European Journal of Plant Pathology

, Volume 148, Issue 4, pp 907–917 | Cite as

Morphological and molecular analysis of Paratrichodorus teres (Hooper 1962) (Nematoda: Trichodoridae): a groundwork for discussion on the phylogeny and pathogenicity of Paratrichodorus species

  • Krassimira Ilieva-Makulec
  • Katarzyna Rybarczyk-Mydłowska
  • Grażyna Winiszewska
  • Łukasz Flis
  • Anna Tereba
  • Katarzyna Kowalewska
  • Tadeusz Malewski


Due to its ability to transmit plant viruses, Paratrichodorus teres (Hooper in Nematologica, 7, 273–280, 1962) is recognized as an economically important trichodorid species. Morphological and molecular analyses (18S and 28S rDNA) were performed, and 10 new plant hosts are reported for Polish P. teres populations. Major morphological features and the measurements obtained for the investigated specimens were within the wide ranges indicated for this species. However, a more detailed comparative analysis of Polish and Iranian P. teres showed significant morphological differences, particularly, in the shape and the structure of the walls of pars proximalis vaginae and the shape of the rectum.

Phylogenetic study based on the 18S rDNA data suggests positioning of the Polish P. teres sequences within a cluster of sequences originating from the Netherlands. A comparison of the 28S rDNA fragment from Polish populations with the only P. teres 28S rDNA sequence available (from Iran) in GenBank revealed a sequence variability of 9.3%. The variation across these two representatives was higher than in the case of many other pairs of Trichodoridae species. The results obtained on the Polish P. teres specimens are discussed in the framework of the species taxonomy and phylogenetic relationships.


Stubby root nematodes Virus vector nematodes 18S rDNA 28S rDNA Poland Iran 



This research was conducted by the Museum and Institute of Zoology, Polish Academy of Sciences within the project WND-POIG.01.03.01-00-133/09 “Development of innovative methods for rapid identification of nematodes that cause damage to the economy” under the Operational Programme Innovative Economy 2007–2013, which is co-financed by EU funds. We wish to kindly thank Prof. Dr. Wilfrida Decraemer and Dr. Yves Samyn from Royal Belgian Institute of Natural Sciences, Brussels, Belgium for loaning us the specimens of P. teres described by Heydari et al. (2014a) from Iran. We also wish to thank Dr. Johannes Helder from the Wageningen University for making available the photographic documentation of P. teres individuals from the Netherlands and for providing information that sequences of 18S rDNA for that species available in GenBank (FJ040484, KJ636337, KJ636338) were derived from specimens collected in the Netherlands.


  1. Aballay, E., & Eriksson, B. (2006). Trichodorid nematodes in the central area of Chile. Nematologia Mediterranea, 34, 43–48.Google Scholar
  2. Bik, H. M., Hawkins, L. E., Hughes, J. A., & Lambshead, J. D. (2009). Rapid decline of PCR amplification from genomic extracts of DESS-preserved, slide-mounted nematodes. Nematology, 11, 827–834.CrossRefGoogle Scholar
  3. Boutsika, K., Phillips, M. S., MacFarlane, S. A., Brown, D. J. F., Holeva, R. C., & Blok, V. C. (2003). Molecular diagnostics of trichodorid nematodes and their associated tobacco rattle virus (TRV). Plant Pathology, 53, 110–116.CrossRefGoogle Scholar
  4. Decraemer, W. (1995). The family Trichodoridae: stubby root and virus vector nematodes. Dordrecht: Kluwer Academic Publishers 360 pp.CrossRefGoogle Scholar
  5. Decraemer, W., Radivojević, M., & De La Peña, E. (2008). Trichodoridae (Nematoda: Triplonchida) from the Tara National Park, Serbia, and proposal of Trichodorus pseudobursatus n.Sp. Nematology, 10, 405–431.CrossRefGoogle Scholar
  6. Duarte, I. M., Almeida, M. T. M., Brown, D. J. F., Marques, I., Neilson, R., & Decraemer, W. (2010). Phylogenetic relationships, based on SSU rDNA sequences, among the didelphic genera of the family Trichodoridae from Portugal. Nematology, 12, 171–180.CrossRefGoogle Scholar
  7. Duarte, I. M., Almeida, M. T. M., Duarte, M. M., Brown, D. J. F., & Neilson, R. (2011). Molecular diagnosis of trichodorid species from Portugal. Plant Pathology, 60, 586–594.CrossRefGoogle Scholar
  8. Fauna Europea. (2013). Fauna Europea subversion 2.6c-22. Web Service available online at
  9. Hall, T.A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98; The Find Model web implementation:
  10. Heydari, R., Tanha Maafi, Z., Omati, F., & Decraemer, W. (2014a). First report of Paratrichodorus teres (Diphtherophorina, Trichodoridae) from Iran. Australasian Plant Disease Notes. doi: 10.1007/s13314-014-0131-4.Google Scholar
  11. Heydari, R., Tanha Maafi, Z., & Decraemer, W. (2014b). Morphological and molecular characterization of Trichodorus golestanensis (Nematoda: Trichodoridae), a new species from Iran. European Journal of Plant Pathology, 140, 329–340.CrossRefGoogle Scholar
  12. Holeva, R., Phillips, M. S., Neilson, R., Brown, D. J. F., Young, V., Boutsika, K., & Blok, V. C. (2006). Real-time PCR detection and quantification of vector trichodorid nematodes and tobacco rattle virus. Molecular and Cellular Probes, 20, 203–211.CrossRefPubMedGoogle Scholar
  13. Hooper, D. J. (1962). Three new species of Trichodorus (Nematoda: Dorylaimoidea) and observation on T. minor Colbran, 1956. Nematologica, 7, 273–280.CrossRefGoogle Scholar
  14. Karanastasi, E., Decraemer, W., Kyriakopoulou, P. E., & Neilson, R. (2005). First report of the stubby-root nematode Paratrichodorus teres associated with artichoke (Cynara scolymus) in Greece. Disease Notes, 89(6), 685.Google Scholar
  15. Koressaar, T., & Remm, M. (2007). Enhancements and modifications of primer design program Primer3. Bioinformatics, 23(10), 1289–1291.CrossRefPubMedGoogle Scholar
  16. Kuiper, K., & Loof, P. A. A. (1962). Trichodorus flevensis n. Sp. (Nematoda: Enoplida), a plant nematode from new polder soil. Verslagen en Mededelingen van de Plantenziektenkundige Dienst te Wageningen, 136, 193–200.Google Scholar
  17. Kumari, S., & Subbotin, S. A. (2012). Molecular characterization and diagnostics of stubby root and virus vector nematodes of the family Trichodoridae (Nematoda: Triplonchida) using ribosomal RNA genes. Plant Pathology, 61, 1021–1031.CrossRefGoogle Scholar
  18. Loof, P. A. A. (1965). Trichodorus anemones n. Sp. with a note on T. teres Hooper, 1962 (Nematoda: Enoplida). Verslagen en Mededelingen van de Plantenziektenkundige Dienst te Wageningen, 142, 132–136.Google Scholar
  19. Loof, P. A. A. (1975). Taxonomy of Trichodoridae. In F. Lamberti, C. E. Taylor, & J. W. Seinhorst (Eds.), Nematode vectors of plant viruses (pp. 103–127). Plenum Press: London & New York.CrossRefGoogle Scholar
