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Molecular and functional characterization of the barley yellow striate mosaic virus genes encoding phosphoprotein, P3, P6 and P9

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Abstract

Plants rely on RNA silencing (RS) as a major layer of innate defense to neutralize invading viruses. In an opposite way, plant viruses evolved a survival mechanism, based on viral suppressors of RS (RSS), able to hinder the host RS activation system. In the present study, the sequences of the barley yellow striate mosaic virus (BYSMV) proteins P3, P6, P9 and of Phosphoprotein (P), from Chahar Mahall (Iran) isolate, were determined. Furthermore, we carried out agroinfiltration assays in leaves of Nicotiana benthamiana (16c line) to explore the RS suppression mechanism of these proteins. Analyses showed that P and P3 act as weak local and limited short-term systemic inducers of RSS. A reduction of RNA-dependent RNA polymerase 6 (RDR6) gene expression was observed in presence of BYSMV P and P3 proteins, which imply their putative role in interfering with systemic RS, in which RDR6 is involved. In addition, P and P3 RSS activity were reduced when co-expressed with other BYSMV accessory proteins, indicating that, in the system used, only free P or P3 proteins lead to RSS. The BYSMV P protein lacked any detectable Glycine-Tryptophan (WG/GW) or F-box motifs, known to interfere with the AGO1 slicing activity. On the opposite, two WG/GW were identified in P3 sequence.

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References

  • Almasi, R., Afsharifar, A., Niazi, A., Pakdel, A., & Izadpanah, K. (2010). Analysis of the complete nucleotide sequence of the polymerase gene of barley yellow striate mosaic virus- iranian isolate. Journal of Phytopathology, 158, 351–356.

    Article  CAS  Google Scholar 

  • Almasi, R., Miller, W. A., & Ziegler-Graff, V. (2015). Mild and severe cereal yellow dwarf viruses differ in silencing suppressor efficiency of the P0 protein. Virus Research, 208, 199–206.

    Article  CAS  PubMed  Google Scholar 

  • Amari, K., Vazquez, F., & Heinlein, M. (2012). Manipulation of plant host susceptibility: An emerging role for viral movement proteins? Frontiers in Plant Science, 3–10.

  • Bayne, E. H., Rakitina, D. V., Morozov, S. Y., & Baulcome, D. C. (2005). Cell-to-cell movement of potato Potexvirus X is dependent on suppression of RNA silencing. Plant Journal, 44(3), 471–482.

    Article  CAS  Google Scholar 

  • Bejerman, N., Giolitti, F., de Breuil, S., Trucco, V., Nome, C., Lenardon, S., & Dietzegen, R. G. (2015). Complete genome sequence and integrated protein localization and interaction map for alfalfa dwarf virus, which combines properties of both cytoplasmic and nuclear plant rhabdoviruses. Virology, 483, 275–283.

    Article  CAS  PubMed  Google Scholar 

  • Bejerman, N., Mann, K. S., & Dietzgen, R. G. (2016). Alfalfa dwarf cytorhabdovirus P protein is a local and systemic RNA silencing suppressor which inhibits programmed RISC activity and prevents transitive amplification of RNA silencing. Virus Research, 224, 19–28.

    Article  CAS  PubMed  Google Scholar 

  • Boccara, M., Sarazin, A., Thiebeauld, O., Jay, F., Voinnet, O., Navarro, L., & Colot, V. (2014). The Arabidopsis miR472-RDR6 silencing pathway modulates PAMP-and effector-triggered immunity through the post-transcriptional control of disease resistance genes. PLoS Pathogens, 10(1), e1003883.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Burgyán, J., & Havelda, Z. (2011). Viral suppressors of RNA silencing. Trends in Plant Science, 16(5), 265–272.

    Article  PubMed  CAS  Google Scholar 

  • Cao, Q., Xu, W. Y., Gao, Q., Jiang, Z. H., Liu, S. Y., Fang, X. D., Gao, D. M., Wang, Y., & Wang, X. B. (2018). Transmission characteristics of barley yellow striate mosaic virus in its planthopper vector Laodelphax striatellus. Frontiers in Microbiology, 9, 1419.

    Article  PubMed  PubMed Central  Google Scholar 

  • Carbonell, A., & Carrington, J. C. (2015). Antiviral roles of plant ARGONAUTES. Current Opinion in Plant Biology, 27, 111–117.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carluccio, A. V., Zicca, S., & Stavolone, L. (2014). Hitching a ride on vesicles: Cauliflower mosaic virus movement protein trafficking in the endomembrane system. Plant Physiology, 164(3), 1261–1270. https://doi.org/10.1104/pp.113.234534.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carluccio, A. V., Prigigallo, M. I., Rosas-Diaz, T., Lozano-Duran, R., & Stavolone, L. (2018). S-acylation mediates Mungbean yellow mosaic virus AC4 localization to the plasma membrane and in turns gene silencing suppression. PLoS Pathogens, 14(8), e1007207. https://doi.org/10.1371/journal.ppat.1007207.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chapman, E. J., & Carrington, J. C. (2007). Specialization and evolution of endogenous small RNA pathways. Nature Reviews Genetics, 8(11), 884–896.

