Türkiye’de patates üretim alanlarında, Steinernema feltiae Filipjev, 1934 (Rhabditida: Steinernematidae) ve Heterorhabditis bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae) genetik çeşitliliği

Abstract

Entomopatojen nematodlar (EPN) en önemli biyolojik mücadele ajanlarından biridir ve çeşitli böcek zararlılarına karşı biyolojik savaşta başarılarını kanıtlamıştır. Ancak çeşitli türlerin ve EPN popülasyonlarının genetik yapısına ilişkin bilgiler sınırlıdır. Bu nedenle, bu çalışma, patates alanlarından elde edilen EPN'lerin filogenetik çeşitliliğini ortaya koymak ve tel kurtlarının, özellikle Agriotes spp. (Coleoptera: Elateridae) türlerinin mücadelesi için alternatif mücadele yöntemlerini belirlemek amacıyla 2020 yılında Bolu Abant İzzet Baysal Üniversitesi’nde yapılmıştır. Ribozomal DNA dizileme yoluyla, Steinernema ve Heterorhabditis türlerinin izolatları arasındaki genetik farklılıklar araştırılmıştır. Afyonkarahisar, Bolu, İzmir, Sivas, Niğde, Kayseri ve Konya illerini kapsayan geniş bir örnekleme ile, toplamda 795 hektarlık bir alanı kapsayarak, örneklerin %10'unu oluşturan iki EPN izolatının elde edilmiştir. Moleküler karakterizasyon, ribozomal DNA dizileme içermekte ve 41 popülasyonun dizileriyle incelendiğinde, Steinernema feltiae Filipjev, 1934 (Rhabditida: Steinernematidae) ve Heterorhabditis bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae)’nın varlığını doğrulayarak, çoğu Steinernema ve Heterorhabditis kladlerinde yer almıştır. Bu araştırma, bu EPN'lerin Türkiye'deki önemli patates yetiştirme alanlarında yaygın olarak bulunduğunu göstermekte ve bunların tarımsal öneme sahip arthropod zararlılara karşı biyolojik savaşta potansiyellerini vurgulamaktadır.

Keywords

• Faydalı nematodlar
• genetik çeşitlilik
• ribosomal DNA sekans

Genetic diversity of Steinernema feltiae Filipjev, 1934 (Rhabditida: Steinernematidae) and Heterorhabditis bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae) in potato production areas of Türkiye

Abstract

Entomopathogenic nematodes (EPNs) are one of the most important biological control agents and have proved their biocontrol success against a variety of insect pests. However, limited knowledge exists regarding the genetic structure of various species and populations of EPNs. Thus, this study was conducted to isolate and elucidate the EPN's phylogenetic diversity sourced from potato (Solanum tuberosum L.) (Solanales: Solanaceae) crops in 2020 at Bolu Abant Izzet Baysal University. Through ribosomal DNA sequencing, we investigated genetic variability within and among isolates of Steinernema and Heterorhabditis species. Widespread sampling across Afyonkarahisar, Bolu, İzmir, Sivas, Niğde, Kayseri, and Konya provinces, covering a total area of 795 hectares, led to the recovery of two EPN isolates, constituting 10% of the samples. Molecular characterization involved ribosomal DNA sequencing, which, upon integration with sequences from 41 populations, confirmed the identification of Steinernema feltiae Filipjev, 1934 (Rhabditida: Steinernematidae) and Heterorhabditis bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae), displaying monophyly in most Steinernema and Heterorhabditis clades, respectively. This survey emphasizes the common occurrence of these EPNs in key potato-growing areas in Türkiye, highlighting their biocontrol potential against arthropod pests of agricultural importance.

Keywords

• Beneficial nematodes
• genetic variability
• ribosomal DNA sequencing

References

1. Adams, B. J., 1998. Species concepts and the evolutionary paradigm in modem nematology. Journal of Nematology, 30 (1): 1-21.
2. Akhurst, R. J. & R. A. Bedding, 1986. Natural occurrence of insect pathogenic nematodes (Steinernematidae and Heterorhabditidae) in soil in Australia. Australian Journal of Entomology, 25 (3): 241-244.
3. Bhat, A. H., A. K. Chaubey & T. H. Askary, 2020. Global distribution of entomopathogenic nematodes, Steinernema and Heterorhabditis. Egyptian Journal of Biological Pest Control, 30 (1): 1-15.
4. Boemare, N., 2002. Interactions between the partners of the entomopathogenic bacterium nematode complexes, Steinernema-Xenorhabdus and Heterorhabditis-Photorhabdus. Nematology, 4 (5): 601-603.
5. Canhilal, R., L. Waeyenberge, H. Toktay, R. Bozbuga, R. Çerintas & M. Imren, 2016. Distribution of Steinernematids and Heterorhabditids (Rhabditida: Steinernematidae and Heterorhabditidae) in the southern Anatolia region of Turkey. Egyptian Journal of Biological Pest Control, 26 (4): 1-6.
6. Del Pino, F. G. & A. Palomo, 1996. Natural occurrence of entomopathogenic nematodes (Rhabditida: Steinernematidae and Heterorhabditidae) in Spanish soils. Journal of Invertebrate Pathology, 68 (1): 84-90.
7. Dreyer, J., A. P. Malan & L. M. Dicks, 2018. Bacteria of the genus Xenorhabdus, a novel source of bioactive compounds. Frontiers in Microbiology, 9 (1): 1-14.
8. Ehlers, R. U., 1996. Current and future use of nematodes in biocontrol: practice and commercial aspects with regard to regulatory policy issues. Biocontrol Science and Technology, 6 (3): 303-316.

