ORIGINAL ARTICLE
Characterization of cereal cyst nematodes (Heterodera spp.) in Morocco based on morphology, morphometrics and rDNA-ITS sequence analysis
 
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1
National Institute for Agricultural Research (INRA), Agadir, Morocco
 
2
Institute for Agricultural and Fisheries Research, Plant, Crop Protection, Burg. Van Gansberghelaan 96, B-9820 Merelbeke, Belgium
 
3
Department of Biology, Ghent University, K.L. Ledeganckstraat 35, B-9000 Ghent, Belgium
 
4
CIMMYT (International Maize and Wheat Improvement Centre) P.K. 39 06511, Emek, Ankara, Turkey
 
5
Faculty of Bio-science Engineering, Ghent University, Coupure links 653, B-9000 Ghent, Belgium
 
 
Submission date: 2017-04-22
 
 
Acceptance date: 2017-06-18
 
 
Corresponding author
Fouad Mokrini
National Institute for Agricultural Research (INRA), Agadir, Morocco
 
 
Journal of Plant Protection Research 2017;57(3):219-227
 
KEYWORDS
TOPICS
ABSTRACT
Morphological and molecular diversity among 11 populations of cereal cyst nematodes from different wheat production areas in Morocco was investigated using light microscopy, species-specific primers, complemented by the ITS-rDNA sequences. Morphometrics of cysts and second-stage juveniles (J2s) were generally within the expected ranges for Heterodera avenae; only the isolate from Aïn Jmaa showed morphometrics conforming to those of H. latipons. When using species-specific primers for H. avenae and H. latipons, the specific bands of 109 bp and 204 bp, respectively, confirmed the morphological identification. In addition, the internal transcribed spacer (ITS) regions were sequenced to study the diversity of the 11 populations. These sequences were compared with those of Heterodera species available in the GenBank database (www.ncbi.nlm.nih.gov) and confirmed again the identity of the species. Ten sequences of the ITS-rDNA were similar (99–100%) to the sequences of H. avenae published in GenBank and three sequences, corresponding with one population, were similar (97–99%) to H. latipons.
CONFLICT OF INTEREST
The authors have declared that no conflict of interests exist.
 
REFERENCES (32)
1.
Abdollahi M. 2009. Analysis of cyst and cone top morphometrics of Indian populations of maize cyst nematode. Journal of Plant Protection Research 49 (1): 41–47.
 
2.
Abidou H., Valette S., Gauthier G.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 (2): 146–154.
 
3.
Ammati M. 1987. Nematode status on food legumes in Morocco. p. 169–172. In:” Nematodes Parasitic to Cereals and Legumes in Temperate Semi-arid Regions” (M.C. Saxena, R.A. Sikora, J.P. Srivastava, eds.). International Centre for Agricultural Research in the Dry Areas (ICARDA), Aleppo, Syria, 217 pp.
 
4.
Baklawa M., Niere B., Heuer H., Massoud S. 2015. Characterisation of cereal cyst nematodes in Egypt based on morphometrics, RFLP and rDNA-ITS sequence analyses. Nematology 17 (1): 103–115. DOI: 10.1163/15685411-00002855.
 
5.
Cobb N.A. 1918. Estimating the nema populations of soil. United States Department of Agriculture (USDA) Technical Circular 1, 48 pp.
 
6.
Dababat A.A., Imren M., Gul Erginbas O., Ashrafi S., Yavuzaslanoglu E., Toktay T., Pariyar S.H., Elekcioglu H., Morgounov A., Mekete T. 2015. The importance and management strategies of cereal cyst nematodes, Heterodera spp., in Turkey. Euphytica 202 (2): 173–188. DOI: 10.1007/s10681-014-1269-z.
 
7.
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 (2): 177–184.
 
8.
Ferris V.R., Ferris J.M., Faghini J., Ireholm A. 1994. Comparisons of isolates of Heterodera avenae using 2-D PAGE protein patterns and ribosomal DNA. Journal of Nematology 26 (2): 144–151.
 
9.
Franklin M.T. 1969. Heterodera latipons n. sp., a cereal cyst nematode from the Mediterranean region. Nematologica 15: 535–542.
 
10.
Greco N., Volvas 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 Division of Plant Industry. https://www.freshfromflorida.c....
 
11.
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.
 
12.
Handoo Z.A. 2002. A key and compendium to species of the Heterodera avenae group (Nematoda: Heteroderidae). Journal of Nematology 34 (3): 250–262.
 
13.
Holgado R., Andersson S., Rowe J.A., Magnus-Son C. 2004. First record of Heterodera filipjevi in Norway. Nematologia Mediterranea 32: 205–211.
 
