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Non-homogenized ITS regions in the parasitic nematode Cooperia oncophora

Published online by Cambridge University Press:  06 August 2004

T. H. M. MES
Affiliation:
Department of Parasitology and Tropical Veterinary Medicine, Institute of Infectious Diseases and Immunology, Utrecht University, PO Box 80165, 3508 TD Utrecht, The Netherlands
A. W. C. A. CORNELISSEN
Affiliation:
Department of Parasitology and Tropical Veterinary Medicine, Institute of Infectious Diseases and Immunology, Utrecht University, PO Box 80165, 3508 TD Utrecht, The Netherlands

Abstract

Here, the validity of the assumption of concerted evolution of ribosomal regions in larval and adult Cooperia oncophora was assessed. In each of 4 individuals of this parasitic nematode, at least 78% of the sequences comprised different ITS variantsNucleotide sequence data are available in the DDBJ/EMBL/GenBank databases under the Accession numbers AJ544390–AJ544465.. This implies that concerted evolution is not acting, which is corroborated by the scarcity of signatures of gene conversion and recombination. Mis-incorporation of nucleotides and illegitimate PCR-induced recombination turned out to be unlikely, and positions with substantial frequencies of alternative nucleotides corresponded to ambiguous positions in published ITS2 sequences of this and other Cooperia species based on direct sequencing. The ITS regions of each individual C. oncophora displayed a significant excess of unique mutations in agreement with expansion of the ribosomal gene family. Interesting corollaries of the inferred size changes of this gene family are genomic rearrangements that occur during larval development such as multiple rounds of endoduplication (in Rhabditidae), chromatin diminution (in Ascaris), and non-compensatory mutations on the secondary structure of the ITS2. It is yet unknown which process is important in trichostrongylids. Finally, although it can not be rigorously assessed in Cooperia, the ITS polymorphisms can readily be envisioned to affect phylogenetic reconstructions of closely related nematodes.

