Skip to main content
Log in

Morphological and molecular identification of potato and cereal cyst nematode isolates from Algeria and their phylogenetic relationships with other populations from distant theirgeographical areas

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

An Erratum to this article was published on 23 November 2016

Abstract

A nematode survey conducted in 2013 in Algeria, revealed that potato cyst nematodes (PCN) and cereal cyst nematodes (CCN) are widely distributed in several potato and cereal growing regions of the country. Sixteen PCN populations from five localities and five CCN populations from four of these localities were collected and characterized at the morphological and molecular levels. The PCN populations were identified as Globodera rostochiensis and G. pallida occurring separately or in mixed populations. Two species of CCN were detected. Heterodera avenae was found in four localities, whereas H. hordecalis only in one locality in association with H. avenae. The morphological and morphometric identification of PCN and CCN was confirmed by diagnostic ITS-RFLP profiles and sequencing. Phylogenetic analysis of the ITS, D2-D3 expansion domains of the 28S rRNA gene and 18S rRNA gene was made for PCN and CCN populations. Globodera pallida and G. rostochiensis from Algeria show great similarity with European and South American populations. Because of the high divergence among Algerian populations of G. pallida and G. rostochiensis it can be assumed that they were multi-introduced in Algeria. The most divergent population of G. pallida, that formed a well-separated group with some populations from Chile and Peru, suggests a later or independent introduction of this population into Algeria. Heterodera avenae and H. hordecalis formed a well-supported cluster with the corresponding populations.

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
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

References

  • Abidou, H., Valetten, S., Gauthier, P., Rivoal, R., El-Ahmed, A., & Yahyaoui, A. (2005). Molecular polymorphism and morphometrics of species of the Heterodera avenae group in Syria and Turkey. Journal of Nematology, 37, 146–154.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Abrantes, I. M., De, O., Vieira Dos Santos, M. C., da Conceição, I. L. P. M., Cunha, M. J. M. D., Santos, M. S. N., et al. (2004). Biochemical and molecular characterization of plant-parasitic nematodes. Phytopathologia Mediterranea, 43, 232–258.

  • Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W., et al. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research, 25, 3389–3402.

  • Andersson, S. (1975). Heterodera hordecalis n. sp. (Nematoda: Heteroderidae) a cyst nematode of cereals and grasses in southern Sweden. Nematologica, 20, 445–454.

  • Baldwin, J. G., & Mundo-Ocampo, M. (1991). Heteroderinae, cyst and non-cyst-forming nematodes. In W. R. Nickle (Ed.), Manual of agricultural nematology (pp. 275–362). New York: Marcel Dekker.

    Google Scholar 

  • De Luca, F., Fanelli, E., Di Vito, M., Reyes, A., & De Giorgi, C. (2004). Comparisons of the sequences of the D3 expansion of the 26S ribosomal genes reveals different degrees of heterogeneity in different populations and species of Pratylenchus from the Mediterranean region. European Journal of Plant Pathology, 110, 949–957.

    Article  Google Scholar 

  • De Luca, F., Vovlas, N., Lucarelli, G., Troccoli, A., Radicci, V., Fanelli, E., et al. (2013). Heterodera elachista the Japanese cyst nematode parasitizing corn in Northern Italy: integrative diagnosis and bionomics. European Journal of Plant Pathology, 136, 857–872.

  • Den Nijs, L. J. M. F. (1992). Interaction between Globodera rostochiensis and G. pallida in simultaneous infections on potatoes with different resistance properties. Fundamental and Applied Nematology, 15, 173–178.

    Google Scholar 

  • Douda, O., Zouhar, M., Renčo, M., & Marek, M. (2014). Molecular and morphological of a mixed population of two potato-parasiting nematode species, Globodera rostochiensis and G. pallida. Helminthologia, 51, 3–6.

    Article  Google Scholar 

  • DSA, Ain Defla (2013)- Statistical data. Direction of Agricultural Services of Ain Defla. Unpublished internal document.

