Skip to main content
PMC home page
Genetics logoLink to Genetics
. 1999 Jun;152(2):641–652. doi: 10.1093/genetics/152.2.641

Mytilus mitochondrial DNA contains a functional gene for a tRNASer(UCN) with a dihydrouridine arm-replacement loop and a pseudo-tRNASer(UCN) gene.

C T Beagley 1, R Okimoto 1, D R Wolstenholme 1
PMCID: PMC1460622  PMID: 10353906

Abstract

A 2500-nucleotide pair (ntp) sequence of F-type mitochondrial (mt) DNA of the Pacific Rim mussel Mytilus californianus (class Bivalvia, phylum Mollusca) that contains two complete (ND2 and ND3) and two partial (COI and COIII) protein genes and nine tRNA genes is presented. Seven of the encoded tRNAs (Ala, Arg, His, Met(AUA), Pro, Ser(UCN), and Trp) have the potential to fold into the orthodox four-armed tRNA secondary structure, while two [tRNASer(AGN) and a second tRNASer(UCN)] will fold only into tRNAs with a dihydrouridine (DHU) arm-replacement loop. Comparison of these mt-tRNA gene sequences with previously published, corresponding M. edulis F-type mtDNA indicates that similarity between the four-armed tRNASer(UCN) genes is only 63.8% compared with an average of 92.1% (range 86.2-98. 5%) for the remaining eight tRNA genes. Northern blot analysis indicated that mature tRNAs encoded by the DHU arm-replacement loop-containing tRNASer(UCN), tRNASer(AGN), tRNAMet(AUA), tRNATrp, and tRNAPro genes occur in M. californianus mitochondria, strengthening the view that all of these genes are functional. However, Northern blot and 5' RACE (rapid amplification of cDNA ends) analyses indicated that the four-armed tRNASer(UCN) gene is transcribed into a stable RNA that includes the downstream COI sequence and is not processed into a mature tRNA. On the basis of these observations the M. californianus and M. edulis four-armed tRNASer(UCN) sequences are interpreted as pseudo-tRNASer(UCN) genes.

