Skip to main content

Advertisement

Log in

V3 protein encoded by mulberry crinkle leaf virus acts as a pathogenicity determinant in Nicotiana benthamiana

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Chapman, S., Kavanagh, T., & Baulcombe, D. (1992). Potato virus X as a vector for gene expression in plants. The Plant Journal, 2, 549–557.

    CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Czosnet, H., & Laterrot, H. (1997). A worldwide survey of tomato yellow leaf curl viruses. Archives of Virology, 142, 1391–1406.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Hamilton, A., Voinnet, O., Chappell, L., & Baulcombe, D. (2002). Two classes of short interfering RNA in RNA silencing. The EMBO Journal, 21, 4671–4679.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harrison, B. D., & Robinson, D. J. (1999). Natural genomic and antigenic variation in whitefly-transmitted geminiviruses (Begomoviruses). Annual Review of Phytopathology, 37, 369–398.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Moffat, A. S. (1999). Plant pathology-Geminiviruses emerge as serious crop threat. Science, 286, 1835.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • von Arnim, A., & Stanley, J. (1992). Determinants of tomato golden mosaic virus symptom development located on DNA B. Virology, 186, 286–293.

    Article  Google Scholar 

  • Wang, Y. (2013). Identification of pathogenicity determinant and RNA silencing suppressor of wheat dwarf virus (WDH) (pp. 41–55). Hangzhou: Zhejiang University.

    Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

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).

Author information

Authors and Affiliations

Authors

Contributions

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.

Corresponding author

Correspondence to Quan-You Lu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not describe any studies with human participants or animals performed by any of the authors.

Electronic supplementary material

ESM 1

(DOCX 15 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-020-01991-1

Keywords

Navigation