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Molecular characterization of Heterodera cruciferae Franklin, 1945 from cabbage fields in Niğde province, Turkey

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A Correction to this article was published on 14 November 2022

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Abstract

Background

The aim of this study was to identified cyst nematodes in the cabbage production areas in Niğde Province by molecular methods to underpin decision making for field control. The sequences of ribosomal DNA region (rDNA-ITS) and cytochrome oxidase subunit 1 (mtDNA-COI) were used for the first time for identification Heterodera cruciferae (cabbage cyst nematode) in Turkey.

Methods and Results

Heterodera cruciferae populations extracted from cabbage growing areas of Niğde Province and investigated using sequences of rDNA-ITS and mtDNA-COI. Similarities and differences between 13 geographic populations of H. cruciferae were detected in surveys during 2020–2021. DNA from single cysts was successfully amplified, and genetic variability was revealed within nematode populations. Based on these results, H. cruciferae is reported for the first time from Niğde Province, Turkey. This study showed clear discrimination among the sampled populations of H. cruciferae.

Conclusion

This finding is important for control and managing cabbage cyst nematode in cabbage fields in Turkey as more than one Heterodera spp. can occur. Future studies should investigate the population dynamics and control of H. cruciferae in fields in the sampled districts.

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Data Availability

All data needed to conduct this study is provided within the manuscript.

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References

  1. TÜİK (2021) http://tuik.gov.tr/PreTablo.do?alt_id=1001 Türkiye İstatistik Kurumu, Ankara. Accessed 09 November 2021

  2. Bridge J, Starr JL (2007) Plant Nematodes of Agricultural Importance: A Color Handbook. Manson publishing, London

    Book  Google Scholar 

  3. Rimmer SR, Shattuck VI, Buchwaldt L (2007) Compendium of brassica diseases. APS Press, New York

    Google Scholar 

  4. Hallmann J, Meressa BH (2018) Nematode Parasites of Vegetables. In: Luc M, Sikora RA, Bridge J (eds) Plant parasitic nematodes in subtropical and tropical agriculture, 3rd edn. CABI Publishing, Wallingford, pp 346–410

    Chapter  Google Scholar 

  5. Chizhov VN, Pridannikov MV, Nasonova LV, Subbotin SA (2009) Heterodera cruciferae Franklin, 1945, a parasite of Brassica oleraceae L. from floodland fields in the Moscow region. Russ J Nematol 17(2):107–113

    Google Scholar 

  6. Franklin MT (1945) On Heterodera cruciferae n. sp. of brassicas, and on a Heterodera strain infecting clover and dock. J Helminthol 2:71–84

    Article  Google Scholar 

  7. Jabbari H, Niknam G (2008) SEM observations and morphometrics of the cabbage cyst nematode, Heterodera cruciferae Franklin, 1945, collected where Brassica spp. are grown in Tabriz, Iran. Turk J Zool 32(3):253–262

    Google Scholar 

  8. Mennan S, Handoo Z(2012) Heterodera cruciferae Franklin, 1945 (Tylenchida: Heteroderidae) ile bulaşık Brassica oleracea var. capitata subvar. albanın histopatojisi. Turk J Entomol 36 (3):301–310

  9. Stone AR, Rowe JA (1976) Heterodera cruciferae. CIH Descriptions of plant-parasitic nematodes CABI Publishing, Wallingford

    Google Scholar 

  10. Sturhan D, Lišková M (2004) Cyst nematodes in the Slovak Republic. Helminthologia 41(4):217–219

    Google Scholar 

  11. Ravichandra NG (2014) Horticultural nematology. Springer India, New Dehli

    Book  Google Scholar 

  12. Turner SJ, Subbotin SA (2013) Cyst nematodes. In: Moens M, Perry RN (eds) Plant nematology, 2nd edn. CABI Publishing, Wallingford, pp 109–143

    Chapter  Google Scholar 

  13. Handoo ZA, Subbotin SA(2018) Taxonomy, identification and principal species. In: Perry RN, Moens, M. and Jones JT (eds) Cyst nematodes, Wallingford, UK, CAB International pp 365–397

  14. Perry RN, Wright DJ, Chitwood DJ (2013) Reproduction, physiology and biochemistry. In: Moens M, Perry RN (eds) Plant nematology, 2nd edn. CABI Publishing, Wallingford, pp 219–245

    Chapter  Google Scholar 

  15. McCann J (1981) Threshold populations of Heterodera cruciferae and Heterodera schachtii causing damage to cabbage seedlings. Plant dis rep 65:264–266

    Article  Google Scholar 

  16. Sasanelli N, Vovlas N, Trisciuzzi N, Cantalapiedra-Navarrete C, Palomares-Rius JE, Castillo P (2013) Pathogenicity and host–parasite relationships of Heterodera cruciferae in cabbage. Plant dis 97(3):333–338

    Article  CAS  PubMed  Google Scholar 

  17. Anonymous (1987) Nematodes. In: University of California Statewide Integrated Pest Management Project. Integrated Pest Management for Cole Crops and Lettuce. Division of Agriculture and Natural Resources. 3307-81-88

  18. Vrain TC, Wakarchuk DA, Levesque AC, Hamilton RI (1992) Intraspecific rDNA restriction fragment length polymorphism in the Xiphinema americanum group. Fund Appl Nematol 15(6):563–573

    Google Scholar 

  19. Subbotin SA, Deimi AM, Zheng J, Chizhov VN (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

    Article  CAS  Google Scholar 

  20. Yüksel H(1966) Doğu Karadeniz kıyı bölgelerinde bulunan Meloidogyne incognita, Heterodera cruciferae ve Tylenchulus semipenetrans’ ın bazı önemli devreleri üzerinde morfolojik çalışmalar. Atatürk Üniversitesi Ziraat Fakültesi Zirai Araştırma Enstitüsü Teknik Bülteni, No: 15, pp 21

  21. Ecevit O(1975) Lahana kist nematodu (Heterodera cruciferae Franklin) üzerinde biyolojik ve morfolojik çalışmalar. Atatürk Ü. Yayınları, No: 376. İşletme Fakültesi Yayınları No:180, Araştırma Serisi No: 111

  22. Bora A (1970) Studies on plant-parasitic nematodes in the Black Sea region and their distribution and possibilities for chemical control. Bitki Koruma Bulteni 10(1):53–71

    Google Scholar 

  23. Mennan S, Handoo ZA (2006) Plant-parasitic nematodes associated with cabbages (Brassica oleracea) in Samsun (middle Black Sea Region), Turkey. Nematropica 36(1):99–106

    Google Scholar 

  24. Kepenekci İ (2014) Plant parasitic nematodes (Tylenchida: Nematoda) in Turkey. Pak J Nematol 32(1):11–31

    Google Scholar 

  25. Fenwick DW (1940) Methods for the recovery and counting of cysts of Heterodera schachtii from soil. J Helminthol 18(4):155–172

    Article  Google Scholar 

  26. 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. Mol Biol Evol 23(9):1792–1800. https://doi.org/10.1093/molbev/msl044

    Article  CAS  PubMed  Google Scholar 

  27. Subbotin SA, Vovlas N, Yeates GW, Hallmann J, Kiewnick S, Chizhov VN, Manzanilla-Lopez RH, Inserra RN, Castillo P (2015) Morphological and molecular characterisation of Helicotylenchus pseudorobustus (Steiner, 1914) Golden, 1956 and related species (Tylenchida: Hoplolaimidae) with a phylogeny of the genus. Nematology 17(1):27–52

    Article  Google Scholar 

  28. Derycke S, Remerie T, Vierstraete A, Backeljau T, Vanfleteren J, Vincx M, Moens T (2005) Mitochondrial DNA variation and cryptic speciation within the free-living marine nematode Pellioditis marina. Mar Ecol Prog Ser 300:91–103

    Article  CAS  Google Scholar 

  29. Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, USA

    Google Scholar 

  30. Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547–1549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Subbotin SA, Mundo-Ocampo M, Baldwin JG (2010) Description and Diagnosis of Heterodera species. In: Hunt DJ, Perry RN (eds) Systematics of cyst nematodes (Nematoda: Heteroderinae), Part A. Brill, Leiden, pp 7–349

    Chapter  Google Scholar 

  32. Mehalaine K, Imren M, Özer G, Hammache M, Dababat AA (2020) Molecular identification and phylogenetic diversity of cereal cyst nematodes (Heterodera spp.) populations from Algeria. Nematropica 50(2):134–143

    Google Scholar 

  33. Escobar-Avila IM, López-Villegas E, Subbotin SA, Tovar-Soto A (2018) First report of carrot cyst nematode Heterodera carotae in Mexico: morphological, molecular characterization, and host range study. J nematol 50(2):229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Swart A, Knoetze R (2020) Interesting new facts on Heterodera schachtii (Nematoda: Heteroderidae) from South Africa. S Afr J Plant Soil 37(4):326–329

    Article  Google Scholar 

  35. Winslow RD (1954) Provisional lists of host plants of some root eelworms (Heterodera spp.). Ann Appl Biol 41(4):591–605