9. Emelianoff, V., N. Le Brun, S. Pages, S. P. Stock, P. Tailliez, C. Moulia & M. Sicard, 2008. Isolation and identification of entomopathogenic nematodes and their symbiotic bacteria from Hérault and Gard (Southern France). Journal of Invertebrate Pathology, 98 (2): 211-217.
10. FAO, 2021. FAOSTAT, Crop Data Base. Food and Agriculture Organization United Nations. (Web page: http://www.fao.org/faostat/en/#data/QC/visualize) (Date accessed: January 2023).
11. Forst, S., B. Dowds, N. Boemare & E. Stackebrandt, 1997. Xenorhabdus and Photorhabdus spp.: Bugs that kill bugs. Annual Review of Microbiology, 51 (1): 47-72.
12. Furlan, L. & M. Tóth, 2007. Occurrence of click beetle pest (Coleoptera, Elateridae) in Europe as detected by pheromone traps: Chalfant Survey results of 1998-2006. IOBC/WPRS Bulletin, 30 (7): 1-19.
13. Furlan, L., I. Benvegnù, M. F. Bilò, J. Lehmhus & E. Ruzzier, 2021. Species identification of wireworms (Agriotes spp.; Coleoptera: Elateridae) of agricultural importance in Europe: A new "Horizontal identification table". Insects, 12 (6): 1-12.
14. Garriga, A., A. Morton, A. Ribes & F. Garcia-del-Pino, 2020. Soil emergence of Drosophila suzukii adults: a susceptible period for entomopathogenic nematodes infection. Journal of Pest Science, 93 (2): 639-646.
15. Grewal, P. S., 2012. ‘‘Entomopathogenic Nematodes as Tools in Integrated Pest Management, 162-236’’. In: Integrated Pest Management: Principles and Practice (Eds. D. P. Abrol & U. Shankar). CAB International, Wallingford, UK, 489 pp.
16. Hashmi, G., I. Glazer & R. Gaugler, 1996. Molecular comparisons of entomopathogenic nematodes using randomly amplified polymorphic DNA (RAPD) markers. Fundamental and Applied Nematology, 19 (4): 399-406.
17. Hazir, S., H. K. Kaya, S. P. Stock & N. Keskin, 2003a. Entomopathogenic nematodes (Steinernematidae and Heterorhabditidae) for biological control of soil pests. Turkish Journal of Biology, 27 (4): 181-202.
18. Hazir, S., N. Keskin, S. P. Stock, H. K. Kaya & S. Özcan, 2003b. Diversity and distribution of entomopathogenic nematodes (Rhabditida: Steinernematidae and Heterorhabditidae) in Turkey. Biodiversity & Conservation, 12 (2): 375-386.
19. Hominick, W. M., B. R. Briscoe, F. G. Del Pino, J. Heng, D. J. Hunt, E. Kozodoy & M. Yoshida, 1997. Biosystematics of entomopathogenic nematodes: current status, protocols and definitions. Journal of Helminthology, 71 (4): 271-298.
20. Joyce, S. A., A. Reid, F. Driver & J. Curran, 1994. Application of polymerase chain reaction (PCR) methods to the identification of entomopathogenic nematodes. Biotechnology, 5 (2):178-187.
21. Kaya, H. K., & S. P. Stock, 1997. ‘‘Techniques in Insect Nematology, 281-324’’. In: Manual of Techniques in Insect Pathology (Eds. L. Lacey). Academic Press, 448 pp.
22. Keiser, A., M. Häberli & P. Stamp, 2012. Quality deficiencies on potato (Solanum tuberosum L.) tubers caused by Rhizoctonia solani, wireworms (Agriotes ssp.) and slugs (Deroceras reticulatum, Arion hortensis) in different farming systems. Field Crops Research, 128 (6): 147-155.
23. Keskin, N., Z. Kirbas & N. Özer, 1995. Occurrence of entomopathogenic nematodes (Steinernematidae: Heterorhabditidae) in Turkey. Nematologica, 41 (1-4), 639-640.
24. 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.
25. Laznik, Ž., T. Ó. T. H. Tímea, T. Lakatos, M. Vidrih & S. Trdan, 2009. First record of a cold-active entomopathogenic nematode Steinernema kraussei (Steiner) (Rhabditida: Steinernematidae) in Slovenia. Acta Agriculturae Slovenica, 93 (1): 37-42.
26. Librado, P. & J. Rozas, 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25 (11): 1451-1452.
27. Liu, J., R. E. Berry & M. S. Blouin, 1999. Molecular differentiation and phylogeny of entomopathogenic nematodes (Rhabditida: Heterorhabditidae) based on ND4 gene sequences of mitochondrial DNA. The Journal of Parasitology, 85 (4): 709-715.
