Developing virus-free grapevine explants by using silver-nanoparticles and its comparison with chemo and thermotherapy-based approaches

Volume 12, Issue 1
March 2023
Pages 15-27

Document Type : Original Research

Authors

1 Department of Horticulture, Faculty of Agriculture, Ferdowsi University of Mashhad, Iran.

2 Department of Plant Viruses, Iranian Research Institute of Plant Protection, Tehran, Iran.

3 Research and Development Director, Goharbar Co., Ferdowsi University of Mashhad, Iran.

Abstract
Grapevine viruses cause significant losses in the yield of grape. This study describes applying silver nanoparticles (AgNPs) to produce virus-free grapevine plants and compares it with chemo and thermotherapy. Preliminary molecular analysis proved the presence of Grapevine fanleaf virus (GFLV) and grapevine leafroll-associated virus-1 (GLRaV-1) in the ʻAsgariʼ, ʻPeykaniʼ, and ʻShahaniʼ cultivar samples, then single node explants were cultivated in the MS medium. Thermotherapy at 35 ± 1 ºC and cycles of 35/38 ± 1 ºC, chemotherapy with ribavirin 0, 20, 25, and 30 μg.ml-1 and using AgNPs at 0, 10, 15, and 20 ppm in medium and 40, 50, and 60 ppm sprayed during acclimatization stage were applied to obtain virus-free explants. The results indicated that using 20 ppm AgNPs in medium and AgNPs combined treatment (15 ppm AgNPs in medium and sprayed with 50 ppm AgNPs in the acclimatization stage) were the most effective treatments for the elimination of viruses. The best treatment led to 100% eradication of GLRaV-1 and 67% of GFLV in ʻAsgariʼ, 100% eradication of GLRaV-1 and GFLV in ʻPeykaniʼ and 100% eradication of GLRaV-1 and 67% of GFLV in ʻShahaniʼ. Furthermore, applying of AgNPs improved plant growth parameters, including plant height, which in infected plantlets was (18.06, 12.36, and 14.92 cm in ʻAsgariʼ, ʻPeykaniʼ, and ʻShahaniʼ, respectively) less than virus-free plantlets. Leaf number was 45, 34, and 27 in virus-free plantlets of ʻAsgariʼ, ʻPeykaniʼ, and ʻShahaniʼ, respectively, but in infected plantlets, it was 24.40, 19.80, and 12. Leaf area increased from 5.34, 5.50, and 5.94 cm2 in infected plantlets to 9.56, 11.43, and 12.33 cm2 in virus-free plantlets of ʻAsgariʼ, ʻPeykaniʼ, and ʻShahaniʼ, respectively. Complementary results proved that chlorophyll content in virus-free is significantly higher than in virus-infected plantlets, which explains and confirms the change in growth parameters after virus removal.

