Abstract
Recently, a multipartite mitochondrial genome was characterized in the potato cyst nematode, Globodera pallida. Six subgenomic circles were detectable by PCR, while full-length genomes were not. We investigate here whether this subgenomic organization occurs in a close relative of G. pallida. We amplified and sequenced one entire mitochondrial subgenome from the cyst-forming nematode, Globodera rostochiensis. Comparison of the noncoding region of this subgenome with those reported previously for G. pallida facilitated the design of amplification primers for a range of subgenomes from G. rostochiensis. We then randomly sequenced five subgenomic fragments, each representative of a unique subgenome. This study indicates that the multipartite structure reported for G. pallida is conserved in G. rostochiensis. A comparison of subgenomic organization between these two Globodera species indicates a considerable degree of overlap between them. Indeed, we identify two subgenomes with an organization identical with that reported for G. pallida. However, other subgenomes are unique to G. rostochiensis, although some of these have blocks of genes comparable to those in G. pallida. Dot-plot comparisons of pairs of subgenomes from G. rostochiensis indicate that the different subgenomes share fragments with high sequence identity. We interpret this as evidence that recombination is operating in the mitochondria of G. rostochiensis.
References
Armstrong MR, Blok VC, Phillips MS (2000) A multipartite mitochondrial genome in the potato cyst nematode Globodera pallida. Genetics 154:181–192
Armstrong MA, Husmeier D, Phillips MS, Blok VC (2007) Segregation and recombination of a multipartite mitochondrial DNA in populations of the potato cyst nematode Globodera pallida. J Mol Evol 64:689–701
Awata H, Noto T, Endoh H (2005) Differentiation of somatic mitochondria and the structural changes in mtDNA during development of the dicyemid Dicyema japonicum (Mesozoa). Mol Gen Genomics 273:441–449
Eyre-Walker A, Awadalla P (2001) Does human mtDNA recombine? J Mol Evol 53:430–435
Gibson T, Blok VC, Phillips MS, Hong G, Kumarasinghe D, Riley IT, Dowton M (2007) The mitochondrial subgenomes of the nematode Globodera pallida are mosaics: evidence of recombination in an animal mitochondrial genome. J Mol Evol 64:463–471
Hey J (2000) Human mitochondrial DNA recombination: can it be true? Trends Ecol Evol 15:181–182
Howell N (1997) mtDNA recombination: what do in vitro data mean? Am J Hum Genet 61:19–22
Innan H, Nordberg M (2002) Recombination or mutational hot spots in human mtDNA? Mol Biol Evol 19:1122–1127
Kajander OA, Karhunen PJ, Holt IJ, Jacobs HT (2001) Prominent mitochondrial DNA recombination intermediates in human heart muscle. EMBO Rep 2:1007–1012
Kraytsberg Y, Schwartz M, Brown TA, Ebralidse K, Kunz WS, Clayton DA, Vissing J, Khrapko K (2004) Recombination of human mitochondrial DNA. Science 304:981
Ladoukakis ED, Zouros E (2001a) Direct evidence for homologous recombination in mussel (Mytilus galloprovincialis) mitochondrial DNA. Mol Biol Evol 18:1168–1175
Ladoukakis ED, Zouros E (2001b) Recombination in animal mitochondrial DNA: evidence from published sequences. Mol Biol Evol 18:2127–2131
Lang BF, Gray MW, Burger G (1999) Mitochondrial genome evolution and the origin of eukaryotes. Annu Rev Genet 33:351–397
Lowe TM, Eddy SR (1997) tRNAscan-SE: A program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:955–964
Lunt DH, Hyman BC (1997) Animal mitochondrial DNA recombination. Nature 387:247
Maynard Smith J, Smith NH (2002) Recombination in animal mitochondrial DNA. Mol Biol Evol 19:2330–2332
Mita S, Rizzuto R, Moraes CT, Shanske S, Arnaudo E, Fabrizi GM, Koga Y, DiMauro S, Schon EA (1990) Recombination via flanking direct repeats is a major cause of large-scale deletions of human mitochondrial DNA. Nucleic Acids Res 18:561–567
Moritz C, Dowling TE, Brown WM (1987) Evolution of animal mitochondrial DNA: relevance for population biology and systematics. Annu Rev Ecol Syst 18:269–292
Mulholland V, Carde L, O’Donnell JJ, Fleming CC, Powers TO (1996) Use of the polymerase chain reaction to discriminate potato cyst nematode at the species level. BCPC Symp Diagnostics Crop Prod 65:247–252
Rokas A, Ladoukakis E, Zouros E (2003) Animal mitochondrial DNA recombination revisited. Trends Ecol Evol 18:411–417
Subbotin SA, Vierstraete A, De Ley P, Rowe J, Waeyenberge L, Moens M, Vanfleteren JR (2001) Phylogenetic relationships within the cyst-forming nematodes (Nematoda, Heteroderidae) based on analysis of sequences from the ITS regions of ribosomal DNA. Mol Phylogenet Evol 21:1–16
Suematsu T, Sato A, Sakurai M, Watanabe K, Ohtsuki T (2005) A unique tRNA recognition mechanism of Caenorhabditis elegans mitochondrial EF-Tu2. Nucleic Acids Res 33:4683–4691
Ujvari B, Dowton M, Madsen T (2007) Mitochondrial DNA recombination in a free-ranging Australian lizard. Biol Lett 3:189–192
Wiuf C (2001) Recombination in human mitochondrial DNA? Genetics 159:749–756
Acknowledgments
Thanks to Ian Riley for helpful discussions on nematode biology, and to two anonymous reviewers who provided insightful comments on an earlier version of this article. This work was funded by grants from the Australian Research Council, the Scottish Executive Environment and Rural Affairs Department, and EU AIR3 CT-92-0062.
Author information
Authors and Affiliations
Corresponding author
Additional information
Reviewing Editor: Dr. Rafael Zardoya
Electronic supplementary material
Rights and permissions
About this article
Cite this article
Gibson, T., Blok, V.C. & Dowton, M. Sequence and Characterization of Six Mitochondrial Subgenomes from Globodera rostochiensis: Multipartite Structure Is Conserved Among Close Nematode Relatives. J Mol Evol 65, 308–315 (2007). https://doi.org/10.1007/s00239-007-9007-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00239-007-9007-y