sequence of the Rattus norvegicus mitochondrial genome: cryptic signals revealed by comparative analysis between vertebrates. J Mol Evol 28:497–516

    Google Scholar 

  • Garey JR, Wolstenholme DR (1989) Platyhelminth mitochondrial DNA: Evidence for early evolutionary origin of a tRNAser(AGN) that contains a dihydrouridine arm replacement-loop, and of serine-specifying AGA and AGG Codons. J Mol Evol 28:374–387

    Google Scholar 

  • Gutell RR, Weiser B, Woese CR, Noller HF (1985) Comparative anatomy of 16S-like ribosomal RNA. Prog Nucleic Acids Res Mol Biol 32:155–216

    Google Scholar 

  • Himeno H, Masaki H, Kawai T, Ohta T, Kumagi I, Miura I, Watanabe K (1987) Unusual genetic codes and a novel gene structure for tRNAserAGY in starfish mitochondrial DNA. Gene 56:219–230

    Google Scholar 

  • Hoffmann RJ, Boore JL, Brown WM (1992) A novel mitochondrial genome organization for the blue mussel, Mytilus edulis. Genetics 131:397–412

    Google Scholar 

  • Hong GF (1982) A systematic DNA sequencing strategy. J Mol Biol 158:539–549

    Google Scholar 

  • Jacobs HT, Elliot DJ, Math VB, Farquharson A (1988) Nucleotide sequence and gene organization of sea urchin mitochondrial DNA. J Mol Biol 202:185–217

    Google Scholar 

  • Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:333–348

    Google Scholar 

  • McCabe PC (1990) Production of single-stranded DNA by assymetric PCR. In: Innis MA, Gefland DH, Sninsky JJ, White TJ (eds) PCR protocols, a guide to methods and applications. Academic Press, San Diego, pp 28–38

    Google Scholar 

  • Noller HF, Asire M, Barta A, Douthwaite S, Goldstein T, Gutell RR, Moazed D, Normanley J, Prince JB, Stern S, Triman K, Turner S, Van Stolk B, Wheaton V, Weiser B, Woese CR (1986) Studies on the structure and function of ribosomal RNAs. In Hardesty B, Kramer G (eds) Structure, function and genetics of ribosomes. Springer Series in Molecular Biology (ed: Rich A) Springer-Verlag, NY, pp 141–163

    Google Scholar 

  • Ohama T, Osawa S, Watanabe K, Jukes TH (1990) Evolution of the mitochondrial genetic code IV. AAA as an asparagine codon in some animal mitochondria. J Mol Evol 30:329–332

    Google Scholar 

  • Ojala D, Montoya J, Attardi G (1981) tRNA punctuation model of RNA processing in human mitochondria. Nature 290:470–474

    Google Scholar 

  • Okimoto R, Macfarlane JL, Wolstenholme DR (1990) 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 18:6113–6118

    Google Scholar 

  • Okimoto R, Macfarlane JL, Wolstenholme DR (1992) The mitochondrial genomes of two nematodes, Caenorhabditis elegans and Ascaris suum. Genetics 130:471–498

    Google Scholar 

  • Okimoto R, Wolstenholme DR (1990) A set of tRNAs that lack either the TΨC arm or the dihydrouridine arm: towards a minimal tRNA adaptor. EMBO J 9:3405–3411

    Google Scholar 

  • Osawa S, Jukes TH, Watanabe K, Muto A (1992) Recent evidence for evolution of the genetic code. Microbiol Rev 56:229–264

    Google Scholar 

  • Rich A, RajBhandary UL (1976) Transfer RNA: molecular structure, sequence and properties. Ann Rev Biochem 45:805–860

    Google Scholar 

  • Roe BA, Ma DP, Wilson RK, Wong JF-H (1985) The complete nucleotide sequence of the Xenopus laevis mitochondrial genome. J Biol Chem 260:9759–9774

    Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, second edition. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY

    Google Scholar 

  • Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467

    Google Scholar 

  • Shine J, Dalgamo L (1974) The 3′-terminal sequence of Escherichia coli 16S ribosomal RNA: complementary to nonsense triplets and ribosome binding sites. Proc Natl Acad Sci USA 71:1342–1346

    Google Scholar 

  • Singhal RP, Fallis PAM (1979) Structure, function, and evolution of transfer RNAs. Prog Nucleic Acids Res Mol Biol 23:227–290

    Google Scholar 

  • Sprinzl M, Hartmann T, Weber J, Blank J, Zeidler R (1989) Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res 17:(Suppl)r1-r72

    Google Scholar 

  • Tzeng C-S, Hui C-F, Shen S-C, Huang PC (1992) The complete nucleotide sequence of the Crossostoma lacustre mitochondrial genome: conservation and variations among vertebrates. Nucleic Acids Res 20:4853–4858

    Google Scholar 

  • Van Etten RA, Michael NL, Bibb MJ, Brennicke A, Clayton DA (1982) Expression of the mouse mitochondrial DNA genome. In: P Slonimski, P Borst, G Attardi (eds) Mitochondrial genes. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, pp 73–88

    Google Scholar 

  • Wahleithner JA, Wolstenholme DR (1987) Mitochondrial plasmid DNAs of broad bean: nucleotide sequences, complex secondary structures, and transcription. Curr Genet 12:55–67

    Google Scholar 

  • Warrior R, Gall J (1985) The mitochondrial DNA of Hydra attenuata and Hydra littoralis consists of two linear molecules. Arch. Sc. Geneve 38:439–445

    Google Scholar 

  • Wolstenholme DR (1992a) Animal mitochondrial DNA: structure and evolution. In: Wolstenholme DR, Jeon KW (eds) Mitochondrial genomes. International review of cytology, vol 141. Academic Press, New York, pp 173–216

    Google Scholar 

  • Wolstenholme DR (1992b) Genetic novelties in mitochondrial genomes of multicellular animals. Curr Opin Genet Dev 2:918–925

    Google Scholar 

  • Wolstenholme DR, Fauron CMR (1976) A partial map of the circular mitochondrial genome of Drosophila melanogaster: location of EcoRI-sensitive sites and the adenine-thymine-rich region. J Cell Biol 71:434–448

    Google Scholar 

  • 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 84:1324–1328

    Google Scholar 

  • Wolstenholme DR, Okomoto R, Macfarlane JL, Pont GA, Chamberlin HM, Garey JR, Okada NA (1989) Unusual features of lower invertebrate mitochondrial genomes. In: Quaglieriello E, Papa S, Palmieri F, Saccone C (eds) Structure, function and biogenesis of energy transfer systems. Elsevier Science Publishers B.V., Amsterdam, pp 103–106

    Google Scholar 

  • Yokobori S, Ueda T, Watanabe K (1993) Codons AGA and AGG are read as glycine in ascidian mitochondria. J Mol Evol 36:1–8

    Google Scholar 

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Correspondence to: D.R. Wolstenholme

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Pont-Kingdon, G.A., Beagley, C.T., Okimoto, R. et al. Mitochondrial DNA of the sea anemone, Metridium senile (Cnidaria): Prokaryote-like genes for tRNAf-Met and small-subunit ribosomal RNA, and standard genetic code specificities for AGR and ATA codons. J Mol Evol 39, 387–399 (1994). https://doi.org/10.1007/BF00160271

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