Screening of Sugar Beet Genotypes to Beet Curly Top Virus and Sugar Beet Cyst Nematode (Heterodera schachtii)

Authors
R. Kazemi 1
M. Saadati 1
A. Mokhtasi 2
M. Pedram 1
M. R. Atighi 1
M. Shams-Bakhsh 1
1 Department of Plant Pathology, Faculty of Agriculture, Tarbiat Modares University, Tehran, Islamic Republic of Iran.
2 Department of Agronomy, FacDepartment of Agronomy, Faculty of Agriculture, Tarbiat Modares University, P. O. Box: 14115-336, Tehran, Islamic Republic of Iran.ulty of Agriculture, Tarbiat Modares University, PO Box 14115-336, Tehran, Iran
10.48311/jast.2025.24129
Abstract
The beet cyst nematode (BCN) (Heterodera schachtii) and beet curly top virus-severe (BCTV-Svr) (Curtovirus betae) are two important pathogens worldwide. In present study, the reaction of 14 genotypes to BCN and BCTV-Svr was separately assessed, using Jolgeh and Sanetta cultivars as susceptible and resistant controls, respectively, in completely randomized design experiments. Reactions were based on the cyst and egg counts and symptoms severity index. Experiments were performed in the greenhouse of Tarbiat Modares University, Tehran, Iran, and were repeated twice independently. Based on the results of initial experiments, the S1-960090, S1-940324, S1-960294, and S1-960284 genotypes resistant to the BCN, were selected for further investigation. Furthermore, the reaction of the four selected genotypes to BCN, BCTV-Svr, and the mixture of the two pathogens was evaluated by analyzing their growth, physiological, and biochemical characteristics, and virus accumulation. Resistant genotypes showed higher levels of defense-related enzymes such as catalase, guaiacol peroxidase, and polyphenol oxidase, whereas susceptible genotypes exhibited significant reductions in photosynthesis, greenness, and chlorophyll a, b, and carotenoid content compared to non-inoculated and resistant plants. This is the first study conducted to search for dual-resistance sources against two devastating pathogens that frequently occur in the sugar beet-growing regions of Iran. Based on the results of this research, genotypes S1-960090 and S1-940324 were identified as resistant to both pathogens and are recommended for breeding purposes.

Keywords

REFERENCES
1. Ahmed, N., Abbasi, M. W., Shaukat, S. S., and Zaki, M. J. 2009. Physiological changes in leaves of mungbean plants infected with Meloidogyne javanica. Phytopathol. Mediterr., 48(2): 262-268.
2. Anzlovar, S., Kovac, M. and Ravnikar, M. 1996. Photosynthetic pigments in healthy and virus-infected potato plantlets (Solanum tuberosum L.) grown in vitro. Phyton, 36:221-230.
3. Beffagna, N. and Lutzu, I. 2007. Inhibition of catalase activity as an early response of Arabidopsis thaliana cultured cells to the phytotoxin fusicoccin. J. Exp. Bot., 58:4183–4194. https://doi.org/10.1093/jxb/erm275
4. Briar, S. S., Wichman, D. and Reddy, G. V. P. 2016. Plant-parasitic nematode problems in organic agriculture. In: Nandwani D (ed) Organic Farming for Sustainable Agriculture. Springer., pp 107–122
5. De Meutter, J., Tytgat, T., Prinsen, E. and et al. 2005. Production of auxin and related compounds by the plant parasitic nematodes Heterodera schachtii and Meloidogyne incognita. Commun. Agric. Appl. Biol. Sci., 70:51–60.
6. De Meutter, J., Tytgat, T., Witters, E. Gheysen, G., Van Onckelen, H., and Gheysen, G. 2003. Identification of cytokinins produced by the plant parasitic nematodes Heterodera schachtii and Meloidogyne incognita. Mol. Plant Pathol., 4:271–277. https://doi.org/10.1046/j.1364-3703.2003.00176.x
7. Debona, D., Rodrigues, F. Á., Rios, J. A. and Nascimento, K. J. T. 2012. Biochemical changes in the leaves of wheat plants infected by Pyricularia oryzae. Phytopathology, 102:1121–1129. https://doi.org/10.1094/PHYTO-06-12-0125-R
