Advertisement

Journal of Molecular Evolution

, Volume 61, Issue 6, pp 819–833 | Cite as

The Mitochondrial Genome of Xiphinema americanum sensu stricto (Nematoda: Enoplea): Considerable Economization in the Length and Structural Features of Encoded Genes

  • Y. He
  • J. Jones
  • M. Armstrong
  • F. Lamberti
  • M. MoensEmail author
Article

Abstract

The complete sequence of the mitochondrial genome of the plant parasitic nematode Xiphinema americanum sensu stricto has been determined. At 12626bp it is the smallest metazoan mitochondrial genome reported to date. Genes are transcribed from both strands. Genes coding for 12 proteins, 2 rRNAs and 17 putative tRNAs (with the tRNA-C, I, N, S1, S2 missing) are predicted from the sequence. The arrangement of genes within the X. americanum mitochondrial genome is unique and includes gene overlaps. Comparisons with the mtDNA of other nematodes show that the small size of the X. americanum mtDNA is due to a combination of factors. The two mitochondrial rRNA genes are considerably smaller than those of other nematodes, with most of the protein encoding and tRNA genes also slightly smaller. In addition, five tRNAs genes are absent, lengthy noncoding regions are not present in the mtDNA, and several gene overlaps are present.

Keywords

Xiphinema americanum Mitochondrial genome 

Notes

Acknowledgments

This work was funded by EU Contract SMT4-CT98-2229 and Scottish Executive Environment and Rural Affairs Department Project SCR/561/00 (J.J.).

