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European Journal of Plant Pathology

, Volume 151, Issue 4, pp 875–889 | Cite as

Investigation of resistance to Pratylenchus penetrans and P. thornei in international wheat lines and its durability when inoculated together with the cereal cyst nematode Heterodera avenae, using qPCR for nematode quantification

  • Fouad Mokrini
  • Nicole Viaene
  • Lieven Waeyenberge
  • Abdelfattah A. Dababat
  • Maurice Moens
Article
  • 184 Downloads

Abstract

The root lesion nematodes Pratylenchus penetrans and P. thornei cause high yield losses in rain-fed wheat fields in Morocco, as well as worldwide. Growing resistant varieties is one of the most effective methods for controlling nematodes. Therefore, a collection of 14 lines of spring wheat and 11 lines of winter wheat (Triticum aestivum and T. durum), provided by CIMMYT, were screened for resistance to P. penetrans and P. thornei in tubes (15 × 20 × 120 mm3) under greenhouse conditions. The resistance level was evaluated based on the numbers of nematodes extracted from roots and soil 9 weeks after infestation. Three lines (L9, L12 and L13) were found moderately resistant (reproduction factor < 1) to P. thornei and one of these (L9) was also moderately resistant to P. penetrans. To investigate the durability of this resistance, we co-inoculated juveniles of Heterodera avenae, a cereal cyst nematode widely present in Moroccan wheat fields, and assessed the reproduction of both lesion nematodes on the three lines. Our results showed that the lines L9, L12, L13 remained moderately resistant in the presence of H. avenae. Moreover, the numbers of Pratylenchus spp. were generally lower when plants were co-inoculated with H. avenae. The number of P. penetrans or P. thornei were determined visually using a microscope and with a qPCR assay. The counts with qPCR were even lower than microscopic counts. These findings on resistance are promising but the field performance of these lines against root lesion nematode attacks should be evaluated.

Keywords

Co-inoculation Durability qPCR Screening 

Notes

Acknowledgements

The first author thanks the awarding of a PhD scholarship from the Islamic Development Bank (IDB) and a Special Research Fund (BOF) scholarship from Ghent University. The authors wish to thank warmly Ms. Nancy de Sutter for maintaining the nematode populations.

