Skip to main content

Advertisement

Log in

Cereal cyst nematodes: importance, distribution, identification, quantification, and control

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

Abstract

Small grain cereals, such as wheat, barley and oats are considered among the most important food sources. Plant-parasitic nematodes play a considerable role in decreasing cereal yields. The three-major species of cereal cyst nematodes (CCN) Heterodera avenae, H. latipons, and H. filipjevi are distributed worldwide and cause considerable damage. This review provides information regarding the global distribution of these nematode species, yield loss due to CCN, their biology and pathogenic relation to plants, identification and control through agricultural practices, biological agents and resistance breeding. As morphological identification of CCN is difficult and time-consuming, several molecular techniques for the identification of these CCN species have been developed in recent years. The restrictions on the use of nematicides demand for resistance to CCN. Resistance genes in several lines are known and are used in numerous breeding programmes against CCN; pyramiding these resistance genes into high yielding cultivars that could become commercially available for farmers is progressing.

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

Similar content being viewed by others

Reference

  • Abidou, H., El-Ahmed, A., Nicol, J. M., Bolat, N., Rivoal, R., & Yahyaoui, A. (2005a). Occurrence and distribution of species of the Heterodera avenae group in Syria and Turkey. Nematologia Mediterranea, 33, 195–201.

    Google Scholar 

  • Abidou, H., Valette, S., Gauthier, J. P., Rivoal, R., El-Ahmed, A., & Yahyaoui, A. (2005b). 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 

  • Al-Abed, A., Al-Momany, A., & Al-Banna, L. (2009). Epidemiological studies on the Mediterranean cereal cyst nematode, Heterodera latipons, attacking barley in Jordan. In I. T. Riley, J. M. Nicol, & A. A. Dababat (Eds.), Cereal cyst nematodes: Status, research and outlook (pp. 183–188). Ankara: CIMMYT.

    Google Scholar 

  • Al-Abed, A., Al-Momany, A., & Al-Banna, L. (2013). The effect of initial inoculum on the reproduction of Heterodera latipons. Jordan Journal of Agricultural Sciences, 9, 336–342.

    Google Scholar 

  • Alexandratos, N. & Bruinsma, J. (2012). World agriculture towards 2030/2050: the 2012 revision. ESA Working Paper No. 12–03. FAO, Agricultural Development Economics Division.

  • Al-Hazmi, A. S., Cook, R., & Ibrahim, A. A. M. (2001). Pathotype characterisation of the cereal cyst nematode, Heterodera avenae, in Saudi Arabia. Nematology, 3, 379–382.

    Google Scholar 

  • Amiri, S., Subbotin, S. A., & Moens, M. (2001). An efficient method for identification of the Heterodera schachtii sensu stricto group using PCR with specific primers. Nematologia Mediterranea, 29, 241–246.

    Google Scholar 

  • Amiri, S., Subbotin, S. A., & Moens, M. (2002). Identification of the beet cyst nematode Heterodera schachtii by PCR. European Journal of Plant Pathology, 108, 497–506.

    CAS  Google Scholar 

  • Andersen, S. (1959). Resistance of barley to various populations of the cereal root eelworm (Heterodera avenae). Nematologica, 4, 91–98.

    Google Scholar 

  • Andersen, S. (1961). Resistens mod Harveal Heterodera avenae. Meddelelse Nr. 68 fra den KG1. Veterinaerog Landbohojskoles, Copenhagen, Denmark.

  • Andersen, S., & Andersen, K. (1982). Suggestions for determination and terminology of pathotypes and genes for resistance in cyst-forming nematodes, especially Heterodera avenae. EPPO Bulletin, 12, 379–386.

    Google Scholar 

  • Andersson, S. (1973). En sannolikt ny cystnematod på stråsäd. Växtskyddsnotiser, 37, 74–76.

    Google Scholar 

  • Andersson, S. (1974). Heterodera hordecalis n. sp. (Nematoda: Heteroderidae) a cyst nematode of cereals and grasses in southern Sweden. Nematologica, 20, 445–454.

    Google Scholar 

  • Andrés, M. F., Romero, M. D., Montes, M. J., & Delibes, A. (2001). Genetic relationships and isozyme variability in the Heterodera avenae complex determined by isoelectric focusing. Plant Pathology, 50, 270–279.

  • Anon. (2005). Heterodera latipons. Distribution maps of plant disease. October (edition 1) map 960. Wallingford: CAB International.

    Google Scholar 

  • Ashoub, A. H., & Amara, M. T. (2010). Biocontrol activity of some bacterial genera against root-knot nematode, Meloidogyne incognita. Journal of American Science, 6, 321–328.

    Google Scholar 

  • Asiedu, R., Fisher, J. M., & Driscoll, C. J. (1990). Resistance to Heterodera avenae in the rye genome of triticale. Theoretical and Applied Genetics, 79, 331–336.

    CAS  PubMed  Google Scholar 

  • Balakhnina, V. P. (1989). Resistance of varieties of Triticum durum Desf. and Triticum aestivum L. to the oat cyst nematode. Gelmintologiya Segonya: Problemy Perspectivy. Tezisy Dokladov Nauchnoi Konferentsii, 4–6 April (pp. 36–37). Moscow: USSR.

  • Bansal, R. K., Dahiya, R. S., Lakshminarayana, K., Suneja, S., Anand, R. C., & Narula, N. (1999). Effect of rhizospheric bacteria on plant growth of wheat infected with Heterodera avenae. Nematologica Mediterranea, 27, 311–314.

    Google Scholar 

  • Banyer, R., & Fisher, J. M. (1971). Effect of temperature on hatching of eggs of Heterodera avenae. Nematologica, 17, 519–534.

    Google Scholar 

  • Barloy, D., Lemoine, J., Abelard, P., Tanguy, A. M., Rivoal, R., & Jahier, J. (2007). Marker-assisted pyramiding of two cereal cyst nematode resistance from Aegilops variabilis. Molecular Breeding, 20, 31–40.

    CAS  Google Scholar 

  • Bastian, H. C. (1865). Monograph of the Anguillulidae, or free nematoids, marine, land, and freshwater; with descriptions of 100 new species. The Transactions of the Linnean Society of London. Volume XXV, Part II (pp 73–184).

  • Bekal, S., Gauthier, J. P., & Rivoal, R. (1997). Genetic diversity among a complex of cereal cyst nematodes inferred from RFLP analysis of the ribosomal internal transcribed spacer region. Genome, 40, 479–486.

    CAS  PubMed  Google Scholar 

  • Bekal, S., Jahier, J., & Rivoal, R. (1998). Host responses of different Triticeae to species of the cereal cyst nematode complex in relation to breeding resistant durum wheat. Fundamental and Applied Nematology, 21, 359–370.

    Google Scholar 

  • Bishnoi, S. P., & Bajaj, H. (2002). Response of resistant barley cultivars to the Indian populations of Heterodera avenae complex. Indian Journal of Nematology, 32, 125–128.

    Google Scholar 

  • Bonfil, D. J., Dolgin, B., Mufradi, I., & Asido, S. (2004). Bioassay to forecast cereal cyst nematode damage to wheat in fields. Precision Agriculture, 5, 329–344.

    Google Scholar 

  • Bossis, M., & Rivoal, R. (1996). Protein variability in cereal cyst nematodes from different geographic regions assesses by two dimensional gel electrophoresis. Fundamental and Applied Nematology, 19, 25–34.

    Google Scholar 

  • Breiman, A., & Graur, D. (1995). Wheat evolution. Israel Journal of Plant Sciences, 43, 85–98.

