Journal of Molecular Evolution

, Volume 64, Issue 6, pp 689–701 | Cite as

Segregation and Recombination of a Multipartite Mitochondrial DNA in Populations of the Potato Cyst Nematode Globodera pallida

  • Miles R. Armstrong
  • Dirk Husmeier
  • Mark S. Phillips
  • Vivian C. BlokEmail author


The discovery that the potato cyst nematode Globodera pallida has a multipartite mitochondrial DNA (mtDNA) composed, at least in part, of six small circular mtDNAs (scmtDNAs) raised a number of questions concerning the population-level processes that might act on such a complex genome. Here we report our observations on the distribution of some scmtDNAs among a sample of European and South American G. pallida populations. The occurrence of sequence variants of scmtDNA IV in population P4A from South America, and that particular sequence variants are common to the individuals within a single cyst, is described. Evidence for recombination of sequence variants of scmtDNA IV in P4A is also reported. The mosaic structure of P4A scmtDNA IV sequences was revealed using several detection methods and recombination breakpoints were independently detected by maximum likelihood and Bayesian MCMC methods.


Multipartite mitochondrial DNA Recombination Globodera pallida Breakpoint detection 



The authors acknowledge the constructive comments made on the manuscript by Dr. Craig Simpson and Dr. Frank Wright and the technical assistance of Ailsa Smith and Anne Holt with this work. Funding was received from EU AIR3 CT-92-0062 and the Scottish Executive Environment and Rural Affairs Department (SEERAD).

