Abstract
A potential pathogenicity determinant and its critical amino acid (aa) sequences of mulberry crinkle leaf virus (MCLV) were determined through expression of MCLV genes in Nicotiana benthamiana using a potato virus X (PVX) vector. Among six genes encoded by MCLV, expression of only V3 resulted in a severe downward-leaf-curling symptom in newly emerging leaves of N. benthamiana plants, which suggested that the V3 protein is a pathogenicity determinant of MCLV. Analyses of truncation mutations indicated that the 94 residues at the N terminus of V3 are sufficient to maintain the function of the pathogenicity determinant V3 in N. benthamiana.
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Al Rwahnih, M., Dave, A., Anderson, M. M., Rowhani, A., Uyemoto, J. K., & Sudarshana, M. R. (2013). Association of a DNA virus with grapevines affected by red blotch disease in California. Phytopathology, 103, 1069–1076.
Amin, I., Ilyas, M., Qazi, J., Bashir, R., Yadav, J. S., Mansoor, S., Fauquet, C. M., & Briddon, R. W. (2011). Identification of a major pathogenicity determinant and suppressors of RNA silencing encoded by a South Pacific isolate of Banana bunchy top virus originating from Pakistan. Virus Genes, 42(2), 272–281.
Brigneti, G., Voinnet, O., Li, W. X., Ji, L. H., Ding, S. W., & Baulcombe, D. C. (1998). Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana. The EMBO Journal, 17(22), 6739–6746.
Brown, J. K., Fauquet, C. M., Briddon, R. W., Zerbini, M., Moriones, E., & Navas-Castillo, J. (2012). Family Geminiviridae. In A. M. Q. King, M. J. Adams, E. B. Carstens, & E. J. Lefkowitz (Eds.), Virus taxonomy: Classification and nomenclature of viruses: Ninth report of the international committee on taxonomy of viruses (pp. 351–373). Amsterdam: Elsevier/Academic Press.
Cameron, J. M., McDougall, I., Marsden, H. S., Preston, V. J., Ryan, D. M., & Subak-sharpe, J. H. (1988). Ribonucleotide reductase encoded by herpes simplex virus is a determinant of the pathogenicity of the virus in mice and a valid antiviral target. The Journal of General Virology, 69, 2607–2612.
Chapman, S., Kavanagh, T., & Baulcombe, D. (1992). Potato virus X as a vector for gene expression in plants. The Plant Journal, 2, 549–557.
Cui, X., Tao, X., Xie, Y., Xie, Y., Fauquet, C. M., & Zhou, X. (2004). A DNAβ associated with tomato yellow leaf curl China virus is required for symptom induction. Journal of Virology, 78(24), 13966–13974.
Czosnet, H., & Laterrot, H. (1997). A worldwide survey of tomato yellow leaf curl viruses. Archives of Virology, 142, 1391–1406.
Deng, X., Kelloniemi, J., Haikonen, T., Vuorinen, A. L., Elomaa, P., Teeri, T. H., & Valkonen, J. P. T. (2013). Modification of Tobacco rattle virus RNA1 to serve as a VIGS vector reveals that the 29K movement protein is an RNA silencing suppressor of the virus. Mol Plant Microbe In, 26(5), 503–514.
Dogra, S. C., Eini, O., Rezaian, M. A., & Randles, J. W. (2009). A novel shaggy-like kinase interacts with the tomato leaf curl virus pathogenicity determinant C4 protein. Plant Molecular Biology, 71, 25–38.
Duan, Y. P., Powell, C. A., Purcifull, D. E., Broglio, P., & Hiebert, E. (1997). Phenotypic variation in transgenic tobacco expressing mutated geminivirus movement/pathogenicity (BC1) proteins. Mol Plant Microbe In, 10, 1065–1074.
Hamilton, A., Voinnet, O., Chappell, L., & Baulcombe, D. (2002). Two classes of short interfering RNA in RNA silencing. The EMBO Journal, 21, 4671–4679.
Harrison, B. D., & Robinson, D. J. (1999). Natural genomic and antigenic variation in whitefly-transmitted geminiviruses (Begomoviruses). Annual Review of Phytopathology, 37, 369–398.
Hou, Y. M., Sanders, R., Ursin, V. M., & Gilbertson, R. L. (2000). Transgenic plants expressing geminivirus movement proteins: Abnormal phenotypes and delayed infection by Tomato mottle virus in transgenic tomatoes expressing the Bean dwarf mosaic virus BV1 or BC1 proteins. Mol Plant Microbe In, 13, 297–308.
Hussain, M., Mansoor, S., Iram, S., Fatima, A. N., & Zafar, Y. (2005). The nuclear shuttle protein of Tomato Leaf Curl New Delhi Virus is a pathogenicity determinant. Journal of Virology, 79(7), 4434–4439.
Ingham, D. J., Pascal, E., & Lazarowitz, S. G. (1995). Both bipartite geminivirus movement proteins define viral host range, but only BL1 determines viral pathogenicity. Virology, 207, 191–204.
Jenner, C. E., Sánchez, F., Nettleship, S. B., Foster, G. D., Ponz, F., & Walsh, J. A. (2000). The cylindrical inclusion gene of turnip mosaic virus encodes a pathogenic determinant to the Brassica resistance gene TuRB01. MPMI, 13(10), 1102–1108.
Krenz, B., Thompson, J. R., Fuchs, M., & Perry, K. L. (2012). Complete genome sequence of a new circular DNA virus from grapevine. Journal of Virology, 86(14), 7715.
Kumar, J., Kumar, J., Singh, S. P., & Tuli, R. (2014). bC1 is a pathogenicity determinant: Not only for begomoviruses but also for a mastrevirus. Archives of Virology, 159, 3071–3076.
Li, F. F., Xu, X. B., Huang, C. J., Gu, Z. H., Cao, L. G., Hu, T., Ding, M., Li, Z. H., & Zhou, X. P. (2015). The AC5 protein encoded by Mungbean yellow mosaic India virus is a pathogenicity determinant that suppresses RNA silencing-based antiviral defenses. New Phytologist, 208, 555–569.
Liang, P., Navarro, B., Zhang, Z., Wang, H., Lu, M., Xiao, H., Wu, Q., Zhou, X., Di Serio, F., & Li, S. (2015). Identification and characterization of a novel geminivirus with a monopartite genome infecting apple tree. The Journal of General Virology, 96(8), 2411–2420.
Loconsole, G., Saldarelli, P., Doddapaneni, H., Savino, V., Martelli, G. P., & Saponari, M. (2012). Identification of a single-stranded DNA virus associated with citrus chlorotic dwarf disease, a new member in the family Geminiviridae. Virology, 432, 162–172.
Lu, Q. Y., Wu, Z. J., Xia, Z. S., & Xie, L. H. (2015). Complete genome sequence of a novel monopartite geminivirus identified in mulberry (Morus alba L.). Archives of Virology, 160, 2135–2138.
Lu, Q. Y., Yang, L., Huang, J., Zheng, L., & Sun, X. (2019). Identification and subcellular location of an RNA silencing suppressor encoded by mulberry crinkle leaf virus. Virology, 526, 45–51.
Ma, Y., Navarro, B., Zhang, Z., Lu, M., Zhou, X., Chi, S., Di Serio, F., & Li, S. (2015). Identification and molecular characterization of a novel monopartite geminivirus associated with mulberry mosaic dwarf disease. The Journal of General Virology, 96, 2421–2434.
Moffat, A. S. (1999). Plant pathology-Geminiviruses emerge as serious crop threat. Science, 286, 1835.
Novembre, F. J., Johnson, P. R., Lewis, M. G., Anderson, D. C., Klumpp, S., Mcclure, H. M., & Hirsch, V. M. (1993). Multiple viral determinants contribute to pathogenicity of the acutely lethal simian immunodeficiency virus SIVsmmPBj variant. Journal of Virology, 67(5), 2466–2474.
Pascal, E., Goodlove, P. E., Wu, L. C., & Lazarowitz, S. G. (1993). Transgenic tobacco plants expressing the geminivirus BL1 protein exhibit symptoms of viral disease. Plant Cell, 5, 795–807.
Poojari, S., Alabi, O. J., Fofanov, V. Y., & Naidu, R. A. (2013). A leafhopper-transmissible DNA virus with novel evolutionary lineage in the family Geminiviridae implicated in grapevine redleaf disease by next-generation sequencing. PLoS One, 8, e64194.