28. Nadler, S. A., E. Bolotin & S. P. Stock, 2006. Phylogenetic relationships of Steinernema travassos, 1927 (Nematoda: Cephalobina: Steinernematidae) based on nuclear, mitochondrial and morphological data. Systematic Parasitology, 63 (3): 159-179.
29. Özdemir, E., E. İnak, E. Evlice, E. Yüksel, R. A. Delialioğlu & I. A. Susurluk, 2021. Effects of insecticides and synergistic chemicals on the efficacy of the entomopathogenic nematode Steinernema feltiae (Rhabditida: Steinernematidae) against Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). Crop Protection, 144 (4): 105605.
30. Peat, S. M., B. C. Hyman, & B. J. Adams, 2009. ‘‘Phylogenetics and Population Genetics of Entomopathogenic and Insect-Parasitic Nematodes, 166-184’’. In: Insect Pathogens: Molecular Approaches and Techniques (Eds. S. P. Stock, I. Glazer, N. Boemare & J. Vandenberg). CABI, Oxfordshire, UK, 417 pp.
31. Peçen, A. & İ. Kepenekci, 2022. Efficacy of entomopathogenic nematode isolates from Turkey against wheat stink bug, Aelia rostrata Boheman (Hemiptera: Pentatomidae) adults under laboratory conditions. Egyptian Journal of Biological Pest Control, 32 (1): 91.
32. Poinar Jr, G. O., G. K. Karunakar & H. David, 1992. Heterorhabditis indicus n. sp. (Rhabditida: Nematoda) from India: separation of Heterorhabditis spp. by infective juveniles. Fundamental and Applied Nematology, 15 (5): 467-472.
33. Reddy, G. V. & K. Tangtrakulwanich, 2014. Potential application of pheromones in monitoring, mating disruption, and control of click beetles (Coleoptera: Elateridae). International Scholarly Research Notices, 2014 (1): 531061.
34. Shamseldean, M. M. & M. M. Abd-Elgawad, 1994. Natural occurrence of insect pathogenic nematodes (Rhabditida: Heterorhabditidae) in Egyptian soils. Afro-Asian Journal of Nematology, 4 (2): 151-154.
35. Shoemaker, J. S. & W. M. Fitch, 1989. Evidence from nuclear sequences that invariable sites should be considered when sequence divergence is calculated. Molecular Biology and Evolution, 6 (3): 270-289.
36. Stock, S. P. & D. J. Hunt, 2005. Morphology and Systematics of Nematodes Used in Biocontrol, 3-43’’. In: Nematodes as Biocontrol Agents (Eds. P. S. Grewal, R. Ehlers & D. Shapıro-Ilan). Wallingford UK: CABI Publishing, 505 pp.
37. Stock, S. P., 2009. ‘‘Molecular Approaches and the Taxonomy of Insect-Parasitic and Pathogenic Nematodes, 71-94’’. In: Insect Pathogens: Molecular Approaches and Techniques (Eds. S. P. Stock, I. Glazer, N. Boemare & J. Vandenberg). CABI, Oxfordshire, 417 pp.
38. Tarasco, E., O. Triggiani, M. Zamoum & M. Oreste, 2016. Natural enemies emerged from Thaumetopoea pityocampa (Denis & Sciffermüller) (Lepidoptera Notodontidae) pupae in Southern Italy. Redia, 98 (1): 103-108.
39. Tavaré, S., 1984. Line-of-descent and genealogical processes, and their applications in population genetics models. Theoretical Population Biology, 26 (2): 119-164.
40. Wakil, W., S. Gulzar, S. M. Prager, M. U. Ghazanfar & D. I. Shapiro‐Ilan, 2023. Efficacy of entomopathogenic fungi, nematodes and spinetoram combinations for integrated management of Thrips tabaci. Pest Management Science, 79 (9): 3227-3238.
41. Wright, P. J., 1992. Cool temperature reproduction of Steinernematid and Heterorhabditid nematodes. Journal of Invertebrate Pathology, 60 (2): 148-151.
42. Yang, Z., 1994. Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: approximate methods. Journal of Molecular Evolution, 39 (3): 306-314.
43. Yavuzaslanoglu, E., U. Gozel, C. Gozel & M. Aydogdu, 2021. Distribution of the entomopathogenic nematodes in apple growing areas of Karaman, Turkey. Pakistan Journal of Nematology, 39 (1): 53-62
44. Yüksel, E., 2022. Biocontrol potential of endosymbiotic bacteria of entomopathogenic nematodes against the tomato leaf miner, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Egyptian Journal of Biological Pest Control, 32 (1): 135.
45. Yüksel, E. & R. Canhilal, 2019. Isolation, identification, and pathogenicity of entomopathogenic nematodes occurring in Cappadocia Region, Central Turkey. Egyptian Journal of Biological Pest Control, 29 (6): 1-7.