  • EPPO/OEPP PM 7/40 (2) (2009). Globodera rostochiensis and Globodera pallida. EPPO Bulletin, 39, 354–368.

  • EPPO/OEPP PM 7/40 (3) (2013). Globodera rostochiensis and Globodera pallida. EPPO Bulletin, 43, 119–111.

  • Evans, K., Franco, J., & De Scurrah, M. M. (1975). Distribution of species of potato cyst-nematodes in South America. Nematologica, 21, 365–369.

    Article  Google Scholar 

  • Franklin, M. T. (1969). Heterodera latipons n. sp., a cereal cyst nematode from the Mediterranean region. Nematologica, 15, 535–542.

    Article  Google Scholar 

  • Frezal, P. (1954). Importance et répercussions de la contamination de l'Algérie par le nématode doré (Heterodera rostochiensis Wooll. [Woll.]. Journal Comptes Rendus des Séances de l'Académie d'Agriculture de France, 40, 71–74.

    Google Scholar 

  • Fu, B., Yuan, H., Zhang, P., Xing, X., Sun, B., Riley, I. T., et al. (2011). Molecular characterisation of cereal cyst nematodes in winter wheat on the Huang-Huai floodplain of China using RFLP and rDNA-ITS sequence analyses. Australasian Plant Pathology, 40, 277–285.

  • Golden, A. M. (1986). Morphology and identification of cyst nematodes. In F. Lamberti & C. E. Taylor (Eds.), Cyst Nematodes (pp. 23–45). New York: Plenum Press.

    Chapter  Google Scholar 

  • Greco, N., Di Vito, M., Brandonisio, A., Giordano, I., & De Marinis, G. (1982). The effect of Globodera pallida and G. rostochiensis on potato yield. Nematologica, 28, 379–386.

    Article  Google Scholar 

  • Grenier, E., Bossis, M., Fouville, D., Renault, L., & Mugniery, D. (2001). Molecular approaches to the taxonomic position of Peruvian potato cyst nematodes and gene pool similarities in indigenous and imported populations of Globodera. Heredity, 86, 277–290.

    Article  CAS  PubMed  Google Scholar 

  • Haddadi, F., Mokabli, A., & Smiley, R. W. (2013). Characterization of virulence reactions for Heterodera avenae populations from two localities in Algeria. Phytoparasitica, 41, 449–456.

    Article  Google Scholar 

  • Hafez, S. L., Sundararaj, P. S., & Turner, J. (2008). Incursion management of potato cyst nematode and restoration of pest area freedom. Fifth International Congress of Nematology, Brisbane, Australia, 73.

  • 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.

    CAS  Google Scholar 

  • Hlaoua, W., Horrigue-Raouani, N., Fouville, D., & Mugniery, D. (2008). Morphological and molecular characterisation of potato cyst nematode populations from Tunisia and survey of their probable geographical origine. Biotechnology, 7, 651–659.

    Article  CAS  Google Scholar 

  • Holgado, R., Andersson, S., Rowe, J. A., & Magnusson, C. (2004). First record of Heterodera filipjevi in Norway. Nematologia Mediterranea, 32, 205–211.

    Google Scholar 

  • Hooper, D. J. (1970). Handling, fixing, staining and mounting nematodes. In J. F. Southey (Ed.), Laboratory methods for work with plant and soil nematodes (5th ed., pp. 59–80). London: Her Majesty’s Stationery Office.

    Google Scholar 

  • Ibrahim, S. K., Minnis, S., Barker, A. D. P., Russel, M. D., Haydock, P. P. J., Evans, K., et al. (2001). Evaluation of PCR, IEF and ELISA techniques for the detection and identification of potato cyst nematodes from field soil samples in England and Wales. Pest Management Science, 57, 1068–1074.

