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Identification, distribution and genetic diversity of Globodera rostochiensis (Wollenweber, 1923) Skarbilovich, 1959 (Tylenchida: Heteroderidae) populations in Turkey

Year 2020, Volume: 44 Issue: 3, 385 - 397, 01.09.2020
https://doi.org/10.16970/entoted.740223

Abstract

The golden nematode, Globodera rostochiensis (Wollenweber, 1923) Skarbilovich, 1959 (Tylenchida: Heteroderidae) is one of the most economically important pests of potato in the world. Tests for this nematode are routinely performed for outbreaks and densities in potato growing areas. The morphological and molecular analyses for precise determination of the nematode are employed to establish appropriate management strategies. This study showed that 96% of soil samples obtained from Bozdağ and Ödemiş Districts of İzmir Province, during 2017 and 2018 potato growing seasons, were positive for G. rostochiensis. The mean number of cysts ranged from 0.01 to 3.70 cysts g-1 soil in the fields examined. The examination of the morphological and morphometric features of the second-stage juveniles and cysts of the G. rostochiensis revealed slight differences among the populations obtained from Bozdağ and Ödemis. To assess the accuracy of the identification, partial sequences of ribosomal DNA for all populations were amplified, sequenced, and deposited in GenBank. The comparisons of the sequences with those of corresponding G. rostochiensis populations available in GenBank showed 99.89-100% nucleotide similarity. The results of this study will help to better understand the physiology, ecology and biology of the nematode to quarantine this pest more effectively.

Thanks

The authors would like to thank the Doğal Pesticides and Chemicals Industry Trade S.A. for providing the funding for this study. For technical assistance, we also thank Nancy De Sutter from the Flanders Research Institute for Agriculture, Fisheries and Food, Belgium.