Compliance with ethical standards

This study does not involve human participants nor vertebrate animals, so no informed consent is needed.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Berry, S. D., Fargette, M., Spaull, V. W., Morand, S., & Cadet, P. (2008). Detection and quantification of root-knot nematode (Meloidogyne javanica), lesion nematode (Pratylenchus zeae) and dagger nematode (Xiphinema elongatum) parasites of sugarcane using real-time PCR. Molecular and Cellular Probes, 22, 168–176.CrossRefPubMedGoogle Scholar
  2. Bertrand, B., Cilas, C., Hervé, G., Anthony, F., Etienne, H., & Villain, L. (1998). Relations entre les populations des nématodes Meloidogyne exigua et Pratylenchus spp. dans les racines de Coffea arabica au Costa Rica. Plantations Recherche Développement, 5, 279–286.Google Scholar
  3. Bradley, E. B., & Duffy, M. (1982). The value of plant resistance to soybean cyst nematodes: A case study of Forrest soybeans. NRS staff report. Washington, DC: US Department of Agriculture.Google Scholar
  4. Brinkman, E. P., Duyts, H., & van der Putten, W. H. (2005). Competition between endoparasitic nematodes and effect on biomass of Ammophila arenaria (marram grass) as affected by timing of inoculation and plant age. Nematology, 7, 169–178.CrossRefGoogle Scholar
  5. Dababat, A., Pariyar, S., Nicol, J. M., & Duveiller, E. (2011). Cereal cyst nematodes: An unnoticed threat to global cereal production. CGIAR SP-IPM technical innovation brief 11SP-IPM secretariat, (web page: www.spimp.cgiar.org.).
  6. Dababat, A. A., Erginbas-Orakci, G., Toktay, H., Imren, M., Akın, B., Braun, H. J., Dreisigacker, S., Elekcioglu, I. H., & Morgounov, A. (2014). Resistance of winter wheat to Heterodera filipjevi in Turkey. Turkish Journal of Agriculture and Forestry, 38, 180–186.CrossRefGoogle Scholar
  7. Dababat, A. A., Imren, M., Erginbas-Orakci, G., Ashrafi, S., Yavuzaslanoglu, E., Toktay, T., Pariyar, S. H., Elekcioglu, I. H., Morgounov, A., & Mekete, T. (2015). The importance and management strategies of cereal cyst nematodes, Heterodera spp., in Turkey. Euphytica, 202, 173–188.CrossRefGoogle Scholar
  8. Dababat, A. A., Hugo Ferney, G.-B., Erginbas-Orakci, G., Dreisigacker, S., Imren, M., Toktay, H., Elekcioglu, H. I., Mekete, M., Nicol, J. M., Ansari, O., & Ogbonnaya, F. (2016). Association analysis of resistance to cereal cyst nematodes (Heterodera avenae) and root lesion nematodes (Pratylenchus neglectus and P. thornei) in CIMMYT advanced spring wheat lines for semi-arid conditions. Breeding Science, 66(5), 692–702.CrossRefPubMedPubMedCentralGoogle Scholar
  9. Eisenback, J. D. (1985). Interactions among concomitant populations of nematodes. In J. N. Sasser & C. C. Carter (Eds.), An advanced treatise on Meloidogyne. Vol 1, Biology and control (pp. 193–213). Raleigh: Department of Plant Pathology, North Carolina State University.Google Scholar
  10. Eisenback, J. D. (1993). Interactions between nematodes in cohabitance. In N. W. Khan (Ed.), Nematode interactions (pp. 134–174). London: Chapman & Hall.CrossRefGoogle Scholar
  11. Estores, R. A., & Chen, T. A. (1972). Interactions of Pratylenchus penetrans and Meloidogyne incognita as coinhabitants in tomato. Journal of Nematology, 4, 170–174.PubMedPubMedCentralGoogle Scholar
  12. Gay, C., & Bird, G. W. (1973). Influence of concomitant Pratylenchus brachyurus and Meloidogyne spp. on root penetration and population dynamics. Journal of Nematology, 5, 212–217.PubMedPubMedCentralGoogle Scholar
  13. Hendrickx, G. (1995). An automated apparatus for extracting free-living nematode stages from soil. Nematologica, 41, 308.Google Scholar
  14. Hervé, G., Bertrand, B., Villain, L., Licardié, D., & Cilas, C. (2005). Distribution analyses of Meloidogyne spp. and Pratylenchus coffeae Sensu Lato in coffee plots in Costa Rica and Guatemala. Plant Pathology, 54, 471–475.CrossRefGoogle Scholar
  15. Holterman, M., van der Wurff, A., van den Elsen, S., van Megen, H., Bongers, T., Holovachov, O., Bakker, J., & Helder, J. (2006). Phylum-wide analysis of SSU rDNA reveals deep phylogenetic relationships among nematodes and accelerated evolution toward crown clades. Molecular Biology and Evolution, 23, 1792–1800.CrossRefPubMedGoogle Scholar
  16. Keil, T., Laubach, E., Sharma, S., & Jung, M. (2009). Screening for resistance in the primary and secondary gene pool of barley against the root-lesion nematode Pratylenchus neglectus. Plant Breeding, 128, 436–442.CrossRefGoogle Scholar