  • Joyce, S.A., Reid, A., Driver, F., & Curran, J. (1994). Application of polymerase chain reaction (PCR) methods to the identification of entomopathogenic nematodes. In: Burnell, A.M., Ehlers, R.-U. & Masson, J.-P. (Eds). COST 812 Biotechnology: Genetics of entomopathogenic nematodes bacterium complexes. Proceedings of symposium and workshop, St Patrick’s College, Maynooth, County Kildare, Ireland. Luxembourg, European Commission, DGXII, pp. 178–187.

  • Lamberti, F., Greco, N., & Zaouchi, H. (1975). A nematological survey of date palm and other major crops in Algeria. FAO Plant Protection Bulletin, 23, 156–160.

    Google Scholar 

  • Madani, M., Vovlas, N., Castillo, P., Subbotin, S. A., & Moens, M. (2004). Molecular characterization of cyst nematode species (Heterodera spp.) from the Mediterranean Basin using RFLPs and sequences of ITS-rDNA. Journal of Phytopathology, 152, 229–234.

    Article  CAS  Google Scholar 

  • Madani, M., Word, L. G., & De Boer, S. H. (2008). Multiplex real time polymerase chain reaction for identifying potato cyst nematodes, Globodera pallida and Globodera rostochiensis and the tobacco cyst nematode, Globodera tabacum. Canadian Journal of Plant Pathology, 30, 554–564.

    Article  CAS  Google Scholar 

  • Madani, M., Subbotin, S. A., Ward, L. J., Li, X., & De Boer, S. H. (2010). Molecular characterization of Canadian populations of potato cyst nematodes, Globodera rostochiensis and G. pallida using ribosomal nuclear RNA and cytochrome b genes. Canadian Journal of Plant Pathology, 32, 252–263.

    Article  CAS  Google Scholar 

  • Madzhidov, A. R. (1981). [New species Bidera filipjevi sp. nov. (Heteroderina: Tylenchida) from Tadzhikistan]. Izvestiya Akademii Nauk Tadzikshoi S.S.R., Biobgicheskie Nauki, 83, 40–44. (In Russian).

  • Mai, W. F. (1977). Worldwide distribution of potato cyst nematodes and their importance in crop production. Journal of Nematology, 9, 30–34.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Manduric, S., Olsson, E., England, J. E., & Andersson, S. (2004). Separation of Globodera rostochiensis and G. pallida (Tylenchida: Heteroderidae) using morphology and morphometrics. Nematology, 6, 171–181.

    Article  Google Scholar 

  • Marshall, J. W. (1993). Detecting the presence and distribution of Globodera rostochiensis and G. pallida mixed populations in New Zealand using DNA probes. New Zealand Journal of Crop and Horticultural Science, 21, 219–223.

    Article  Google Scholar 

  • McDonald, A. H., & Nicol, J. M. (2005). Nematodes parasites of cereals. In M. Luc, R. A. Sikora, & J. Bridge (Eds.), Plant parasitic nematodes in subtropical and tropical agriculture (Second ed., pp. 131–191). Wallingford: CABI publishing.

    Chapter  Google Scholar 

  • Mokabli, A. (2002). Biologie des nématodes à kystes (Heterodera) des céréales en Algérie (66 p). INA, Algier: Virulence de quelques populations à l’égard de diverses variétés et lignées de céréales. Doctorat thesis.

  • Mokabli, A., Valette, S., Gauthier, J. P., & Rivoal, R. (2001). Influence of the temperature on the hatch of Heterodera avenae Woll. Populations from Algeria. Nematology, 3, 171–178.

    Article  Google Scholar 

  • Mokrini, F., Abbad Andaloussi, F., Alaoui, Y., & Troccoli, A. (2009). Importance and distribution of the main cereal nematodes in Morocco. In Cereal cyst nematodes: status, research and outlook (pp. 45–50). Antalya, Turkey: Proceedings of the First Workshop of the International Cereal Cyst Nematode Initiative.

    Google Scholar 

  • Mugnièry, D. (1984). Les nematodes de la pomme de terre. Agronomie, 3, 45–50.