References

  • Al-Banna, L., A. T. Ploeg, V. M. Williamson & I. Kaloshian, 2004. Discrimination of six Pratylenchus species using PCR and species-specific primers. Journal of Nematology, 36 (2): 142-146.
  • Andres, M. F., R. Alonso & A. Alemany, 2006. First report of Globodera rostochiensis in Mallorca Island, Spain. Plant Disease, 90 (9): 1262-1262.
  • Baldwin, J. G. & M. Mundo-Ocampo, 1991. “Heteroderinae, Cyst and Non-Cyst Forming Nematodes, 275-362”. In: Manual of Agricultural Nematology (Eds. W. R. Nickle & M. Dekker). CRC Press, 1035 pp.
  • Chitwood, D. J., 2003. Research on plant-parasitic nematode biology conducted by the United States Department of Agriculture-Agricultural Research Service. Pest Management Science (formerly Pesticide Science), 59 (6-7): 748-753.
  • Dale, M. F. B., 1988. Breeding for tolerance to potato cyst nematode. Aspects of Applied Biology, 17 (1): 95-101.
  • Demirbaş Pehlivan, H., G. Kaşkavalcı, E. B. K. Uludamar, H. Toktay & H. Elekcioğlu, 2020. Identification and prevalence of potato cyst nematodes and root-knot nematodes in the potato production areas of İzmir Province, Turkey. Turkish Journal of Entomology, 44 (2): 259-272.
  • Enneli, S. & G. Öztürk, 1996.” Important Plant parasitic nematodes damaging potatoes in Central Anatolia Region in Turkey, 396-403”. Proceedings of the Third Turkish National Congress of Entomology (24-28 September 1996, Ankara, Turkey) Ankara University Printing House, 716 pp.
  • EPPO, 2013. European and Mediterranean Plant Protection Organization. EPPO Bulletin, 43: 471-495.
  • FAOSTAT, 2020. Food and Agriculture Organization Statistical Database. (Web page: http://www.fao.org/faostat/en/#data/QC) (Date accessed: 15 March 2020).
  • Felsenstein, J., 1985. Confidence limits on phylogenies: An approach using the bootstrap. Evolution, 39 (4): 783-791.
  • Ferris, V. R., J. M. Ferris & J. Faghihi, 1993. Variations in spacer ribosomal DNA in some cyst-forming species of plant parasitic nematodes. Fundamental and Applied Journal of Nematology, 16 (2): 177-184.
  • Ferris, V. R., L. I. Miller, J. Faghihi & J. M. Ferris, 1995. Ribosomal DNA comparisons of Globodera from two continents. Journal of Nematology, 27 (3): 273-283.
  • Fleming, C. C. & T. O. Powers, 1998. “Potato Cyst Nematodes: Species, Pathotypes and Virulence Concepts, 51-57”. In: Potato Cyst Nematodes Biology, Distribution and Control (Eds. R. J. Marksand & B. B. Brodie). CAB International, 424 pp.
  • Ganguly, A. K. & U. Rao, 2003. “Application of Molecular Biology in Nematology, 312-317”. In: Advances in Nematology (Ed. P. C. Trivedi). Scientific Publishers, 317 pp.
  • Gitty, M. & Z. Tanha Maafi, 2010. First report of a potato cyst nematode, Globodera rostochiensis, on potato in Iran. Plant Pathology, 59 (2): 412.
  • Golden, A. M., 1986. “Morphology and Identification of Cyst Nematodes, 23-79”. In: Cyst Nematodes (Eds. F. Lamberti & C. E. Taylor). Plenum Press, 478 pp.
  • Golden, A. M., 1990. “Preparation and Mounting Nematodes for Microscopic Observation, 197-205”. In: Plant Nematology Laboratory Manual (Eds. B. M. Zuckerman, W. F. Mai & L.R. Krusberg). Amherst MA Press, 115 pp.
  • Golden, A. M. & D. M. S. Ellington, 1972. Redescription of Heterodera rostochiensis (Nematoda: Heteroderidae) with a key and notes on closely related species. Proceedings of the Helminthological Society of Washington, 39 (1): 64-78.
  • Greco, N., M. Di Vito, A. Brandonisio, I. Giordano & G. De Marinis, 1982. The effect of Globodera pallida and G. rostochiensis on potato yield. Nematologica, 28 (4): 379-386.
  • Holterman, M., A. Van Der Wurff & S. Van Den Elsen, 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.
  • Hooper, D. J., 1970. Handling, fixing, staining and mounting nematodes. Ministry of Agriculture, Fisheries and Food’s Technical Bulletin, 5 (2): 39-54.
  • Ibrahim, I. K. A., Z. A. Handoo & A. A. El-Sherbiny, 2000. A survey of phytoparasitic nematodes on cultivated and non-cultivated plants in Northwestern Egypt. Journal of Nematology, 32 (4S): 478- 485.
  • Imren, M., 2018. Determination of plant parasitic nematodes in potato growing areas in Bolu Province. International Journal of Agriculture and Wildlife Science, 4 (2): 26-32.
  • Indarti, S., B. Mulyadi & B. Triman, 2004. First record of potato cyst nematode Globodera rostochiensis in Indonesia. Australasian Plant Pathology, 33 (2): 325-326.
  • Jones, J. T., A. Haegeman, E. Danchin, H. Gaur, J. Helder, M. G. Jones, T. Kikuchi, R. Manzanilla-López, J. E. Palomares-Rius, W. M. Wesemael & R. N. Perry, 2013. Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular Plant Pathology, 14 (9): 946-961.
  • Kepenekci, İ., 2012. Nematology (Plant Parasitic and Entomopathogen Nematodes). Education Directorate of Publications and Publications, Agricultural Science Series, 1155 pp.