References

  1. Armstrong MR, Blok VC, Phillips MS (2000) A multipartitie mitochondrial genome in the potato cyst nematode Globodera pallida. Genetics 154:181–192PubMedGoogle Scholar
  2. Beagley CT, Macfarlane GA, Pont–Kingdon, Okimo R, Okada N, Wolstenholme DR (1995) Mitochodrial genome of Anthozoa (Cnidaria). In: Palmieri F (ed). Progr Cell Res 5:149–153Google Scholar
  3. Beagley CT, Okada N, Wolstenholme DR (1996) 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 USA 93:5619–5623PubMedCrossRefGoogle Scholar
  4. Beagley CT, Okimo R, Wolstenholme DR (1998) The mitochondrial genome of sea anemone Metridium senile (Cnidaria): introns, a paucity of tRNA, genes and a near-standard genetic code. Genetics 148:1091–1109PubMedGoogle Scholar
  5. Beaton MJ, Roger AJ, Cavalier-Smith T (1998) Sequence analysis of the mitochondrial genome of Sarcophyton glaucum: conserved gene order among octocorals. J Mol Evol 47:697–708PubMedGoogle Scholar
  6. Blaxter ML, De ley P, Garey JR, Liu LX, Scheldeman P, Vierstraete A, Vanfleteren JR, Mackey LY, Dorris M, Frisse LM, Vida JT, Thomas WK (1998) A molecular evolutionary framework for the phylum Nematoda. Nature 392(5):71–75PubMedGoogle Scholar
  7. Blanchette M, Kunisawa T, Sankoff D (1999) Gene order breakpoint evidence in animal mitochondrial phylogeny. J Mol Evol 49:193–203PubMedGoogle Scholar
  8. Boore JL (1999) Survey and summary: Animal mitochondrial genomes. Nucleic Acids Res 27:1767–1780PubMedCrossRefGoogle Scholar
  9. Boore JL, Brown WM (1998) Big trees from little genomes: mitochondrial gene order as a phylogenetic tool. Curr Opin Genet Dev 8:668–674PubMedCrossRefGoogle Scholar
  10. Boore JL, Collins TM, Stanton D, Daehler LL, Brown WM (1995) Deducing the pattern of arthropod phylogeny from mitochondrial DNA rearrangements. Nature 376:163–165PubMedCrossRefGoogle Scholar
  11. Boore JL, Lavrov D, Brown WM (1998) Gene translocation links insects and crustaceans. Nature 393:667–668Google Scholar
  12. Bridge 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 89:8750–8753PubMedGoogle Scholar
  13. Cheng S, Stoneking M (1996) Complete mitochondrial genome amplification. Nat Genet 7:350–351Google Scholar
  14. De Rijk P, De Wachter R (1997) RNAviz, a program for the visualization of RNA secondary structure. Nucleic Acids Res 25:4679–4684PubMedGoogle Scholar
  15. Döner M, Altmann M, Pääbo S, Mörl M (2001) Evidence for import of a lysyl-tRNA into marsupial mitochondria. Mol Biol Cell 12:2688–2698Google Scholar
  16. Gutell RR (1994) Collection of small subunit (16S- and 16S-like) ribosomal RNA structures. Nucleic Acids Res 22:3505–3507Google Scholar
  17. Gutell RR (1995) Comparative sequence analysis and the structure of 16S and 23S rRNA. In: Zimmermann RA, Dahlberg AE (eds) Ribosomal RNA. Structure, evolution, processing and function in protein biosynthesis. CRC Press, New York, pp 111–128Google Scholar
  18. Gutell RR, Gray MW, Schnare MN (1993) A compilation of large subunit (23S- and 23S-like) ribosomal RNA structures. Nucleic Acids Res 21:3055–3074PubMedGoogle Scholar
  19. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98Google Scholar
  20. Hixton JE, Wong TW, Clayton DA (1986) Both the conserved stem-loop and divergent 5′-flanking sequences are required for initiation at the human mitochondrial origin of light-strand DNA replication. J Biol Chem 261:2384–2390Google Scholar
  21. Hoffmann RJ, Boore JL, Brown WM (1992) A novel mitochondrial genome organization for the blue mussel, Mytilus edulis. Genetics 131:397–412PubMedGoogle Scholar
  22. Hu M, Chilton NG, Gasser RB (2002) The mitochondrial genomes of the human hookworms, Ancylostoma duodenale and Necator americanus (Nematoda: Secernentea). Int J Parasitol 32:145–158PubMedGoogle Scholar
  23. Hu M, Chilton NB, Gasser RB (2004) The mitochondrial genomics of parasitic nematodes of socio-economic importance: recent progress, and implications for population genetics and systematics. Adv Paratitol 56:133–212Google Scholar
  24. Hyman BC, Azevedo JLB (1996) Similar evolutionary patterning among repeated and single copy nematode mitochondrial genes. Mol Biol Evol 13:221–232PubMedGoogle Scholar
  25. Keddie EM, Higazi T, Unnasch TR (1998) The mitochondrial genome of Onchocerca volvulus: sequences, structure and phylogenetic analysis. Mol Biochem Parasitol 95:111–127PubMedCrossRefGoogle Scholar
  26. Khaitovich P, Mankin AS (1999) Effects of antibiotics on large ribosomal subunit assembly reveals possible function of 5 S rRNA. J Mol Biol 291:1025–1034PubMedCrossRefGoogle Scholar
  27. Kyte J, Doolittle RF (1982) A simple method for displaying the hydrophobic character of a protein. J Mol Biol 157:105–142PubMedCrossRefGoogle Scholar
  28. L’Abbé D, Duhaime DJ, Lang BF, Morais R (1991) The transcription of DNA in chicken mitochondria initiates from one major bi-directional promoter. J Biol Chem 266:10844–10850PubMedGoogle Scholar
  29. Lavrov DV, Brown WM (2001) Trichinella spiralis mtDNA: A nematode mitochondrial genome that encodes a putative ATP8 and normally structured tRNAs and has a gene arrangement relatable to those of coelamate metazoans. Genetics 157:621–637PubMedGoogle Scholar