    Article  CAS  PubMed  Google Scholar 

  • Csorba, T., & Burgyán, J. (2016). Antiviral silencing and suppression of gene silencing in plants p1–33 In: Wang, A., Zhou, X. (eds), Current research topics in plant virology. Springer International Publishing.

  • Dietzgen, R. G., Kondo, H., Goodin, M. M., Kurath, G., & Vasilakis, N. (2017). The family Rhabdoviridae: Mono- and bipartite negative-sense RNA viruses with diverse genome organization and common evolutionary origins. Virus Research, 227, 158–170.

    Article  CAS  PubMed  Google Scholar 

  • Dietzgen, R. G., Bejerman, N. E., Goodin, M. M., Higgins, C. M., Huot, O. B., Kondo, H., Martin, K. M., & Whitfield, A. E. (2020). Diversity and epidemiology of plant rhabdoviruses. Virus Research, 281, 197942.

    Article  CAS  PubMed  Google Scholar 

  • Giner, A., Lakatos, L., García-Chapa, M., López-Moya, J. J., & Burgyán, J. (2010). Viral protein inhibits RISC activity by argonaute binding through conserved WG/GW motifs. PLoS Pathogens, 6(7), e1000996.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Guo, H., Song, X., Xie, C., Huo, Y., Zhang, F., Chen, X., Geng, Y., & Fang, R. (2013). Rice yellow stunt rhabdovirus protein 6 suppresses systemic RNA silencing by blocking RDR6-mediated secondary siRNA synthesis. Molecular Plant-Microbe Interactions, 26(8), 927–936.

    Article  CAS  PubMed  Google Scholar 

  • Guo, Q., Liu, Q., Smith, N. A., Liang, G., & Wang, M. B. (2016). RNA silencing in plants: Mechanisms, technologies and applications in horticultural crops. Current Genomics, 17, 476–489.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hammer, Ø., Harper, D. A. T., & Ryan, P. D. (2001). PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica, 4(1), 1–9.

    Google Scholar 

  • Hong, W., Qian, D., Sun, R., Jiang, L., Wang, Y., Wei, C., Zhang, Z., & Li, Y. (2015). OsRDR6 plays role in host defense against double-stranded RNA virus, Rice dwarf Phytoreovirus. Scientific Reports, 5, 11324.

    Article  PubMed  PubMed Central  Google Scholar 

  • Huang, Y. W., Geng, Y. F., Ying, X. B., Chen, X. Y., & Fang, R. X. (2005). Identification of a movement protein of rice yellow stunt rhabdovirus. Jornal of Virolology, 79(4), 2108–2114.

    CAS  Google Scholar 

  • Ivanov, I., Yabukarski, F., Ruigrok, R. W., & Jamin, M. (2011). Structural insights into the rhabdovirus transcription/replication complex. Virus Research, 162(1–2), 126–137.

    Article  CAS  PubMed  Google Scholar 

  • Izadpanah, K., Ebrahim-Nesbat, F., & Afsharifar, A. R. (1991). Barley yellow striate mosaic virus as the cause of a major disease of wheat and millet in Iran. Journal of Phytopathology, 131(4), 290–296.

    Article  Google Scholar 

  • Jackson, A. O., & Li, Z. (2016). Developments in plant negative-Strand RNA virus reverse genetics. Annual Review of Phytopathology, 54, 469–498.

    Article  CAS  PubMed  Google Scholar 

  • Jackson, A. O., Dietzgen, R. G., Goodin, M. M., Bragg, J., & Deng, M. (2005). Biology of plant rhabdoviruses. Annual Review of Phytopathology, 43, 623–660.

    Article  CAS  PubMed  Google Scholar 

  • Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018). MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35(6), 1547–1549.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leyrat, C., Gérard, F. C., de Almeida Ribeiro Jr., E., Ivanov, I., Ruigrok, R. W., & Jamin, M. (2010). Structural disorder in proteins of the rhabdoviridae replication complex. Protein and Peptide Letters, 17(8), 979–987.

    Article  CAS  PubMed  Google Scholar 

  • Liu, Y., Du, Z., Wang, H., Zhang, S., Cao, M., & Wang, X. (2018). Identification and characterization of wheat yellow striate virus, a novel leafhopper-transmitted nucleorhabdovirus infecting wheat. Frontiers in Microbiology, 9, 468.

    Article  PubMed  PubMed Central  Google Scholar 

  • Livak, K. J., & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods, 25(4), 402–408.

    Article  CAS  PubMed  Google Scholar 

  • Mann, K. S., Johnson, K. N., & Dietzgen, R. G. (2015). Cytorhabdovirus phosphoprotein shows RNA silencing suppressor activity in plants, but not in insect cells. Virology, 476, 413–418.