  • Knoetze, R., A. Swart & L. R. Tiedt, 2013. Description of Globodera capensis n. sp. (Nematoda: Heteroderidae) from South Africa. Nematology, 15 (2): 233-250.
  • Kort, J., H. Ross, H. J. Rumpenhorst & A. R. Stone, 1977. An international scheme for identifying and classifying pathotypes of potato cyst nematodes Globodera rostochiensis and G. pallida. Nematologica, 23 (3): 333-339.
  • Kumar, S., G. Stecher, M. Li, C. Knyaz & K. Tamura, 2018. MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35 (6): 1547-1549.
  • Madani, M., S. A. Subbotin & M. Moens, 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 (2): 81-86.
  • Madani, M., S. A. Subbotin, L. J. Ward, X. Li & S. H. De Boer, 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 (2): 252-263.
  • Madani, M., L. J. War & S. H. De Boer, 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 (4): 554-564.
  • Manduric, S., E. Olsson, J. E. Englund & S. Andersson, 2004. Separation of Globodera rostochiensis and G. pallida (Tylenchida:Heteroderidae) using morphology and morphometrics. Nematology, 6 (2): 171-181.
  • Mugniéry, D., M. S. Phillips, H. J. Rumpenhorst, A. R. Stone, A. Treur & D. L. Trudgill, 1989. Assessment of partial resistance of potato to, and pathotype and virulence differences in, potato cyst nematodes. EPPO Bulletin, 19 (1): 7-25.
  • Özarslandan, A., D. Dinçer, R. Bozbuga, M. İmren & İ. H. Elekçioğlu, 2019. Study on the presence of potato cyst nematodes: Globodera rostochiensis (Wollenweber, 1923) Skarbilovich, 1959 and Globodera pallida Stone 1973 (Tylenchida: Heteroderidae) in Nevşehir Province, Turkey. Turkish Journal of Agriculture and Natural Sciences, 6 (2): 125-129.
  • Sasser, J. N. & D. W. Freckman, 1987. “A World Perspective on Nematology: The Role of the Society, 7-14”. In: Vistas on Nematology (Eds. A. Veech & D. W.Dickerson). Journal of Society of Nematologists, 509 pp.
  • Scurrah, M. I., B. Niere & J. Bridge, 2005. “Nematode Parasites of Solanum and Sweet Potatoes, 193-219”. In: Plant Parasitic Nematodes in Subtropical and Tropical Agriculture (Eds. M. Luc, R. A. Sikora & J. Bridge). CABI Publishing, 841 pp.
  • Shapiro, S. S. & M. B. Wilk, 1965. An analysis of variance test for normality (complete samples). Biometrika, 52 (3/4): 591-611.
  • Siddiqi, M. R., 2000. Tylenchida, Parasites of Plants and Insects. CABI Publishing, 848 pp.
  • Skantar, A. M., Z. A. Handoo, L. K. Carta & D. J. Chitwood, 2007. Morphological and molecular identification of Globodera pallida associated with potato in Idaho. Journal of Nematology, 39 (2): 133-144.
  • Southey, J. F., 1986. Laboratory Methods for Work with Plant and Soil Nematodes. London: CABI Publishing, 202 pp.
  • Subbotin, S. A., A. Mundo-Ocampo & J. G. Baldwin, 2010. Systematics of Cyst Nematodes (Nematode: Heteroderinae). Nematology Monographs and Perspectives, 8A. Brill, 364 pp.
  • Subbotin, S., R. Perry, A. Warry & P. Halford, 2000. Variations in ribosomal DNA sequences and phylogeny of Globodera parasitizing solanaceous plants. Nematology, 2 (6): 591-604.
  • Subbotin, S. A., D. Sturhan, H. J. Rumpenhorst & M. Moens, 2003. Molecular and morphological characterization of the Heterodera avenae species complex (Tylenchida: Heteroderidae). Nematology, 5 (4): 515-538.
  • Subbotin, S. A., L. Waeyenberge, I. A. Molokanova & M. Moens, 1999. Identification of Heterodera avenae group species by morphometrics and rDNA-RFLPs. Nematology, 1 (2): 195-207.
  • Szalanski, A. L., D. D. Sui, T. S. Harris & T. O. Powers, 1997. Identification of cyst nematodes of agronomic and regulatory concern with PCR-RFLP of ITS1. Journal of Nematology, 29 (3): 255-267.
  • Tamura, K. & M. Nei, 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology Evolution, 10 (3): 512-526.
  • Thompson, J. D., D. G. Higgins & T. J. Gibson, 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.
  • Toktay, H., E. Evlice, M. Imren, G. Özer, M. A. Ali & A. Dababat, 2020. Characterization of potato golden cyst nematode populations (Globodera rostochiensis) in Turkey. International Journal of Agriculture and Biology, 23 (6): 1095-1100.
  • Ulutaş, E., A. Özarslandan, G. Kaşkavalcı & İ. H. Elekcioglu, 2012. Ege Bölgesi patates alanlarında Globodera rostochiensis Wollenweber, 1923’ in moleküler yöntemlerle saptanması. Türkiye Entomoloji Dergisi, 36 (1): 155-160.
  • Waeyenberge, L., A. Ryss, M. Moens, J. Pinochet & T. Vrain, 2000. Molecular characterisation of 18 Pratylenchus species using rDNA restriction fragment length polymorphism. Nematology, 2 (2): 135-142.
  • Wouts, W. M. & J. G. Baldwin, 1998. “Taxonomy and Identification, 83-122”. In: The Cyst Nematodes (Ed. S. B. Sharma). Dordrecht, Kluwer, 452 pp.