Type
Research Article
Copyright
2004 Cambridge University Press

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References

REFERENCES

ADAMS, B. J., BURNELL, A. M. & POWERS, T. O. ( 1998). A phylogenetic analysis of Heterorhabditis (Nematoda: Rhabditidae) based on internal transcribed spacer 1 DNA sequence data. Journal of Nematology 30, 2239.Google Scholar
BECKENBACH, K., BLAXTER, M. L. & WEBSTER, J. M. ( 1999). Phylogeny of Bursaphelenchus species derived from analysis of ribosomal internal transcribed spacer DNA sequences. Nematology 1, 539548.CrossRefGoogle Scholar
BERNSEN, M. R., DIJKMAN, H. B. P. M., DE VRIES, E., FIGDOR, C. G., RUITER, D. J., ADEMA, G. J. & VAN MUIJEN, G. N. P. ( 1998). Identification of multiple mRNA and DNA sequences from small tissue samples isolated by laser-assisted microdissection. Laboratory Investigation 78, 12671273.Google Scholar
BETRÁN, E., ROZAS, J., NAVARRO, A. & BARBADILLA, A. ( 1997). The estimation of the number and the length distribution of gene conversion tracts from population DNA sequence data. Genetics 146, 8999.Google Scholar
BLOUIN, M. S., YOWELL, C. A., COURTNEY, C. H. & DAME, J. B. ( 1998). Substitution bias, rapid saturation, and the use of mtDNA for nematode systematics. Molecular Biology and Evolution 15, 17191727.CrossRefGoogle Scholar
CADWELL, R. C. & JOYCE, G. F. ( 1994). Mutagenic PCR. PCR Methods and Applications 3, S136S140.CrossRefGoogle Scholar
CAMPBELL, C. S., WOJCIECHOWSKI, M. F., BALDWIN, B. G., ALICE, L. A. & DONOGHUE, M. J. ( 1997). Persistent nuclear ribosomal DNA sequence polymorphism in the Amelanchier agamic complex (Rosaceae). Molecular Biology and Evolution 14, 8190.CrossRefGoogle Scholar
CHILTON, N. B., HOSTE, H., NEWTON, L. A., BEVERIDGE, I. & GASSER, R. B. ( 1998). Common secondary structures for the second internal transcribed spacer pre-rRNA of two subfamilies of trichostrongylid nematodes. International Journal for Parasitology 28, 17651773.CrossRefGoogle Scholar
CHILTON, N. B., NEWTON, L. A., BEVERIDGE, I. & GASSER, R. B. ( 2001). Evolutionary relationships of Trichostrongyloid nematodes (Strongylida) inferred from ribosomal DNA sequence data. Molecular Phylogenetics and Evolution 19, 367386.CrossRefGoogle Scholar
CHITWOOD, B. G. & CHITWOOD, M. B. ( 1972). Introduction to Nematology. University Park Press.
CRONN, R., CEDRONI, M., HASELKORN, T., GROVER, C. & WENDEL, J. F. ( 2002). PCR-mediated recombination in amplification products derived from polyploid cotton. Theoretical and Applied Genetics 104, 482489.CrossRefGoogle Scholar
ELBADRI, G. A. A., DE LEY, P., WAEYENBERGE, L., VIERSTRAETE, A., MOENS, M. & VANFLETEREN, J. ( 2002). Intraspecific variation in Radopholus similis isolates assessed with restriction fragment length polymorphism and DNA sequencing of the internal transcribed spacer region of the ribosomal RNA cistron. International Journal for Parasitology 32, 199205.CrossRefGoogle Scholar
ETTER, A., BERNARD, V., KENZELMANN, M., TOBLER, H. & MULLER, F. ( 1994). Ribosomal heterogeneity from chromatin diminution in Ascaris lumbricoides. Science 265, 954956.CrossRefGoogle Scholar
FLEMMING, A. J., SHEN, Z. Z., CUNHA, A., EMMONS, S. W. & LEROI, A. M. ( 2000). Somatic polyploidization and cellular proliferation drive body size evolution in nematodes. Proceedings of the National Academy of Sciences, USA 97, 52855290.CrossRefGoogle Scholar
FLOYD, R., ABEBE, E., PAPERT, A. & BLAXTER, M. ( 2002). Molecular barcodes for soil nematode identification. Molecular Ecology 11, 839850.CrossRefGoogle Scholar
GASSER, R. B., CHILTON, N. B., HOSTE, H. & BEVERIDGE, I. ( 1993). Rapid sequencing of rDNA from single worms and eggs of parasitic helminths. Nucleic Acids Research 21, 25252526.CrossRefGoogle Scholar
GASSER, R. B., ZHU, X. Q., CHILTON, N. B., NEWTON, L. A., NEDERGAARD, T. & GULDBERG, P. ( 1998). Analysis of sequence homogenization in rDNA arrays of Haemonchus contortus by denaturing gradient gel electrophoresis. Electrophoresis 19, 23912395.CrossRefGoogle Scholar
HIGAZI, T. B., KATHOLI, C. R., MAHMOUD, B. M., BARAKA, O. Z., MUKHTAR, M. M., AL QUBATI, Y. & UNNASCH, T. R. ( 2001). Onchocerca volvulus: Genetic diversity of parasite isolates from Sudan. Experimental Parasitology 97, 2434.CrossRefGoogle Scholar
HILLIS, D. M., MORITZ, C., PORTER, C. A. & BAKER, R. J. ( 1991). Evidence for biased gene conversion in concerted evolution of ribosomal DNA. Science 251, 308310.CrossRefGoogle Scholar
HUGALL, A., STANTON, J. & MORITZ, C. ( 1999). Reticulate evolution and the origins of ribosomal internal transcribed spacer diversity in apomictic Meloidogyne. Molecular Biology and Evolution 16, 157164.CrossRefGoogle Scholar
JENTSCH, S., TOBLER, H. & MULLER, F. ( 2002). New telomere formation during the process of chromatin diminution in Ascaris suum. International Journal of Developmental Biology 46, 143148.Google Scholar
KANOBANA, K., VERVELDE, L., VAN DER VEER, M., EYSKER, M. & PLOEGER, H. W. ( 2001). Characterization of host responder types after a single Cooperia oncophora infection: kinetics of the systemic immune response. Parasite Immunology 23, 641653.CrossRefGoogle Scholar