Keywords

Subjects
Barba, M., Ilardi, V. and Pasquini, G. 2015. Control of pome and stone fruit virus diseases. Advances in Virus Research, Academic Press, 91: 47-83. doi: 10.1016/bs.aivir.2014.11.001.
Cai, L., Cai, L., Jia, H., Liu, C., Wang, D. and Sun, X. 2020. Foliar exposure of Fe3O4 nanoparticles on Nicotiana benthamiana: evidence for nanoparticles uptake, plant growth promoter and defense response elicitor against plant virus. Journal of Hazardous Materials, 393: 122415. doi: 10.1016/j.jhazmat.2020.122415.
Cai, L., Liu, C., Fan, G., Liu, C. and Sun, X. 2019. Preventing viral disease by ZnONPs through directly deactivating TMV and activating plant immunity in Nicotiana benthamiana. Environmental Science: Nano, 6(12): 3653-3669. doi: 10.1039/C9EN00850K.
Carvalho, R., Jones, J. B. and Paret, M. L. 2022. Utility of nanoparticles in management of plant viruses. Nanotechnology-Based Sustainable Alternatives for the Management of Plant Diseases, 233-241. doi: 10.1016/B978-0-12-823394-8.00001-9.
Chalak, L., Elbeaino, T., Elbitar, A., Fattal, T. and Choueiri, E. 2015. Removal of viruses from Lebanese fig varieties using tissue culture and thermotherapy. Phytopathologia Mediterranea, 54: 531-535.
Cuny, G. D., Suebsuwong, C. and Ray, S. S. 2017. Inosine-5’-monophosphate dehydrogenase (IMPDH) inhibitors: a patent and scientific literature review (2002-2016). Expert Opinion on Therapeutic Patents, 27(6): 677-690. doi: 10.1080/13543776.2017.1280463.
De Clercq, E. 2004. Antivirals and antiviral strategies. Nature Reviews Microbiology, 2: 704-720. doi: 10.1038/nrmicro975.
Dutta, P., Kumari, A., Mahanta, M., Biswas, K. K., Dudkiewicz, A., Thakuria, D. and Mazumdar, N. 2022. Advances in nanotechnology as a potential alternative for plant viral disease management. Frontiers in Microbiology, 13: 1-12. doi: 10.3389/fmicb.2022.935193.
El Gamal, A. Y., Tohamy, M. R., Abou-Zaid, M. I., Atia, M. M., El Sayed, T. and Farroh, K. Y. 2022. Silver nanoparticles as a veridical agent to inhibit plant-infecting viruses and disrupt their acquisition and transmission by their aphid vector. Archives of virology, 167(1): 85-97. doi: 10.1007/s00705-021-05280-y.
Elazzazy, A., Elbeshehy, E. and Betiha, M. 2017. In vitro assessment of activity of graphene silver composite sheets against multidrug-resistant bacteria and Tomato Bushy Stunt Virus. Tropical Journal of Pharmaceutical Research, 16: 2705-2711. doi: 10.4314/tjpr.v16i11.19.
El-shazly, M., Attia, Y., Kabil, F., Anis, E. and Hazman, M. 2017. Inhibitory Effects of Salicylic Acid and Silver Nanoparticles on Potato Virus Y-Infected Potato Plants in Egypt. Middle East Journal of Agriculture Research, 6: 835-848.
Galdiero, S., Falanga, A., Vitiello, M., Cantisani, M., Marra, V. and Galdiero, M. 2011. Silver nanoparticles as potential antiviral agents. Molecules, 16: 8894-8918. doi: 10.3390/molecules16108894.
Hedstrom, L. 2009. IMP dehydrogenase: structure, mechanism, and inhibition. Chemical reviews, 109(7): 2903-2928. doi: 10.1021/cr900021w.
Hill, J. and Whitham, S. 2014. Control of Virus Diseases in Soybeans. Advances in virus research, 90: 355-390. doi: 10.1016/B978-0-12-801246-8.00007-X.
Hoseinzadeh, E., Makhdoumi, P., Taha, P., Stelling, J., Hossini, H., Kamal, M. and Ashraf, G. A. 2016. Review on nano-antimicrobials: metal nanoparticles, methods and mechanisms. Current Drug Metabolism, 18(2): 120-128.
Hu, G. J., Dong, Y. F., Zhang, Z. P., Fan, X. D. and Fang, R. E. N. 2021. Elimination of grapevine fleck virus and grapevine rupestris stem pitting-associated virus from Vitis vinifera 87-1 by ribavirin combined with thermotherapy. Journal of Integrative Agriculture, 20(9): 2463-2470. doi: 10.1016/S2095-3119(20)63336-6.
Hu, G. J., Dong, Y. F., Zhang, Z. P., Fan, X. D., Ren, F. and Zhou, J. 2015. Virus elimination from in vitro apple by thermotherapy combined with chemotherapy. Plant Cell, Tissue and Organ Culture, 121: 435-443. doi: 10.1007/s11240-015-0714-6.
Hu, G. J., Dong, Y. F., Zhang, Z. P., Fan, X. D., Ren, F., Li, Z. N. and Zhang, S. N. 2018. Elimination of Grapevine rupestris stem pitting-associated virus from Vitis vinifera ‘Kyoho’ by an antiviral agent combined with shoot tip culture. Scientia Horticulturae, 229: 99-106. doi: 10.1007/s11240-015-0714-6.
Hu, G. J., Hong, N., Wang, L. P., Hu, H. J. and Wang, G. P. 2012. Efficacy of virus elimination from in vitro-cultured sand pear (Pyrus pyrifolia) by chemotherapy combined with thermotherapy. Crop Protection, 37: 20-25. doi: 10.1016/j.cropro.2012.02.017.
Karimpour, S., Davarynejad, G. H., ZakiAghl, M., Safarnejad, M. R., Martínez-Gómez, P., and Rubio, M. 2021. Rapid assessment of sanitary and physiological state of thermotherapy-treated apple shoots by chlorophyll content evaluation, European Journal of Horticultural Science, 86(2): 205-211. doi: 10.17660/eJHS.2021/86.2.11.
Komínek, P., KomÍnková, M. and Jandová, B. 2016. Effect of repeated Ribavirin treatment on grapevine viruses. Acta Virologica, 60: 400-403. doi: 10.4149/av_2016_04_400.