  17. Khan, M. W. (1993). Mechanisms of interactions between nematodes and other plant pathogens. In M. W. Khan (Ed.), Nematode interactions (pp. 55–78). London: Chapman and Hall.CrossRefGoogle Scholar
  18. Kranti, K. V. V. S., & Kanwar, R. S. (2012). Evaluation of wheat varieties for resistance against Pratylenchus thornei and effect of sowing dates on its reproduction. Indian Journal of Nematology, 42, 34–37.Google Scholar
  19. Lamberti, F., Ciccarese, F., Sasanelli, N., Ambrico, A., Addabbo, T. D., & Schiavone, D. (2001). Relationships between plant parasitic nematodes and Verticillium dahlia on olive. Nematologia Mediterranea, 29, 3–9.Google Scholar
  20. Lasserre, F., Rivoal, R., & Cook, R. (1994). Interactions between Heterodera avenae and Pratylenchus neglectus on wheat. Journal of Nematology, 26, 336–344.PubMedPubMedCentralGoogle Scholar
  21. Melakeberhan, H. (1998). Pathogenicity of Pratylenchus penetrans, Heterodera glycines, and Meloidogyne incognita on soybean genotypes. Journal of Nematology, 30, 93–99.PubMedPubMedCentralGoogle Scholar
  22. Melakeberhan, H., & Dey, J. (2003). Competition between Heterodera glycines and Meloidogyne incognita or Pratylenchus penetrans: Independent infection rate measurements. Journal of Nematology, 35, 1–6.PubMedPubMedCentralGoogle Scholar
  23. Min, Y., Toyota, K., & Sato, E. (2012). A novel nematode diagnostic method using the direct quantification of major-parasitic nematodes in soil by real-time PCR. Nematology, 14, 265–276.CrossRefGoogle Scholar
  24. Moens, M., & Perry, R. N. (2009). Migratory plant endoparasitic nematodes: A group rich in contrasts and divergence. Annual Review of Phytopathology, 47, 313–332.CrossRefPubMedGoogle Scholar
  25. Mokrini, F., Abbad Andaloussi, F., Alaoui, Y., & Troccoli, A. (2009). Importance and distribution of the main cereal nematodes in Morocco. In I. T. Riley, J. M. Nicol, & A. A. Dababat (Eds.), Cereal cyst nematodes: status, research and outlook. Proceedings of the first workshop of the international cereal cyst nematode initiative, 21-23 October 2009, Antalya, Turkey (pp. 45–50). Addis Ababa, Ethiopia: International Maize and Wheat Improvement Centre (CIMMYT).Google Scholar
  26. Mokrini, F., Waeyenberge, L., Viaene, N., & Moens, M. (2012). Occurrence of nematodes of the Heterodera avenae group and Pratylenchus spp. on wheat and barley in Morocco. In Proceedings of the 31st international symposium of the European Society of Nematologists, 23-27 September 2012, Adana, Turkey (p. 107). Adana, Turkey: Cukurova University.Google Scholar
  27. Mokrini, F., Waeyenberge, L., Viaene, N., Abbad Andaloussi, F., & Moens, M. (2013). Quantitative detection of the root-lesion nematode Pratylenchus penetrans using real-time PCR. European Journal of Plant Pathology, 137(2), 403–413.CrossRefGoogle Scholar
  28. Mokrini, F., Waeyenberge, L., Viaene, N., Abbad Andaloussi, F., & Moens, M. (2014). β-1,4-endoglucanase gene suitable for the molecular quantification of the root- lesion nematode, Pratylenchus thornei. Nematology, 16(7), 789–796.CrossRefGoogle Scholar
  29. Mokrini, F., Waeyenberge, L., Viaene, N., Abbad Andaloussi, F., & Moens, M. (2016). Diversity of root-lesion nematodes (Pratylenchus spp.) associated with wheat (Triticum aestivum and T. durum) in Morocco. Nematology, 18(7), 781–801.CrossRefGoogle Scholar
  30. Moody, E. H., Lownsbery, B. F., & Ahmed, J. M. (1973). Culture of the root-lesion nematode Pratylenchus vulnus on carrot disks. Journal of Nematology, 19, 125–126.CrossRefGoogle Scholar
  31. Niblack, T. L., Hussey, R. S., & Boerma, H. R. (1986). Effects of interactions among Heterodera glycines, Meloidogyne incognita, and host genotypes on soybean yield and nematode population densities. Journal of Nematology, 18, 436–443.PubMedPubMedCentralGoogle Scholar
  32. Nicol, J. M., & Rivoal, R. (2008). Global knowledge and its application for the integrated control and management of nematodes on wheat. In A. Ciancio & K. G. Mukerji (Eds.), Integrated management and biocontrol of vegetable and grain crops nematodes (pp. 243–287). Dordrecht: Springer.Google Scholar
  33. Nicol, J., Rivoal, R., Taylor, S., & Zaharieva, M. (2003). Global importance of cyst (Heterodera spp.) and lesion nematodes (Pratylenchus spp.) on cereals: Distribution, yield loss, use of host resistance and integration of molecular tools. In R. Cook & D. J. Hunt (Eds.), Proceedings of the fourth international congress of nematology, 8-13 June 2002, Tenerife, Spain, Nematology monographs and perspectives 2 (pp. 1–19). Leiden: Brill.Google Scholar