Full Text

The Full Text of this article is available as a PDF (366.9 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Arnason U., Xu X., Gullberg A. Comparison between the complete mitochondrial DNA sequences of Homo and the common chimpanzee based on nonchimeric sequences. J Mol Evol. 1996 Feb;42(2):145–152. doi: 10.1007/BF02198840. [DOI] [PubMed] [Google Scholar]
  2. Asakawa S., Himeno H., Miura K., Watanabe K. Nucleotide sequence and gene organization of the starfish Asterina pectinifera mitochondrial genome. Genetics. 1995 Jul;140(3):1047–1060. doi: 10.1093/genetics/140.3.1047. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Beagley C. T., Okada N. A., Wolstenholme D. R. Two mitochondrial group I introns in a metazoan, the sea anemone Metridium senile: one intron contains genes for subunits 1 and 3 of NADH dehydrogenase. Proc Natl Acad Sci U S A. 1996 May 28;93(11):5619–5623. doi: 10.1073/pnas.93.11.5619. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Beagley C. T., Okimoto R., Wolstenholme D. R. The mitochondrial genome of the sea anemone Metridium senile (Cnidaria): introns, a paucity of tRNA genes, and a near-standard genetic code. Genetics. 1998 Mar;148(3):1091–1108. doi: 10.1093/genetics/148.3.1091. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Beagley C. T., Taylor K. A., Wolstenholme D. R. Gender-associated diverse mitochondrial DNA molecules of the mussel Mytilus californianus. Curr Genet. 1997 Apr;31(4):318–324. doi: 10.1007/s002940050211. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. Boore J. L., Brown W. M. Complete DNA sequence of the mitochondrial genome of the black chiton, Katharina tunicata. Genetics. 1994 Oct;138(2):423–443. doi: 10.1093/genetics/138.2.423. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Boore J. L., Brown W. M. Complete sequence of the mitochondrial DNA of the annelid worm Lumbricus terrestris. Genetics. 1995 Sep;141(1):305–319. doi: 10.1093/genetics/141.1.305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Brown G. G., Simpson M. V. Novel features of animal mtDNA evolution as shown by sequences of two rat cytochrome oxidase subunit II genes. Proc Natl Acad Sci U S A. 1982 May;79(10):3246–3250. doi: 10.1073/pnas.79.10.3246. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. 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]
  12. Clary D. O., Goddard J. M., Martin S. C., Fauron C. M., Wolstenholme D. R. Drosophila mitochondrial DNA: a novel gene order. Nucleic Acids Res. 1982 Nov 11;10(21):6619–6637. doi: 10.1093/nar/10.21.6619. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. 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]
  14. Clayton D. A. Replication of animal mitochondrial DNA. Cell. 1982 Apr;28(4):693–705. doi: 10.1016/0092-8674(82)90049-6. [DOI] [PubMed] [Google Scholar]
  15. Clayton D. A. Transcription and replication of animal mitochondrial DNAs. Int Rev Cytol. 1992;141:217–232. doi: 10.1016/s0074-7696(08)62067-7. [DOI] [PubMed] [Google Scholar]
  16. Dale R. M., McClure B. A., Houchins J. P. A rapid single-stranded cloning strategy for producing a sequential series of overlapping clones for use in DNA sequencing: application to sequencing the corn mitochondrial 18 S rDNA. Plasmid. 1985 Jan;13(1):31–40. doi: 10.1016/0147-619x(85)90053-8. [DOI] [PubMed] [Google Scholar]
  17. DeSalle R., Freedman T., Prager E. M., Wilson A. C. Tempo and mode of sequence evolution in mitochondrial DNA of Hawaiian Drosophila. J Mol Evol. 1987;26(1-2):157–164. doi: 10.1007/BF02111289. [DOI] [PubMed] [Google Scholar]
  18. Freier S. M., Kierzek R., Jaeger J. A., Sugimoto N., Caruthers M. H., Neilson T., Turner D. H. Improved free-energy parameters for predictions of RNA duplex stability. Proc Natl Acad Sci U S A. 1986 Dec;83(24):9373–9377. doi: 10.1073/pnas.83.24.9373. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Garey J. R., Wolstenholme D. R. Platyhelminth mitochondrial DNA: evidence for early evolutionary origin of a tRNA(serAGN) that contains a dihydrouridine arm replacement loop, and of serine-specifying AGA and AGG codons. J Mol Evol. 1989 May;28(5):374–387. doi: 10.1007/BF02603072. [DOI] [PubMed] [Google Scholar]
  20. Hatzoglou E., Rodakis G. C., Lecanidou R. Complete sequence and gene organization of the mitochondrial genome of the land snail Albinaria coerulea. Genetics. 1995 Aug;140(4):1353–1366. doi: 10.1093/genetics/140.4.1353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Hyman B. C., Beck J. L., Weiss K. C. Sequence amplification and gene rearrangement in parasitic nematode mitochondrial DNA. Genetics. 1988 Nov;120(3):707–712. doi: 10.1093/genetics/120.3.707. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]