    Google Scholar 

  • Brown, R. H., Meagher, J. W., & Swain, N. K. (1970). Chemical control of the cereal cyst nematode (Heterodera avenae) in the Victorian Mallee. Australian Journal of Experimental Agriculture and Animal Husbandry, 10, 172–173.

    CAS  Google Scholar 

  • Chen, P. S., Wang, M. Z., & Peng, D. L. (1989). Preliminary report of identification on cereal cyst nematode of wheat in China. Scientia Agricultura Sinica, 24, 89 [in Chinese].

    Google Scholar 

  • Cook, R., & Evans, K. (1987). Resistance and tolerance. In R. H. Brown & B. R. Kerry (Eds.), Principles and practice of nematode control in crops (pp. 179–231). Sydney: Academic Press.

    Google Scholar 

  • Cook, R., & Noel, G. R. (2002). Cyst nematodes: Globodera and Heterodera species. In J. L. Starr, R. Cook, & J. Bridge (Eds.), Plant resistance to parasitic nematodes (pp. 71–105). Wallingford: CABI Publishing.

    Google Scholar 

  • Cook, R., & Rivoal, R. (1998). Genetics of resistance and parasitism. In S. B. Sharma (Ed.), The cyst nematodes (pp. 322–352). London: Chapman Hall.

    Google Scholar 

  • Cook, R., & Starr, J. L. (2006). Resistant cultivars. In R. N. Perry & M. Moens (Eds.), Plant nematology (pp. 370–389). Wallingford: CABI International.

    Google Scholar 

  • Coomans, A. (1989). Overzicht van de vrijlevende nematofauna van België. Proceedings of the symposium “Invertebraten van België”, Brussels, Belgium K.B.I.N., 25-26 November 1988 (pp. 43–56). Royal Belgian Institute of Natural Sciences.

  • Cui, J. K., Huang, W. K., Peng, H., Liu, S. M., Wang, G. F., Kong, L. A., & Peng, D. L. (2015). A new pathotype characterization of Daxing and Huangyuan populations of cereal cyst nematode (Heterodera avenae) in China. Journal of Integrative Agriculture, 14, 724–731.

    Google Scholar 

  • Cui, L., Sun, L., Gao, X., Song, X., Wang, X. M., Li, H. L., Liu, Z. Y., Tang, W. H., & Li, H. J. (2016). The impact of resistant and susceptible wheat cultivars on the multiplication of Heterodera filipjevi and H. avenae in parasite-infested soil. Plant Pathology, 65, 1192–1199.

    Google Scholar 

  • Dababat, A.A., Pariyar, S., Nicol, J. & Duveiller, E. (2011). Cereal cyst nematode: an unnoticed threat to global cereal production (p. 11). Ibadan: CGIAR SP-IPM Technical Innovation Brief.

  • Dababat, A. A., Imren, M., Erginbas-Orakci, G., Ashrafi, S., Yavuzaslanoglu, E., Toktay, H., Pariyar, S. R., Elekçioğlu, I. H., Morgounov, A. I., & Mekete, T. (2014). The importance and management strategies of cereal cyst nematodes, Heterodera spp., in Turkey. Euphytica, 202, 173–188.

    Google Scholar 

  • Dababat, A. A., Muminjanov, H., & Smiley, R. W. (2015). Nematodes of small grain cereals: Current status and research. FAO: Ankara.

    Google Scholar 

  • Damadzadeh, M., & Ansaripour, B. (2001). Identification and distribution of Heterodera filipjevi in the Esfahan area of Iran. Russian Journal of Nematology, 9, 57–58.

    Google Scholar 

  • Davidson, J. (1930). Eelworms (Heterodera schachtii Schm.) affecting cereals in South Australia. Journal of the Department of Agriculture, South Australia, 34, 578–385.

    Google Scholar 

  • Davis, E. L., Hussey, R. S., Baum, T. J., Bakker, J., & Schots, A. (2000). Nematode parasitism genes. Annual Review of Phytopathology, 38, 365–396.

    CAS  PubMed  Google Scholar 

  • Dawabah, A. A. M., Al-Hazmi, A. S., & Al-Yahya, F. A. (2015). Management of cereal cyst nematode (Heterodera avenae) in a large scale wheat production. In A. A. Dababat, H. Muminjanov, & R. W. Smiley (Eds.), Nematodes of small grain cereals: Current status and research (pp. 277–284). FAO: Ankara.

    Google Scholar 

  • Delanoue, P. (1953). L’anguillulose des céréales. Moyens susceptibles d’en limiter les dégats en Tunisie. La Tunisie Agricole, 23.

  • Delibes, A., Romero, D., Aguaded, S., Duce, A., Mena, M., Lopez-Brana, I., Andres, M. F., Martin-Sanchez, J. A., & Garcia-Olmedo, F. (1993). Resistance to the cereal cyst nematode (Heterodera avenae Woll.) transferred from the wild grass Aegilops ventricosa to hexaploid wheat by a “stepping stone” procedure. Theoretical and Applied Genetics, 87, 402–408.

    CAS  PubMed  Google Scholar 

  • Dosba, F., Doussinault, G. & Rivoal, R. (1978). Extraction, identification and utilization of the addition lines Triticum aestivum-Aegilops ventricosa. In: Ramamujan, S. (Ed). Proceedings 5 th International Wheat Genetics Symposium Indian Society of Genetics and Plant Breeding IARI (pp. 332–337). New Delhi.

  • Eastwood, R. F., Lagudah, E. S., Appels, R., Hannah, M., & Kollmorgen, J. F. (1991). Triticum tauschii: a novel source of resistance to the cereal cyst nematode (Heterodera avenae). Australian Journal of Agricultural Research, 42, 69–77.

    Google Scholar 

  • Esbenshade, P. R., & Triantaphyllou A. C. (1988). Genetic analysis of esterase polymorphism in the soybean cyst nematode, Heterodera glycines. Journal of Nematology, 20, 486–492.

  • Ferris, V. R., Ferris, J. M., & Faghihi, J. (1993). Variation in spacer ribosomal DNA in some cyst-forming species of plant-parasitic nematodes. Fundamental and Applied Nematology, 16, 177–184.

    Google Scholar 

  • Ferris, V. R., Faghihi, J., Ireholm, A., & Ferris, J. M. (1994). Comparisons of isolates of Heterodera avenae using 2-D PAGE protein patterns and ribosomal DNA. Journal of Nematology, 26, 144–151.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Filipjev, I. & Schuurmans, S. (1941). A manual of agricultural helminthology. Leiden. E- Journal: Brill.

  • Fisher, J. M. (1982a). Problems with the use of resistance in wheat to the Australian pathotypes of Heterodera avenae. EPPO Bulletin, 12, 417–421.

    Google Scholar 

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

    Google Scholar 

  • Fu, B., Yuan, H. X., Zhang, Y., Hou, X. S., Nian, G. L., Zhang, P., Xing, X. P., Sun, B. J., Riley, I. T., & Li, H. L. (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.

    CAS  Google Scholar 

  • Gair, R., Mathias, P. L., & Harvey, P. N. (1969). Studies of cereal nematode populations and cereal yields under continuous or intensive culture. Annals of Applied Biology, 63, 503–512.

    Google Scholar 

  • Gill, J. S., & Swarup, G. (1971). On the host range of the cereal cyst nematode, Heterodera avenae Woll. 1924, the causal organism of ‘Molya’ disease of wheat and barley in Rajasthan, India. Indian Journal of Nematology, 1, 63–67.

    Google Scholar 

  • Gokte, N., & Swarup, G. (1988). On the potential of some bacterial biocides against root-knot and cyst nematodes. Indian Journal Nematology, 18, 152–153.