Globodera rostochiensis (Wollenweber, 1923) Skarbilovich, 1959 (Tylenchida: Heteroderidae)’in Türkiye popülasyonlarının tanımlanması, yaygınlık ve genetik çeşitliliği

Year 2020, Volume: 44 Issue: 3, 385 - 397, 01.09.2020
https://doi.org/10.16970/entoted.740223

Abstract

Altın nematod, Globodera rostochiensis (Wollenweber, 1923) Skarbilovich, 1959 (Tylenchida: Heteroderidae) dünyada ekonomik açıdan en önemli patates zararlılarından birisidir. Genellikle patates yetiştirilen alanlarındaki dağılımları ve yoğunluklarını belirlemek amacıyla bu nematod için rutin olarak testler gerçekleştirilmektedir. Morfolojik ve moleküler analizler bu nematodun kesin tanısını yapmak ve mücadele stratejilerini oluşturmak amacıyla kullanılmaktadır. Bu çalışma, İzmir İli’nin Bozdağ ve Ödemiş ilçelerinden 2017 ve 2018 yılları patates yetiştiriciliği sezonlarında alınan toprak örneklerinin %96'sının G. rostochiensis ile enfekte olduğunu göstermiştir. Bulaşık alanlardaki ortalama kist sayısı, 0.01 ila 3.70 kist g-1 toprak arasında değişmiştir. Globodera rostochiensis'in ikinci dönem larva ve kistlerinin morfolojik ve morfometrik karakterlerinin incelenmesi, Bozdağ ve Ödemiş’ten elde edilen popülasyonlarda arasındaki hafif farklılıkları ortaya koymuştur. Tanımlamanın doğruluğunu değerlendirmek için, tüm popülasyonlar için kısmi ribozomal DNA sekansları amplifiye edilmiş, sekanslanmış ve GenBank veritabanına kaydedilmiştir. Morfolojik ölçümler ve filogenetik analizler sonucunda Bozdağ ve Ödemiş'ten elde edilen popülasyonlar arasında küçük farklılıkların olduğu belirlenmiştir. Sekansların GenBank'ta mevcut karşılık gelen G. rostochiensis popülasyonlarıyla karşılaştırılması sonucunda nükleotid benzerliği %99.89-100 oranında görülmüştür. Bu çalışmanın sonuçları, bu zararlıyı daha etkili bir şekilde karantinaya almak için nematodun fizyolojisini, ekolojisini ve biyolojisini daha iyi anlamaya yardımcı olacaktır.

