European Journal of Plant Pathology

, Volume 151, Issue 1, pp 155–172 | Cite as

Description and molecular phylogeny of one new and one known needle nematode of the genus Paralongidorus (Nematoda: Longidoridae) from grapevine in Portugal using integrative approach

  • Carlos Gutiérrez-Gutiérrez
  • Manuel Mota
  • Pablo Castillo
  • Margarida Teixeira Santos
  • Juan E. Palomares-Rius
Article

Abstract

A new and a known longidorid nematode, Paralongidorus lusitanicus n. sp. and Paralongidorus plesioepimikis, are described and illustrated from populations extracted from soil associated with grapevine (Vitis vinifera L.) from Escaroupim and Pó (central-Western Portugal), respectively. The new needle nematode P. lusitanicus n. sp. is characterised by a very large body size (8072–12,022 μm), an expanded and rounded lip region, ca 30 μm wide, with a clear constriction followed by a depression posterior to the amphidial aperture, amphidial fovea very large (11.0–19.0 μm), stirrup-shaped, with conspicuous slit-like aperture as shown in scanning electron microscopy studies, a very long and flexible odontostyle (180.0–223.0 μm), guiding ring located at 28.0–41.5 μm from anterior end, vulva anterior to the mid-body (34–41%), a dorsally convex-conoid tail with rounded terminus (29–42 μm long), bearing two or three pairs of caudal pores and males common (ratio 1:1.6 females) with spicules ca 80 μm long. Morphological and morphometric traits for P. plesioepimikis fit well with the original description, and is reported for the first time in Portugal. Integrative diagnosis of both species was completed with molecular data obtained using D2-D3 expansion segments of 28S rDNA, ITS1-rDNA and partial 18S–rDNA. The phylogenetic relationships of these species with other Paralongidorus spp. using these three molecular markers indicated that P. lusitanicus n. sp. clustered together with other Paralongidorus spp. forming a sister clade with P. plesioepimikis, both of them sharing a large body, long odontostyle, an anteriorly located vulva and an expanded and rounded lip region with a clear constriction followed by a depression posterior to the amphidial aperture.

Keywords

Bayesian inference Longidorids Paralongidorus Phylogeny rDNA Taxonomy 

Notes

Acknowledgements

This research was financially supported by FCT - Foundation for Science and Technology postdoctoral fellowship SFRH/ BPD/95315/2013 and FEDER Funds through the Operational Programme for Competitiveness Factors - COMPETE and National Funds through FCT under the Strategic Projects PEst-C/AGR/UI0115/2011 and PEst-OE/ AGR/UI0115/2014 (Portugal). This research is partially supported by grant AGR-136 from ‘Consejería de Economía, Innvovación y Ciencia’ from Junta de Andalucía, and Union Europea, Fondo Europeo de Desarrollo regional, “Una manera de hacer Europa”. Authors thank A. Candeias from HERCULES Laboratory, Universidade de Évora and J. A. Paulo Mirão from Instituto de Ciências da Terra (ICT) for their help with SEM studies, I. Ferreira and G. Albarrán Madrigal from Instituto de Ciências Agrárias e Ambientais Mediterrânicas (ICAAM)-Universidade of Évora for the excellent technical assistance and C. Cantalapiedra-Navarrete (IAS-CSIC) for critical reading of the manuscript before submission and for the excellent technical assistance.

Compliance with Ethical Standards

Conflict of interest

All authors certify that 1) they do not have any actual or potential conflict of interest, 2) the study described is original and has not been published previously, and is not under consideration for publication elsewhere, 3) all prevailing local, national and international regulations and conventions, and normal scientific ethical practices, have been respected. We also certify that all authors have reviewed the manuscript and approved the final version of manuscript before submission.

Research involving Human Participants and/or Animals

No specific permits were required for the described fieldwork studies. Permission for sampling the vineyards was granted by the landowner. The sites are not protected in any way.