  34. Nicol, J. M., Ogbonnaya, F., Singh, A. K., Bishnoi, S. P., Kanwar, R. S., Li, H. L., Chen, S. L., Peng, D. L., Bolat, N., Şahin, E., & Elekçioglu, I. H. (2009). Current global knowledge of the usability of the cereal cyst nematode resistant bread wheat germplasm through international germplasm exchange and evaluation. In I. T. Riley, J. M. Nicol, & A. A. Dababat (Eds.), Cereal cyst nematodes: status, research and outlook. Proceedings of the first workshop of the international cereal cyst nematode initiative, 21-23 October 2009, Antalya, Turkey (pp. 149–153). Addis Ababa, Ethiopia: International Maize and Wheat Improvement Centre (CIMMYT).Google Scholar
  35. Nombela, G., & Romero, D. (1999). Host response to Pratylenchus thornei of wheat line carrying the Cr2 gene for resistance to Heterodera avenae. Nematology, 1, 381–388.CrossRefGoogle Scholar
  36. O'Bannon, J. H., Radewald, J. D., Tomerlin, A. T., & Inserra, R. N. (1976). Comparative influence of Radopholus similis and Pratylenchus coffeae on citrus. Journal of Nematology, 8, 58–63.PubMedPubMedCentralGoogle Scholar
  37. OEPP/EPPO. (2013). PM7/119. Nematode extraction. OEPP/EPPO Bulletin, 43, 471–495.CrossRefGoogle Scholar
  38. Ophel-Keller, K., McKay, A., Hartley, D., Herdina, H., & Curran, J. (2008). Development of a routine DNA-based testing service for soilborne diseases in Australia. Australasian Plant Pathology, 37, 243–253.CrossRefGoogle Scholar
  39. Powell, N. T. (1979). Internal synergisms among organisms inducing disease. In J. G. Horsfall & E. B. Cowling (Eds.), Plant Disease IV (pp. 113–133). New York: Academic Press.Google Scholar
  40. Rivoal, R., Lasserre, F., & Cook, R. (1995). Consequences of longterm cropping with resistant cultivars on the population dynamics of the endoparastic nematodes Heterodera avenae and Pratylenchus neglectus in a cereal production ecosystem. Nematologica, 4, 516–529.CrossRefGoogle Scholar
  41. Roberts, P. A. (2002). Resistance to nematodes: Definitions, concepts and consequences. In J. L. Starr, J. Bridge, & R. Cook (Eds.), Plant resistance to parasitic nematodes (pp. 23–41). Wallingford: CAB International.CrossRefGoogle Scholar
  42. Şahin, E., Nicol, J. M., Elekcioglu, H., & Rivoal, R. (2009). Hatching of Heterodera filipjevi in controlled and natural temperature conditions in Turkey. Nematology, 12, 277–287.Google Scholar
  43. Sato, E., Min, Y. Y., Sgirakashi, T., Wada, S., & Toyota, K. (2007). Detection of the root- lesion nematode, Pratylenchus penetrans (cobb), in a nematode community using real- time PCR. Journal of Nematology, 37, 38–92.Google Scholar
  44. Shepherd, A. M. (1986). Extraction and estimation of cyst nematodes. In J. F. Southey (Ed.), Laboratory methods for work with plant and soil nematodes (pp. 51–58). London: Her Majesty's stationery office.Google Scholar
  45. Smiley, R. W., & Nicol, J. N. (2009). Nematodes which challenge global wheat production. In B. F. Carver (Ed.), Wheat science and trade (pp. 171–187). Ames: Wiley Blackwell.CrossRefGoogle Scholar
  46. Stetina, S. R., Russin, J. S., & McGawley, E. C. (1997). Replacement series: A tool for characterizing competition between phytoparasitic nematodes. Journal of Nematology, 29, 35–42.PubMedPubMedCentralGoogle Scholar
  47. Thompson, J. P., & Seymour, N. P. (2011). Inheritance of resistance to root-lesion nematode (P. thornei) in wheat landraces and cultivars from the West Asia and North Africa (WANA) region. Crop & Pasture Science, 62, 82–93.CrossRefGoogle Scholar
  48. Thompson, J. P., Brennan, P. S., Clewett, T. G., Sheedy, J. G., & Seymour, N. P. (1999). Progress in breeding wheat for tolerance and resistance to root-lesion nematode (Pratylenchus thornei). Australasian Plant Pathology, 28, 45–52.CrossRefGoogle Scholar
  49. Thompson, J. P., Owen, K. J., Stirling, G. R., & Bell, M. J. (2008). Root-lesion nematodes (Pratylenchus thornei and P. neglectus): A review of recent progress in managing a significant pest of grain crops in northern Australia. Australasian Plant Pathology, 37, 235–242.CrossRefGoogle Scholar
  50. Thompson, J. P., O’Reilly, M. M., & Clewett, T. G. (2009). Resistance to the root-lesion nematode Pratylenchus thornei in wheat landraces and cultivars from the West Asia and North Africa (WANA) region. Crop & Pasture Science, 60, 1209–1217.CrossRefGoogle Scholar
