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.
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.
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.
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.
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.
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.
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.
Franklin, M. T. (1969). Heterodera latipons n. sp., a cereal cyst nematode from the Mediterranean region. Nematologica, 15, 535–542.
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.
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.
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.
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.
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.
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.
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.
Holgado, R., Andersson, S., Rowe, J. A., & Magnusson, C. (2004). First record of Heterodera filipjevi in Norway. Nematologia Mediterranea, 32, 205–211.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Mugnièry, D. (1984). Les nematodes de la pomme de terre. Agronomie, 3, 45–50.
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.
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.
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.
Rammah, A. (1994). Cereal cyst nematode (Heterodera avenae) in Morocco. Arab and Near East Plant Protection Newsletter, 19, 40.
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.
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 d’Etude 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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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
Corresponding author
Additional information
An erratum to this article is available at http://dx.doi.org/10.1007/s10658-016-1100-x.
Rights and permissions
About this article
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
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10658-016-0965-z