  20. Miller, M. A., Pfeiffer, W., Schwartz, T. (2010). Creating the CIPRES Science Gateway for Inference of Large Phylogenetic Trees. In SC10 Workshop on Gateway Computing Environments (GCE10).Google Scholar
  21. Ploeg, A. T., & Decraemer, W. (1996). The occurrence and distribution of trichodorid nematodes and their associated tobraviruses in Europe and the former soviet union. Nematologica, 43, 228–251.CrossRefGoogle Scholar
  22. Ploeg, A. T., Brown, D. J. F., & Robinson, D. J. (1992). The association between species of Trichodorus and Paratrichodorus vector nematodes and serotypes of tobacco rattle tobravirus. Annals of Applied Biology, 121, 619–630.CrossRefGoogle Scholar
  23. Ploeg, A. T., Frans, C. Z., & Maas, P. W. T. (1996). Transmission efficiency of five tobravirus strains by Paratrichodorus teres. European Journal of Plant Pathology, 102, 123–126.CrossRefGoogle Scholar
  24. Posada, D., & Crandall, K. A. (1998). MODELTEST: testing the model of DNA substitution. Bioinformatics, 14(9), 817–818.CrossRefPubMedGoogle Scholar
  25. Rambaut, A., Suchard, M. A., Xie, D., Drummond, A. J. (2014). Tracer v.1.6, available from
  26. Riga, E., & Neilson, R. (2005). First report of the stubby-root nematode, Paratrichodorus teres, from potato in the Columbia basin of Washington state. Disease notes, 89(12), 1361.Google Scholar
  27. Riga, E., Larsen, R., Eastwell, K., Guerra, N., Guerra, L., & Crosslin, J. M. (2009). Rapid detection of tobacco rattle tobravirus in viruliferous Paratrichodorus allius from greenhouse and field specimens. Journal of Nematology, 41, 60–63.PubMedPubMedCentralGoogle Scholar
  28. Ronquist, F., & Huelsenbeck, J. P. (2003). MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574. doi: 10.1093/bioinformatics/btg180.CrossRefPubMedGoogle Scholar
  29. Seinhorst, J. W. (1959). A rapid method for the transfer of nematodes from fixative to anhydrous glycerine. Nematologica, 4, 67–69.CrossRefGoogle Scholar
  30. Siddiqi, M. R. (1974). Systematics of the genus Trichodorus Cobb, 1913 (Nematoda: Dorylaimida), with descriptions of three new species. Nematologica, 19, 259–278.Google Scholar
  31. Stamatakis, A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30(9), 1312–1313 doi: 10.1093/bioinformatics/btu033.
  32. Taylor, C. E. & Brown, D. J. F. (1997). Nematode vectors of plant viruses. Wallingford, UK, CABI Publishing, 286 pp.Google Scholar
  33. Untergasser, A., Cutcutache, I., Koressaar, T., Ye, J., Faircloth, B. C., Remm, M., & Rozen, S. G. (2012). Primer3 – new capabilities and interfaces. Nucleic Acids Research, 40(15), e115.CrossRefPubMedPubMedCentralGoogle Scholar
  34. van der Wilk, F., Korsman, M., & Zoon, F. (1994). Detection of tobacco rattle virus in nematodes by reverse transcription and polymerase chain reaction. European Journal of Plant Pathology, 100, 109–122.CrossRefGoogle Scholar
  35. van Hoof, H. A. (1962). Trichodorus pachydermus and T. teres, vectors of the early browning virus of peas. Tijdschrift Plantenziekten, 68, 391–396.Google Scholar
  36. van Megen, H., van den Elsen, S., Holterman, M., Karssen, G., Mooyman, P., Bongers, T., Holovachov, O., Bakker, J., & Helder, J. (2009). A phylogenetic tree of nematodes based on about 1200 full-length small subunit ribosomal DNA sequences. Nematology, 11, 927–950.CrossRefGoogle Scholar
  37. Yoder, M., De Ley, I. T., King, I., Mundo-Ocampo, M., Mann, J., Blaxter, M., Poiras, L., & De Ley, P. (2006). DESS: a versatile solution for preserving morphology and extractable DNA of nematodes. Nematology, 8, 367–376.CrossRefGoogle Scholar

Copyright information

© Koninklijke Nederlandse Planteziektenkundige Vereniging 2017

Authors and Affiliations

  • Krassimira Ilieva-Makulec
    • 1
  • Katarzyna Rybarczyk-Mydłowska
    • 2
  • Grażyna Winiszewska
    • 2
  • Łukasz Flis
    • 2
  • Anna Tereba
    • 2
  • Katarzyna Kowalewska
    • 2
  • Tadeusz Malewski
    • 2
  1. 1.Institute of Ecology and BioethicsKardynał Stefan Wyszyński University in WarsawWarsawPoland
  2. 2.Museum and Institute of Zoology PASWarsawPoland

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