Supplementary material


  1. Akaike H (1974): A new look at the statistical model identification. IEEE Trans Autonom Contr 19:716–723CrossRefGoogle Scholar
  2. Armstrong, MA (1998) The mitochondrial genome of potato cyst nematode Globodera pallida: structure and use as a marker in population genetic analysis. PhD thesis. University of Dundee, Dundee, ScotlandGoogle Scholar
  3. Armstrong MA, Blok VC, Phillips MS (2000) A multipartite mitochondrial genome in the potato cyst nematode Globodera pallida. Genetics 154:181–192PubMedGoogle Scholar
  4. Avise JC, Quattro JM, Vrijenhoek RC (1992) Molecular clones within organismal clones: mitochondrial DNA phylogenies and the evolutionary histories of unisexual vertebrates. Evol Biol 26:225–246Google Scholar
  5. Blanchard JL, Lynch (2000) Organellar genes—Why do they end up in the nucleus? Trends Genet 16:315–320PubMedCrossRefGoogle Scholar
  6. Blok VC, Phillips MS (1995) The use of repeat sequence primers for investigating genetic diversity between populations of potato cyst nematodes with differing virulence. Fundam Appl Nematol 18:575–582Google Scholar
  7. Blok VC, Phillips MS, Harrower BE (1997). Comparison of British populations of potato cyst nematodes with populations from continental Europe and South America using RAPDs. Genome 40:286–293PubMedGoogle Scholar
  8. Burzynski A, Zbawicka M, Skibinski DOF, Wenne R (2003) Evidence for recombination of mtDNA in the marine mussel Mytilus trossulus from the Baltic. Mol Biol Evol 20:388–392PubMedCrossRefGoogle Scholar
  9. Casella G, George EI (1992) Explaining the Gibbs sampler. Am Stat 46:167–174CrossRefGoogle Scholar
  10. Feinberg AP, Vogelstein B (1983) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132:6–13PubMedCrossRefGoogle Scholar
  11. Felsenstein J (1978) Cases in which parsimony or compatibility methods will be positively misleading. Syst Zool 27:401–440CrossRefGoogle Scholar
  12. Folkertsma RT, Van der Voort JNAM, Vangentpelzer MPEK, Degroot E, Vandenbos WJ, Schots A, Bakker J, Gommers FJ (1994) Interspecific and intraspecific variation between populations of Globodera rostochiensis and Globodera pallida revealed by Random Amplified Polymorphic DNA. Phytopathology 84:807–811CrossRefGoogle Scholar
  13. Gantenbein B, Fet V, Gantenbein-Ritter IA, Balloux F (2005) Evidence for recombination in scorpion mitochondrial DNA (Scorpiones: Buthidae) Proc R Soc B 272:697–794PubMedCrossRefGoogle Scholar
  14. Guindon S, Gascuel O (2003): A simple, fast, and accurate algorithm to estimate large phylogeneies by maximum likelihood. Syst Biol 52 (5):696–704PubMedCrossRefGoogle Scholar
  15. Guo X, Liu S, Liu Y (2006) Evidence for recombination of mitochondrial DNA in triploid crucian carp. Genetics 172:1745–1749PubMedCrossRefGoogle Scholar
  16. Hasegawa M, Kishino H, Yano T (1985) Dating the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174PubMedCrossRefGoogle Scholar
  17. Hastings WK (1970) Monte Carlo sampling methods using Markov chains and their applications. Biometrika 57:97–109CrossRefGoogle Scholar
  18. He Y, Jones J, Armstrong M, Lamberti F, Moens M (2005) The mitochondrial genome of Xiphinema americanuum sensu stricto (Nematoda: Enoplea): considerable economization in the length and structural features of encoded genes. J Mol Evol 61:819–833PubMedCrossRefGoogle Scholar
  19. Hein J (1993) A heuristic method to reconstruct the history of sequences subject to recombination. J Mol Evol 36:396–405CrossRefGoogle Scholar
  20. Hoarau G, Holla S, Lescasse R, Stam WT, Olsen JL (2002) Heteroplasmy and evidence for recombination in the mitochondrial control region of the flatfish Platichthys flesus. Mol Biol Evol 19:2261–2264PubMedGoogle Scholar
  21. Hu M, Gasser RB (2006) Mitochondrial genomes of parasitic nematodes—progress and perspectives. Trends Parasitol 22:78–84PubMedCrossRefGoogle Scholar
  22. Hu M, Chilton NB, Gasser RB (2003) The mitochondrial genome of Strongyloides stercoralis (Nematoda)—idiosyncratic gene order and evolutionary implications. Int J Parsitol 33:1393–1408CrossRefGoogle Scholar
  23. Huelsenbeck JP, Ronquist F, Nielsen R, Bollback JP (2001) Bayesian inference of phylogeny and its impact on evolutionary biology science. Science 294:2310–2314PubMedCrossRefGoogle Scholar
  24. Husmeier D (2005) Discriminating between rate heterogeneity and interspecific recombination in DNA sequence alignments with phylogenetic factorial hidden Markov models. Bioinformatics 21:166–172Google Scholar
  25. Husmeier D, McGuire G (2003) Detecting recombination in 4-taxa DNA sequence alignments with Bayesian hidden Markov models and Markov chain Monte Carlo. Mol Biol Evol 20(3):315–337PubMedCrossRefGoogle Scholar
  26. Husmeier D, Wright F (2001) Probabilistic divergence measures for detecting interspecies recombination. Bioinformatics 17 (Suppl 1):S123–S131PubMedGoogle Scholar
  27. Husmeier D, Dybowski R, Roberts S (2005) Probabilistic modeling in bioinformatics and medical informatics. Springer Verlag, New YorkGoogle Scholar
  28. Hyman BC, Azevedo JLB (1996) Similar evolutionary patterning among repeated and single copy nematode mitochondrial genes. Mol Biol Evol 13:221–232PubMedGoogle Scholar
  29. Kajander GA, Kajander OA, Rovio AT, Majamaa K, Poulton J, Spelbrink JN, Holt IJ, Karhunen PJ, Jacobs HT (2000) Human mtDNA sublimons resenmbe rearranged mitochondrial genomes found in pathological states. Hum Mol Genet 9:2821–2835PubMedCrossRefGoogle Scholar
  30. 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