Rigden, J. E., Krake, L. R., Rezaian, M. A., & Dry, I. B. (1994). ORF C4 of tomato leaf curl geminivirus is a determinant of symptom severity. Virology, 204, 847–850.
Saeed, M., Behjatnia, S. A. A., Mansoor, S., Zafar, Y., Hasnain, S., & Rezaian, M. A. (2005). A single complementary-sense transcript of a geminiviral DNA b satellite is determinant of pathogenicity. Mol Plant Microbe In, 18, 7–14.
Sharma, P., Ikegami, M., & Kon, T. (2010). Identification of the virulence factors and suppressors of posttranscriptional gene silencing encoded by Ageratum yellow vein virus, a monopartite begomovirus. Virus Research, 149, 19–27.
Shepherd, D. N., Martin, D. P., Van Der, W. E., Dent, K., Varsani, A., & Rybicki, E. P. (2010). Maize streak virus: An old and complex 'emerging' pathogen. Molecular Plant Pathology, 11, 1–12.
Smith, D. R., & Maxwell, D. P. (1994). Requirement of the common region of DNA-B and the BL1 open reading frame of bean golden mosaic geminivirus for infection of Phaseolus vulgaris. Phytopathology, 84, 133–138.
Sunter, G., Sunter, J. L., & Bisaro, D. M. (2001). Plants expressing tomato golden mosaic virus AL2 or beet curly top virus L2 transgenes show enhanced susceptibility to infection by DNA and RNA viruses. Virology, 285, 59–70.
van Wezel, R., Liu, H., Tien, P., Stanley, J., & Hong, Y. (2001). Gene C2 of the monopartite geminivirus tomato yellow leaf curl virus-China encodes a pathogenicity determinant that is localized in the nucleus. Mol Plant Microbe In, 14, 1125–1128.
Varsani, A., Navas-Castillo, J., Moriones, E., Hernández-Zepeda, C., Idris, A., Brown, J. K., Murilo Zerbini, F., & Martin, D. P. (2014). Establishment of three new genera in the family Geminiviridae: Becurtovirus, Eragrovirus and Turncurtovirus. Archives of Virology, 159, 2193–2203.
Varsani, A., Roumagnac, P., Fuchs, M., Navas-Castillo, J., Moriones, E., Idris, A., Briddon, R. W., Rivera-Bustamante, R., Murilo Zerbini, F., & Martin, D. P. (2017). Capulavirus and Grablovirus: Two new genera in the family Geminiviridae. Archives of Virology, 162, 1819–1831.
von Arnim, A., & Stanley, J. (1992). Determinants of tomato golden mosaic virus symptom development located on DNA B. Virology, 186, 286–293.
Wang, Y. (2013). Identification of pathogenicity determinant and RNA silencing suppressor of wheat dwarf virus (WDH) (pp. 41–55). Hangzhou: Zhejiang University.
Xie, J., Wang, X., Liu, Y., Peng, Y., & Zhou, G. (2007). First report of the occurrence of wheat dwarf virus in wheat in China. Plant Disease, 91(1), 111–111.
Zerbini, F. M., Briddon, R. W., Idris, A., Martin, D. P., Moriones, E., Navas-Castillo, J., Rivera-Bustamante, R., Roumagnac, P., Varsani, A., & ICTV Report Consortium. (2017). ICTV Virus Taxonomy Profile: Geminiviridae. The Journal of General Virology, 98, 131–133.
Acknowledgments
This work was supported by a grant from the Natural Science Foundation of Jiangsu Province, China (No. BK20151320), the Natural Science Foundation of the Jiangsu Higher Education Institutions of China (No. 18KJA210001) and the Doctor Startup Fund Program of Jiangsu University of Science and Technology (No. 1732931601).
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QYL conceived and designed the experiments. QYL, JY, YYC, and LY performed the experiments. XS cultivated the N. benthamiana plants. QYL wrote the paper. All of the authors read and approved the final manuscript.
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Lu, QY., Yu, J., Cheng, YY. et al. V3 protein encoded by mulberry crinkle leaf virus acts as a pathogenicity determinant in Nicotiana benthamiana. Eur J Plant Pathol 157, 141–149 (2020). https://doi.org/10.1007/s10658-020-01991-1
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DOI: https://doi.org/10.1007/s10658-020-01991-1