    Google Scholar 

  • Goto, K., Sato, E., & Toyota, K. (2009). A novel detection method for the soybean cyst nematode Heterodera glycines Ichinohe using soil compaction and real-time PCR. Nematological Research, 39, 1–7.

    Google Scholar 

  • Grandison, G. S., & Halliwell, H. G. (1975). A new pest of cereals. New Zealand Journal of Agriculture, 130, 64–65.

    Google Scholar 

  • Greco, N., Vovlas, N., Troccoli, A., & Inserra, R. N. (2002). The Mediterranean cereal cyst nematode, Heterodera latipons: a menace to cool season cereals of the United States. Nematology Circular 221. Florida Department of Agriculture and Conservation Services: Gainesville.

    Google Scholar 

  • Grosse, E., & Kohlmüller, S. (2004). Untersuchungen zur Verbreitung von Getreidezystennematoden nach einer neuen Differentialmethode. Mitteilungen aus der Biologischen Bundesanstalt für Land- und Forstwirtschaft Berlin-Dahlem, 396, 563–564.

    Google Scholar 

  • Grujicic, G. (1966). Phytoparasitic nematodes on the territory of the S.R. of Serbia with special reference to bioecologic investigations of Heterodera schachtii and Anguina tritici (Steinbuch). Filipjev. Bulletin Sciences Section, 11, 272–273.

    Google Scholar 

  • Hafez, S. L., & Golden, A. M. (1984). First report of oat cyst nematode in eastern Washington. Plant Disease, 68, 351.

    Google Scholar 

  • Hafez, S. L., & Golden, A. M. (1985). First report of oat cyst nematode (Heterodera avenae) on barley in Idaho. Plant Disease, 69, 360.

    Google Scholar 

  • Hafez, S. L., Golden, A. M., Rashid, F., & Handoo, Z. (1992). Plant-parasitic nematodes associated with crops in Idaho and eastern Oregon. Nematropica, 22, 193–204.

    Google Scholar 

  • Hajihasani, A., Tanha, M. Z., Nicol, J. M., & Rezaee, S. (2010a). Effect of the cereal cyst nematode, Heterodera filipjevi, on wheat in microplot trials. Nematology, 12, 357–363.

    Google Scholar 

  • Hajihasani, A., Tanha, M. Z., Nicol, J. M., & Seraji, A. (2010b). Relationships between population densities of the cereal cyst nematode, Heterodera latipons and yield losses of winter wheat in microplots. Australasian Plant Pathology, 39, 330–355.

    Google Scholar 

  • Handa, D. K., & Yadav, B. D. (1991). Comparative losses in husked, huskless barley and wheat due to Heterodera avenae in Rajasthan, India. Current Nematology, 2, 99–102.

    Google Scholar 

  • Hashmi, S., & Krusberg, L. R. (1995). Factors influencing emergence of juveniles from cysts of Heterodera zeae. Journal of Nematology, 27, 362–369.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hassan, G. A., Al-Assas, K., & Jamal, M. (2010). Damage potential and reproduction of Heterodera avenae on wheat under Syrian field conditions. Nematologia Mediterranea, 38, 73–78.

    Google Scholar 

  • Hirschmann, H., Paschalaki-Kourtzi, N., & Triantaphyllou, A. C. (1966). A survey of plant-parasitic nematodes in Greece. Annales de l’Institut Phytopathologique Benaki. New Series, 7, 144–156.

    Google Scholar 

  • Holgado. R., & Crump, D. H. (2003). First record on the occurrence of nematophagous fungi parasitizing cyst nematodes in Norway. International Journal of Nematology 13, 65–71.

  • Holgado, R., Stoen, M., Magnusson, C., & Hammeraas, B. (2003). The occurrence and hosts of cereal cyst nematodes (Heterodera spp.) in Norway. International Journal of Nematology, 13, 1–19.

    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 

  • Ibrahim, S. K., Perry, R. N., Plowright, R. A., & Rowe, J. (1993). Hatching behaviour of the rice cyst nematodes Heterodera sacchari and H. oryzicola in relation to age of host plant. Fundamental and Applied Nematology, 16, 23–29.

    Google Scholar 

  • Ibrahim, A., Al Hazmi, A. S., Al Yahya, F. A., & Alderfasi, A. A. (1999). Damage potential and reproduction of Heterodera avenae on wheat and barley under Saudi field conditions. Nematology, 1, 625–630.

    Google Scholar 

  • Imren, M., Waeyenberge, L., Viaene, N., Toktay, H., Dababat, A., & Elekcioğlu, H. (2012). Molecular characterization of cereal cyst nematodes from south Anatolian region in Turkey using ITS-rDNA sequences. Turkish Journal of Entomology, 4, 491–499.

    Google Scholar 

  • Ireholm, A. (1996). Long-term storage of Heterodera avenae cysts. Fundamental and Applied Nematology, 19, 357–361.

    Google Scholar 

  • Ismail, S., Schuster, R. P., & Sikora, R. A. (2000). Factors influencing dormancy of the Mediterranean cereal cyst nematode Heterodera latipons on barley. Communications in Agriculture and Applied Biological Sciences, 65, 529–535.

    Google Scholar 

  • Ismail, S., Sikora, R. A., & Schuster, R. P. (2001). Occurrence and biodiversity of egg pathogenic fungi of Mediterranean cereal cyst nematode Heterodera latipons. Communications in Agriculture and Applied Biological Sciences, 66, 645–653.

    CAS  Google Scholar 

  • Jahier, J., Tanguy, A. M., Abelard, P., & Rivoal, R. (1996). Utilization of deletions to localize a gene for resistance to the cereal cyst nematode, Heterodera avenae, on an Aegilops ventricosa chromosome. Plant Breeding, 115, 282–284.

    Google Scholar 

  • Jahier, J., Rivoal, R., Yu, M. Q., Abe’lard, P., Tanguy, A. M., & Barloy, D. (1998). Transfer of genes for resistance to cereal cyst nematode from Aegilops variabilis Eig to wheat. Journal of Genetics and Breeding, 52, 253–257.

    Google Scholar 

  • Jahier, J., Abe´lard, P., Tanguy, A. M., Dedryver, F., Rivoal, R., Khatkar, S., & Bariana, H. S. (2001). The Aegilops ventricosa segment on chromosome 2AS of the wheat cultivar VPM1 carries the cereal cyst nematode gene Cre5. Plant Breed, 120, 125–128.

  • Jensen, H. J., Eshtiaghi, H., Koepsell, P. A., & Goetze, H. (1975). The oat cyst nematode, Heterodera avenae, occurs on oats in Oregon. Plant Disease Report, 59, 1–3.

    Google Scholar 

  • Kaur, D. J., Sharma, V. S., Sohu, V. S., & Bains, N. S. (2008). Reaction of wheat genotypes to a population of Heterodera avenae from Punjab, India. Nematologia Mediterranea, 36, 157–160.

    Google Scholar 

  • Kerry, B. R. (2000). Rhizosphere interactions and the exploitation of microbial agents for the biological control of plant-parasitic nematodes. Annual Review of Pathology, 38, 423–441.

    CAS  Google Scholar 

  • Kerry, B. R., Crump, D. H., & Mullen, L. A. (1982a). Natural control of the cereal cyst nematode, Heterodera avenae Woll., by soil fungi at three sites. Crop Protection, 1, 99–109.

    Google Scholar 

  • Kerry, B. R., Crump, D. H., & Mullen, L. A. (1982b). Studies of the cereal cyst-nematode Heterodera avenae under continuous cereals, 1975–1978. II. Fungal parasitism of nematode females and eggs. Annals of Applied Biology, 100, 489–499.

