Stability of resistance against beet curly top disease in the presence of cucumber mosaic virus in Arabidopsis thaliana

Volume 9, Issue 2
June 2020
Pages 233-249

Document Type : Original Research

Authors

Department of Plant Pathology, Faculty of Agriculture, Tarbiat Modares University, Tehran, Iran.

Abstract
Curly top is one of the most important viral diseases of sugar beet. Use of resistance sources is a promising strategy for control of this disease. In the present study, the efficiency of four gene silencing constructs (OUT-hp، IN-hp، sense and antisense) against two major causes of curly top disease in Iran, beet curly top virus-Svr (BCTV) and beet curly top Iran virus (BCTIV), were evaluated in transgenic plants. Selection of transgenic plant seeds was carried out on selective medium 1/2MS containing glufosinate-ammonium (Basta) and the results showed that the pBCTV-IN-hp construct resulted in the highest germinated seeds. Selected plants were transferred to greenhouse and evaluated for resistance to basta and detection of silencing constructs in the transgenic plants. Afterwards, resistance of the selected transgenic plants to beet curly top viruses and resistance stability against cucumber mosaic virus (CMV) was evaluated in a completely randomized design with six treatments in a factorial experiment. The results showed that the transformed lines with each of four constructs were significantly different in severity of symptoms, plant height and number of flowering stems compared to their respective controls. Although these transgenic plants were resistant to BCTV-Svr and BCTIV, in their challenge inoculation experiments it was shown that this resistance was suppressed by CMV infection.

Keywords

Subjects
Al-kaff, N. S., Covey, S. N., Kreike, M. M., Page, A. M., Pinder, R. and Dale, P. J. 1998. Transcriptional and posttranscriptional plant gene silencing in response to a pathogen. Science, 279: 2113-2115.
Azizi, A. and Shams-bakhsh, M. 2014. Impact of cucumber mosaic virus infection on the varietal traits of common bean cultivars in Iran. VirusDisease, 25, 447-454.
Bennett, C. W. 1971. Curly top disease of sugarbeet and other plants. American Phytopathological Society, 7: 68-81.
Bent, A. 2006. Arabidopsis thaliana floral dip transformation method. Methods in Molecular Biology, 343: 87-103.
Bisaro, D. M. 2006. Silencing suppression by geminivirus proteins. Virology, 344: 158-168.
Bolok-Yazdi, H. R., Heydarnejad, J. and Massumi, H. 2008. Genome characterization and genetic diversity of beet curly top Iran virus: a geminivirus with a novel nonanucleotide. Virus Genes, 36: 539-545.
Briddon, R. W., Stenger, D. C., Bedford, I. D., Stanley, J., Izadpanah, K. and Markham, P. G. 1998. Comparison of a beet curly top virus isolate originating from the old world with those from the new world. European Journal of Plant Pathology, 104: 77-84.
Brown, J., Fauquet, C., Briddon, R., Zerbini, M., Moriones, E. and Navas-Castillo, J. 2011. Geminivirdae. Virus taxonomy: classification and nomenclature of viruses: Ninth Report of the International Committee on Taxonomy of Viruses. Elsevier Academic Press, Sandiego: 251-374.
Burgyán, J. and Havelda, Z. 2011. Viral suppressors of RNA silencing. Trends in Plant Science, 16 (5): 265-272.
Chen, L. F., Brannigan, K., Clark, R. and Gilbertson, R. L. 2010. Characterization of curtoviruses associated with curly top disease of tomato in California and monitoring for these viruses in beet leafhoppers. Plant Disease, 94: 99-108.
Csorba, T., Lózsa, R., Hutvágner, G. and Burgyán, J. 2010. Polerovirus protein P0 prevents the assembly of small RNA-containing RISC complexes and leads to degradation of ARGNAUTE1. The Plant Journal, 62 (3): 463-472.
Diaz-Pendon, J. A., Li, F., Li, W. X. and Ding, S. W. 2007. Suppression of antiviral silencing by cucumber mosaic virus 2b protein in Arabidopsis is associated with drastically reduced accumulation of three classes of viral small interfering RNAs. The Plant Cell, 19 (6): 2053-2063.
Ding, S. W. and Voinnet, O. 2007. Antiviral immunity directed by small RNAs. Cell, 130 (3): 413-426.
Doyle, J. J. 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin, 19: 11-15.
Duan, C. G., Fang, Y.Y., Zhou, B.-J., Zhao, J.-H., Hou, W. N., Zhu, H., Ding, S. W. and Guo, H. S. 2012. Suppression of Arabidopsis ARGONAUTE1-mediated slicing, transgene-induced RNA silencing, and DNA methylation by distinct domains of the Cucumber mosaic virus 2b protein. The Plant Cell, 24 (1): 259-274.
Ebadzad, G., Behjatnia, S. A. A. and Izadpanah, K. 2008. Infectivity of the cloned genome of Iranian isolate of beet severe curly top virus in experimental hosts. Iranian Journal of Plant Pathology, 44: 9-15.
Faria, J. C., Dias, B. B. A., Cancado, L. J., Cuncado, L. J., Cunha, N. B. C., Silva, L. M., and Vianna, G. R., Aragao, F. J. L., 2006. Partial resistance to Bean golden mosaic virus in a transgenic common bean (Phaseolus vulgaris) line expressing a mutated Rep gene. Plant Science, 171: 565-571.
González, I., Martínez, L., Rakitina, D. V., Lewsey, M. G., Atencio, F. A., Llave, C., Kalinina, N. O., Carr, J. P., Palukaitis, P. and Canto, T. 2010. Cucumber mosaic virus 2b protein subcellular targets and interactions their significance to RNA silencing suppressor activity. Molecular Plant-Microbe Interactions, 23 (3): 294-303.
Havelda, Z., Hornyik, C., Crescenzi, A. and Burgyán, J. 2003. In situ characterization of Cymbidium ringspot tombusvirus infection-induced posttranscriptional gene silencing in Nicotiana benthamiana. Journal of Virology, 77 (10): 6082-6086.
Heydarnejad, J., Keyvani, N., Razavinejad, S., Massumi, H. and Varsani, A. 2012. Fulfilling Koch’s postulates for beet curly top Iran virus and proposal for consideration of new genus in the family Geminiviridae. Archives of Virology 158(2):435-43.
Heydarnejad, J., Zakiaghl, M., Mehrvar, M., Kraberger, S. and Varsani, A. 2013. Diversity of Beet curly top Iran virus isolated from different hosts in Iran. Virus Genes, 46: 571–575.
Hosseini Abhari, E., Heydarnejad, J., Massumi, H., Hosseini Pour, A. and Izadpanah, K. 2005. Natural hosts, vector and molecular detection of Beet curly top virus (BCTV) in Southeast of Iran. The second Asian conference on plant pathology, Singapore.
Jaubert, M., Bhattacharjee, S., Mello, A. F., Perry, K. L. and Moffett, P. 2011. ARGONAUTE2 mediates RNA-silencing antiviral defenses against Potato virus X in Arabidopsis. Plant Physiology, 156 (3): 1556-1564.