8. Doyle, J. J. and Doyle, J. L. 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem. bull., 19:11-15
9. FAO. World Food and Agriculture - Statistical Yearbook 2020. Rome: FAO; 2020.
10. Faria, J. C., Albino, M. M. C., Dias, B. B. A., Cançado, L. J., da Cunha, N. B., Silva, L. D. M. and Aragão, F. J. 2006. Partial resistance to Bean golden mosaic virus in a transgenic common bean (Phaseolus vulgaris L.) line expressing a mutated rep gene. Plant Sci., 171:565–571. https://doi.org/https://doi.org/10.1016/j.plantsci.2006.06.010
11. Ghaemi, R., Pourjam, E., Safaie, N. Mahmoudi, S. B. and Mehrabi, R. 2018. Evaluation of sugar beet cultivars resistance to beet cyst nematode under in vitro conditions. J. Sugar Beet, 34:65–74. https://doi.org/10.22092/jsb.2017.115911.1166
12. Grimsley, N., Hohn, B., Hohn, T. and Walden, R. 1986. “Agroinfection,” an alternative route for viral infection of plants by using the Ti plasmid. Proc. Natl. Acad. Sci. U S A., 83:3282–3286. https://doi.org/10.1073/pnas.83.10.3282
13. Gaur, R. K., Sharma, P. and Czosnek, H. 2022. Geminivirus: Detection, Diagnosis and Management. Elsevier.
14. Harveson, R. M. and Jackson, T. A. 2008. Sugar beet cyst nematode. Univ Nebraska, USA
15. Harveson, R. M., Hanson, L. E., and Hein, G. L. 2009. Compendium of beet diseases and pests (No. Ed. 2). American Phytopathological Society (APS Press)
16. Jing, H. and Strader, L. C. 2019. Interplay of auxin and cytokinin in lateral root development. Int. J. Mol. Sci., 20:486. https://doi.org/10.3390/ijms20030486
17. Julkowska, M. 2018. Releasing the cytokinin brakes on root growth. Plant Physiol., 177:865–866. https://doi.org/10.1104/pp.18.00660
18. Junior, M. A. D., Edzang, R. W. N., Catto, A. L. and Raimundo, J. M. 2022. Quinones as an efficient molecular scaffold in the antibacterial/antifungal or antitumoral arsenal. Int. J. Mol. Sci., 14108. https://doi.org/10.3390/ijms232214108
19. Laohavisit, A., Wakatake, T., Ishihama, N., Laohavisit, A., Wakatake, T., Ishihama, N., Mulvey, H., Takizawa, K., Suzuki, T. and Shirasu, K. 2020. Quinone perception in plants via leucine-rich-repeat receptor-like kinases. Nature, 587:92–97. https://doi.org/10.1038/s41586-020-2655-4
20. Larsen, R. C., Kurowski, C. J., and Miklas, P. N. 2010. Two independent quantitative trait loci are responsible for novel resistance to Beet curly top virus in common bean landrace G122. Phytopathology, 100:972-978.
21. Li, L. and Steffens, J. C. 2002. Overexpression of polyphenol oxidase in transgenic tomato plants results in enhanced bacterial disease resistance. Planta, 215:239–247. https://doi.org/10.1007/s00425-002-0750-4
22. Li, Q., Qin, X., Qi, J., Dou, W., Dunand, C., Chen, S. and He, Y. 2020. CsPrx25, a class III peroxidase in Citrus sinensis, confers resistance to citrus bacterial canker through the maintenance of ROS homeostasis and cell wall lignification. Hortic. Res., 7:192. https://doi.org/10.1038/s41438-020-00415-9
23. Macarisin, D., Cohen, L., Eick, A., Rafael, G.I.N.A.T., Belausov, E.D.U.A.R.D., Wisniewski, M. and Droby, S.A.M.I.R. 2007. Penicillium digitatum suppresses production of hydrogen peroxide in host tissue during infection of citrus fruit. Phytopathology, 97(11):1491–1500. https://doi.org/10.1094/PHYTO-97-11-1491
24. Maehly, A. C. and Chance, B. 1954. The assay of catalases and peroxidases. Methods Biochem. Anal., 1:357–424. https://doi.org/10.1002/9780470110171.ch14
25. Montazeri, R., Shams-Bakhsh, M., Mahmoudi, S.B. and Rajabi, A. 2016. Evaluation of sugar beet lines for resistance to Beet curly top viruses. Euphytica, 210:31–40. https://doi.org/10.1007/S10681-016-1693-3
26. Motieeian, L., Nasr Esfahani, M. and Olia, M. 2016. Screening of sugar beet genotypes to beet cyst nematode. J. Sugar Beet, 32(2), 107-121.