  51. Thompson, J. P., Clewett, T. G., Sheedy, J. G., Reen, R. A., O’Reilly, M. M., & Bell, K. L. (2010). Occurrence of root-lesion nematodes (Pratylenchus thornei and P. neglectus) and stunt nematode (Merlinius brevidens) in the northern grain region of Australia. Australasian of Plant Pathology, 39, 254–264.CrossRefGoogle Scholar
  52. Thompson, J. P., Clewett, T. G., & O’Reilly, M. M. (2015). Temperature response of root-lesion nematode (Pratylenchus thornei) reproduction on wheat cultivars has implications for resistance screening and wheat production. Annals of Applied Biology, 167, 1–10.CrossRefGoogle Scholar
  53. Toktay, H., Yavuzaslanoglu, E., Imren, M., Nicol, J. M., Elekcioglu, I. H., & Dababat, A. A. (2012). Screening for resistance to Heterodera filipjevi (Madzhidov) Stelter (Tylenchina: Heteroderidae) and Pratylenchus thornei (Sher & Allen) (Tylenchida: Pratylenchidae) sister lines of spring wheat. Turkish Journal of Entomology, 36, 455–461.Google Scholar
  54. Toumi, F., Waeyenberge, L., Viaene, N., Dababat, A. A., Nicol, J. M., Ogbonnaya, F., & Moens, M. (2013). Development of two species-specific primer sets to detect the cereal cyst nematodes Heterodera avenae and H. filipjevi. European Journal of Plant Pathology, 136, 613–624.CrossRefGoogle Scholar
  55. Umesh, K. C., Ferris, H., & Bayer, D. E. (1994). Competition between the plant-parasitic nematodes Pratylenchus neglectus and Meloidogyne chitwoodi. Journal of Nematology, 26, 286–295.PubMedPubMedCentralGoogle Scholar
  56. Vanstone, V. A., Rathjen, A. J., Ware, A. H., & Wheeler, R. D. (1998). Relationship between root lesion nematodes (Pratylenchus neglectus and P. thornei) and performance of wheat varieties. Australian Journal of Experimental Agriculture, 38, 181–189.CrossRefGoogle Scholar
  57. Vanstone, V. A., Hollaway, G. J., & Stirling, G. R. (2008). Managing nematode pests in the southern and western regions of the Australian cereal industry: Continuing progress in a challenging environment. Australasian Plant Pathology, 37, 220–234.CrossRefGoogle Scholar
  58. Wyss, U., & Zunke, U. (1986). Observations on the behaviour of second stage juveniles of Heterodera schachtii inside host roots. Revue de Nématologie, 9, 153–165.Google Scholar
  59. Yan, G., Smiley, R. W., Okubara, P. A., Skantar, A., Easley, S. A., Sheedy, J. G., & Thompson, A. L. (2008). Detection and discrimination of Pratylenchus neglectus and P. thornei in DNA extracts from soil. Plant Disease, 92, 1480–1487.CrossRefGoogle Scholar
  60. Yan, G. P., Smiley, R. W., & Okubara, P. A. (2012). Detection and quantification of Pratylenchus thornei in DNA extracted from soil using real-time PCR. Phytopathology, 102, 14–22.CrossRefPubMedGoogle Scholar
  61. Yang, H., Powell, N. T., & Barker, K. R. (1976). Interactions of concomitant species of nematodes and Fusarium oxysporum f. Sp. vasinfectum on cotton. Journal of Nematology, 8, 74–80.PubMedPubMedCentralGoogle Scholar
  62. Znasni, Y. (2003). Caractérisation de certaines populations marocaines des nématodes à kystes des céréales Heterodera avenae (pp. 25–31). Hassan II de Rabat: Mémoire de fin d‘étude à l‘Institut Agronomique et Vétérinaire.Google Scholar
  63. Zunke, U. (1990). Observations on the invasion and endoparasitic behavior of the root lesion nematode Pratylenchus penetrans. Journal of Nematology, 22, 309–320.PubMedPubMedCentralGoogle Scholar
  64. Zwart, R. S., Thompson, J. P., & Godwin, I. D. (2005). Identification of quantitative trait loci for resistance to two species of root-lesion nematode (Pratylenchus thornei and P. neglectus) in wheat. Australian Journal of Biological Science, 56, 345–352.Google Scholar

Copyright information

© Koninklijke Nederlandse Planteziektenkundige Vereniging 2018

Authors and Affiliations

  • Fouad Mokrini
    • 1
  • Nicole Viaene
    • 2
    • 3
  • Lieven Waeyenberge
    • 2
  • Abdelfattah A. Dababat
    • 4
  • Maurice Moens
    • 2
    • 5
  1. 1.National Institute for Agricultural Research (INRA)Inzegane, AgadirMorocco
  2. 2.Flanders Research Institute for Agriculture, Fisheries and Food (ILVO), Plant, Crop ProtectionMerelbekeBelgium
  3. 3.Department of BiologyGhent UniversityGhentBelgium
  4. 4.International Maize and Wheat Improvement Center (CIMMYT)AnkaraTurkey
  5. 5.Faculty of Bio-science EngineeringGhent UniversityGhentBelgium

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