Kanazawa, A., Inaba, J.i., Shimura, H., Otagaki, S., Tsukahara, S., Matsuzawa, A., Kim, B.M., Goto, K. and Masuta, C. 2011. Virus-mediated effcient induction of epigenetic modifications of endogenous genes with phenotypic changes in plants. The Plant Journal, 65(1): 156-168
King, A. M., Adams, M. J. and Lefkowitz, E. J. 2011. Virus taxonomy: classification and nomenclature of viruses. Ninth Report of the International Committee on Taxonomy of Viruses, Elsevier.
Lakatos, L., Csorba, T., Pantaleo, V., Chapman, E. J., Carrington, J. C., Liu, Y. P., Dolja, V. V., Calvino, L. F., Lopez-Moya, J. J. and Burgyan, J. 2006. Small RNA binding is a common strategy to suppress RNA silencing by several viral suppressors. The EMBO Journal, 25 (12): 2768-2780.
Lee, S., Stenger, D. C., Bisaro, D. M. and Davies, K. R. 1994. Identification of loci in Arabidopsis that confer resistance to geminivirus infection. The Plant Journal, 6: 525-535.
Mitter, N., Sulistyowati, E. and Dietzgen, R. G. 2003. Cucumber mosaic virus infection transiently breaks dsRNA-induced transgenic immunity to Potato virus Y in tobacco. Molecular Plant-Microbe Interactions, 16 (10): 936-944
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 (1): 31-40.
Mumford, D.L. 1974. Procedure for inducing curly top epidemics in field plots. Journal of the American Society of Sugar Beet Technologist, 18: 20-23.
Nomura, K., Uekusa, H. and Kita, N. 2014. Suppression of transgene RNA silencing in transgenic Arabidopsis thaliana by a mild strain of Cucumber mosaic virus. Journal of General Plant Pathology, 80 (5): 443-448.
Park, J., Hwang, H., Shim, H., Im, K., Auh, C. K., Lee, S. and Davis, K. R. 2004. Altered cell shapes, hyperplasia, and secondary growth in Arabidopsis caused by beet curly top geminivirus infection. Molecules and Cells, 17 (1): 117-124.
Pooggin, M., Shivaprasad, P., Veluthambi, K. and Hohn, T. 2003. RNAi targeting of DNA virus in plants. Nature Biotechnology, 21: 131-132.
Rodríguez-Negrete, E. A., Carrillo-Tripp, J. and Rivera-Bustamante, R. F. 2009. RNA silencing against geminivirus: complementary action of posttranscriptional gene silencing and transcriptional gene silencing in host recovery. Journal of Virology, 83 (3): 1332-1340.
Simo´n-Mateo C, Lo´pez-Moya JJ, Guo HS, Gonza´lez E, Garcı ´a JA. 2003. Suppressor activity of potyviral and cucumoviral infections in potyvirus-induced transgene silencing. Journal of General Virology, 84: 2877–2883
Soto, M.J., Chen, L. F., Seo, Y. S. and Gilbertson, R. L. 2005. Identification of regions of the Beet mild curly top virus (family Geminiviridae) capsid protein involved in systemic infection, virion formation and leafhopper transmission. Virology, 341: 257-270.
Soto, M. J. and Gilbertson, R. L. 2003. Distribution and rate of movement of the curtovirus Beet mild curly top virus (family Geminiviridae) in the beet leafhopper. Phytopathology, 93: 478-484.
Stenger, D. C., Carbonaro, D. and Duffus, J. E. 1990. Genomic characterization of phenotypic variants of beet curly top virus. Journal of General Virology, 71: 2211-2216.
Stenger, D. C., Davis, K. R. and Bisaro, D. M. 1994. Recombinant beet curly top virus genomes exhibit both parental and novel pathogenic phenotypes. Virology, 200: 677-685.
Strausbaugh, C. A., Gillen, A. M., Camp, S., Shock, C. C., Eldredge, E. P. and Gallian, J. J. 2007. Relationship of beet curly top foliar ratings to sugar beet yield. Plant Disease, 91: 1459-1463.
Taheri, H., Izadpanah, K. and Behjatnia, S. A. A. 2014. Synergistic interaction between Beet severe curly top virus and Beet curly top Iran virus in sugar beet and tomato. In: Proceedings of the 21st Iranian Plant Protection Conference, p. 398. Urmia University, Urmia, Iran.
Vanitharani, R., Chellappan, P. and Fauquet, C. M. 2003. Short interfering RNA-mediated interference of gene expression and viral DNA accumulation in cultured plant cells. Proceedings of the National Academy of Sciences, 100: 9632-9636.
Velasquez-Valle, R., Mena-Covarrubias, J., Reveles-Torres, L. R., Argüello-Astorga, G. R., Salas-Luevano, M. A. and Mauricio-Castillo, J. A. 2012. First report of Beet mild curly top virus in dry bean in Zacatecas, Mexico. Plant Disease, 96: 771-772.
Wintermantel, W. M., and Kaffka, S. R. 2006. Sugar beet performance with curly top is related to virus accumulation and age at infection. Plant Disease, 90:657-662.
Yang, X., Xie, Y., Raja, P., Li, S., Wolf, J. N., Shen, Q., Bisaro, D. M. and Zhou, X. 2011. Suppression of methylation-mediated transcriptional gene silencing by βC1-SAHH protein interaction during geminivirus-betasatellite infection. PLoS Pathogens, 7 (10): e1002329.
Zhang, X., Yuan, Y. R., Pei, Y., Lin, S. S., Tuschl, T., Patel, D. J. and Chua, N. H. 2006. Cucumber mosaic virus-encoded 2b suppressor inhibits Arabidopsis Argonaute1 cleavage activity to counter plant defense. Genes and Development, 20 (23): 3255-3268.