References

  • Al-Banna, L., A. T. Ploeg, V. M. Williamson & I. Kaloshian, 2004. Discrimination of six Pratylenchus species using PCR and species-specific primers. Journal of Nematology, 36 (2): 142-146.
  • Andres, M. F., R. Alonso & A. Alemany, 2006. First report of Globodera rostochiensis in Mallorca Island, Spain. Plant Disease, 90 (9): 1262-1262.
  • Baldwin, J. G. & M. Mundo-Ocampo, 1991. “Heteroderinae, Cyst and Non-Cyst Forming Nematodes, 275-362”. In: Manual of Agricultural Nematology (Eds. W. R. Nickle & M. Dekker). CRC Press, 1035 pp.
  • Chitwood, D. J., 2003. Research on plant-parasitic nematode biology conducted by the United States Department of Agriculture-Agricultural Research Service. Pest Management Science (formerly Pesticide Science), 59 (6-7): 748-753.
  • Dale, M. F. B., 1988. Breeding for tolerance to potato cyst nematode. Aspects of Applied Biology, 17 (1): 95-101.
  • Demirbaş Pehlivan, H., G. Kaşkavalcı, E. B. K. Uludamar, H. Toktay & H. Elekcioğlu, 2020. Identification and prevalence of potato cyst nematodes and root-knot nematodes in the potato production areas of İzmir Province, Turkey. Turkish Journal of Entomology, 44 (2): 259-272.
  • Enneli, S. & G. Öztürk, 1996.” Important Plant parasitic nematodes damaging potatoes in Central Anatolia Region in Turkey, 396-403”. Proceedings of the Third Turkish National Congress of Entomology (24-28 September 1996, Ankara, Turkey) Ankara University Printing House, 716 pp.
  • EPPO, 2013. European and Mediterranean Plant Protection Organization. EPPO Bulletin, 43: 471-495.
  • FAOSTAT, 2020. Food and Agriculture Organization Statistical Database. (Web page: http://www.fao.org/faostat/en/#data/QC) (Date accessed: 15 March 2020).
  • Felsenstein, J., 1985. Confidence limits on phylogenies: An approach using the bootstrap. Evolution, 39 (4): 783-791.
  • Ferris, V. R., J. M. Ferris & J. Faghihi, 1993. Variations in spacer ribosomal DNA in some cyst-forming species of plant parasitic nematodes. Fundamental and Applied Journal of Nematology, 16 (2): 177-184.
  • Ferris, V. R., L. I. Miller, J. Faghihi & J. M. Ferris, 1995. Ribosomal DNA comparisons of Globodera from two continents. Journal of Nematology, 27 (3): 273-283.
  • Fleming, C. C. & T. O. Powers, 1998. “Potato Cyst Nematodes: Species, Pathotypes and Virulence Concepts, 51-57”. In: Potato Cyst Nematodes Biology, Distribution and Control (Eds. R. J. Marksand & B. B. Brodie). CAB International, 424 pp.
  • Ganguly, A. K. & U. Rao, 2003. “Application of Molecular Biology in Nematology, 312-317”. In: Advances in Nematology (Ed. P. C. Trivedi). Scientific Publishers, 317 pp.
  • Gitty, M. & Z. Tanha Maafi, 2010. First report of a potato cyst nematode, Globodera rostochiensis, on potato in Iran. Plant Pathology, 59 (2): 412.
  • Golden, A. M., 1986. “Morphology and Identification of Cyst Nematodes, 23-79”. In: Cyst Nematodes (Eds. F. Lamberti & C. E. Taylor). Plenum Press, 478 pp.
  • Golden, A. M., 1990. “Preparation and Mounting Nematodes for Microscopic Observation, 197-205”. In: Plant Nematology Laboratory Manual (Eds. B. M. Zuckerman, W. F. Mai & L.R. Krusberg). Amherst MA Press, 115 pp.
  • Golden, A. M. & D. M. S. Ellington, 1972. Redescription of Heterodera rostochiensis (Nematoda: Heteroderidae) with a key and notes on closely related species. Proceedings of the Helminthological Society of Washington, 39 (1): 64-78.
  • Greco, N., M. Di Vito, A. Brandonisio, I. Giordano & G. De Marinis, 1982. The effect of Globodera pallida and G. rostochiensis on potato yield. Nematologica, 28 (4): 379-386.
  • Holterman, M., A. Van Der Wurff & S. Van Den Elsen, 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.
  • Hooper, D. J., 1970. Handling, fixing, staining and mounting nematodes. Ministry of Agriculture, Fisheries and Food’s Technical Bulletin, 5 (2): 39-54.
  • Ibrahim, I. K. A., Z. A. Handoo & A. A. El-Sherbiny, 2000. A survey of phytoparasitic nematodes on cultivated and non-cultivated plants in Northwestern Egypt. Journal of Nematology, 32 (4S): 478- 485.
  • Imren, M., 2018. Determination of plant parasitic nematodes in potato growing areas in Bolu Province. International Journal of Agriculture and Wildlife Science, 4 (2): 26-32.
  • Indarti, S., B. Mulyadi & B. Triman, 2004. First record of potato cyst nematode Globodera rostochiensis in Indonesia. Australasian Plant Pathology, 33 (2): 325-326.
  • Jones, J. T., A. Haegeman, E. Danchin, H. Gaur, J. Helder, M. G. Jones, T. Kikuchi, R. Manzanilla-López, J. E. Palomares-Rius, W. M. Wesemael & R. N. Perry, 2013. Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular Plant Pathology, 14 (9): 946-961.
  • Kepenekci, İ., 2012. Nematology (Plant Parasitic and Entomopathogen Nematodes). Education Directorate of Publications and Publications, Agricultural Science Series, 1155 pp.