Kumar, G. P. and Prabhavathi P. K. 2022. Proximate analysis and phytochemical extraction from grape seeds and applications of the grape seed extract. Journal of Academia and Industrial Research, 10(2): 21-25.
Laimer, M. and Barba, M. 2011. Elimination of systemic pathogens by thermotherapy, tissue culture, or in vitro micro grafting. Virus and Virus-like Diseases of Pome and Stone Fruits, 389-393.
Leyssen, P., Balzarini, J., De Clercq, E. and Neyts, J. 2005. The predominant mechanism by which ribavirin exerts its antiviral activity in vitro against flavi viruses and paramyxo viruses is mediated by inhibition of IMP dehydrogenase. Journal of virology, 79(3): 1943-1947. doi: 10.1128/JVI.79.3.1943-1947.2005.
Mahfouze, H. A., El-Dougdoug, N. K. and Mahfouze, S. A. 2020. Veridical activity of silver nanoparticles against Banana bunchy top virus (BBTV) in banana plants. Bulletin of the National Research Centre, 44(1): 1-11. Doi: 10.1186/s42269-020-00433-6.
Martelli, G. P. 2017. An overview on grapevine viruses, viroids, and the diseases they cause. Grapevine viruses: molecular biology, diagnostics and management, 31-46. doi: 10.1007/978-3-319-57706-7_2.
Meng, B., Martelli, G. P., Golino, D. A. and Fuchs, M. 2017. Grapevine viruses: molecular biology, diagnostics and management. Cham: Springer International Publishing, 257-288. doi: 10.1007/978-3-319-57706-7.
Moradi, R., Koolivand, D., Eini, O. and Hajizadeh, M. 2017. Phylogenetic analysis of two Iranian grapevine virus A isolates using coat protein gene sequence. Iranian Journal of Genetics and Plant Breeding, 6(1): 48-57. doi: 10.30479/ijgpb.2017.1373.
Murashige, T. and Skoog, F. 1962. A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiologia plantarum, 15(3): 473-497.
Panattoni, A., D’Anna, F., Cristani, C. and Triolo, E. 2007. Grapevine viti virus A eradication in Vitis vinifera explants by antiviral drugs and thermotherapy. Journal of virological methods, 146(1-2): 129-135. doi: 10.1016/j.jviromet.2007.06.008.
Panattoni, A., Luvisi, A. and Triolo, E. 2013. Review elimination of viruses in plants: Twenty years of progress. Spanish Journal of Agricultural Research, 11: 173-188.
Rienth, M., Vigneron, N., Walker, R. P., Castellarin, S. D., Sweetman, C. and Burbidge, C. A. 2021. Modifications of grapevine berry composition induced by main viral and fungal pathogens in a climate change scenario. Frontiers in Plant Science, 12: 717223. doi: 10.3389/fpls.2021.717223.
Rodríguez-Verástegui, L. L., Ramírez-Zavaleta, C. Y., Capilla-Hernández, M. F. and Gregorio-Jorge, J. 2022. Viruses infecting trees and herbs that produce edible fleshy fruits with a prominent value in the global market: An evolutionary perspective. Plants, 11(2): 203. doi: 10.3390/plants11020203.
Salama, H. M. H. 2012. Effects of silver nanoparticles in some crop plants, common bean (Phaseolus vulgaris L.) and corn (Zea mays L.). International Research Journal of Biotechnology, 3(10): 190-197.
Shafie, R. M., Salama, A. M. and Farroh, K.Y. 2018. Silver nanoparticles activity against Tomato spotted wilt virus. Middle East Journal of Applied Sciences, 7: 1251-1267.
Tan, R., Wang, L., Hong, N. and Wang, G. 2010. Enhanced efficiency of virus eradication following thermotherapy of shoot-tip cultures of pear. Plant Cell, Tissue and Organ Culture, 101(2): 229-235. doi: 10.1007/s11240-010-9681-0.
Tripathi, M., Kumar, S., Kumar, A., Tripathi, P. and Kumar, S. 2018. Agro-nanotechnology: A future technology for sustainable agriculture. International Journal of Current Microbiology and Applied Sciences, 7: 196-200.
Vargas-Hernandez, M., Macias-Bobadilla, I., Guevara-Gonzalez, R. G., Rico-Garcia, E., Ocampo-Velazquez, R. V., Avila-Juarez, L. and Torres-Pacheco, I. 2020. Nanoparticles as potential antivirals in agriculture. Agriculture, 10(10): 444. doi: 10.3390/agriculture10100444.
Wahid, A., Gelani, S., Ashraf, M. and Foolad, M. 2007. Heat tolerance in plants: an overview. Environmental and Experimental Botany, 61: 199-223. doi: 10.1016/j.envexpbot.2007.05.011.
Wang, M. R., Cui, Z. H., Li, J. W., Hao, X. Y., Zhao, L. and Wang, Q. C. 2018. In vitro thermotherapy-based methods for plant virus eradication. Plant methods, 14(1): 1-18. doi: 10.1186/s13007-018-0355-y.
Wang, Q. and Valkonen, J. 2009. Improved recovery of cryotherapy-treated shoot tips following thermotherapy of in vitro-grown stock shoots of raspberry (Rubus idaeus L.). Cryo Letters, 30: 171-182.
Xiao, H., Shabanian, M., Moore, C., Li, C. and Meng, B. 2018. Survey for major viruses in commercial Vitis vinifera wine grapes in Ontario. Virology Journal, 15: 127. doi: 10.1186/s12985-018-1036-1.
Yan, K., Du, X. and Mao, B. 2022. Production of virus-free chrysanthemum (Chrysanthemum morifolium Ramat) by tissue culture techniques. In Plant Virology, 171-186. doi: 10.1007/978-1-0716-1835-6_17.
Zhao, L., Wang, M. R., Cui, Z. H., Chen, L., Volk, G. M. and Wang, Q. C. 2018. Combining thermotherapy with cryotherapy for efficient eradication of Apple stem grooving virus from infected in-vitro-cultured apple shoots. Plant Disease, 102: 1-7. doi: 10.1094/PDIS-11-17-1753-RE.