Informed Consent

All the authors certify that the work carried out in this research followed the principles of ethical and professional conduct have been followed. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

References

  1. Abolafia, J., Liébanas, G., & Peña-Santiago, R. (2002). Nematodes of the order Rhabditida from Andalucia Oriental, Spain. The subgenus Pseudacrobeles Steiner, 1938, with description of a new species. Journal of Nematode Morphology and Systematic, 4, 137–154.Google Scholar
  2. Altherr, E. (1963). Contribution a la connaissance de la faune des sables submerges en Lorraine. Nematodes. Ann. Speleologie, 18, 53–98.Google Scholar
  3. Andrássy, I. (1986). Egy új tufonálféreg faj Magyarországról: Paralongidorus rex sp. n. (Nematoda: Longidoridae). Állattani Közlemények, 73, 115–118.Google Scholar
  4. Archidona-Yuste, A., Navas-Cortés, J. A., Cantalapiedra-Navarrete, C., Palomares-Rius, J. E., & Castillo, P. (2016a). Unravelling the biodiversity and molecular phylogeny of needle nematodes of the genus Longidorus (Nematoda: Longidoridae) in olive and a description of six new species. PLoS One, 11, e0147689.  https://doi.org/10.1371/journal.pone.0147689.CrossRefPubMedCentralPubMedGoogle Scholar
  5. Archidona-Yuste, A., Navas-Cortés, J. A., Cantalapiedra-Navarrete, C., Palomares-Rius, J. E., & Castillo, P. (2016b). Remarkable diversity and prevalence of dagger nematodes of the genus Xiphinema Cobb, 1913 (Nematoda: Longidoridae) in olives revealed by integrative approaches. PLoS One, 11, e0165412.  https://doi.org/10.1371/journal.pone.0165412.CrossRefPubMedCentralPubMedGoogle Scholar
  6. Barsi, L., & Luca, F. D. (2017). Morphological and molecular characterisation of Paralongidorus francolambertii sp. n. (Nematoda: Longidoridae) from Serbia. Nematology, 19, 681–695.  https://doi.org/10.1163/15685411-00003080.CrossRefGoogle Scholar
  7. Barsi, L., Répási, V., Nagy, P., Agostinelli, A., & Coiro, M. I. (2007). A new record of Paralongidorus rex Andrássy, 1986 from Hungary and comments on head morphology of P. maximus (Bütschli, 1874) Siddiqi, 1964 (Nematoda: Dorylaimida). Nematologia Mediterranea, 35, 61–67.Google Scholar
  8. Bravo, M. A., & Lemos, R. M. (1997). Longidorus, Paralongidorus and Xiphinema in Portugal. In M. S. Santos, A. de, I. O. Abrantes, D. J. F. Brown, & R. M. Lemos (Eds.), An introduction to virus vector nematodes and their associated viruses. Instituto do Ambiente e Vida (pp. 421–441). Coimbra: Universidade de Coimbra.Google Scholar
  9. Castillo, P., Vovlas, N., Subbotin, S., & Troccoli, A. (2003). A new root-knot nematode, Meloidogyne baetica n. sp. (Nematoda: Heteroderidae), parasitizing wild olive in Southern Spain. Phytopathology, 93, 1093–1102.CrossRefPubMedGoogle Scholar
  10. Castresana, J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution, 17, 540–552.CrossRefPubMedGoogle Scholar
  11. Cherry, T., Szalanski, T. C., Todd, T. C., & Powers, T. O. (1997). The internal transcribed spacer region of Belonolaimus (Nemata: Belonolaimidae). Journal of Nematology, 29, 23–29.Google Scholar
  12. Coomans, A. (1985). A phylogenetic approach to the classification of the Longidoridae (Nematoda: Dorylaimida). Agriculture, Ecosystems and Environment, 12, 335–354.CrossRefGoogle Scholar
  13. Coomans, A. (1996). Phylogeny of the longidoridae. Russian Journal of Nematology, 4, 51–60.Google Scholar
  14. Dalmasso, A. (1969). Étude anatomique et taxonomique des genres Xiphinema, Longidorus et Paralongidorus (Nematoda: Dorylaimida). Mémoires du Muséum National d’Histoire Naturelle, Nouvelle Série, A. Zoologie, 61, 34–82.Google Scholar
  15. Darriba, D., Taboada, G. L., Doallo, R., & Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9, 772.CrossRefPubMedCentralPubMedGoogle Scholar
  16. De Ley, P., Félix, M. A., Frisse, L. M., Nadler, S. A., Sternberg, P. W., & Thomas, K. W. (1999). Molecular and morphological characterization of two reproductively isolated species with mirror-image anatomy (Nematoda: Cephalobidae). Nematology, 1, 591–612.CrossRefGoogle Scholar
  17. Decraemer, W., & Robbins, R. T. (2007). The who, what and where of Longidoridae and Trichodoridae. Journal of Nematology, 39, 295–297.PubMedCentralPubMedGoogle Scholar
  18. Escuer, M., & Arias, M. (1997). Paralongidorus iberis sp. n. and P. monegrensis sp. n. from Spain with a polytomous key to the species of the genus Paralongidorus Siddiqi, Hooper & Khan, 1963 (Nematoda: Longidoridae). Fundamental and Applied Nematology, 20, 135–148.Google Scholar
  19. Flegg, J. J. M. (1967). Extraction of Xiphinema and Longidorus species from soil by a modification of Cobb’s decanting and sieving technique. Annals of Applied Biology, 60, 429–437.CrossRefGoogle Scholar
  20. Gutiérrez-Gutiérrez, C., Bravos, M. A., Santos, M. T., Vieira, P., & Mota, M. (2016). An update on the genera Longidorus, Paralongidorus and Xiphinema (Family Longidoridae) in Portugal. Zootaxa, 4189, 99–114.CrossRefGoogle Scholar
  21. Gutiérrez-Gutiérrez, C., Cantalapiedra-Navarrete, C., Montes-Borrego, M., Palomares-Rius, J. E., & Castillo, P. (2013a). Molecular phylogeny of the nematode genus Longidorus (Nematoda: Longidoridae) with description of three new species. Zoological Journal of the Linnean Society, 167, 473–500.CrossRefGoogle Scholar
  22. Gutiérrez-Gutiérrez, C., Cantalapiedra-Navarrete, C., Remesal, E., Palomares-Rius, J. E., Navas-Cortés, J. A., & Castillo, P. (2013b). New insight into the identification and molecular phylogeny of dagger nematodes of the genus Xiphinema (Nematoda: Longidoridae) with description of two new species. Zoological Journal of the Linnean Society, 169, 548–579.CrossRefGoogle Scholar
  23. Gutiérrez-Gutiérrez, C., Palomares-Rius, J. E., Cantalapiedra-Navarrete, C., Landa, B. B., & Castillo, P. (2011). Prevalence, polyphasic identification, and molecular phylogeny of dagger and needle nematodes infesting vineyards in southern Spain. European Journal of Plant Pathology, 129, 427–453.CrossRefGoogle Scholar
  24. Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98NT. Nucleic Acids Symposium Serial, 41, 95–98.Google Scholar
  25. He, Y., Subbotin, S., Rubtsova, T. V., Lamberti, F., Brown, D. J. F., & Moens, M. (2005). A molecular phylogenetic approach to Longidoridae (Nematoda: Dorylaimida). Nematology, 7, 111–124.CrossRefGoogle Scholar
  26. Heyns, J. (1975). Paralongidorus maximus. CIH Description of plant parasitic nematodes, Set 5, No. 75. St (4pp). Albans, UK: Commonwealth Institute of Helminthology.Google Scholar
  27. Holterman, M., Van Der Wurff, A., Van Den Elsen, S., Van Megen, H., Bongers, T., Holovachov, O., & Helder, J. (2006). Phylum-wide analysis of SSU rDNA reveals deep phylogenetic relationships among nematodes and accelerated evolution toward crown clades. Molecular Phylogenetics Evolution, 23, 1792–1800.Google Scholar
  28. Hunt, D. J. (1993). Aphelenchida, Longidoridae and Trichodoridae: Their systematics and bionomics (352 pp). Wallingford: CABI Publishing.Google Scholar
  29. Jairajpuri, M. S., & Ahmad, W. (1992). Dorylaimida. Freeliving, predaceous and plant-parasitic nematodes. New Delhi, India: Oxford & IBH Publishing Co..Google Scholar
  30. Jocobs, P. J. F., & Heyns, J. (1982). Siddiqia species from sugar cane in Natal (Nematoda: Longidoridae). Phytophylactica, 14, 169–178.Google Scholar
  31. Jones, A. T., Brown, D. J. F., McGavin, W. J., Rūdel, M., & Altmayer, B. (1994). Properties of an unusual isolate of raspberry ringspot virus from grapevine in Germany and evidence for its possible transmission by Paralongidorus maximus. Annals of Applied Biology, 124, 283–300.CrossRefGoogle Scholar
  32. Katoh, K., & Standley, D. M. (2013). MAFFT multiple sequence alignment 542 software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30, 772–780.CrossRefPubMedCentralPubMedGoogle Scholar
  33. Kornobis, F. W., Susulovska, S., Susulovsky, A., & Subbotin, S. A. (2015). Morphological and molecular characterisation of Paralongidorus rex Andrássy, 1986 (Nematoda: Longidoridae) from Poland and Ukraine. European Journal of Plant Pathology, 141, 385–395.CrossRefGoogle Scholar
  34. Kumari, S. (2014). Characterization of Longidorus caespiticola (Nematoda: Longidoridae) from the Czech Republic. Helminthologia, 51, 153–157.CrossRefGoogle Scholar
  35. Lamberti, F., Choleva, B., & Agostinelli, A. (1983). Longidoridae from Bulgaria (Nematoda, Dorylaimida) with descriptions of three new species of Longidorus and two new species of Xiphinema. Nematologia Mediterranea, 11, 49–72.Google Scholar
  36. Lazarova, S. S., Malloch, G., Oliveira, C. M. G., Hübschen, J., & Neilson, R. (2006). Ribosomal and mitochondrial DNA analyses of Xiphinema americanum-group populations. Journal of Nematology, 38, 404–410.PubMedCentralPubMedGoogle Scholar
  37. Lazarova, S., Peneva, V., & Kumari, S. (2016). Morphological and molecular characterisation, and phylogenetic position of X. browni sp. n., X. penevi sp. n. and two known species of Xiphinema americanum-group (Nematoda, Longidoridae). ZooKeys, 574, 1–42.CrossRefGoogle Scholar
  38. Lišková, M., & Brown, D. J. F. (1998). Longidoridae (Nematoda) associated with walnut trees (Juglans regia L.) in Slovak Republic. Helminthologia, 35, 93–99.Google Scholar
  39. Lišková, M., & Brown, D. J. F. (1999). The occurrence of Longidoridae (Nematoda) in forests in the Slovak Republic. Helminthologia, 36, 49–56.Google Scholar
  40. Lišková, M., & Brown, D. J. F. (2003). Longidoridae (Nematoda: Dorylaimida) in the Slovak Republic. Helminthologia, 40, 165–172.Google Scholar
  41. Lišková, M. (1995). Nematode-virus vectors in the rhizosphere of fruit trees and soft fruits in Slovakia. Helminthologia, 32, 43–48.Google Scholar
  42. Macara, A. M. (1994). Nematodes associated with forest plants in Portugal (no período de 1987-1992). Revista de Ciências Agrárias, 17, 77–126.Google Scholar
  43. Page, R. D. (1996). TreeView: an application to display phylogenetic trees on personal computers. Computer Applications in the Bioscience, 12, 357–358.Google Scholar
  44. Palomares-Rius, J. E., Cantalapiedra-Navarrete, C., & Castillo, P. (2014). Cryptic species in plant-parasitic nematodes. Nematology, 16, 1105–1118.CrossRefGoogle Scholar
  45. Palomares-Rius, J. E., Cantalapiedra-Navarrete, C., Gutiérrez-Gutiérrez, C., Liébanas, G., & Castillo, P. (2013). Morphological and molecular characterisation of Paralongidorus plesioepimikis n. sp. (Nematoda: Longidoridae) from Southern Spain. Nematology, 15, 363–378.CrossRefGoogle Scholar
  46. Palomares-Rius, J. E., Subbotin, S. A., Landa, B. B., Vovlas, N., & Castillo, P. (2008). Description and molecular characterisation of Paralongidorus litoralis sp. n. and P. paramaximus Heyns, 1965 (Nematoda: Longidoridae) from Spain. Nematology, 10, 87–101.CrossRefGoogle Scholar
  47. Pedram, M., Namjoo, S., Pourjam, E., Atighi, M. R., Cantalapiedra-Navarrete, C., Liébanas, G., Palomares-Rius, J. M., & Castillo, P. (2012). Molecular and morphological characterisation of Paralongidorus iranicus n. sp. and Paralongidorus bikanerensis (Lal & Mathur, 1987) Siddiqi, Baujard & Mounport, 1993 (Nematoda: Longidoridae) from Iran. Nematology, 14, 427–443.CrossRefGoogle Scholar
  48. Robbins, R. T., Brown, D. J. F., Halbrendt, J. M., & Vrain, T. C. (1995). Compendium of Longidorus juvenile stages with observation on L. pisi, L. taniwha and L. diadecturus (Nematoda: Longidoridae). Systematic Parasitology, 32, 33–52.CrossRefGoogle Scholar
  49. Robbins, R. T., Brown, D. J. F., Halbrendt, J. M., & Vrain, T. C. (1996). Compendium of juvenile stages of Xiphinema species (Nematoda: Longidoridae). Russian Journal of Nematology, 4, 163–171.Google Scholar
  50. Roca, F., Lamberti, F., & Agostinelli, A. (1988). I. Longidoridae (Nematoda, Dorylaimida) delle regioni italiane. VII. Il Piemonte e la Valle D’Aosta. Nematologia Mediterranea, 16, 35–51. Google Scholar
  51. Seinhorst, J.W. (1966). Killing nematodes for taxonomic study with hot f.a. 4:1. Nematologica, 12, 178.Google Scholar
  52. Ronquist, F., & Huelsenbeck, J. P. (2003). MRBAYES3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.Google Scholar
  53. Siddiqi, M. R., Baujard, P., & Mounport, D. (1993). Descriptions of Paratylenchus pernoxius sp. n. and Paralongidorus duncani sp. n. from Senegal, and the synonymization of Longidoroides with Paralongidorus. Afro-Asian Journal of Nematology, 3, 81–89.Google Scholar
  54. Subbotin, S. S., Stanley, J. D., Ploeg, A. T., Maafi, Z. T., Tzortzakakis, E. A., Chitambar, J. J., Palomares-Rius, J. E., Castillo, P., & Inserra, R. N. (2015). Characterisation of populations of Longidorus orientalis Loof, 1982 (Nematoda: Dorylaimida) from date palm (Phoenix dactylifera L.) in the USA and other countries and incongruence of phylogenies inferred from ITS1 rRNA and coxI genes. Nematology, 17, 459–477.CrossRefGoogle Scholar
  55. Subbotin, S., Rogozhin, E., & Chizhov, V. (2014). Molecular characterisation and diagnostics of some Longidorus species (Nematoda: Longidoridae) from Russia and other countries using rRNA genes. European Journal of Plant Pathology, 138, 377–390.CrossRefGoogle Scholar
  56. Taylor, C. E., & Brown, D. J. F. (1997). Nematode vectors of plant viruses (296 pp). Wallingford, UK: CABI.Google Scholar
  57. Tulaganov, A. T. (1937). Nematode fauna of tomato Lycopersicon esculentum Mill, and the surrounding soil. Tr. Uzb. Gos. Univ. Samarakanda, 8, 63–102.Google Scholar
  58. Vrain, T. C., Wakarchuk, D. A., Levesque, A. C., & Hamilton, R. I. (1992). Intraspecific rDNA Restriction Fragment Length Polymorphism in the Xiphinema americanum group. Fundamental and Applied Nematology, 15, 563–573.Google Scholar

Copyright information

© Koninklijke Nederlandse Planteziektenkundige Vereniging 2017

Authors and Affiliations

  • Carlos Gutiérrez-Gutiérrez
    • 1
  • Manuel Mota
    • 1
    • 2
  • Pablo Castillo
    • 3
  • Margarida Teixeira Santos
    • 4
  • Juan E. Palomares-Rius
    • 3
  1. 1.NemaLab/ICAAM, Instituto de Ciências Agrárias e Ambientais Mediterrânicas & Departamento de BiologiaUniversidade de ÉvoraÉvoraPortugal
  2. 2.Departamento Ciências da VidaUniversidade Lusófona de Humanidades e Tecnologias, EPCVLisbonPortugal
  3. 3.Institute for Sustainable Agriculture (IAS), Spanish National Research Council (CSIC), Campus de Excelencia Internacional Agroalimentario, ceiA3CórdobaSpain
  4. 4.Instituto Nacional de Investigação Agrária e Veterinária (INIAV), Quinta do MarquêsOeirasPortugal

Personalised recommendations