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Broad bean wilt virus 1 encoded VP47 and SCP are suppressors of plant post-transcriptional gene silencing

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Abstract

Broad bean wilt virus 1 (BBWV-1, genus Fabavirus, family Secoviridae) is a bipartite positive single-stranded RNA (+ssRNA) virus infecting important horticultural and ornamental crops worldwide. RNA1 encodes proteins involved in virus replication, whereas RNA2 encodes the large and small coat proteins (LCP, and SCP, respectively) and two putative movement proteins with overlapping C-terminal but different sizes: 47.2 kDa (VP47) and 37 kDa (VP37). Post-transcriptional gene silencing (PTGS) is a mechanism of gene regulation and defense against pathogens such as viruses. However, most plant viruses encode proteins called viral suppressors of RNA silencing (VSRs) which able to inhibit PTGS. Previously, BBWV-1 VP37 was identified as VSR and here, we have demonstrated that VP47 and SCP, but not LCP, are also VSRs by two approaches: (i) transient expression in Nicotiana benthamiana 16c plants expressing the green fluorescent protein (GFP) constitutively, and (ii) movement complementation assays using a viral vector based on Turnip crinkle virus sequence containing GFP (pTCV-GFP). In contrast LCP but not SCP of Broad been wilt virus 2 (BBWV-2, genus Fabavirus, family Secoviridae) is a VSR, which illustrates that viruses of the same genus can interact differently with the host.

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References

  • Ahlquist, P. (2002). RNA-dependent RNA polymerases, viruses, and RNA silencing. Science, 296, 1270–1273.

    Article  CAS  Google Scholar 

  • Carpino, C., Elvira-González, L., Rubio, L., Peri, E., Davino, S., & Galipienso, L. (2019). A comparative study of viral infectivity, accumulation and symptoms induced by broad bean wilt virus 1 isolates. Journal of Plant Pathology, 101, 275–281.

    Article  Google Scholar 

  • Carpino, C., Ferriol, I., Elvira-González, L., Medina, V., Rubio, L., Peri, E., Davino, S., & Galipienso, L. (2020). RNA2-encoded VP37 protein of broad bean wilt virus 1 is a determinant of pathogenicity, host susceptibility and a suppressor of post-transcriptional gene silencing. Molecular Plant Pathology. https://doi.org/10.1111/mpp.12979.

  • Cañizares, M. C., Taylor, K. M., & Lomonossoff, G. P. (2004). Surface-exposed C-terminal amino acids of the small coat protein of Cowpea mosaic virus are required for suppression of silencing. Journal of General Virology, 85, 3431–3435.

    Article  Google Scholar 

  • Duan, C., Fang, Y., Zhou, B., Zhao, J., Hou, W., Zhu, H., Ding, S., & Guo, H. (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, 259–274.

    Article  CAS  Google Scholar 

  • Dunoyer, P., & Voinnet, O. (2005). The complex interplay between plant viruses and host RNA-silencing pathways. Current Opinion in Plant Biology, 8, 415–423.

    Article  CAS  Google Scholar 

  • Chen, X., & Bruening, G. (1992). Nucleotide sequence and genetic map of Cowpea severe mosaic virus RNA 2 and comparisons with RNA 2 of other comoviruses. Virology, 187, 682–692.

    Article  CAS  Google Scholar 

  • Comellas, M. (2009). Estudio de la interacción entre naranjo amargo y el virus de la tristeza de los cítricos. PhD thesis. Universidad Politécnica de Valencia. https://riunet.upv.es/handle/10251/7323

  • Chiu, M., Chen, I., Baulcombe, D. C., & Tsai, C. (2010). The silencing suppressor P25 of Potato virus X interacts with Argonaute1 and mediates its degradation through the proteasome pathway. Molecular Plant Pathology, 11, 641–649.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Csorba, T., Pantaleo, V., & Burgyán, J. (2009). RNA silencing: An antiviral mechanism. Advances in Virus Research, 75, 35–230.

    Article  CAS  Google Scholar 

  • Ferriol, I., Ruiz-Ruiz, S., & Rubio, L. (2011). Detection and absolute quantitation of Broad bean wilt virus 1 (BBWV-1) and BBWV-2 by real time RT-PCR. Journal of Virological Methods, 177, 202–205.

    Article  CAS  Google Scholar 

  • Ferriol, I., Ambrós, S., Da Silva, D. M., Falk, B. W., & Rubio, L. (2016). Molecular and biological characterization of highly infectious transcripts from full-length cDNA clones of Broad bean wilt virus 1. Virus Research, 217, 71–75.

    Article  CAS  Google Scholar 

  • Huang, J., Yang, M., Lu, L., & Zhang, X. (2016). Diverse functions of small RNAs in different plant–pathogen communications. Frontiers in Microbiology, 7, 1552.

    PubMed  PubMed Central  Google Scholar 

  • Johansen, L. K., & Carrington, J. C. (2001). Silencing on the spot. Induction and suppression of RNA silencing in the agrobacterium-mediated transient expression system. Plant Physiology, 126, 930–938.

    Article  CAS  Google Scholar 

  • Karran, R. A., & Sanfaçon, H. (2014). Tomato ringspot virus coat protein binds to ARGONAUTE 1 and suppresses the translation repression of a reporter gene. Molecular Plant-Microbe Interactions, 27, 933–943.

    Article  CAS  Google Scholar 

  • Kong, L., Wang, Y., Yang, X., Sunter, G., & Zhou, X. (2014). Broad bean wilt virus 2 encoded vp53, vp37 and large capsid protein orchestrate suppression of RNA silencing in plant. Virus Research, 192, 62–73.

    Article  CAS  Google Scholar 

  • Lakatos, L., Szittya, G., Silhavy, D., & Burgyán, J. (2004). Molecular mechanism of RNA silencing suppression mediated by p19 protein of Tombusviruses. EMBO Journal, 23, 876–884.

    Article  CAS  Google Scholar 

  • Lin, J., Guo, J., Finer, J., Dorrance, A. E., Redinbaugh, M. G., & Qu, F. (2014). The Bean pod mottle virus RNA2-encoded 58-kilodalton protein P58 is required in cis for RNA2 accumulation. Journal of Virology, 88, 3213–3222.

    Article  Google Scholar 

  • Liu, L., Grainger, J., Cañizares, M. C., Angell, S. M., & Lomonossoff, G. P. (2004). Cowpea mosaic virus RNA-1 acts as an amplicon whose effects can be counteracted by a RNA-2-encoded suppressor of silencing. Virology, 323, 37–48.

    Article  CAS  Google Scholar 

  • Liu, S., Zhou, J., Hu, C., Wei, C., & Zhang, J. (2017). MicroRNA-mediated gene silencing in plant defense and viral counter-defense. Frontiers in Microbiology, 8, 1801.

    Article  Google Scholar 

  • Llave, C., Kasschau, K. D., & Carrington, J. C. (2000). Virus-encoded suppressor of posttranscriptional gene silencing targets a maintenance step in the silencing pathway. Proceedings of the National Academy of Sciences, 97, 13401–13406.

    Article  CAS  Google Scholar 

  • Powers, J. G., Sit, T. L., Heinsohn, C., George, C. G., Kim, K., & Lommel, S. A. (2008a). The Red clover necrotic mosaic virus RNA-2 encoded movement protein is a second suppressor of RNA silencing. Virology, 381, 277–286.

    Article  CAS  Google Scholar 

  • Powers, J. G., Sit, T. L., Qu, F., Morris, T. J., Kim, K., & Lommel, S. A. (2008b). A versatile assay for the identification of RNA silencing suppressors based on complementation of viral movement. Molecular Plant-Microbe Interactions, 21, 879–890.

    Article  CAS  Google Scholar 

  • Renovell, Á., Vives, M. C., Ruiz-Ruiz, S., Navarro, L., Moreno, P., & Guerri, J. (2012). The Citrus leaf blotch virus movement protein acts as silencing suppressor. Virus Genes, 44, 131–140.

    Article  CAS  Google Scholar 

  • Roth, B. M., Pruss, G. J., & Vance, V. B. (2004). Plant viral suppressors of RNA silencing. Virus Research, 102, 97–108.

    Article  CAS  Google Scholar 

  • Silhavy, D., & Burgyán, J. (2004). Effects and side-effects of viral RNA silencing suppressors on short RNAs. Trends in Plant Science, 9, 76–83.

    Article  CAS  Google Scholar 

  • Smith, N. A., Eamens, A. L., & Wang, M. (2011). Viral small interfering RNAs target host genes to mediate disease symptoms in plants. PLoS Pathogens, 7, e1002022.

    Article  CAS  Google Scholar 

  • Stewart, L. R., Jarugula, S., Zhao, Y., Qu, F., & Marty, D. (2017). Identification of a Maize chlorotic dwarf virus silencing suppressor protein. Virology, 504, 88–95.

    Article  CAS  Google Scholar 

  • Thompson, J. R., Dasgupta, I., Fuchs, M., Iwanami, T., Karasev, A. V., Petrzik, K., Sanfaçon, H., Tzanetakis, I. E., Van der Vlugt, R., & Wetzel, T. (2017). ICTV virus taxonomy profile: Secoviridae. Journal of General Virology, 98, 529–531.

    Article  CAS  Google Scholar 

  • Voinnet, O. (2005). Induction and suppression of RNA silencing: Insights from viral infections. Nature Reviews Genetics, 6, 206–220.

    Article  CAS  Google Scholar 

  • Voinnet, O., Lederer, C., & Baulcombe, D. C. (2000). A viral movement protein prevents spread of the gene silencing signal in Nicotiana benthamiana. Cell, 103, 157–167.

    Article  CAS  Google Scholar 

  • Voinnet, O., & Baulcombe, D. C. (1997). Systemic signalling in gene silencing. Nature, 389, 553.

    Article  CAS  Google Scholar 

  • Wang, M., Masuta, C., Smith, N. A., & Shimura, H. (2012). RNA silencing and plant viral diseases. Molecular Plant-Microbe Interactions, 25, 1275–1285.

    Article  CAS  Google Scholar 

  • Xie, L., Shang, W., Liu, C., Zhang, Q., Sunter, G., Hong, J., & Zhou, X. (2016). Mutual association of Broad bean wilt virus 2 VP37-derived tubules and plasmodesmata obtained from cytological observation. Scientific Reports, 6, 21552.

  • Yaegashi, H., Yamatsuta, T., Takahashi, T., Li, C., Isogai, M., Kobori, T., Ohki, S., & Yoshikawa, N. (2007). Characterization of virus-induced gene silencing in tobacco plants infected with apple latent spherical virus. Archives of Virology, 152, 1839–1849.

    Article  CAS  Google Scholar 

  • Yang, Y., Liu, T., Shen, D., Wang, J., Ling, X., Hu, Z., Chen, T., Hu, J., Huang, J., Yu, W., Dou, D., Wang, M., & Zhang, B. (2019). Tomato yellow leaf curl virus intergenic siRNAs target a host long noncoding RNA to modulate disease symptoms. PLoS Pathogens, 15, e1007534.

    Article  Google Scholar 

Download references

Acknowledgments

We thank Dra. Karelia Vázquez for providing the GFP riboprobe and helping with siRNA extractions, Dr. J. Guerri for providing the modified pCAMBIA-2300 binary plasmid, p35S-p19 and p35S-GFP cDNA constructs and J. G. and Prof. S. Lommel for providing pTCV-GFP cDNA infectious clone.

Funding

This research work was supported by funds of the Instituto Valenciano de Investigaciones Agrarias, Valencia, Spain (PROY-IVIA-2013/14 n°5426). C. Carpino was a recipient of predoctoral fellowships from the Italian government.

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Author notes

  1. Inmaculada Ferriol

    Present address: Centre for Research in Agricultural Genomics (CRAG-CSIC-UAB-UB), Cerdanyola del Vallès, 08193, Barcelona, Spain

Authors and Affiliations

  1. Instituto Valenciano de Investigaciones Agrarias (IVIA), CV-315, Km 10, 46113, Moncada, Valencia, Spain

    Caterina Carpino, Inmaculada Ferriol, Laura Elvira-González, Luis Rubio & Luis Galipienso

  2. Department of Agricultural, Food and Forestry Science, University of Palermo, Viale delle Scienze Bld. 5, 90128, Palermo, Italy

    Caterina Carpino, Ezio Peri & Salvatore Davino

Authors
  1. Caterina Carpino
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  2. Inmaculada Ferriol
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  3. Laura Elvira-González
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  4. Luis Rubio
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  5. Ezio Peri
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  6. Salvatore Davino
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  7. Luis Galipienso
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Correspondence to Luis Galipienso.

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The authors certify that we do not have any actual or potential conflict of interest. The study presented here is original and has not been published previously. All authors have reviewed the manuscript and approved its final version before submission.

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Carpino, C., Ferriol, I., Elvira-González, L. et al. Broad bean wilt virus 1 encoded VP47 and SCP are suppressors of plant post-transcriptional gene silencing. Eur J Plant Pathol 158, 1043–1049 (2020). https://doi.org/10.1007/s10658-020-02117-3

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  • DOI: https://doi.org/10.1007/s10658-020-02117-3

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