    Google Scholar 

  • Namouchi-Kachouri, N., & B’Chir, M. M. (2005). Identification morphométrique et moléculaire de quelques populations tunisiennes d’Heterodera avenae associées aux céréales. Nematologia Mediterranea, 33, 3–9.

    Google Scholar 

  • Nunn, G. B. (1992). Nematode molecular evolution. Ph.D. Thesis, University of Nottingam, Nottingham, UK.

  • Plantard, O., Picard, D., Valette, S., Scurrah, M., Grenier, E., & Mugniéry, D. (2008). Origin and genetic diversity of Western European populations of the potato cyst nematode (Globodera pallida) inferred from mitochondrial sequences and microsatellite loci. Molecular Ecology, 17, 2208–2218.

    Article  CAS  PubMed  Google Scholar 

  • Quader, M., Nambiar, L., & Cunnigton, J. (2008). Conventional and real-time PCR-based species identification and diversity of potato cyst nematodes and diversity of potato cyst nematodes (Globodera spp.) from Victoria, Australia. Nematology, 10, 471–478.

    Article  CAS  Google Scholar 

  • Rammah, A. (1994). Cereal cyst nematode (Heterodera avenae) in Morocco. Arab and Near East Plant Protection Newsletter, 19, 40.

    Google Scholar 

  • Rivoal, R. , Valette, S., Bekal, S. , Gauthier, J.P., & Yahyaoui, A. (2003). Genetic and phenotypic diversity in the graminaceous cyst nematode complex, inferred from PCR-RFLP of ribosomal DNA and morphometric analysis. European Journal of Plant Pathology, 109, 227–241.

    Article  CAS  Google Scholar 

  • Schlùter, K. (1976). The potato cyst eelworm Heterodera rostochiensis Woll. in Morocco: its distribution and economic importance. Zeitschrift für Pflanzenkrankheiten und Pflanzenschutz, 83, 401–406.

  • Scotto La Massese, C. (1961). Aperçu sur les problèmes posés par les nématodes phytoparasites en Algérie. Journée dEtude et d’Information. Association de Coordination Technique Agricole, F.N.G.P.C., Paris, 1-27.

  • Scotto La Massese, C. (1962). Aperçu sur les problèmes posés par les nématodes phytoparasites en Algérie. In: Les nématodes. Paris, France: Association de Coordination Technique Agricole. pp. 83–109.

  • Scurrah, M., Niere, B., & Bridge, J. (2005). Nematode parasites of potato and sweet potato. In M. Luc, R. Sikora, & J. Bridge (Eds.), Plant parasitic nematodes in subtropical and tropical agriculture (pp. 193–221). Wallingford, UK: CAB International.

    Chapter  Google Scholar 

  • Skantar, A. M., Handoo, Z. A., Carta, L. K., & Chitwood, D. J. (2007). Morphological and molecular identification of Globodera pallida associated with potato in Idaho. Journal of Nematology, 39, 133–144.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Skantar, A. M., Handoo, Z. A., Zasada, I. A., Ingham, R. E., Carta, L. K., & Chitwood, D. J. (2011). Morphological and molecular identification of Globodera populations from Oregon and Idaho. Phytopathology, 101, 480–491.

  • Skarbilovich, T. S. (1959). On the structure of the systematics of nematode order Tylenchida Thorne, 1949. Acta Parasitologica Polonica, 7, 117–132.

  • Stone, A. R. (1973). Heterodera pallida n. sp. (Nematoda: Heterodoridae) a second species of potatocyst nematode. Nematologica 18, 591–606.

  • Subbotin, S.A., Waeyenberge, L., Molokanova, I.A., & Moens, M. (1999). Identification of Heterodera avenae group species by morphometrics and rDNA-RFLP. Nematology1, 195–207.

  • Subbotin, S. A., Halford, P. D., Warry, A., & Perry, R. N. (2000). Variations in ribosomal DNA sequences and phylogeny of Globodera parasitising Solanaceous plants. Nematology, 2, 591–604.

    Article  CAS  Google Scholar 

  • Subbotin, S. A., Sturhan, D., Rumpenhorst, H. J. & Moens, M. (2003). Molecular and morphological characterisation of the Heterodera avenae complex species (Tylenchida: Heteroderidae). Nematology, 5, 515–538.

  • Subbotin, S. A., Mundo-Ocampo, M., & Baldwin, J. G. (2010a). Systematics of cyst nematodes (Nematoda Heteroderinae). Nematology monographs and perspectives. A. In D. J. Hunt & R. N. Perry (Eds.), Brill Nv (p. 351). The Netherlands: Leiden.

    Google Scholar 

  • Subbotin, S. A., Mundo-Ocampo, M., & Baldwin, J. G. (2010b). Systematics of cyst nematodes (Nematoda Heteroderinae). Nematology monographs and perspectives B. In D. J. Hunt & R. N. Perry (Eds.), Brill Nv (p. 512). The Netherlands: Leiden.

    Google Scholar 

  • Subbotin, S. A., Cid Del Prado Vera, I., Mundo-Ocampo, M., & Baldwin, J. G. (2011). Identification, phylogeny and phylogeography of circumfenestrate cyst nematodes (Nematoda: Heteroderidae) as inferred from analysis of ITS-rDNA. Nematology, 13, 805–824.

    Article  CAS  Google Scholar 

  • Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30, 2725–2729.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanha Maafi, Z., Subbotin, S. A., & Moens, M. (2003). Molecular identification of cyst forming nematodes (Heteroderidae) from Iran and a phylogeny based on ITS-rDNA sequences. Nematology, 5, 99–11.

    Article  Google Scholar 

  • Tanha Maafi, Z., Sturhan, D., Kheiri, A., & Geraert, E. (2007). Species of the Heterodera avenae group (Nematoda: Heteroderidae) from Iran. Russian Journal of Nematology, 15, 49–58.

    Google Scholar 

  • Tanha Maafi, Z., Ahmadi, A. R., Hajihasani A., Karimipour Fard, H. & Nicol, J.M. (2010). Current progress on cereal cyst nematodes (Heterodera filipjevi, H. avenae type B and H. latipons) of importance on wheat in Iran, 30th international symposium of the European Society of Nematologists, Vienna, Austria, 19–23 September: 226.

  • Thiéry, M., & Mugniéry, D. (1996). Interspecific rDNA restriction fragment length polymorphismin Globodera species, parasites of Solanaceous plants. Fundamental and Applied Nematology, 19, 471–479.

    Google Scholar 

  • Turner, S. J. (1996). Population decline of potato cyst nematodes (Globodera rostochiensis, G. pallida) in field soils in Northern Ireland. Annals of Applied Biology, 129, 315–322.

    Article  Google Scholar 

  • Wollenweber, H. W. (1923). Krankheiten und Beschädigungen der Kartoffel. Arb. Forschungsinst. Kartoffelbau, 7, 1–56.

  • Wollenweber, H. W. (1924). Zur Kenntnis der Kartoffel-Heteroderen. Illustrierte Landwirtschaftliche Zeitung, 44, 100–101.

  • Wouts, W. M., & Sturhan, D. (1995). Heterodera aucklandica sp. n. (Nematoda: Heteroderidae) from a New Zealand native grass, with notes on the species of the H. avenae group. New Zealand Journal of Zoology, 22, 199–207.

    Article  Google Scholar 

Download references

Acknowledgments

The authors wish to thank Dr. Nicola Greco for critical review of the manuscript and helpful suggestions and discussions.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Francesca De Luca.

Additional information

An erratum to this article is available at http://dx.doi.org/10.1007/s10658-016-1100-x.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tirchi, N., Troccoli, A., Fanelli, E. et al. Morphological and molecular identification of potato and cereal cyst nematode isolates from Algeria and their phylogenetic relationships with other populations from distant theirgeographical areas. Eur J Plant Pathol 146, 861–880 (2016). https://doi.org/10.1007/s10658-016-0965-z

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-016-0965-z

Keywords

Navigation