    Google Scholar 

  • King, P. M., Rovira, A. D., Brisbane, P. G., Simon, A., & Brown, R. H. (1982). Population estimates of cereal cyst nematode and response of wheat to granular nematicides. Australian Journal of Experimental Agriculture and Animal Husbandry, 22, 209–220.

    Google Scholar 

  • Kingsnorth, C. S., Kingsnorth, A. J., Lyons, P. A., Chwaesczynska, D. M., & Asher, M. J. C. (2003). Real-time analysis of Polymyxa beta GST expression in infected sugar beet. Molecular Plant Pathology, 4, 171–176.

    PubMed  Google Scholar 

  • Kirjanova, Е. S. (1969). About the structure of the subcrystalline layer of the nematode genus Heterodera (Nematoda: Heteroderidae) with description of two new species. Parazitologiya, 3, 81–91 (in Russian).

    Google Scholar 

  • Kort, J. (1960). A technique for the extraction of Heterodera cysts from wet soil and for the estimation of their egg and larval content. Verslagen en Mededelingen Plantenziektenkundige Dienst, 6, 233.

    Google Scholar 

  • Kort, J. (1972). Nematode diseases of cereals of temperate climates. In J. M. Webster (Ed.), Economic nematology (pp. 97–126). New York: Academic Press.

    Google Scholar 

  • Krusberg, L. R., & Hirschmann, H. (1958). A summary of plant-parasitic nematodes in Peru. Plant Disease Report, 42, 599–608.

    Google Scholar 

  • Kühn, J. (1874). Über das vorkommen von rübennematoden an den wurzeln der halmfrüchte. Zeitschrift für wissenschaftliche Landwirthschaft und Archiv des Königlichen Preussischen Landes-Ökonomie-Kollegiums, 3, 47–50.

    Google Scholar 

  • Lewis, J. G., Matic, M., & McKay, A. C. (2009). Success of cereal cyst nematode resistance in Australia: History and status of resistance screening systems. In I. T. Riley, J. M. Nicol, & A. A. Dababat (Eds.), Cereal cyst nematodes: Status, research and outlook (pp. 137–142). Ankara: CIMMYT.

    Google Scholar 

  • Li, H. T., Li, Y., Zhang, C., Jia, N., Hu, D., Wang, Z. W., & Wang, Q. (2011). Screening and identification of Bacillus strains against cereal cyst nematode in wheat. In M. S. Reddy, Q. Wang, Y. Li, L. Zhang, B. Du, & S. K. R. Yellareddygari (Eds.), Plant growth promoting rhizobacteria (PGPR) for sustainable agriculture (p. 531). Beijing: Proceedings of the 2nd Asian PGPR conference.

    Google Scholar 

  • Liebscher, G. (1892). Beobachtungen über das Auftreten eines Nematoden an Erbsen. Journal für Landwirtschaft, 40, 357–368.

    Google Scholar 

  • Macara, A. M. (1963). Algumas consideracoes sobre nemfitodes, nomeadamente os de interesse agricola: Sua disseminaco e importfincia. Agrosciencia, 46, 99–140.

    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.

    CAS  Google Scholar 

  • Madani, M., Subbotin, S. A., & Moens, M. (2005). Quantitative detection of the potato cyst nematode, Globodera pallida, and the beet cyst nematode, Heterodera schachtii, using real-time PCR with SYBR green I dye. Molecular and Cellular Probes, 19, 81–86.

    CAS  PubMed  Google Scholar 

  • Madzhidov, A. R. (1981). [Bidera filipjevi n. sp. (Heteroderina: Tylenchida) in Tadzhikistan.] Izvestiya Akademii Nauk Tadzhiksköi SSR. Biologicheskie Nauki, 2, 40–44.

    Google Scholar 

  • Maqbool, M. A. (1988). Present status of research on plant-parasitic nematodes in cereals and food and forage legumes in Pakistan. In M. C. Saxena, R. A. Sikora, & J. P. Srivastava (Eds.), Nematodes parasitic to cereals and legumes in temperate semi-arid regions (pp. 173–180). Aleppo: Workshop Proceedings, Larnaca, Cyprus, 1–5 March 1987. ICARDA.

    Google Scholar 

  • Mathur, B. N., Handa, D. K., Swaroop, S., Sethi, C. L., Sharma, G. L., & Yadav, B. D. (1980). On the loss estimation and chemical control of molya disease of wheat caused by Heterodera avenae in India. Indian Journal of Nematology, 16, 152–159.

    Google Scholar 

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

    Google Scholar 

  • Meagher, J.W. (1972). Cereal cyst nematode (Heterodera avenae Woll.). Studies on ecology and control in Victoria. Technical Bulletin 24. Victoria: Department of Agriculture.

  • Meagher, J. W. (1977). World dissemination of the cereal-cyst nematode (Heterodera avenae) and its potential as a pathogen of wheat. Journal of Nematology, 9, 9–15.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Meagher, J. W., & Brown, R. H. (1974). Microplot experiments on the effect of plant hosts on populations of cereal cyst nematode Heterodera avenae and on the subsequent yield of wheat. Nematologica, 20, 337–346.

    Google Scholar 

  • Mezetti, A. (1953). Osservazioni sull’anguillulosi radicale dei cereali in Italia. Annali della sperimentazione agraria N.S. 7, 743–758.

  • Mitchinson, S., Gowen, S. R., & Kerry, B. R. (2009). Increased biodiversity in cereal cyst nematode infestations is not a threat to intensive cereal production in southern Britain. In I. T. Riley, J. M. Nicol, & A. A. Dababat (Eds.), Cereal cyst nematodes: Status, research and outlook (pp. 215–220). Ankara: CIMMYT.

    Google Scholar 

  • Mokabli, A., Valette, S., & Rivoal, R. (2001a). Différenciation de quelques espèces de nématodes à kystes des céréales et des graminées par électrophorèse sur gels d'acétate de cellulose. Nematologia Mediterranea, 29, 103–108.

    Google Scholar 

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

    Google Scholar 

  • Mokabli, A., Valette, S., Gauthier, J. P., & Rivoal, R. (2002). Variation in virulence of cereal cyst nematode populations from North Africa and Asia. Nematology, 4, 521–525.

    Google Scholar 

  • Mokrini, F., Waeyenberge, L., Viaene, N., & Moens, M. (2012). First report of the cereal cyst nematode Heterodera latipons on wheat in Morocco. Plant Disease, 96, 774.

    CAS  PubMed  Google Scholar 

  • Momota, Y. (1979). The first report of Heterodera latipons Franklin, 1969 in Japan. Japanese Journal of Nematology, 9, 73–74.

    Google Scholar 

  • Mor, M., Cohn, E., & Spiegel, Y. (1992). Phenology, pathogenicity and pathotypes of cereal cyst nematodes, Heterodera avenae and H. latipons (Nematoda: Heteroderidae) in Israel. Nematologica, 38, 494–501.

    Google Scholar 

  • Mor, M., Spiegel, Y., & Oka, Y. (2008). Histological study of syncytia induced in cereals by the Mediterranean cereal cyst nematode, Heterodera latipons. Nematology, 10, 279–287.

    Google Scholar 

  • Mulki, M. A., Jighly, A., Ye, G., Emebiri, L. C., Moody, D., Ansari, O., & Ogbonnaya, F. C. (2013). Association mapping for soilborne pathogen resistance in synthetic hexaploid wheat. Molecular Breeding, 31, 299–311.

    CAS  Google Scholar 

  • Mulvey, R. H., & Golden, A. M. (1983). An illustrated key to the cyst-forming genera and species of Heteroderidae in the western hemisphere with species morphometrics and distribution. Journal of Nematology, 15, 1–59.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Namouchi-Kachouri, N., B'chir, M. M., & Hajji, A. (2007). Effect of initial populations of Heterodera avenae Woll. on wheat and barley yield components and on final nematode populations under Tunisian field conditions. Tunisian Journal of Plant Protection, 3, 19–26.

    Google Scholar 

  • Nicol, J. M. (2002). Important nematode pests of cereals. In B. C. Curtis (Ed.), Wheat production and improvement (pp. 345–366). Rome: FAO Plant Production and Protection Series.

    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 (Vol. 2, pp. 243–287). Dordrecht: Springer.

    Google Scholar 

  • Nicol, J. M., Rivoal, R., Trethowan, R. M., Van Ginkel, M., Mergoum, M., & Singh, R. P. (2001). CIMMYT’s approach to identify and use resistance to nematode and soil fungi in developing superior wheat germplasm. In Bedo & L. Lango (Eds.), Wheat in global environment (pp. 381–389). Dordrecht: Kluwer Academic.

    Google Scholar 

  • Nicol, J.M., Rivoal, R., Taylor, S. & Zaharieva, M. (2004). Global importance of cyst (Heterodera spp.) and lesion nematode (Pratylenchus spp.) on cereals: distribution, yield loss, use of host resistance and integration of molecular tools. In: Cook, R. & Hunt, D.J. (Eds). Nematology Monographs and Perspectives. Proceedings of the Fourth International Congress of Nematology, 8-13 June 2002, Tenerife, Spain (pp. 1–19).

  • Nicol, J.M., Bolat, N., Sahin, E., Tülek, A., Yıldırım, A.F., Yorgancılar, A., Kaplan, A. & Braun, H.J. (2006). The cereal cyst nematode is causing economic damage on rain-fed wheat production systems of Turkey. Phytopathology 96, S169. [abstract].

  • 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., & Elekçioğlu, H. (2009). Current global knowledge of the usability of 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 (pp. 149–153). Ankara: CIMMYT.

    Google Scholar 

  • Nilsson-Ehle, H. (1908). Om olika angrepp af hafreålen (Heterodera schachti) på olika kornsorter. Sveriges Utsädesföreninggs Tidskrift, 13, 179–196.

    Google Scholar 

  • Nitao, J. K., Meyer, S. L. F., & Chitwood, D. J. (1999). In vitro assays of Meloidogyne incognita and Heterodera glycines for detection of nematode antagonistic fungal compounds. Journal of Nematology, 31, 172–183.

    CAS  PubMed  PubMed Central  Google Scholar 

  • O’Brien, P. C., & Fisher, J. M. (1977). Development of Heterodera avenae on resistant wheat and barley cultivars. Nematologica, 23, 390–397.

    Google Scholar 

  • Ogbonnaya, F. C., Seah, S., Delibes, A., Jahier, J., Lopez-Brana, I., Eastwood, R. F., & Lagudah, E. S. (2001). Molecular genetic characterisation of a new nematode resistance from Aegilops ventricosa and its derivatives in wheat. Theoretical and Applied Genetics, 102, 623–629.

    CAS  Google Scholar 

  • Ophel-Keller, K., McKay, A., Hartley, D., Herdina, & Curran, J. (2008). Development of a routine DNA-based testing service for soil borne diseases in Australia. Australasian Plant Pathology, 37, 243–253.

    CAS  Google Scholar 

  • Ou, S., Peng, D., Liu, X., Li, Y., & Moens, M. (2008). Identification of Heterodera glycines using PCR with sequence characterised amplified region (SCAR) primers. Nematology, 10, 397–403.

    CAS  Google Scholar 

  • Ozarslandan, M., Ozarslandan, A., Nicol, J. M., & Elekçioğlu, I. H. (2010). Determination of the pathotype group of Heterodera filipjevi (Madzhidov, 1981) population and resistance of H. filipjevi populations against wheat genotypes. Turkish Journal of Entomology, 34, 515–527.

    Google Scholar 

  • Pariyar, S. R., Dababat, A. A., Siddique, S., Erginbas-Orakci, G., Elashry, A., Morgounov, A. & Grundler, F. M. W. (2016). Identification and characterisation of resistance to the cereal cyst nematode Heterodera filipjevi in winter wheat. Nematology 1509–1531. doi:10.1163/15685411-00002964.

    Google Scholar 

  • Paull, J. G., Chalmers, K. J., Karakousis, A., Kretschmer, J. M., Manning, S., & Langridge, P. (1998). Genetic diversity in Australian wheat varieties and breeding material based on RFLP data. Theoretical and Applied Genetics, 96, 435–466.

    CAS  PubMed  Google Scholar 

  • Peng, D., Nicol, J. M., Zhang, D., Chen, S., Waeyenberge, L. & Moens, M. (2007). Occurrence, distribution and research situation of cereal cyst nematode in China. International Plant Protection Conference, Scotland, Glasgow, Sept. 07 [Abstract]. Proceedings International Plant Protection Conference, Glasgow, Scotland, UK. 15–18 Oct. 2007 (pp. 350–351). Alton, Hampshire, UK, British Crop Production Councel.

  • Peng, H., Qi, X., Peng, D., Long, H., He, X., Huang, W., & He, W. (2013). Sensitive and direct detection of Heterodera filipjevi in soil and wheat roots by species-specific SCAR-PCR assays. Plant Disease, 97, 1288–1294.

    CAS  PubMed  Google Scholar 

  • Perry, R. N. (1997). Plant signals in nematode hatching and attraction. In C. Fenoll, F. M. W. Grundler, & S. A. Ohl (Eds.), Cellular and molecular aspects of plant–nematode interactions (pp. 38–50). Dordrecht: Kluwer Academic Press.

    Google Scholar 

  • Philis, I. (1988). Occurrence of Heterodera latipons on barley in Cyprus. Nematologia Mediterranea, 16, 223.

    Google Scholar 

  • Philis, I. (1997). Heterodera latipons and Pratylenchus thornei attacking barley in Cyprus. Nematologia Mediterranea, 25, 305–309.

    Google Scholar 

  • Qi, X.L., Peng, D.L., Peng, H., Long, H.B., Huang, W.K. & He, W.T. (2012). Rapid molecular diagnosis based on SCAR marker system for cereal cyst nematode. Scientia Agricultura Sinica, 45, 4388–4395 [in Chinese].

  • Radice, A. D., Powers, T. O., Sandall, L. J., & Riggs, R. D. (1988). Comparisons of mitochondrial DNA from the sibling species Heterodera glycines and H. schachtii. Journal of Nematology, 20, 443–450.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rasmussen, R., Morrison, T., Herrmann, M., & Wittwer, C. (1998). Quantitative PCR by continuous fluorescence monitoring of a double strand DNA specific binding dye. Biochemica, 2, 8–11.

    Google Scholar 

  • Riggs, R. D., & Schuster, R. P. (1998). Management. In S. B. Sharma (Ed.), The cyst nematodes (pp. 388–416). Dordrecht: Kluwer Academic Publishers.

    Google Scholar 

  • Rivoal, R. (1977). Identification des races biologiques du nématode à kystes des céréales, Heterodera avenae Woll., en France. Annales de Zoologie Ecologie Animale, 9, 261–272.

    Google Scholar 

  • Rivoal, R. (1983). Biologie D’heterodera avenae Wollenweber en France. III. Evolution des diapauses des races Fr1 et Fr4 au cours de plusieurs années consécutives; influence de la température. Revue de Nématologie, 6, 157–164.

    Google Scholar 

  • Rivoal, R. (1986). Biology of Heterodera avenae Wollenweber in France. IV. Comparative study of the hatching cycles of two ecotypes after their transfer to different climatic conditions. Revue de Nématologie, 9, 405–410.

    Google Scholar 

  • Rivoal, R., & Cook, R. (1993). Nematode pests of cereals. In K. Evans, D. L. Trudgill, & J. M. Webster (Eds.), Plant-parasitic nematodes in temperate agriculture (pp. 259–303). Wallingford: CAB International.

    Google Scholar 

  • Rivoal, R., & Nicol, J. (2009). Past research on the cereal cyst nematode complex and future needs. In I. T. Riley, J. M. Nicol, & A. A. Dababat (Eds.), Cereal cyst nematodes: status, research and outlook (pp. 3–10). Ankara, Turkey: CIMMYT.

  • Rivoal, R., & Sarr, E. (1983). Considérations sur l’emploi éventuel de nématicides endothérapiques ou à action de contact, appliqués à faibles doses pour lutter contre le nématode à kyste des céréales. Heterodera avenae Phytiatrie Phytopharmacie, 32, 177–186.

    Google Scholar 

  • Rivoal, R., Dosba, F., Jahier, J., & Pierre, J. S. (1986). Les lignees d’addition ble-Aegilops ventricosa Tausch VI. Etude de la localisation chromosomique de la résistance a l’égard d’ Heterodera avenae Woll. Agronomie, 6, 143–148.

    Google Scholar 

  • Rivoal, R., Jahier, J., & Hulle, M. (1993). Partial resistance to Heterodera avenae in wheat lines with the 6Mv chromosome from Aegilops ventricosa. Journal of Nematology, 25, 265–269.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rivoal, R., Bekal, S., Valette, S., Gauthier, J. P., Fradj, M. B. H., Mokabli, A., Jahier, J., Nicol, J., & Yahyaoui, A. (2001). Variation in reproductive capacity and virulence on different genotypes and resistance genes of Triticeae, in the cereal cyst nematode species complex. Nematology, 3, 581–592.

    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.

    CAS  Google Scholar 

  • Romero, M. D. (1980). Heterodera latipons especie nueva para España. Nematologia Mediterranea, 8, 95–98.

    Google Scholar 

  • Romero, M. D., Andres, M. F., Lopez-Brana, I., & Delibes, A. (1996). A pathogenic and biochemical comparison of two Spanish populations of the cereal cyst nematode. Nematologia Mediterranea, 24, 235–244.

    Google Scholar 

  • Romero, M. D., Montes, M. J., Sin, E., Lopez-Brana, I., Duce, A., Martin-Sanchez, J. A., Andres, M. F., & Delibes, A. (1998). A cereal cyst nematode (Heterodera avenae Woll) resistance gene transferred from Aegilops triuncialis to hexaploid wheat. Theoretical and Applied Genetics, 96, 1135–1140.

    Google Scholar 

  • Rumpenhorst, H. J. (1985). Vergleichende elektrophoretische Untersuchungen von Proteinem einiger Zystennematoden von Getreide und Grasern. Mitteilungen aus der Biologischen Bundesanstalt für Land und Forstwirtschaft Berlin-Dahlen, 226, 64–74.

    Google Scholar 

  • Rumpenhorst, H. J., Elekçioğlu, I. H., Sturhan, D., Ozturk, G., & Enneli, S. (1996). The cereal cyst nematode Heterodera filipjevi (Madzhidov) in Turkey. Nematologia Mediterranea, 24, 135–138.

    Google Scholar 

  • Sabova, M., Valocka, B., Liskova, M., & Vargova, V. (1988). The first finding of Heterodera latipons Franklin, 1969 on grass stands in Czechoslovakia. Helminthologia, 25, 201–206.

    Google Scholar 

  • Sahin, E. (2010). Distribution of the important plant-parasitic nematodes in wheat production area in central Anatolian plateau, and studies on the biology and control of cereal cyst nematode Heterodera filipjevi. Adana: Ph.D. thesis. Çukurova University.

  • Sahin, E., Nicol, J. M., Elekçioğlu, I. H., & Rivoal, R. (2010). Hatching of Heterodera filipjevi in controlled and natural temperature conditions in Turkey. Nematology, 12, 193–200.

    Google Scholar 

  • Sayer, R. M., Wergin, W. P., Schmidt, J. M., & Starr, M. P. (1991). Pateuria nishizawe sp. nov., a mycelia and endospore-forming bacterium parasitic on cyst nematodes of genera Heterodera and Globodera. Research in Microbiology, 142, 551–564.

    Google Scholar 

  • Schmidt, A. (1871). Über den Rüben-Nematoden (Heterodera schachtii A.S.) Zeitschrift des Vereines für die Rübenzucker-Industrie im Zollverein, 21, 1–19.

    Google Scholar 

  • Scholz, U. (2001). Biology, pathogenicity and control of the cereal cyst nematode Heterodera latipons Franklin on wheat and barley under semiarid conditions, and interactions with common root rot Bipolaris sorokiniana (Sacc.) Shoemaker [Teleomorph: Cochliobolus sativus (Ito et Kurib.) Drechs. ex Dastur.]. Bonn: Ph.D. thesis. Bonn University.

  • Scholz, U., & Sikora, R. A. (2004). Hatching behaviour and life-cycle of Heterodera latipons Franklin as affected by agro-ecological conditions existing in semi-arid growing regions. Nematologica, 6, 245–256.

    Google Scholar 

  • Schoomaker, C. H., & Been, T. H. (2013). Plant growth and population dynamics. In R. N. Perry & M. Moens (Eds.), Plant nematology (2nd ed., pp. 302–329). CABI International: Wallingford.

    Google Scholar 

  • Seah, S., Miller, C., Sivasithamparam, K., & Lagudah, E. S. (2000). Root responses to cereal cyst nematode (Heterodera avenae) in hosts with different resistance genes. New Phytologist, 146, 527–533.

    Google Scholar 

  • Sewell, R. (1973). Plant-parasitic nematodes from Canada and abroad. Canadian Plant Disease Survey, 53, 34–35.

    Google Scholar 

  • Sharma, M., Saini, O., Prakash, G., Nupur, G., Arun, K. S., Rajan, S., Vinod, T., & Indu, S. (2013). Tracking of cereal cyst nematode resistance genes in wheat using diagnostic markers. Journal of Wheat Research, 5, 35–40.

    CAS  Google Scholar 

  • Sikora, R. A. (1988). Plant-parasitic nematodes of wheat and barley in temperate and temperate semi-arid regions – a comparative analysis. In M. C. Saxena, R. A. Sikora, & J. P. Srivastava (Eds.), Nematodes parasitic to cereals and legumes in temperate semi-arid regions (pp. 46–48). Aleppo: ICARDA.

    Google Scholar 

  • Sikora, R. A., & Oostendorp, M. (1986). Report: Occurrence of plant-parasitic nematodes in ICARDA experimental fields. Aleppo: ICARDA.

    Google Scholar 

  • Simon, A. (1980). A plant assay of soil to assess potential damage to wheat by Heterodera avenae. Plant Disease, 65, 917–919.

    Google Scholar 

  • Simon, A., & Rovira, A. D. (1982). The relation between wheat yield and early damage of roots by cereal cyst nematode. Australian Journal of Experimental Agriculture and Animal Husbandry, 22, 201–208.

    Google Scholar 

  • Slootmaker, L. A. J., Lange, G., Jochemsen, G., & Schepers, J. (1974). Monosomic analysis in bread wheat of resistance to cereal root eelworm. Euphytica, 23, 497–503.

    Google Scholar 

  • Smiley, R. W. (2009b). Root lesion nematodes reduce yield of intolerant wheat and barley. Agronomy Journal, 101, 1322–1335.

    Google Scholar 

  • Smiley, R. W. (2016). Cereal cyst nematodes: Biology and management in Pacific Northwest wheat, barley and oat crops. PNW Extension Bulletin 620, Oregon State University, Corvallis, OR. 18 p. online at: https://catalog.extension.oregonstate.edu/pnw620.

  • Smiley, R. W., & Nicol, J. M. (2009). Nematodes which challenge global wheat production. In B. F. Carver (Ed.), Wheat science and trade (pp. 171–187). Ames: Wiley-Blackwell.

    Google Scholar 

  • Smiley, R. W., Ingham, R. E., Uddin, W., & Cook, G. H. (1994). Crop sequences for managing cereal cyst nematode and fungal pathogens of winter wheat. Plant Disease, 78, 1142–1149.

    Google Scholar 

  • Smiley, R. W., Yan, G. P., & Handoo, Z. A. (2008). First record of the cyst nematode Heterodera filipjevi on wheat in Oregon. Plant Disease, 92, 1136–1136.

    CAS  PubMed  Google Scholar 

  • Smiley, R. S., Backhouse, D., Lucas, T., & Paulitz, T. C. (2009). Diseases which challenge global wheat production - root, crown, and culm rots. In B. F. Carver (Ed.), Wheat science and trade (pp. 125–153). Ames: Wiley-Blackwell.

    Google Scholar 

  • Smiley, R. W., Yan, G. P., & Pinkerton, J. N. (2011). Resistance of wheat, barley and oat to Heterodera avenae in the Pacific Northwest USA. Nematology, 13, 539–552.

    Google Scholar 

  • Smiley, R. W., Marshall, J. M., Gourlie, J. A., Paulitz, T. C., Kandel, S. L., Pumphrey, M. O., Garland-Campbell, K., Yan, G. P., Anderson, M. D., Flowers, M. D., & Jackson, C. A. (2013). Spring wheat tolerance and resistance to Heterodera avenae in the Pacific Northwest. Plant Disease, 97, 590–600.

    PubMed  Google Scholar 

  • Sosa, M.C. (1966). Contribution à l’étude d’un nématode phytoparasite: Heterodera avenae Woll. Thése Faculté des Sciences de l’Université Paris (pp. 149).

  • Stanton, J. M., & Eyres, M. (1994). Hatching of Western Australian populations of cereal cyst nematode, Heterodera avenae, and effects of sowing time and method of sowing on yield of wheat. Australasian Plant Pathology, 23, 1–7.

    Google Scholar 

  • Stelter, H. (1984). Die Arten der Unterfamilie Heteroderinae (Nematoda: Heteroderidae) und ihre Verbreitung (pp. 56). Berlin: Akademie der Landwirtschatswissenschaten der D.D.R.

  • Stoyanov, D. (1982). Cyst-forming nematodes on cereals in Bulgaria. EPPO Bulletin, 12, 341–344.

    Google Scholar 

  • Sturhan, D., & Rumpenhorst, J. R. (1996). Untersuchungen über den Heterodera avenae – Komplex. Mitteilungen aus der Biologischen Bundesanstalt für Land- und Forstwirtschaft Berlin-Dahlem, Heft, 317, 75–91.

    Google Scholar 

  • Subbotin, A. S. (2015). Heterodera sturhani sp. n. from China, a new species of the Heterodera avenae species complex (Tylenchida: Heteroderidae). Russian Journal of Nematology, 23, 145–152.

    Google Scholar 

  • Subbotin, S. A., Rumpenhorst, H. J., & Sturhan, D. (1996). Morphological and electrophoretic studies on populations of the Heterodera avenae complex from former USSR. Russian Journal of Nematology, 4, 29–39.

    Google Scholar 

  • Subbotin, S. A., Waeyenberge, L., Molokanova, I. A., & Moens, M. (1999). Identification of Heterodera avenae group species by morphometrics and rDNA-RFLPs. Nematology, 1, 195–207.

    Google Scholar 

  • Subbotin, S. A., Waeyenberge, L., & Moens, M. (2000). Identification of cyst forming nematodes of the genus Heterodera (Nematoda: Heteroderidae) based on the ribosomal DNA-RFLPs. Nematology, 2, 153–164.

    CAS  Google Scholar 

  • Subbotin, S. A., Sturhan, D., Rumpenhorst, H. J., & Moens, M. (2002). Description of Australian cereal cyst nematode Heterodera australis sp. n. (Tylenchida: Heteroderidae). Russian Journal of Nematology, 10, 139–148.

    Google Scholar 

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

    CAS  Google Scholar 

  • Subbotin, S. A., Mundo-Ocampo, M., & Baldwin, J. G. (2010a). Description and diagnosis of Heterodera species. In D. J. Hunt & R. N. Perry (Eds.), Systematics of cyst nematodes (Nematoda: Heteroderinae), Part A (pp. 7–349). Leiden: Brill.

    Google Scholar 

  • Subbotin, S. A., Mundo-Ocampo, M., & Baldwin, J. G. (2010b). Description and diagnosis of Heterodera species. In D. J. Hunt & R. N. Perry (Eds.), Systematics of cyst nematodes (Nematoda: Heteroderinae), Part B (pp. 1–512). Brill: Leiden.

    Google Scholar 

  • Talatchian, P., Akhiani, A., Grayeli, Z., Shah-Mohammadi, M., & Teimouri, F. (1976). Survey on cyst forming nematodes in Iran in 1975 and their importance. Iranian Journal of Plant Pathology, 12, 42–43.

    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, 99–111.

    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 

  • Tobar, J. (1963). Especies del genero Heterodera A. Schmidt. 1871 (Heteroderidae: Nematoda) de la provincia de Granada, con descripción de un nuevo procedimiento para el recuento de los quistes y sus larvas infectivas, en casos de infecciones multiples, en analyses rutinarios del suelo. Revista Ibérica de Parasitología, 23, 325–339.

    Google Scholar 

  • Toktay, H., Yavuzaslanoglu, E., Imren, M., Nicol, J., Elekçioğlu, I. H., & Dababat, A. (2012). Screening for resistance to Heterodera filipjevi (Madzhidov) Stelter (Tylenchida: Heteroderidae) and Pratylenchus thornei (Sher & Allen) (Tylenchida: Pratylenchidae) sister lines of spring wheat. Turkish Journal of Entomology, 36, 455–461.

    Google Scholar 

  • Toktay, H., İmren, M., Bozbuga, R., Orakçı, G.E., Dababat, A.V., & Elekcioğlu, I.H. (2013). Pathotype characterization of the cereal cyst nematode Heterodera filipjevi (Madzhidov, 1981) Stelter in Turkey. Turkish Journal of Entomology, 37, 213–219.

  • Toumi, F. (2017). Cereal Cyst Nematodes: molecular identification and quantification, and screening for resistance in wheat (p 228). Ghent: PhD thesis, Ghent University.

  • Toumi, F, Waeyenberge, L., Viaene, N., Dababat, A., Nicol, J.M., Ogbonnaya, F., & Moens, M. (2013a). Development of a species-specific PCR to detect the cereal cyst nematode Heterodera latipons. Nematology, 15, 709–717.

  • Toumi, F., Waeyenberge, L., Viaene, N., Dababat, A., Nicol, J. M., Ogbonnaya, F., & Moens, M. (2013b). Development of two species-specific primer sets to detect the cereal cyst nematodes Heterodera avenae and Heterodera filipjevi. European Journal of Plant Pathology, 136, 613–624.