  24. Krettek A., Gullberg A., Arnason U. Sequence analysis of the complete mitochondrial DNA molecule of the hedgehog, Erinaceus europaeus, and the phylogenetic position of the Lipotyphla. J Mol Evol. 1995 Dec;41(6):952–957. doi: 10.1007/BF00173175. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. 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]
  27. 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]
  28. Moritz C. Evolutionary dynamics of mitochondrial DNA duplications in parthenogenetic geckos, Heteronotia binoei. Genetics. 1991 Sep;129(1):221–230. doi: 10.1093/genetics/129.1.221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Ojala D., Montoya J., Attardi G. tRNA punctuation model of RNA processing in human mitochondria. Nature. 1981 Apr 9;290(5806):470–474. doi: 10.1038/290470a0. [DOI] [PubMed] [Google Scholar]
  30. Okimoto R., Chamberlin H. M., Macfarlane J. L., Wolstenholme D. R. Repeated sequence sets in mitochondrial DNA molecules of root knot nematodes (Meloidogyne): nucleotide sequences, genome location and potential for host-race identification. Nucleic Acids Res. 1991 Apr 11;19(7):1619–1626. doi: 10.1093/nar/19.7.1619. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. 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]
  32. 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]
  33. 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]
  34. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Shadel G. S., Clayton D. A. Mitochondrial DNA maintenance in vertebrates. Annu Rev Biochem. 1997;66:409–435. doi: 10.1146/annurev.biochem.66.1.409. [DOI] [PubMed] [Google Scholar]
  36. Skibinski D. O., Gallagher C., Beynon C. M. Sex-limited mitochondrial DNA transmission in the marine mussel Mytilus edulis. Genetics. 1994 Nov;138(3):801–809. doi: 10.1093/genetics/138.3.801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Terrett J. A., Miles S., Thomas R. H. Complete DNA sequence of the mitochondrial genome of Cepaea nemoralis (Gastropoda: Pulmonata). J Mol Evol. 1996 Feb;42(2):160–168. doi: 10.1007/BF02198842. [DOI] [PubMed] [Google Scholar]
  38. Wahleithner J. A., Wolstenholme D. R. Mitochondrial plasmid DNAs of broad bean: nucleotide sequences, complex secondary structures, and transcription. Curr Genet. 1987;12(1):55–67. doi: 10.1007/BF00420728. [DOI] [PubMed] [Google Scholar]
  39. Wallis G. P. Mitochondrial DNA insertion polymorphism and germ line heteroplasmy in the Triturus cristatus complex. Heredity (Edinb) 1987 Apr;58(Pt 2):229–238. doi: 10.1038/hdy.1987.37. [DOI] [PubMed] [Google Scholar]
  40. Wolstenholme D. R., Fauron C. M. 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. 1976 Nov;71(2):434–448. doi: 10.1083/jcb.71.2.434. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Wolstenholme D. R. Genetic novelties in mitochondrial genomes of multicellular animals. Curr Opin Genet Dev. 1992 Dec;2(6):918–925. doi: 10.1016/s0959-437x(05)80116-9. [DOI] [PubMed] [Google Scholar]
  42. 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]
  43. Wolstenholme D. R., Okimoto R., Macfarlane J. L. Nucleotide correlations that suggest tertiary interactions in the TV-replacement loop-containing mitochondrial tRNAs of the nematodes, Caenorhabditis elegans and Ascaris suum. Nucleic Acids Res. 1994 Oct 11;22(20):4300–4306. doi: 10.1093/nar/22.20.4300. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Yamazaki N., Ueshima R., Terrett J. A., Yokobori S., Kaifu M., Segawa R., Kobayashi T., Numachi K., Ueda T., Nishikawa K. Evolution of pulmonate gastropod mitochondrial genomes: comparisons of gene organizations of Euhadra, Cepaea and Albinaria and implications of unusual tRNA secondary structures. Genetics. 1997 Mar;145(3):749–758. doi: 10.1093/genetics/145.3.749. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Zardoya R., Meyer A. The complete DNA sequence of the mitochondrial genome of a "living fossil," the coelacanth (Latimeria chalumnae). Genetics. 1997 Jul;146(3):995–1010. doi: 10.1093/genetics/146.3.995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Zouros E., Ball A. O., Saavedra C., Freeman K. R. Mitochondrial DNA inheritance. Nature. 1994 Apr 28;368(6474):818–818. doi: 10.1038/368818a0. [DOI] [PubMed] [Google Scholar]
  47. Zouros E., Freeman K. R., Ball A. O., Pogson G. H. Direct evidence for extensive paternal mitochondrial DNA inheritance in the marine mussel Mytilus. Nature. 1992 Oct 1;359(6394):412–414. doi: 10.1038/359412a0. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES