Research Article
BibTex RIS Cite

Türkiye’nin Doğu Karadeniz Bölgesi’nde karalahana, Brassica oleracea var. acephala L. (Brassicales: Brassicaceae) üretim alanlarındaki kist nematodları, Heterodera spp. (Tylenchida: Heteroderidae) ve dağılımları

Year 2024, Volume: 48 Issue: 2, 139 - 154
https://doi.org/10.16970/entoted.1414404

Abstract

Bu çalışma, Türkiye'nin Doğu Karadeniz Bölgesi lahana, Brassica oleracea var. acephala L. (Brassicales: Brassicaceae) üretim alanlarında kist nematodlarını Heterodera spp. (Tylenchida: Heteroderidae) tespit etmek ve dağılımları ve popülasyonlarını belirlemek amacıyla 2021-2022 yıllarında yürütülmüştür. Bu amaçla, bölgedeki Artvin, Giresun, Ordu, Rize ve Trabzon illerine ait 53 ilçeden toplam 77 örnekleme gerçekleştirilmiştir. Toprak örnekleri karalahana bitkilerinin kök çevresinden alınmıştır. Nematodlar santrifüj yöntemi kullanılarak elde edilmiştir. Nematodlar, morfolojik özellikler ve Polimeraz Zincir Reaksiyonu (PCR) yöntemine dayanan moleküler analiz kullanılarak tanımlanmıştır. Moleküler analiz için, 28S ribozomal RNA (rRNA) gen bölgesini (ITS1, 5.8S, ITS2) içeren ribozomal DNA bölgesi TW81/AB28 primer setleri kullanılarak çoğaltılmıştır. Ayrıca, mitokondriyal DNA'nın (mtDNA) Sitokrom Oksidaz I (cox1) bölgesini kapsayan türe özgü primer seti (Car-F/Car-R) kullanılmıştır. Analiz sonucunda bölgedeki karalahana üretim alanlarında Heterodera cruciferae Franklin, 1945, Heterodera carotae Jones, 1950 ve Heterodera fici Kirjanova, 1954 kist nematod türleri teşhis edilmiştir. Heterodera carotae türü Türkiye için ilk kayıt niteliğindedir. Toplanan toplam toprak örneklerinde H. cruciferae, H. carotae ve H. fici sırasıyla %16.9, %3.9 ve %1.3 oranlarında tespit edilmiştir. Çalışmada, %35.3 ile Giresun ili en çok bulaşık olan il olurken, bunu %26.3 ile Trabzon, %21.1 ile Ordu ve %13.3 ile Rize illeri takip etmiştir.

Project Number

B-2205

References

  • Abd-Elgawad, M. M., 2021. Optimizing safe approaches to manage plant-parasitic nematodes. Plants, 10 (9): 1-20.
  • Anonymous, 2023a. Karadeniz Bölgesi (Web page: https://www.efe.name.tr/karadeniz-bolgesi/) (Date accessed: 15 December 2023) (in Turkish).
  • Anonymous, 2023b. Heterodera carotae. (Web page: http://nemaplex.ucdavis.edu/Taxadata/G060S2.aspx) (Date accessed: 15 December 2023).
  • Anonymous, 2024a. About Kale and Collards (Web page: https://www.westcoastseeds.com/blogs/wcs-academy/kale-collards) (Date accessed: 9 March 2024).
  • Anonymous, 2024b. Google Earth (Web page: https://earth.google.com/web/@40.95890424,39.67512947,327. 25744699a,376450.18609285d,30.00000001y,0h,0t,0r/data=OgMKATA) (Date accessed: 9 March 2024).
  • Avendano, F., F. J. Pierce, O. Schabenberger & H. Melakeberhan, 2004. The spatial distribution of soybean cyst nematode in relation to soil texture and soil map unit. Agronomy Journal, 96 (1): 181-194.
  • Ay, A. & R. Kızılkaya, 2021. Ordu ve Giresun illerindeki fındık bahçelerinin toprak özellikleri ile biyolojik özellikleri arasındaki ilişkiler. Toprak Bilimi ve Bitki Besleme Dergisi, 9 (1): 71-78 (in Turkish with abstract in English).
  • Aydinli, G., 2009. Lahana Kist Nematodu (Heterodera cruciferae Franklin) (Nemata: Tylenchida: Heteroderidae)'na Karşı Kimyasal Mücadeleye Alternatif Yöntemler Üzerinde Araştırmalar: Dayanıklı Çeşit Saptanması, Bazı Bitki Ekstraktlarının Etkileri ve Kistlerden Larva Çıkışına Etkili Olan Faktörler. Ondokuz Mayıs Üniversitesi, Fen Bilimleri Enstitüsü,Bitki Koruma Bölümü/Anabilim Dalı (Unpublished) Master Science Thesis, Samsun, Türkiye, 95 s (in Turkish with abstract in English).
  • Aydinli, G. & S. Mennan, 2012. Screening resistance level of Brassicaceae plants to cabbage cyst nematode, Heterodera cruciferae Franklin, 1945 (Tylenchida: Heteroderidae). Turkish Journal of Entomology, 36 (1): 3-10.
  • Balkaya, A. & R. Yanmaz, 2005. Promising kale (Brassica oleracea var. acephala) populations from Black Sea region, Turkey. New Zealand Journal of Crop and Horticultural Science, 33 (1): 1-7.
  • Berney, M. F. & G. W. Bird, 1992. Distribution of Heterodera carotae and Meloidogyne hapla in Michigan carrot production. Journal of Nematology, 24 (4S): 776-778.
  • Chowdhury, I. A., G. Yan & A. Friskop, 2020. Occurrence of vermiform plant-parasitic nematodes in North Dakota corn fields and impact of environmental and soil factors. Canadian Journal of Plant Pathology, 42 (3): 429-444.
  • Di Vito, M. & N. Sasanelli, 1990. The effect of natural and artificial hatching agents on the emergence of juveniles of Heterodera fici. Nematologia Mediterranea, 18 (1): 55-57.
  • Escobar-Avila, I. M., E. Ó. López-Villegas, S. A. Subbotin & A. Tovar-Soto, 2018. First report of Carrot cyst nematode in Mexico: morphological, molecular characterization, and host range study. Journal of Nematology, 50 (2): 229-242.
  • FAO, 2020. FAOSTAT, Crop Data Base. Food and Agriculture Organization United Nations. (Web page: http://www.fao.org/faostat/en/#data/QC/visualize) (Date accessed: August 2022).
  • Fenwick, D. W., 1951. The effect of temperature on the development of potato root eelworm, Heterodera rostochiensis. Annual Applied BioIogy, 38 (3): 615-618.
  • Franklin, M. T., 1945. On Heterodera cruciferae n. sp. of brassicas, and on a Heterodera strain infecting clover and dock. Journal of Helminthology, 21 (2-3): 71-84.
  • Golden, A. M., M. A. Maqbool & F. Zarina, 1988 Redescription of Heterodera fici (Nematoda: Heteroderidae) with SEM observations. Journal of Nematology, 20 (3): 381-391.
  • Goodey, J. B., M. T. Franklin & D. J. Hooper, 1965. The Nematode Parasites of Plants Catalogued under Their Hosts. Common Wealth Agricultural Bureaux, Farnham Royal, Bucks, England. Third Edition, 214 pp.
  • Greco, N, T. D'addabbo, A. Brandonisio & F. Elia, 1993. Damage to Italian crops caused by cyst-forming nematodes. Journal of Nematology, 25 (4S): 832-836.
  • Handoo, Z. A. & S. A. Subbotin, 2018. “Taxonomy, Identification and Principal Species, 365-397”. In: Cyst Nematodes (Eds. R. N. Perry, M. Moens & J. T. Jones). Wallingford, UK, CAB International, 464 pp.
  • Hartman, K. M. & J. N. Sasser, 1985. “Identification of Meloidogyne species on the Basis of Differential Host Test and Perineal-Pattern Morphology, 69-77”. In: An advanced treatise on Meloidogyne Volume II: Methodology (Eds. K. R. Barker, C. C. Carter & J. N. Sasser). North Carolina State University Graphics, Raleigh, North Carolina, USA, 223 pp.
  • Hbirkou, C., G. Welp, K. Rehbein, C. Hillnhütter, M. Daub, M. A. Oliver & S. Pätzold, 2011. The effect of soil heterogeneity on the spatial distribution of Heterodera schachtii within sugar beet fields. Applied Soil Ecology, 51 (1): 25-34.
  • Jabbari, H. & G. Niknam, 2008. SEM observations and morphometrics of the cabbage cyst nematode, Heterodera cruciferae Franklin, 1945, collected where Brassica spp. are grown in Tabriz, Iran. Turkish Journal of Entomology, 32 (3): 253-2628.
  • Jenkins, W. R. B., 1964. A rapid centrifugal-flotation technique for separating nematodes from soil. Plant Disease Reporter, 48: 692.
  • Jensen, H. J., 1972. “Nematodes of Vegetables and Related Crops, 377-409”. In: Economic Nematology (Eds. J. M. Webster), Academic Press, London, 515 pp.
  • Jones, F. G. W., 1950. Observations on the beet eelworm and other cyst-forming species of Heterodera. Annals of Applied Biology, 37 (3): 407-440.
  • Joyce, S. A., A. M. Burnell & T. O. Powers, 1994. Characterization of Heterorhabditis isolates by PCR amplification of segments of mtDNA and rDNA genes. Journal of Nematology, 26 (3): 260-270.
  • Kirjanova, E. S., 1954. Summaries and perspectives in the development of phytonematology in USSR. Zoological Institute of the Academy of Sciences, USSR, Turdy Prob. i Tematicheskikh Soveshchanii, 3 (1): 9-47.
  • Madani, M., J. E. Palomares-Rius, N. Vovlas, P. Castillo & M. Tenuta, 2018. Integrative diagnosis of carrot cyst nematode (Heterodera carotae) using morphology and several molecular markers for an accurate identification. European Journal of Plant Pathology, 150 (4): 1023-1039.
  • Maqbool, M. A., M. Qasim & B. Zarina, 1987. New record of Heterodera fici Kirjanova, 1954 and Meloidogyne javanica (Treub, 1885) Chitwood, 1949 on Ficus carica L. Pakistan Journal of Nematology, 5 (1): 41-42.
  • McCann, J., 1981. Threshold populations of Heterodera cruciferae and H. schachtii causing damage to cabbage seedlings. Plant Disease Reporter, 65 (3): 264-266.
  • Mennan, S. & G. Aydınlı, 2007. “Lahana kist nematodu (Heterodera cruciferae Franklin) (Nemata: Tylenchida: Heteroderidae)’nun yumurta açılımını etkileyen bazı faktörler üzerinde bir araştırma, 27-29”. Türkiye II. Bitki Koruma Kongresi, 80 s (in Turkish with abstract in English).
  • Mennan, S. & Z. Handoo, 2012. Histopathology of Brassica oleracea var. capitata sub var. alba infected with Heterodera cruciferae Franklin, 1945 (Tylenchida: Heteroderidae). Turkish Journal of Entomology, 36 (3): 301-310.
  • Mennan, S., Z. Handoo & O. Ecevit, 2009. Samsun ili lahana ekim alanlarındaki kist nematodları (Tylenchida: Heteroderidae)’nın yayılışı ve bulaşıklık derecesi. Turkish Journal of Entomology, 33 (4): 289-303. (in Turkish with abstract in English)
  • Mulvey, R. H. & A. Morgan Golden, 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):1-59.
  • Mulvey, R. H., 1972. Identification of Heterodera cysts by terminal and cone top structures. Canadian Journal of Zoology, 50 (10): 1277-1292.
  • Muşdağı, S. & U. Gözel, 2015. Çanakkale ili lahana ekim alanlarında kist nematodu türlerinin (Heterodera spp.) belirlenmesi. Türkiye Entomoloji Bülteni, 5 (1): 11-20 (in Turkish with abstract in English).
  • Öztürk, Ö., 2005. Karadeniz: Ansiklopedik Sözlük. Heyamola Yayınları, İstanbul, 1220 pp. (No Title) (in Turkish).
  • Pagan, C., D. Coyne, R. Carneiro, G. Kariuki, N. Luambano, A. Affokpon & V. M. Williamson, 2015. Mitochondrial haplotype-based identification of ethanol-preserved root-knot nematodes from Africa. Phytopathology, 105 (3): 350-357.
  • Pehlivan, H. D., G. Kaşkavalcı, E. B. Kasapoğlu Uludamar, H. Toktay & İ. H. Elekcioğlu, 2020. Identification and prevalence of potato cyst nematodes and root-knot nematodes in the potato production areas of İzmir Province. Turkish Journal of Entomology, 44 (2): 259-272.
  • Ravichandra, N. G., 2014. “Nematode Diseases of Horticultural Crops, 127-205”. In: Horticultural Nematology. Springer, New Delhi, 412 pp.
  • Sambrook, J., E. F. Fritsch & T. Maniatis, 1989. Molecular Cloning: A Laboratory Manual (2nd Editioın). Cold Spring Harbor Laboratory Press, 626 pp.
  • Shepherd, A. M., 1986. “Extraction and Estimation of Cyst Nematodes, 51-58”. In: Laboratory Methods for Work with Plant and Soil Nematodes. (Eds. J. F. Southey). London, UK: Her Majesty’s Stationery Office, 202 pp.
  • Schmidt, K., R. A. Sikora & O. Schuster, 1993. Modelling the population dynamics of the sugar beet cyst nematode Heterodera schachtii. Crop Protection, 12 (7): 490-496.
  • Shubane, A. R., A. Swart, R. Knoetze, L. R. Tiedt & H. Fourie, 2021. Characterization of Heterodera carotae from the Tarlton area, South Africa, and determination of its life cycle under field conditions: a baseline study. Journal of Plant Diseases and Protection, 128 (6): 1637-1655.
  • Stone, A. R. & J. A. Rowe, 1976. Heterodera cruciferae. CIH Descriptions of Plant-Parasitic Nematodes. CABI Publishing, Wallingford. Set 6, No:90. Sturhan, D. & M. Lišková, 2004. Cyst nematodes in the Slovak Republic. Helminthologia, 41 (4): 217-219.
  • Subbotin, S. A., M. Mundo-Ocampo & J. G. Baldwin, 2010. “Description and Diagnosis of Heterodera species, 35-449”. In: Systematics of Cyst Nematodes (Nematoda: Heteroderinae), Vol. 8B. The Netherlands: Koninklijke Brill NV. 414 pp.
  • Subbotin, S. A., A. M. Deimi, J. Zheng & V. N. Chizhov, 2011. Length variation and repetitive sequences of internal transcribed spacer of ribosomal RNA gene, diagnostics and relationships of populations of potato rot nematode, Ditylenchus destructor Thorne, 1945 (Tylenchida: Anguinidae). Nematology, 13 (7): 773-785.
  • Thorne, G., 1961. Principles of Nematology. New York, McGraw-Hill, 553 pp
  • Toktay, H., B. G. Akyol, E. Evlice & M. İmren, 2022. Molecular characterization of Heterodera cruciferae Franklin, 1945 from cabbage fields in Niğde province, Turkey. Molecular Biology Reports, 49 (12): 11557-11562.
  • Turner, S. J. & S. A. Subbotin, 2013. “Cyst Nematodes, 109-143”. In: Plant Nematology (2nd Edition) (Eds. R. N. Perry & M. Moens). CAB International, Wallingford, UK, 542 pp.
  • TUIK, 2021. Türkiye İstatistik Kurumu İstatistik Veri Portalı. (Web page: http://tuik.gov.tr/PreTablo.do?alt_id=1001) (Date accessed: 10 November 2023) (in Turkish).
  • Vural, H., 2008. Lahana Yetiştiriciliği. (Web page: https://www.gencziraat.com/Bahce-Bitkileri/Lahana-Yetistiriciligi-12.html) (Date accessed: 10 November 2023) (in Turkish).
  • Wallace, H. R., 1959. Further observations on some factors influencing the emergence of larvae from cysts of the beet eelworm Heterodera schachtii Schmidt. Nematologica, 4 (4): 245-252.
  • Winslow, R. D., 1955. The effects of some leguminous crops on the soil population level of pea root eelworm. Plant Pathology, 4 (3): 86-88.
  • Yu, Q., E. Ponomareva, D. Van Dyk, M. R. McDonald, F. Sun, M. Madani & M. Tenuta, 2017. First report of the carrot cyst nematode (Heterodera carotae) from carrot fields in Ontario, Canada. Plant Disease, 101 (6): 1056-1056.
  • Yüksel, H., 1973. Türkiye’de bulunan Heterodera (Nematoda: Heteroderidae) türleri, bunların morfolojik ve biyolojik farklılıkları üzerinde araştırmalar. Atatürk Üniversitesi, Ziraat Fakültesi Dergisi, 4 (1): 53-71 (in Turkish with abstract in English).
  • Yuksel, H., 1981. Heterodera fici Kirjanova 1954 in Aegean region. Journal of Turkish Phytopathology, 10 (1): 45-51.

Occurrence and distribution of cyst nematodes, Heterodera spp. (Tylenchida: Heteroderidae) associated with black cabbage, Brassica oleracea var. acephala L. (Brassicales: Brassicaceae) in the Eastern Black Sea Region of Türkiye

Year 2024, Volume: 48 Issue: 2, 139 - 154
https://doi.org/10.16970/entoted.1414404

Abstract

This study was conducted during 2021-2022 to detect and determine distribution and population of cyst nematodes, Heterodera spp. (Tylenchida: Heteroderidae) in black cabbage Brassica oleracea var. acephala L. (Brassicales: Brassicaceae) production areas of the Eastern Black Sea Region of Türkiye. For it, a total of 77 samples were taken from 53 districts belonging to the Artvin, Giresun, Ordu, Rize, and Trabzon provinces in the region. Soil samples were taken from around the root of the kale plants. Nematodes were extracted by using the centrifugal flotation technique. The nematodes were identified using morphological features and molecular analysis based on Polymerase Chain Reaction (PCR) method. For molecular analysis, the ribosomal DNA region including the gene region of 28S ribosomal RNA (rRNA) (ITS1, 5.8S, ITS2) was amplified using primer sets TW81/AB28. Additionally, a species-specific primer set (Car-F/Car-R) covering the Cytochrome Oxidase I (cox1) region of mitochondrial DNA (mtDNA) was used. As a result of the analysis, cyst nematodes Heterodera cruciferae Franklin, 1945, Heterodera carotae Jones, 1950 and Heterodera fici Kirjanova, 1954 species were identified in the kale production areas in the region. Heterodera carotae is the first record of the cyst nematode species in Türkiye. Heterodera cruciferae, H. carotae, and H. fici were detected from the total collected soil samples at 16.9%, 3.9%, and 1.3% relative frequency, respectively. Among all, Giresun was the most infected province with 35.3% infection rate, followed by Trabzon with 26.3%, Ordu with 21.1% and Rize with 13.3%.

Supporting Institution

Ordu Üniversitesi, Bilimsel Araştırmalar Projeleri Koordinasyon Birimi (BAP)

Project Number

B-2205

Thanks

We thank Ordu University for supporting this project by e Scientific Research Project Office (BAP Project No:B-2205).

References

  • Abd-Elgawad, M. M., 2021. Optimizing safe approaches to manage plant-parasitic nematodes. Plants, 10 (9): 1-20.
  • Anonymous, 2023a. Karadeniz Bölgesi (Web page: https://www.efe.name.tr/karadeniz-bolgesi/) (Date accessed: 15 December 2023) (in Turkish).
  • Anonymous, 2023b. Heterodera carotae. (Web page: http://nemaplex.ucdavis.edu/Taxadata/G060S2.aspx) (Date accessed: 15 December 2023).
  • Anonymous, 2024a. About Kale and Collards (Web page: https://www.westcoastseeds.com/blogs/wcs-academy/kale-collards) (Date accessed: 9 March 2024).
  • Anonymous, 2024b. Google Earth (Web page: https://earth.google.com/web/@40.95890424,39.67512947,327. 25744699a,376450.18609285d,30.00000001y,0h,0t,0r/data=OgMKATA) (Date accessed: 9 March 2024).
  • Avendano, F., F. J. Pierce, O. Schabenberger & H. Melakeberhan, 2004. The spatial distribution of soybean cyst nematode in relation to soil texture and soil map unit. Agronomy Journal, 96 (1): 181-194.
  • Ay, A. & R. Kızılkaya, 2021. Ordu ve Giresun illerindeki fındık bahçelerinin toprak özellikleri ile biyolojik özellikleri arasındaki ilişkiler. Toprak Bilimi ve Bitki Besleme Dergisi, 9 (1): 71-78 (in Turkish with abstract in English).
  • Aydinli, G., 2009. Lahana Kist Nematodu (Heterodera cruciferae Franklin) (Nemata: Tylenchida: Heteroderidae)'na Karşı Kimyasal Mücadeleye Alternatif Yöntemler Üzerinde Araştırmalar: Dayanıklı Çeşit Saptanması, Bazı Bitki Ekstraktlarının Etkileri ve Kistlerden Larva Çıkışına Etkili Olan Faktörler. Ondokuz Mayıs Üniversitesi, Fen Bilimleri Enstitüsü,Bitki Koruma Bölümü/Anabilim Dalı (Unpublished) Master Science Thesis, Samsun, Türkiye, 95 s (in Turkish with abstract in English).
  • Aydinli, G. & S. Mennan, 2012. Screening resistance level of Brassicaceae plants to cabbage cyst nematode, Heterodera cruciferae Franklin, 1945 (Tylenchida: Heteroderidae). Turkish Journal of Entomology, 36 (1): 3-10.
  • Balkaya, A. & R. Yanmaz, 2005. Promising kale (Brassica oleracea var. acephala) populations from Black Sea region, Turkey. New Zealand Journal of Crop and Horticultural Science, 33 (1): 1-7.
  • Berney, M. F. & G. W. Bird, 1992. Distribution of Heterodera carotae and Meloidogyne hapla in Michigan carrot production. Journal of Nematology, 24 (4S): 776-778.
  • Chowdhury, I. A., G. Yan & A. Friskop, 2020. Occurrence of vermiform plant-parasitic nematodes in North Dakota corn fields and impact of environmental and soil factors. Canadian Journal of Plant Pathology, 42 (3): 429-444.
  • Di Vito, M. & N. Sasanelli, 1990. The effect of natural and artificial hatching agents on the emergence of juveniles of Heterodera fici. Nematologia Mediterranea, 18 (1): 55-57.
  • Escobar-Avila, I. M., E. Ó. López-Villegas, S. A. Subbotin & A. Tovar-Soto, 2018. First report of Carrot cyst nematode in Mexico: morphological, molecular characterization, and host range study. Journal of Nematology, 50 (2): 229-242.
  • FAO, 2020. FAOSTAT, Crop Data Base. Food and Agriculture Organization United Nations. (Web page: http://www.fao.org/faostat/en/#data/QC/visualize) (Date accessed: August 2022).
  • Fenwick, D. W., 1951. The effect of temperature on the development of potato root eelworm, Heterodera rostochiensis. Annual Applied BioIogy, 38 (3): 615-618.
  • Franklin, M. T., 1945. On Heterodera cruciferae n. sp. of brassicas, and on a Heterodera strain infecting clover and dock. Journal of Helminthology, 21 (2-3): 71-84.
  • Golden, A. M., M. A. Maqbool & F. Zarina, 1988 Redescription of Heterodera fici (Nematoda: Heteroderidae) with SEM observations. Journal of Nematology, 20 (3): 381-391.
  • Goodey, J. B., M. T. Franklin & D. J. Hooper, 1965. The Nematode Parasites of Plants Catalogued under Their Hosts. Common Wealth Agricultural Bureaux, Farnham Royal, Bucks, England. Third Edition, 214 pp.
  • Greco, N, T. D'addabbo, A. Brandonisio & F. Elia, 1993. Damage to Italian crops caused by cyst-forming nematodes. Journal of Nematology, 25 (4S): 832-836.
  • Handoo, Z. A. & S. A. Subbotin, 2018. “Taxonomy, Identification and Principal Species, 365-397”. In: Cyst Nematodes (Eds. R. N. Perry, M. Moens & J. T. Jones). Wallingford, UK, CAB International, 464 pp.
  • Hartman, K. M. & J. N. Sasser, 1985. “Identification of Meloidogyne species on the Basis of Differential Host Test and Perineal-Pattern Morphology, 69-77”. In: An advanced treatise on Meloidogyne Volume II: Methodology (Eds. K. R. Barker, C. C. Carter & J. N. Sasser). North Carolina State University Graphics, Raleigh, North Carolina, USA, 223 pp.
  • Hbirkou, C., G. Welp, K. Rehbein, C. Hillnhütter, M. Daub, M. A. Oliver & S. Pätzold, 2011. The effect of soil heterogeneity on the spatial distribution of Heterodera schachtii within sugar beet fields. Applied Soil Ecology, 51 (1): 25-34.
  • Jabbari, H. & G. Niknam, 2008. SEM observations and morphometrics of the cabbage cyst nematode, Heterodera cruciferae Franklin, 1945, collected where Brassica spp. are grown in Tabriz, Iran. Turkish Journal of Entomology, 32 (3): 253-2628.
  • Jenkins, W. R. B., 1964. A rapid centrifugal-flotation technique for separating nematodes from soil. Plant Disease Reporter, 48: 692.
  • Jensen, H. J., 1972. “Nematodes of Vegetables and Related Crops, 377-409”. In: Economic Nematology (Eds. J. M. Webster), Academic Press, London, 515 pp.
  • Jones, F. G. W., 1950. Observations on the beet eelworm and other cyst-forming species of Heterodera. Annals of Applied Biology, 37 (3): 407-440.
  • Joyce, S. A., A. M. Burnell & T. O. Powers, 1994. Characterization of Heterorhabditis isolates by PCR amplification of segments of mtDNA and rDNA genes. Journal of Nematology, 26 (3): 260-270.
  • Kirjanova, E. S., 1954. Summaries and perspectives in the development of phytonematology in USSR. Zoological Institute of the Academy of Sciences, USSR, Turdy Prob. i Tematicheskikh Soveshchanii, 3 (1): 9-47.
  • Madani, M., J. E. Palomares-Rius, N. Vovlas, P. Castillo & M. Tenuta, 2018. Integrative diagnosis of carrot cyst nematode (Heterodera carotae) using morphology and several molecular markers for an accurate identification. European Journal of Plant Pathology, 150 (4): 1023-1039.
  • Maqbool, M. A., M. Qasim & B. Zarina, 1987. New record of Heterodera fici Kirjanova, 1954 and Meloidogyne javanica (Treub, 1885) Chitwood, 1949 on Ficus carica L. Pakistan Journal of Nematology, 5 (1): 41-42.
  • McCann, J., 1981. Threshold populations of Heterodera cruciferae and H. schachtii causing damage to cabbage seedlings. Plant Disease Reporter, 65 (3): 264-266.
  • Mennan, S. & G. Aydınlı, 2007. “Lahana kist nematodu (Heterodera cruciferae Franklin) (Nemata: Tylenchida: Heteroderidae)’nun yumurta açılımını etkileyen bazı faktörler üzerinde bir araştırma, 27-29”. Türkiye II. Bitki Koruma Kongresi, 80 s (in Turkish with abstract in English).
  • Mennan, S. & Z. Handoo, 2012. Histopathology of Brassica oleracea var. capitata sub var. alba infected with Heterodera cruciferae Franklin, 1945 (Tylenchida: Heteroderidae). Turkish Journal of Entomology, 36 (3): 301-310.
  • Mennan, S., Z. Handoo & O. Ecevit, 2009. Samsun ili lahana ekim alanlarındaki kist nematodları (Tylenchida: Heteroderidae)’nın yayılışı ve bulaşıklık derecesi. Turkish Journal of Entomology, 33 (4): 289-303. (in Turkish with abstract in English)
  • Mulvey, R. H. & A. Morgan Golden, 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):1-59.
  • Mulvey, R. H., 1972. Identification of Heterodera cysts by terminal and cone top structures. Canadian Journal of Zoology, 50 (10): 1277-1292.
  • Muşdağı, S. & U. Gözel, 2015. Çanakkale ili lahana ekim alanlarında kist nematodu türlerinin (Heterodera spp.) belirlenmesi. Türkiye Entomoloji Bülteni, 5 (1): 11-20 (in Turkish with abstract in English).
  • Öztürk, Ö., 2005. Karadeniz: Ansiklopedik Sözlük. Heyamola Yayınları, İstanbul, 1220 pp. (No Title) (in Turkish).
  • Pagan, C., D. Coyne, R. Carneiro, G. Kariuki, N. Luambano, A. Affokpon & V. M. Williamson, 2015. Mitochondrial haplotype-based identification of ethanol-preserved root-knot nematodes from Africa. Phytopathology, 105 (3): 350-357.
  • Pehlivan, H. D., G. Kaşkavalcı, E. B. Kasapoğlu Uludamar, H. Toktay & İ. H. Elekcioğlu, 2020. Identification and prevalence of potato cyst nematodes and root-knot nematodes in the potato production areas of İzmir Province. Turkish Journal of Entomology, 44 (2): 259-272.
  • Ravichandra, N. G., 2014. “Nematode Diseases of Horticultural Crops, 127-205”. In: Horticultural Nematology. Springer, New Delhi, 412 pp.
  • Sambrook, J., E. F. Fritsch & T. Maniatis, 1989. Molecular Cloning: A Laboratory Manual (2nd Editioın). Cold Spring Harbor Laboratory Press, 626 pp.
  • Shepherd, A. M., 1986. “Extraction and Estimation of Cyst Nematodes, 51-58”. In: Laboratory Methods for Work with Plant and Soil Nematodes. (Eds. J. F. Southey). London, UK: Her Majesty’s Stationery Office, 202 pp.
  • Schmidt, K., R. A. Sikora & O. Schuster, 1993. Modelling the population dynamics of the sugar beet cyst nematode Heterodera schachtii. Crop Protection, 12 (7): 490-496.
  • Shubane, A. R., A. Swart, R. Knoetze, L. R. Tiedt & H. Fourie, 2021. Characterization of Heterodera carotae from the Tarlton area, South Africa, and determination of its life cycle under field conditions: a baseline study. Journal of Plant Diseases and Protection, 128 (6): 1637-1655.
  • Stone, A. R. & J. A. Rowe, 1976. Heterodera cruciferae. CIH Descriptions of Plant-Parasitic Nematodes. CABI Publishing, Wallingford. Set 6, No:90. Sturhan, D. & M. Lišková, 2004. Cyst nematodes in the Slovak Republic. Helminthologia, 41 (4): 217-219.
  • Subbotin, S. A., M. Mundo-Ocampo & J. G. Baldwin, 2010. “Description and Diagnosis of Heterodera species, 35-449”. In: Systematics of Cyst Nematodes (Nematoda: Heteroderinae), Vol. 8B. The Netherlands: Koninklijke Brill NV. 414 pp.
  • Subbotin, S. A., A. M. Deimi, J. Zheng & V. N. Chizhov, 2011. Length variation and repetitive sequences of internal transcribed spacer of ribosomal RNA gene, diagnostics and relationships of populations of potato rot nematode, Ditylenchus destructor Thorne, 1945 (Tylenchida: Anguinidae). Nematology, 13 (7): 773-785.
  • Thorne, G., 1961. Principles of Nematology. New York, McGraw-Hill, 553 pp
  • Toktay, H., B. G. Akyol, E. Evlice & M. İmren, 2022. Molecular characterization of Heterodera cruciferae Franklin, 1945 from cabbage fields in Niğde province, Turkey. Molecular Biology Reports, 49 (12): 11557-11562.
  • Turner, S. J. & S. A. Subbotin, 2013. “Cyst Nematodes, 109-143”. In: Plant Nematology (2nd Edition) (Eds. R. N. Perry & M. Moens). CAB International, Wallingford, UK, 542 pp.
  • TUIK, 2021. Türkiye İstatistik Kurumu İstatistik Veri Portalı. (Web page: http://tuik.gov.tr/PreTablo.do?alt_id=1001) (Date accessed: 10 November 2023) (in Turkish).
  • Vural, H., 2008. Lahana Yetiştiriciliği. (Web page: https://www.gencziraat.com/Bahce-Bitkileri/Lahana-Yetistiriciligi-12.html) (Date accessed: 10 November 2023) (in Turkish).
  • Wallace, H. R., 1959. Further observations on some factors influencing the emergence of larvae from cysts of the beet eelworm Heterodera schachtii Schmidt. Nematologica, 4 (4): 245-252.
  • Winslow, R. D., 1955. The effects of some leguminous crops on the soil population level of pea root eelworm. Plant Pathology, 4 (3): 86-88.
  • Yu, Q., E. Ponomareva, D. Van Dyk, M. R. McDonald, F. Sun, M. Madani & M. Tenuta, 2017. First report of the carrot cyst nematode (Heterodera carotae) from carrot fields in Ontario, Canada. Plant Disease, 101 (6): 1056-1056.
  • Yüksel, H., 1973. Türkiye’de bulunan Heterodera (Nematoda: Heteroderidae) türleri, bunların morfolojik ve biyolojik farklılıkları üzerinde araştırmalar. Atatürk Üniversitesi, Ziraat Fakültesi Dergisi, 4 (1): 53-71 (in Turkish with abstract in English).
  • Yuksel, H., 1981. Heterodera fici Kirjanova 1954 in Aegean region. Journal of Turkish Phytopathology, 10 (1): 45-51.
There are 59 citations in total.

Details

Primary Language English
Subjects Nematology
Journal Section Articles
Authors

Buğra Güvercin 0000-0003-4472-4513

Faruk Akyazı 0000-0002-5239-2849

Project Number B-2205
Publication Date
Submission Date January 3, 2024
Acceptance Date April 25, 2024
Published in Issue Year 2024 Volume: 48 Issue: 2

Cite

APA Güvercin, B., & Akyazı, F. (n.d.). Occurrence and distribution of cyst nematodes, Heterodera spp. (Tylenchida: Heteroderidae) associated with black cabbage, Brassica oleracea var. acephala L. (Brassicales: Brassicaceae) in the Eastern Black Sea Region of Türkiye. Turkish Journal of Entomology, 48(2), 139-154. https://doi.org/10.16970/entoted.1414404
AMA Güvercin B, Akyazı F. Occurrence and distribution of cyst nematodes, Heterodera spp. (Tylenchida: Heteroderidae) associated with black cabbage, Brassica oleracea var. acephala L. (Brassicales: Brassicaceae) in the Eastern Black Sea Region of Türkiye. TED. 48(2):139-154. doi:10.16970/entoted.1414404
Chicago Güvercin, Buğra, and Faruk Akyazı. “Occurrence and Distribution of Cyst Nematodes, Heterodera Spp. (Tylenchida: Heteroderidae) Associated With Black Cabbage, Brassica Oleracea Var. Acephala L. (Brassicales: Brassicaceae) in the Eastern Black Sea Region of Türkiye”. Turkish Journal of Entomology 48, no. 2 n.d.: 139-54. https://doi.org/10.16970/entoted.1414404.
EndNote Güvercin B, Akyazı F Occurrence and distribution of cyst nematodes, Heterodera spp. (Tylenchida: Heteroderidae) associated with black cabbage, Brassica oleracea var. acephala L. (Brassicales: Brassicaceae) in the Eastern Black Sea Region of Türkiye. Turkish Journal of Entomology 48 2 139–154.
IEEE B. Güvercin and F. Akyazı, “Occurrence and distribution of cyst nematodes, Heterodera spp. (Tylenchida: Heteroderidae) associated with black cabbage, Brassica oleracea var. acephala L. (Brassicales: Brassicaceae) in the Eastern Black Sea Region of Türkiye”, TED, vol. 48, no. 2, pp. 139–154, doi: 10.16970/entoted.1414404.
ISNAD Güvercin, Buğra - Akyazı, Faruk. “Occurrence and Distribution of Cyst Nematodes, Heterodera Spp. (Tylenchida: Heteroderidae) Associated With Black Cabbage, Brassica Oleracea Var. Acephala L. (Brassicales: Brassicaceae) in the Eastern Black Sea Region of Türkiye”. Turkish Journal of Entomology 48/2 (n.d.), 139-154. https://doi.org/10.16970/entoted.1414404.
JAMA Güvercin B, Akyazı F. Occurrence and distribution of cyst nematodes, Heterodera spp. (Tylenchida: Heteroderidae) associated with black cabbage, Brassica oleracea var. acephala L. (Brassicales: Brassicaceae) in the Eastern Black Sea Region of Türkiye. TED.;48:139–154.
MLA Güvercin, Buğra and Faruk Akyazı. “Occurrence and Distribution of Cyst Nematodes, Heterodera Spp. (Tylenchida: Heteroderidae) Associated With Black Cabbage, Brassica Oleracea Var. Acephala L. (Brassicales: Brassicaceae) in the Eastern Black Sea Region of Türkiye”. Turkish Journal of Entomology, vol. 48, no. 2, pp. 139-54, doi:10.16970/entoted.1414404.
Vancouver Güvercin B, Akyazı F. Occurrence and distribution of cyst nematodes, Heterodera spp. (Tylenchida: Heteroderidae) associated with black cabbage, Brassica oleracea var. acephala L. (Brassicales: Brassicaceae) in the Eastern Black Sea Region of Türkiye. TED. 48(2):139-54.