    CAS  Google Scholar 

  • Toumi, F., Waeyenberge, L., Viaene, N., Dababat, A. A., Nicol, J. M., Ogbonnaya, F. C., & Moens, M. (2015a). Development of qPCR assays for quantitative detection of Heterodera avenae and H. latipons. European Journal of Plant Pathology, 10, 658–681.

    Google Scholar 

  • Toumi, F., Hassan, G., Waeyenberge, L., Viaene, N., Dababat, A. A., Nicol, J. M., Ogbonnaya, F. C., Al-Assas, K., Al-Fadil, T. A., & Moens, M. (2015b). Distribution of the cereal cyst nematodes (Heterodera spp.) in wheat and barley fields in north-eastern regions of Syria. Journal of Plant Diseases and Protection, 122, 255–263.

    Google Scholar 

  • Turner, S. T., & Rowe, J. A. (2006). Cyst nematodes. In R. N. Perry & M. Moens (Eds.), Plant nematology (pp. 91–120). Wallingford: CABI International.

    Google Scholar 

  • Turner, S. T., & Subbotin, S. A. (2013). Cyst nematodes. In R. N. Perry & M. Moens (Eds.), Plant nematology 2nd edition (pp. 109–143). Wallingford: CABI International.

    Google Scholar 

  • Turner, S. J., Stone, A. R., & Perry, J. N. (1983). Selection of potato cyst nematodes on resistant solarium vernei hybrids. Euphytica, 32, 911.

    Google Scholar 

  • Vanholme, B., De Meutter, J., Tytgat, T., Van Montagu, M., Coomans, A., & Gheysen, G. (2004). Secretions of plant-parasitic nematodes: a molecular update. Gene, 332, 13–27.

    CAS  PubMed  Google Scholar 

  • Vasudeva, R.S. (1958). Annual report of the division of mycology and plant pathology. Indian Agricultural Research Institute, New Delhi, 57, 86–100.

  • Viaene, N., Coyne, D. L., & Kerry, B. R. (2006). Biological and cultural management. In R. N. Perry & M. Moens (Eds.), Plant nematology (pp. 347–369). Wallingford: CABI International.

    Google Scholar 

  • Vrain, T. C., Wakarchuk, D. A., Lévesque, 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 

  • Waeyenberge, L., Viaene, N., Subbotin, S.A. & Moens, M. (2009). Molecular identification of Heterodera spp., an overview of fifteen years of research. Proceedings of the first workshop of the international cereal cyst nematode initiative, 21–23 October 2009 (pp. 109–114). Antalya: CIMMYT.

  • Wendt, K. R., Vrain, T. C., & Webster, J. M. (1993). Separation of three species of Ditylenchus and some host races of D. dipsaci by restriction fragment length polymorphism. Journal of Nematology, 25, 555–563.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Whitehead, A. G. (1998). Plant nematode control. New York: CAB International.

    Google Scholar 

  • Williams, K. J., & Fisher, J. M. (1993). Development of Heterodera avenae Woll. and host cellular responses in susceptible and resistant wheat. Fundamental and Applied Nematology, 16, 417–423.

    Google Scholar 

  • Wollenweber, H. W. (1923). Krankheiten und Beschädigungen der Kartoffel. Arbeiten des Forschungsinstitutes für Kartoffelbau, 7, 52.

    Google Scholar 

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

    Google Scholar 

  • Wouts, W. W., Schoemaker, A., Sturhan, D., & Burrows, P. R. (1995). Heterodera spinicauda sp. n. (Nematoda: Heteroderidae) from mud flats in the Netherlands, with a key to the species of the H. avenae group. Nematology, 41, 575–583.

    Google Scholar 

  • Wright, D. J., & Perry, R. N. (2006). Reproduction, physiology and biochemistry. In R. N. Perry & M. Moens (Eds.), Plant nematology (pp. 188–207). Wallingford: CAB International.

    Google Scholar 

  • Yan, G. P., & Smiley, R. W. (2009). Distinguishing Heterodera filipjevi and H. avenae using polymerase chain reaction-restriction fragment length polymorphism and cyst morphology. Phytopathology, 100, 216–224.

    Google Scholar 

  • Yan, G. P., Smiley, R. W., Okubara, P. A., & Skantar, A. (2013). Species-specific PCR assays for differentiating Heterodera filipjevi and H. avenae. Plant Disease, 97, 1611–1619.

    CAS  PubMed  Google Scholar 

  • Yousef, D. M., & Jacob, J. J. (1994). A nematode survey of vegetable crops and some orchards in the Ghor of Jordan. Nematologia Mediterranea, 22, 11–15.

    Google Scholar 

  • Youssif, G.M. (1987). Effect of Heterodera avenae populations in infested field patches of wheat cultivation on plant growth and yield. Abstracts of the tenth symposium on the biological aspects of Saudi Arabia, 20-24 April 1987, Jeddah (p. 183). [Abstract].

  • Yuan, H. X., Sun, J. W., Yang, W. X., Xing, X. P., Wang, Z. Y., Riley, I. T., & Li, H. L. (2010). New pathotypes of Heterodera avenae (cereal cyst nematode) from winter wheat in Zhengzhou, Henan, China. Australasian Plant Pathology, 39, 107–111.

    Google Scholar 

  • Zhang, S. W., Gan, Y. T., Xua, B. L., & Xue, Y. Y. (2014). The parasitic and lethal effects of Trichoderma longibrachiatum against Heterodera avenae. Biological Control, 72, 1–8.

    Google Scholar 

  • Zhang, J., Li, Y., Yuan, H., Sun, B., & Li, H. (2015). Biological control of the cereal cyst nematode (Heterodera filipjevi) by Achromobacter xylosoxidans isolate 09X01 and Bacillus cereus isolate 09B18. Biological Control, 92, 1–6.

    Google Scholar 

  • Zhang, J., Wang, L. M., Li, Y. H., Ding, S. L., Yuan, H. X., Riley, I. T., & Li, H. L. (2016). Biocontrol of cereal cyst nematode by Streptomyces anulatus isolate S07. Australasian Plant Pathology, 45, 57.

    Google Scholar 

  • Zhao, J., Zhang, G., Niu, X. Y., Peng, D. L., & Kang, Z. S. (2011). Sequence and RFLP analysis of rDNA-ITS region of cereal cyst nematode on wheat from Shaanxi Province. Acta Phytopathologica Sinica, 41, 561–569.

    Google Scholar 

  • Zijlstra, C., Lever, A. E. M., Uenk, B. J., & Vansilhout, C. H. (1995). Differences between ITS regions of isolates of root-knot nematodes Meloidogyne hapla and M. chitwoodi. Phytopathology, 85, 1231–1237.

    CAS  Google Scholar 

Download references

Acknowledgements

The authors are grateful for Dr. Roger Rivoal for careful reading of the manuscript and for valuable suggestions and comments.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fateh Toumi.

Ethics declarations

Funding

The work was done via the financial support of Monsanto’s Beachell-Borlaug International Scholars Program (MBBISP); no potential conflicts of interest (financial or non-financial); no human was used; no animal was involved as well. All authors have been personally and actively involved in substantive work leading to the manuscript and will hold themselves jointly and individually responsible for its content.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Toumi, F., Waeyenberge, L., Viaene, N. et al. Cereal cyst nematodes: importance, distribution, identification, quantification, and control. Eur J Plant Pathol 150, 1–20 (2018). https://doi.org/10.1007/s10658-017-1263-0

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-017-1263-0

Keywords

Navigation