    Article  Google Scholar 

  36. Yüksel H(1966) ab) “Heterodera schachtii, Schmidt 1871 ile Türkiye’de yeni bulunan H. cruciferae Franklin, 1945, Sist nematodları üzerinde mukayeseli morfolojik çalışmalar.” Atatürk Üniversitesi, Ziraat Fakültesi, Zirai Araştırma Enstitüsü Teknik Bülteni, No: 8, 23 s, Erzurum

  37. Erdal F, Durmuş F, Kepenekçi İ, Ökten ME (2001) Türkiye’de tahıl, baklagil, endüstri bitkileri, sebze, meyve, bağ ve turunçgil alanlarında saptanan Tylenchida (Nematoda) türlerinin ilk listesi. Turk Entomol Derg 25(1):49–64

    Google Scholar 

  38. Mennan S, Handoo Z, Ecevit O (2009) Samsun ili lahana ekim alanlarındaki kist nematodları (Tylenchida: Heteroderidae)’nın yayılışı ve bulaşıklık derecesi. Turk Entomol Derg 33(4):289–303

    Google Scholar 

  39. Aydınlı G, Mennan S(2012) Screening resistance level of Brassicaceae plants to cabbage cyst nematode, Heterodera cruciferae Franklin, 1945 (Tylenchida: Heteroderidae). Turk Entomol Derg 36: 3–10

  40. Muşdağı S, Gözel U (2015) Çanakkale ili lahana ekim alanlarında kist nematodu türlerinin (Heterodera spp.) belirlenmesi. Türk Entomol Bült 5(1):11–20

    Article  Google Scholar 

  41. Oro V (2018) Domestikacija kupusa i cistolika nematoda kupusa, Heterodera cruciferae (nematoda: Heteroderidae). Biljni lekar 46(3):368–374

    Google Scholar 

  42. Cui JK, Erginbas-Orakci G, Peng H, Huang W, Liu S, Qiao F, İmren M, Dababat AA, Peng DL (2016) First report of sugar beet nematode, Heterodera schachtii Schmidt, 1871 (Nemata: Heteroderidae) in sugar beet growing areas of Sanliurfa, Turkey. Turk Entomol Derg 40(3):303–314

    Google Scholar 

  43. Amiri S, Subbotin SA, Moens M (2002) Identification of the beet cyst nematode Heterodera schachtii by PCR. Eur J Plant Pathol 108(6):497–506

    Article  CAS  Google Scholar 

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Acknowledgements

This study was funded by TUBITAK project no. 219 O 455 of (Turkey Scientific and Technical Research Council). The authors thank Prof. Ian Riley for advice during preparation of this manuscript, A/Prof. Eminur Elci for asissited molecular analyses in Nigde Omer Halisdemir University and A/Prof. Goksel Ozer in Bolu Abant Izzet Baysal for to molecular analyses. Authors would like to express their gratitude to cabbage farmers who allowed them to take soil samples from their fields in Nigde province.

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Authors and Affiliations

  1. Department of Plant Production and Technologies, Faculty of Agricultural Sciences and Technologies, University of Nigde, Nigde, Turkey

    Halil Toktay & Badel G. Akyol

  2. Department of Plant Protection, Faculty of Agriculture and Natural Sciences, University of Bolu Abant Izzet Baysal, Bolu, Turkey

    Mustafa İmren

  3. Department of Plant Protection, Faculty of Agricultural Sciences and Technologies, Sivas University of Science and Technology, 58140, Sivas, Turkey

    Emre Evlice

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  1. Halil Toktay
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Contributions

Contributions HT planed and designed the experimental work and wrote the manuscript. HT and BGA performed the laboratory work and experimental data. HT, EE and MI drafted the manuscript. All authors reviewed the manuscript critically and approved the submission of the final manuscript.

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Correspondence to Halil Toktay.

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The authors declare that they have no conflict of interest. All authors read the study and showed their willingness to publish this study. This manuscript does not contain any research activity involving the animals or human participants performed by any of the authors.

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The original online version of this article was revised: The affiliation of the third author Prof. Emre Evlice was incorrectly published. It is corrected as "Department of Plant Protection, Faculty of Agricultural Sciences and Technologies, Sivas University of Science and Technology, 58140, Sivas, Turkey

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Toktay, H., Akyol, B.G., Evlice, E. et al. Molecular characterization of Heterodera cruciferae Franklin, 1945 from cabbage fields in Niğde province, Turkey. Mol Biol Rep 49, 11557–11562 (2022). https://doi.org/10.1007/s11033-022-07860-w

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