  31. Ladoukakis ED, Zouros E (2001) Direct evidence for homologous recombination in mussel (Mytilus galloprovincialis) mitochondrial DNA. Mol Biol Evol 18:1168–1175PubMedGoogle Scholar
  32. Lakshmipathy U, Campbell C (1999a) Double strand break rejoining by mammalian mitochondrial extracts. Nucleic Acids Res 27:1198–1204PubMedCrossRefGoogle Scholar
  33. Lakshmipathy U, Campbell (1999b) The human DNA ligase III gene encodes nuclear and mitochondrial proteins. Mol Cell Biol 19:3869–3876PubMedGoogle Scholar
  34. Larget B, Simon DL (1999) Markov chain Monte Carlo algorithms for the Bayesian analysis of phylogenetic trees. Mol Biol Evol 16:750–759Google Scholar
  35. Larget B, Simon DL (2001) BAMBE: Bayesian Analysis in Molecular Biology and Evolution Software; available at:
  36. 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 coelomate metazoans. Genetics 157:621–637PubMedGoogle Scholar
  37. Lunt DH, Hyman BC (1997) Animal mitochondrial DNA recombination. Nature 387:247PubMedCrossRefGoogle Scholar
  38. McGuire G, Wright F (2000) TOPAL 2.0: improved detection of mosaic sequences within multiple alignments. Bioinformatics 16:130–134PubMedCrossRefGoogle Scholar
  39. McGuire G, Wright F, Prentice MJ (1997) A graphical method for detecting recombination in phylogenetic data sets. Mol Biol Evol 14:1125–1131PubMedGoogle Scholar
  40. Milne I, Wright F, Rowe G, Marshall D F, Husmeier D, McGuire G (2004) TOPALi: Software for automatic identification of recombinant sequences within DNA multiple alignments. Bioinformatics 20:1806–1807PubMedCrossRefGoogle Scholar
  41. Montiel R, Lucena MA, Medeiros J, Simões (2006) The complete mitochondrial genome of the entomopathogenic nematodo Steinernema carpocapsae: insights into nematodo mitochondrial DNA evolution and phylogeny. J Mol Evol 62:211–225PubMedCrossRefGoogle Scholar
  42. Okimoto R, Wolstenholme DR. (1990) A set of transfer-RNAs that lack either the T-Psi-C arm or the dihydrouridine arm—towards a minimal transfer-RNA adapter. EMBO J 9:3405–3411PubMedGoogle Scholar
  43. 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 18:6113–6118PubMedCrossRefGoogle Scholar
  44. 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
  45. Pastrik HK, Rumpenhorst HJ, Burgermeister W (1995) Random amplified polymorphic DNA analysis of a Globodera pallida population selected for virulence. Fundam Appl Nematol 18:109–111Google Scholar
  46. Phillips MS, Trudgill DL (1998) Variation of virulence, in terms of quantitative reproduction of Globodera pallida populations, from Europe and South America, in relation to resistance from Solanum vernei and S. tuberosum ssp. andigena CPC 2802. Nematologica 44:409–423CrossRefGoogle Scholar
  47. Piganeau G., Gardner M, Eyre-Walker A (2004) A broad survey of recombination in animal mitochondria. Mol Biol Evol 21:2319–2325PubMedCrossRefGoogle Scholar
  48. Posada D, Crandall KA (2001) Selecting the best-fit model of nucleotide substitution. Syst Biol 50(4):580–601PubMedCrossRefGoogle Scholar
  49. Rand DM, Harrison RG (1986) Mitochondrial DNA transmission genetics in crickets. Genetics 114:955–970PubMedGoogle Scholar
  50. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  51. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NYGoogle Scholar
  52. Schmidt HA, Strimmer K, Vingron M, von Haeseler A (2002) TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18:502–504PubMedCrossRefGoogle Scholar
  53. Schwarz G. (1974) Estimating the dimension of a model. Ann Stat 6:461–464Google Scholar
  54. Stanton JM, McNicol DD, Steele V (1998) Non-manual lysis of second-stage Meloidogyne juveniles for identification of pure and mixed samples based on the polymerase chain reaction. Australas J Plant Path 27:112–115CrossRefGoogle Scholar
  55. Strimmer K, von Haeseler A (1996) Quartet puzzling: a quartet maximum likelihood method for reconstructing tree topologies. Mol Biol Evol 13:964–969Google Scholar
  56. Sutovsky P, Moreno RD, Ramalho-Santos J, Dominko T, Simerly C, Schatten G (2000) Ubiquitated sperm mitochondria, selective proteolysis, and the regulation of mitochondrial inheritance in mammalian embryos. Biol Reprod 63:582–590PubMedCrossRefGoogle Scholar
  57. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10(3):512–526PubMedGoogle Scholar
  58. Thompson JD, Higgins DG, Gibson TJ (1994) Clustal-W—improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680PubMedCrossRefGoogle Scholar
  59. Thyagarajan B, Padua RA, Cambell C (1996) Mammalian mitochondria possess homologous DNA recombination activity. J Biol Chem 271:27536–27534PubMedCrossRefGoogle Scholar
  60. Tsaousis AD, Martin DP, Ladoukakis ED, Posada D, Zouros E (2005) Widespread recombination in published animal mtDNA sequences. Mol Biol Evol 22:925–933PubMedCrossRefGoogle Scholar
  61. 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
  62. Wolstenholme DR (1992) Animal mitochondrial DNA: structure and evolution. Int Rev Cytol 141:173–216PubMedCrossRefGoogle Scholar
  63. Yang Z (1994) Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: approximate methods. J Mol Evol 39:306–314PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • Miles R. Armstrong
    • 1
  • Dirk Husmeier
    • 2
  • Mark S. Phillips
    • 1
  • Vivian C. Blok
    • 1
    Email author
  1. 1.Plant Pathogen ProgrammeScottish Crop Research InstituteInvergowrieUK
  2. 2.Biomathematics & Statistics Scotland (BioSS)James Clerk Maxwell Building, The King’s BuildingsEdinburghUK

Personalised recommendations