  30. Lavrov DV, Brown WM, Boore JL (2000) A novel type of RNA editing occurs in the mitochondrial tRNAs of the centipede Lithobius forficatus. Pro Natl Acad Sci USA 97:13738–13742Google Scholar
  31. Le TH, Blair D, Agatsuma, T et al. (2000) Phylogenies inferred from mitochondrial gene orders: a cautionary tale from the parasitic flatworms. Mol Biol Evol 17(7):1123–1125PubMedGoogle Scholar
  32. Lewis DL, Farr CL, Farquhar AL, Kaguni LS (1994) Sequence, organization, and evolution of the A+T region of Drosophila melanoganster mitochondrial DNA. Mol Biol Evol 11:523–38PubMedGoogle Scholar
  33. Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:955–964PubMedCrossRefGoogle Scholar
  34. Mörl M, Dörner M, Pääbo S (1995) C to U editing and modifications during the maturation of the mitochondrial tRNA(Asp) in marsupials. Nucleic Acids Res 23:3380–3384PubMedGoogle Scholar
  35. Ohtsuki T, Watanabe Y, Takemoto C, Kawai G, Ueda T, Kita K, Kojima S, Kaziro Y, Nyborg J, Watanabe K (2001) An “elongated” translation elongation factor Tu for truncated tRNAs in nematode mitochondria. J Biol Chem 276:21571–21577PubMedCrossRefGoogle Scholar
  36. Ohtsuki T, Sakurai M, Sato A, Watanabe K (2002) Characterization of the interaction between the nucleotide exchange factor EU-Ts from nematode mitochondria and elongation factor Tu. Nucleic Acids Res 30(24):5444–5451PubMedCrossRefGoogle Scholar
  37. Ojala DC, Merkel C, Gelfand R, Attardi G (1980) The tRNA genes punctuate the reading of genetic information in human mitochondrial DNA. Cell 22:393–403PubMedCrossRefGoogle Scholar
  38. Ojala D, Montoya J, Attardi G (1981) tRNA punctuation model of RNA processing in human mitochondria. Nature 290:470–474PubMedCrossRefGoogle Scholar
  39. Okimoto R, Macfarlane JL, Clary DO, Wolstenholme DR (1992) The mitochondrial genomes of two nematodes, Caenorhabditis elegans and Ascaris suum. Genetics 130:471–498PubMedGoogle Scholar
  40. Orr AT, Rabets JC, Horton TL, Landweber LF (1997) RNA editing missing in mitochondria. RNA 3:335–336PubMedGoogle Scholar
  41. Pont-Kingdon GA, Okada N, Macfarlane JL, Beagley CT, Watkins-Sims CD, Cavlier-Smith T, Clark-Walker GD, Wolstenholme DR (1998) Mitochondrial DNA of the coral Sarcophyton glaucum contains a gene for a homolog of bacterial MutS: a possible case of gene transfer from the nucleus to the mitochondrion. J Mol Evol 46:419–431PubMedGoogle Scholar
  42. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: A laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NYGoogle Scholar
  43. Smith MJ, Amdt A, Gotsky S, Fajber E (1993) The phylogeny of echinoderm classes based on mitochondrial gene arrangements. J Mol Evol 36:545–554PubMedCrossRefGoogle Scholar
  44. Suzuki T, Terasaki M, Takemoto-Hori C, Hanada T, Ueda T, Wada A, Watanabe K (2001) Proteomic analysis of the mammalian mitochondrial ribosome. J Biol Chem 276:33181–33195PubMedGoogle Scholar
  45. Taanman JW (1999) Review: The mitochondrial genome: structure, transcription, translation and replication. Biochim Biophys Acta 1410:103–123PubMedGoogle Scholar
  46. Tan THP, Bochud-Allemann N, Horn EK, Schneider A (2002) Eukaryotic-type elongator tRNAMet of Trypanosoma brucei becomes formylated after import into mitochondria. Proc Natl Acad Sci USA 99:1152–1157PubMedGoogle Scholar
  47. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882Google Scholar
  48. Tomita K, Ueda T, Watanabe K (1996) RNA editing in the acceptor stem of squid mitochondrial tRNATyr. Nucleic Acids Res 24:4987–4991PubMedCrossRefGoogle Scholar
  49. Watanabe KI, Bessho Y, Kawasaki M, Hori H (1999) Mitochondrial genes are found on minicircle DNA molecules in the mesazoan animal Dicyema. J Mol Biol 286:645–650PubMedCrossRefGoogle Scholar
  50. Watanabe Y, Tsurui H, Ueda T, Furushima R, Takamiya S, Kita K, Nishikawa K, Watanabe K (1994) Primary and higher order structure of nematode (Ascaris suum) mitochondrial tRNAs lacking either the T or D stem. J Biol Chem 269:22902–22906PubMedGoogle Scholar
  51. Wolstenholme DR (1992) Animal mitochondrial DNA: structure and evolution. Int Rev Cytol 141:173–216PubMedGoogle Scholar
  52. Wolstenholme DR, Okimoto R, Macfarlane JL (1994) Nucleotide correlation that suggest tertiary interactions in the TV-replacement loop-containing mitochondrial tRNAs of the nematodes, Caenorhabditis elegans and Ascaris suum. Nucleic Acids Res 22:4300–4306PubMedGoogle Scholar
  53. Yokobori S, Pääbo S (1995a) tRNA editing in metazoans. Nature 377:490CrossRefGoogle Scholar
  54. Yokobori S, Pääbo S (1995b) Transfer RNA editing in land snail mitochondria. Proc Natl Acad Sci USA 92:10432–10435Google Scholar
  55. Zuker M, Mathews DH, Turner DH (1999) Algorithms and thermodynamics for RNA secondary structure prediction: a practical guide. In: Barciszewski J, Clark BFC (eds) RNA biochemistry and biotechnology. NATO ASI Series. Kluwer Academic, New York, pp 11–43Google Scholar

Copyright information

© Springer Science+Business Media, Inc. 2005

Authors and Affiliations

  • Y. He
    • 1
  • J. Jones
    • 2
  • M. Armstrong
    • 2
  • F. Lamberti
    • 3
  • M. Moens
    • 1
    Email author
  1. 1.Gewasbescherming-CLOMerelbekeBelgium
  2. 2.Plant-Pathogen Interactions ProgrammeScottish Crop Research InstituteInvergowrieUK
  3. 3.Istituto di Nematologia AgrariaCNRBari

Personalised recommendations