KLOOSTERMAN, A., ALBERS, G. A. A. & VAN DEN BRINK, R. ( 1978). Genetic variation among calves in resistance to nematode parasites. Veterinary Parasitology 4, 353368.CrossRefGoogle Scholar
LIANG, Q. W., CHEN, L. S. & FULCO, A. J. ( 1995). An efficient and optimized PCR method with high fidelity for site-directed mutagenesis. PCR Methods and Applications 4, 269274.CrossRefGoogle Scholar
MAFF ( 1977). Manual of Veterinary Parasitological Laboratory Techniques. Technical Bulletin 18. Her Majesty's Stationary Office, London, UK.
MES, T. H. M. ( 2003). Demographic expansion of parasitic nematodes of livestock based on mitochondrial DNA regions that conflict with the infinite-sites model. Molecular Ecology 12, 15551566.CrossRefGoogle Scholar
MULLER, F. & TOBLER, H. ( 2000). Chromatin diminution in the parasitic nematodes Ascaris suum and Parascaris univalens. International Journal for Parasitology 30, 391399.CrossRefGoogle Scholar
NADLER, S. A., HOBERG, E. P., HUDSPETH, D. S. S. & RICKARD, L. G. ( 2000). Relationships of Nematodirus species and Nematodirus battus isolates (Nematoda: Trichostrongyloidea) based on nuclear ribosomal DNA sequences. Journal of Parasitology 86, 588601.CrossRefGoogle Scholar
NEWTON, L. A., CHILTON, N. B., BEVERIDGE, I. & GASSER, R. B. ( 1998). Genetic evidence indicating that Cooperia surnabada and Cooperia oncophora are one species. International Journal for Parasitology 28, 331336.CrossRefGoogle Scholar
POSADA, D. & CRANDALL, K. A. ( 1998). Modeltest: testing the model of nucleotide substitution. Bioinformatics 14, 817818.CrossRefGoogle Scholar
POWERS, T. O., TODD, T. C., BURNELL, A. M., MURRAY, P. C. B., FLEMING, C. C., SZALANSKI, A. L., ADAMS, B. A. & HARRIS, T. S. ( 1997). The rDNA internal transcribed spacer region as a taxonomic marker for nematodes. Journal of Nematology 29, 441450.Google Scholar
ROBERTS, F. H. S. & O'SULLIVAN, P. J. ( 1950). Methods for egg counts and larval cultures for strongyles infecting the gastro-intestinal tract of cattle. Australian Journal of Agricultural Research 1, 99102.CrossRefGoogle Scholar
ROZAS, J. & ROZAS, R. ( 1999). DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15, 174175.CrossRefGoogle Scholar
ROZAS, J., GULLAUD, M., BLANDIN, G. & AGUADE, M. ( 2001). DNA variation at the rp49 gene region of Drosophila simulans: evolutionary inferences from an unusual haplotype structure. Genetics 158, 11471155.Google Scholar
SAWYER, S. A. ( 1989). Statistical tests for detecting gene conversion. Molecular Biology and Evolution 6, 526538.Google Scholar
SAWYER, S. A. ( 1999). GENECONV: a computer package for the statistical detection of gene conversion. Distributed by the author, Dept. of Mathematics, Washington University in St Louis, available at http://www.math.wustl.edy/~sawyer.
SHI, Y. & BLACKWELL, T. K. ( 2003). A two-tiered transcription regulation mechanism that protects germ cell identity. Molecular Cell 12, 10621064.CrossRefGoogle Scholar
SHIN, T. H. & MELLO, C. C. ( 2003). Chromatin regulation during C. elegans germline development. Current Opinion in Genetics and Development 13, 455462.CrossRefGoogle Scholar
SIJEN, T. & PLASTERK, R. H. A. ( 2003). Transposon silencing in the Caenorhabditis elegans germ line by natural RNAi. Nature, Genetics 426, 310314.CrossRefGoogle Scholar
STEVENSON, L. A., CHILTON, N. B. & GASSER, R. B. ( 1995). Differentiation of Haemonchus placei from H. contortus (Nematoda: Trichostrongylidae) by the ribosomal DNA second internal transcribed spacer. International Journal for Parasitology 25, 483488.Google Scholar
STEVENSON, L. A., GASSER, R. B. & CHILTON, N. B. ( 1996). The ITS-2 rDNA of Teladorsagia circumcincta, T-trifurcata and T-davtiani (Nematoda: Trichostrongylidae) indicates that these taxa are one species. International Journal for Parasitology 26, 11231126.CrossRefGoogle Scholar
SUBBOTIN, S. A., HALFORD, P. D., WARRY, A. & PERRY, R. N. ( 2000 a). Variations in ribosomal DNA sequences and phylogeny of Globodera parasitising solanaceous plants. Nematology 2, 591604.Google Scholar
SUBBOTIN, S. A., WAEYENBERGE, L. & MOENS, M. ( 2000 b). Identification of cyst forming nematodes of the genus Heterodera (Nematoda: Heteroderidae) based on the ribosomal DNA-RFLP. Nematology 2, 153164.Google Scholar
SWOFFORD, D. L. ( 1998). PAUP*. Phylogenetic Analysis using Parsimony (* and other Methods). Sinauer Associates, Sunderland, Massachusetts.
SZALANSKI, A. L., SUI, D. D., HARRIS, T. S. & POWERS, T. O. ( 1997). Identification of cyst nematodes of agronomic and regulatory concern with PCR-RFLP of ITS1. Journal of Nematology 29, 255267.Google Scholar
TAJIMA, F. ( 1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585595.Google Scholar
TRIANTAPHYLLOU, A. C. ( 1991). Further studies on the role of polyploidy in the evolution of Meloidogyne. Journal of Nematology 23, 249253.Google Scholar
WARD, J. G., BLOMBERG, P., HOFFMAN, N. & YAO, M. C. ( 1997). The intranuclear organization of normal, hemizygous and excision-deficient rRNA genes during developmental amplification in Tetrahymena thermophila. Chromosoma 106, 233242.CrossRefGoogle Scholar