14.
Holterman M., van der Wurff A., van den Elsen S., van Megen H., Bongers T., Holovachov O., Bakker J., Helder J. 2006. Phylum-wide analysis of SSU rDNA reveals deep phylogenetic relationships among nematodes and accelerated evolution toward crown clades. Molecular Biology and Evolution 23 (9): 1792–1800. DOI:10.1093/molbev/msl044.
 
15.
Hooper D.J. 1986. Handling, fixing, staining and mounting nematodes. p. 59–80. In: “Laboratory Methods for Work with Plant and Soil Nematodes” (J.F. Southey, ed.). CAB International, London, UK, 569 pp.
 
16.
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 (4): 229–234. DOI: 10.1111/j.1439-0434.2004.00835.x.
 
17.
Mokrini F., Abbad Andaloussi F., Alaoui Y., Troccoli A. 2009. Importance and distribution of the main cereal nematodes in Morocco. p. 45–50. In: Proceedings of the first Workshop of the International Cereal Cyst Nematode Initiative, 21–23 October 2009, Antalya, Turkey.
 
18.
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 (5): 774. DOI: https://doi.org/10.1094/PDIS-1....
 
19.
Mokrini F., Abbad Andaloussi F., Waeyenberge L., Viaene N., Moens M. 2016. Diversity of root-lesion nematodes (Pratylenchus spp.) associated with wheat (Triticum aestivum and T. durum) in Morocco. Nematology 18 (7): 781–801. DOI: 10.1163/15685411-00002993.
 
20.
Ritter M. 1982. Importance des nématodes à kystes des céréales. Bulletin OEPP 12 (4): 307–316. DOI: 10.111/j.1365-2338. 1982.tb01807.x.
 
21.
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 (3): 227–241. DOI:10.1023/A:1022838806268.
 
22.
Rumpenhorst H.J., Elekçioğlu I.H., Sturhan D., Öztürk G., Eneli S. 1996. The cereal cyst nematode Heterodera filipjevi (Madzhidov) in Turkey. Nematologia Mediterranea 24 (1): 135–138.
 
23.
Smiley R.W., Nicol J.N. 2009. Nematodes which challenge global wheat production. p. 171–187. In: “Wheat Science and Trade” (B.F. Carver, ed.). Ames, IA, Wiley Blackwell, 202 pp.
 
24.
Subbotin S.A., Waeyenberge L., Molokanova I.A., Moens M. 1999. Identification of Heterodera avenae group species by morphometrics and rDNA-RFLPs. Nematology 1 (2): 195–207. DOI: 10.1163/156854199508018.
 
25.
Subbotin S.A., Waeyenberge L., Moens M. 2000. Identification of cyst forming nematodes of the genus Heterodera (Nematoda: Heteroderidae) based on the ribosomal DNA-RFLP. Nematology 2 (2): 153–164. DOI: 10.1163/156854100509042.
 
26.
Subbotin S.A., Sturhan D., Rumpenhorst H.J., Moens M. 2003. Molecular and morphological characterization of the Heterodera avenae species complex (Tylenchida: Heteroderidae). Nematology 5 (4): 515–538. DOI: 10.1163/156854103322683247.
 
27.
Thompson J.D., Higgins D.G., Gibson T.J. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22 (22): 4673–4680. DOI: 10.1093/nar/22.22.4673.
 
28.
Toumi F., Waeyenberge L., Viaene N., Dababat A., Nicol J.N., Ogbonnaya F., Moens M. 2013a. Development of two species-specific primer sets to detect the cereal cyst nematodes Heterodera avenae and H. filipjevi. European Journal of Plant Pathology 136: 613–624. DOI: 10.1007/s10658-013-0192-9.
 
29.
Toumi F., Waeyenberge L., Viaene N., Dababat A., Nicol J.N., Ogbonnaya F., Moens M. 2013b. Development of a species-specific PCR to detect the cereal cyst nematode, Heterodera latipons. Nematology 15 (6): 709–717. DOI: 10.1163/15685411-00002713.
 
30.
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 (2): 199–207. DOI: http://dx.doi.org/10.1080/0301....
 
31.
Yan G.P., Smiley R.W., Okubara P.A., Skantar A.M. 2013. Species-specific PCR assays for differentiating H. filipjevi and H. avenae. Plant Disease 97 (12): 1611–1619. DOI: http://dx.doi.org/10.1094/PDIS....
 
32.
Zheng J., Subbotin S.A., Waeyenberge L., Moens M. 2000. Molecular characterisation of Chinese Heterodera glycines and H. avenae populations based on RFLPs and sequences of rDNA-ITS regions. Russian Journal of Nematology 8 (2): 109–113.
 
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