27. Nafady, N.A., Sultan, R., El-Zawahry, A.M., Mostafa, Y.S., Alamri, S., Mostafa, R.G., Hashem, M. and Hassan, E.A. 2022. Effective and promising strategy in management of tomato root-knot nematodes by Trichoderma harzianum and Arbuscular Mycorrhizae. Agronomy, 12(2):315. https://doi.org/10.3390/agronomy12020315
28. Nielsen, E. L., Baltensperger, D. D., Kerr, E. D. and Rife, C. L. 2003. Host suitability of rapeseed for Heterodera schachtii. J. Nematol., 35(1), 35-38.
29. Saadati, M., Rajabi, A. and Shams-Bakhsh, M. 2021. Identification of resistant sugar beet (Beta vulgaris L.) genotypes against beet curly top disease. J. Agr. Sci. Tech., 23(2):473–484
30. Saadati, M., Ayari, M. and Shams-bakhsh, M. 2023. The effect of beet curly top virus on growth and phytochemical constituents of coriander (Coriandrum sativum L.). S. Afr. J. Bot., 162:804-812. https://doi.org/10.1016/j.sajb.2023.10.009
31. Saadati, M., Azarian, A., Ayari, M. and Shams-bakhsh, M. 2024. Screening of coriander (Coriandrum sativum L.) genotypes to beet curly top virus-severe and beet curly top Iran virus infection. Physiol. Mol. Plant Pathol., 129:102210. https://doi.org/10.1016/j.pmpp.2023.102210
32. Sahebani, N. and Gholamrezaee, N. 2022. The ability of Meloidogyne javanica to suppress salicylic acid-induced plant defence responses. Nematology, 1–10. https://doi.org/https://doi.org/10.1163/15685411-bja10145
33. Santos, C. and Franco, O. L. 2023. Pathogenesis-Related Proteins (PRs) with enzyme activity activating plant defense responses. Plants, 12(11):2226.
34. Shah, D.A. and Madden, L.V. 2004. Nonparametric analysis of ordinal data in designed factorial experiments. Phytopathology, 94(1):33–43. https://doi.org/10.1094/PHYTO.2004.94.1.33
35. Siguemoto, E. S. and Gut, J. A. W. 2017. Validation of spectrophotometric microplate methods for polyphenol oxidase and peroxidase activities analysis in fruits and vegetables. Food Sci. Technol., 37:148–153
36. Vasil’eva, I. S., Vanyushkin, S. A., Zinov’eva, S. V., Udalova, Z. V., Bolychevtseva, Y. V. and Paseshnichenko, V. A. 2003. Photosynthetic pigments of tomato plants under conditions of biotic stress and effects of furostanol glycosides. Appl. Biochem. Microbiol., 39:606–612. https://doi.org/10.1023/A:1026290704338
37. Wang, K.l., Deng, Q.q., Chen, Jw. and Shen, W. K. 2020. Physiological and molecular mechanisms governing the effect of virus-free chewing cane seedlings on yield and quality. Sci. Rep., 10: 10306. https://doi.org/10.1038/s41598-020-67344-4
38. Warren, C. R. 2008. Rapid measurement of chlorophylls with a microplate reader. J. Plant Nutr., 31:1321–1332. https://doi.org/10.1080/01904160802135092
39. Zhang, Y. B., Xie ZhongKui, X. Z., Wang RuoYu, W. R., Kutcher, H. R., Wang YaJun, W. Y. and Guo ZhiHong, G. Z. 2014. Single and mixed viral infection reduced growth and photosynthetic pigment content, damaged chloroplast ultrastructure and enhanced virus accumulation in oriental lily (Lilium auratum cv. Sorbonne). Philippine Agric. Sci., 97:138–147.
Journal of Agricultural Science and Technology
Volume 27, Issue 5
July and August 2025
Pages 1199-1213