Skip to main content
Log in

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

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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.).

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 

  • Eisenback, J. D. (1993). Interactions between nematodes in cohabitance. In N. W. Khan (Ed.), Nematode interactions (pp. 134–174). London: Chapman & Hall.

    Chapter  Google Scholar 

  • Estores, R. A., & Chen, T. A. (1972). Interactions of Pratylenchus penetrans and Meloidogyne incognita as coinhabitants in tomato. Journal of Nematology, 4, 170–174.

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Hendrickx, G. (1995). An automated apparatus for extracting free-living nematode stages from soil. Nematologica, 41, 308.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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 

  • 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 

  • Lasserre, F., Rivoal, R., & Cook, R. (1994). Interactions between Heterodera avenae and Pratylenchus neglectus on wheat. Journal of Nematology, 26, 336–344.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Melakeberhan, H. (1998). Pathogenicity of Pratylenchus penetrans, Heterodera glycines, and Meloidogyne incognita on soybean genotypes. Journal of Nematology, 30, 93–99.

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Moens, M., & Perry, R. N. (2009). Migratory plant endoparasitic nematodes: A group rich in contrasts and divergence. Annual Review of Phytopathology, 47, 313–332.

    Article  PubMed  CAS  Google Scholar 

  • 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).

  • 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.

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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 

  • 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.

  • 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).

  • 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.

    Article  Google Scholar 

  • 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • OEPP/EPPO. (2013). PM7/119. Nematode extraction. OEPP/EPPO Bulletin, 43, 471–495.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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.

    Chapter  Google Scholar 

  • 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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 

  • Zunke, U. (1990). Observations on the invasion and endoparasitic behavior of the root lesion nematode Pratylenchus penetrans. Journal of Nematology, 22, 309–320.

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nicole Viaene.

Ethics declarations

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.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mokrini, F., Viaene, N., Waeyenberge, L. et al. 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. Eur J Plant Pathol 151, 875–889 (2018). https://doi.org/10.1007/s10658-018-1420-0

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-018-1420-0

Keywords

Navigation