  • Knoetze, R., A. Swart & L. R. Tiedt, 2013. Description of Globodera capensis n. sp. (Nematoda: Heteroderidae) from South Africa. Nematology, 15 (2): 233-250.
  • Kort, J., H. Ross, H. J. Rumpenhorst & A. R. Stone, 1977. An international scheme for identifying and classifying pathotypes of potato cyst nematodes Globodera rostochiensis and G. pallida. Nematologica, 23 (3): 333-339.
  • Kumar, S., G. Stecher, M. Li, C. Knyaz & K. Tamura, 2018. MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35 (6): 1547-1549.
  • Madani, M., S. A. Subbotin & M. Moens, 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 (2): 81-86.
  • Madani, M., S. A. Subbotin, L. J. Ward, X. Li & S. H. De Boer, 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 (2): 252-263.
  • Madani, M., L. J. War & S. H. De Boer, 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 (4): 554-564.
  • Manduric, S., E. Olsson, J. E. Englund & S. Andersson, 2004. Separation of Globodera rostochiensis and G. pallida (Tylenchida:Heteroderidae) using morphology and morphometrics. Nematology, 6 (2): 171-181.
  • Mugniéry, D., M. S. Phillips, H. J. Rumpenhorst, A. R. Stone, A. Treur & D. L. Trudgill, 1989. Assessment of partial resistance of potato to, and pathotype and virulence differences in, potato cyst nematodes. EPPO Bulletin, 19 (1): 7-25.
  • Özarslandan, A., D. Dinçer, R. Bozbuga, M. İmren & İ. H. Elekçioğlu, 2019. Study on the presence of potato cyst nematodes: Globodera rostochiensis (Wollenweber, 1923) Skarbilovich, 1959 and Globodera pallida Stone 1973 (Tylenchida: Heteroderidae) in Nevşehir Province, Turkey. Turkish Journal of Agriculture and Natural Sciences, 6 (2): 125-129.
  • Sasser, J. N. & D. W. Freckman, 1987. “A World Perspective on Nematology: The Role of the Society, 7-14”. In: Vistas on Nematology (Eds. A. Veech & D. W.Dickerson). Journal of Society of Nematologists, 509 pp.
  • Scurrah, M. I., B. Niere & J. Bridge, 2005. “Nematode Parasites of Solanum and Sweet Potatoes, 193-219”. In: Plant Parasitic Nematodes in Subtropical and Tropical Agriculture (Eds. M. Luc, R. A. Sikora & J. Bridge). CABI Publishing, 841 pp.
  • Shapiro, S. S. & M. B. Wilk, 1965. An analysis of variance test for normality (complete samples). Biometrika, 52 (3/4): 591-611.
  • Siddiqi, M. R., 2000. Tylenchida, Parasites of Plants and Insects. CABI Publishing, 848 pp.
  • Skantar, A. M., Z. A. Handoo, L. K. Carta & D. J. Chitwood, 2007. Morphological and molecular identification of Globodera pallida associated with potato in Idaho. Journal of Nematology, 39 (2): 133-144.
  • Southey, J. F., 1986. Laboratory Methods for Work with Plant and Soil Nematodes. London: CABI Publishing, 202 pp.
  • Subbotin, S. A., A. Mundo-Ocampo & J. G. Baldwin, 2010. Systematics of Cyst Nematodes (Nematode: Heteroderinae). Nematology Monographs and Perspectives, 8A. Brill, 364 pp.
  • Subbotin, S., R. Perry, A. Warry & P. Halford, 2000. Variations in ribosomal DNA sequences and phylogeny of Globodera parasitizing solanaceous plants. Nematology, 2 (6): 591-604.
  • Subbotin, S. A., D. Sturhan, H. J. Rumpenhorst & M. Moens, 2003. Molecular and morphological characterization of the Heterodera avenae species complex (Tylenchida: Heteroderidae). Nematology, 5 (4): 515-538.
  • Subbotin, S. A., L. Waeyenberge, I. A. Molokanova & M. Moens, 1999. Identification of Heterodera avenae group species by morphometrics and rDNA-RFLPs. Nematology, 1 (2): 195-207.
  • Szalanski, A. L., D. D. Sui, T. S. Harris & T. O. Powers, 1997. Identification of cyst nematodes of agronomic and regulatory concern with PCR-RFLP of ITS1. Journal of Nematology, 29 (3): 255-267.
  • Tamura, K. & M. Nei, 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology Evolution, 10 (3): 512-526.
  • Thompson, J. D., D. G. Higgins & T. J. Gibson, 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.
  • Toktay, H., E. Evlice, M. Imren, G. Özer, M. A. Ali & A. Dababat, 2020. Characterization of potato golden cyst nematode populations (Globodera rostochiensis) in Turkey. International Journal of Agriculture and Biology, 23 (6): 1095-1100.
  • Ulutaş, E., A. Özarslandan, G. Kaşkavalcı & İ. H. Elekcioglu, 2012. Ege Bölgesi patates alanlarında Globodera rostochiensis Wollenweber, 1923’ in moleküler yöntemlerle saptanması. Türkiye Entomoloji Dergisi, 36 (1): 155-160.
  • Waeyenberge, L., A. Ryss, M. Moens, J. Pinochet & T. Vrain, 2000. Molecular characterisation of 18 Pratylenchus species using rDNA restriction fragment length polymorphism. Nematology, 2 (2): 135-142.
  • Wouts, W. M. & J. G. Baldwin, 1998. “Taxonomy and Identification, 83-122”. In: The Cyst Nematodes (Ed. S. B. Sharma). Dordrecht, Kluwer, 452 pp.
There are 52 citations in total.

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Primary Language English
Journal Section Articles
Authors

Ahmet Altaş This is me 0000-0001-8089-8452

Emre Evlice 0000-0001-6402-0287

Göksel Özer 0000-0002-3385-2520

Abdelfattah Dababat 0000-0002-3172-0452

Mustafa İmren 0000-0002-7217-9092

Publication Date September 1, 2020
Submission Date May 21, 2020
Acceptance Date June 17, 2020
Published in Issue Year 2020 Volume: 44 Issue: 3

Cite

APA Altaş, A., Evlice, E., Özer, G., Dababat, A., et al. (2020). Identification, distribution and genetic diversity of Globodera rostochiensis (Wollenweber, 1923) Skarbilovich, 1959 (Tylenchida: Heteroderidae) populations in Turkey. Turkish Journal of Entomology, 44(3), 385-397. https://doi.org/10.16970/entoted.740223
AMA Altaş A, Evlice E, Özer G, Dababat A, İmren M. Identification, distribution and genetic diversity of Globodera rostochiensis (Wollenweber, 1923) Skarbilovich, 1959 (Tylenchida: Heteroderidae) populations in Turkey. TED. September 2020;44(3):385-397. doi:10.16970/entoted.740223
Chicago Altaş, Ahmet, Emre Evlice, Göksel Özer, Abdelfattah Dababat, and Mustafa İmren. “Identification, Distribution and Genetic Diversity of Globodera Rostochiensis (Wollenweber, 1923) Skarbilovich, 1959 (Tylenchida: Heteroderidae) Populations in Turkey”. Turkish Journal of Entomology 44, no. 3 (September 2020): 385-97. https://doi.org/10.16970/entoted.740223.
EndNote Altaş A, Evlice E, Özer G, Dababat A, İmren M (September 1, 2020) Identification, distribution and genetic diversity of Globodera rostochiensis (Wollenweber, 1923) Skarbilovich, 1959 (Tylenchida: Heteroderidae) populations in Turkey. Turkish Journal of Entomology 44 3 385–397.
IEEE A. Altaş, E. Evlice, G. Özer, A. Dababat, and M. İmren, “Identification, distribution and genetic diversity of Globodera rostochiensis (Wollenweber, 1923) Skarbilovich, 1959 (Tylenchida: Heteroderidae) populations in Turkey”, TED, vol. 44, no. 3, pp. 385–397, 2020, doi: 10.16970/entoted.740223.
ISNAD Altaş, Ahmet et al. “Identification, Distribution and Genetic Diversity of Globodera Rostochiensis (Wollenweber, 1923) Skarbilovich, 1959 (Tylenchida: Heteroderidae) Populations in Turkey”. Turkish Journal of Entomology 44/3 (September 2020), 385-397. https://doi.org/10.16970/entoted.740223.
JAMA Altaş A, Evlice E, Özer G, Dababat A, İmren M. Identification, distribution and genetic diversity of Globodera rostochiensis (Wollenweber, 1923) Skarbilovich, 1959 (Tylenchida: Heteroderidae) populations in Turkey. TED. 2020;44:385–397.
MLA Altaş, Ahmet et al. “Identification, Distribution and Genetic Diversity of Globodera Rostochiensis (Wollenweber, 1923) Skarbilovich, 1959 (Tylenchida: Heteroderidae) Populations in Turkey”. Turkish Journal of Entomology, vol. 44, no. 3, 2020, pp. 385-97, doi:10.16970/entoted.740223.
Vancouver Altaş A, Evlice E, Özer G, Dababat A, İmren M. Identification, distribution and genetic diversity of Globodera rostochiensis (Wollenweber, 1923) Skarbilovich, 1959 (Tylenchida: Heteroderidae) populations in Turkey. TED. 2020;44(3):385-97.