    Article  CAS  PubMed  Google Scholar 

  • Mann, K. S., Bejerman, N., Johnson, K. N., & Dietzgen, R. G. (2016). Cytorhabdovirus P3 genes encode 30K-like cell-to-cell movement proteins. Virology, 489, 20–33.

    Article  CAS  PubMed  Google Scholar 

  • Mascia, T., Cillo, F., Fanelli, V., Finetti-Sialer, M. M., De Stradis, A., Palukaitis, P., & Gallitelli, D. (2010). Characterization of the interactions between cucumber mosaic virus and potato virus Y in mixed infections in tomato. Molecular Plant-Microbe Interactions, 23(11), 1514–1524.

    Article  CAS  PubMed  Google Scholar 

  • Reichel, C., Mathur, J., Eckes, P., Langenkemper, K., Koncz, C., Schell, J., Reiss, B., & Maas, C. (1996). Enhanced green fluorescence by the expression of an Aequorea victoria green fluorescent protein mutant in mono- and dicotyledonous plant cells. Proceedings of the National Academy of Sciences of the United States of America, 93(12), 5888–5893.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schägger, H., & von Jagow, G. (1987). Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Analytical Biochemistry, 166(2), 368–379.

    Article  PubMed  Google Scholar 

  • Schott, G., Mari-Ordoñez, A., Himber, C., Alioua, A., Voinnet, O., & Dunoyer, P. (2012). Differential effects of viral silencing suppressors on siRNA and miRNA loading support the existence of two distinct cellular pools of ARGONAUTE1. The European Molecular Biology Organization Journal, 31(11), 2553–2565.

    Article  CAS  Google Scholar 

  • Tahmasebi, A., Afsharifar, A., Rabiee, S., & Izadpanah, K. (2017). Altered expression of autophagy-related genes in Nicothiana benthamiana plants in response to potato virus a HC-pro silencing suppressor. Iranian Journal of Plant Pathology, 53(1), 63–74.

    Google Scholar 

  • Vance, V., & Vaucheret, H. (2001). RNA silencing in plants--defense and counterdefense. Science, 292, 2277–2280.

    Article  CAS  PubMed  Google Scholar 

  • Várallyay, E., & Havelda, Z. (2013). Unrelated viral suppressors of RNA silencing mediate the control of ARGONAUTE1 level. Molecular Plant Pathology, 14(6), 567–575.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Walker, P. J., Dietzgen, R. G., Joubert, D. A., & Blasdell, K. R. (2011). Rhabdovirus accessory genes. Virus Research, 162(1–2), 110–125.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Walker, P. J., Blasdell, K. R., Calisher, C. H., Dietzgen, R. G., Kondo, H., Kurath, G., Longdon, B., Stone, D. M., Tesh, R. B., Tordo, N., Vasilakis, N., Whitfield, A. E., & ICTV Report Consortium. (2018). ICTV report consortium ICTV virus taxonomy profile: Rhabdoviridae. Journal of General Virology, 99(4), 447–448.

    Article  CAS  PubMed  Google Scholar 

  • Xie, W., Liang, C., & Birchler, J. A. (2011). Inhibition of RNA interference and modulation of transposable element expression by cell death in Drosophila. Genetics, 188(4), 823–834.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan, T., Zhu, J. R., Di, D., Gao, Q., Zhang, Y., Zhang, A., Yan, C., Miao, H., & Wang, X.-B. (2015). Characterization of the complete genome of Barley yellow striate mosaic virus reveals a nested gene encoding a small hydrophobic protein. Virology, 478, 112–122.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, Z. J., Gao, Q., Fang, X. D., Ding, Z. H., Gao, D. M., Xu, W. Y., Cao, Q., Qiao, J. H., Yang, Y. Z., Han, C., Wang, Y., Yuan, X., Li, D., & Wang, X. B. (2020). CCR4, a RNA decay factor, is hijacked by a plant cytorhabdovirus phosphoprotein to facilitate virus replication. Elife, 24, 9.

    Google Scholar 

  • Zielezinski, A., & Karlowski, W. M. (2011). Agos-a universal web tool for GW Argonaute-binding domain prediction. Bioinformatics, 27(9), 1318–1319.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank D. Baulcombe for providing seeds of N. benthamiana transgenic line 16c and Dr. Livia Stavolone (IPSP, CNR) for kindly supplying the binary vector.

Availability of data and material

The material used for this publication is available upon request to the authors.

Funding

This work was financially supported by the Center of excellence in Plant Virology, Research and Technology, College of Agriculture, Shiraz University, Iran, as part of the first author PhD requirements.

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Authors and Affiliations

  1. Plant Virology Research Center, College of Agriculture, Shiraz University, Shiraz, Iran

    Samira Rabieifaradonbeh & Alireza Afsharifar

  2. Istituto di Bioscienze e Biorisorse, Consiglio Nazionale delle Ricerche, Via G. Amendola 165/A, 70126, Bari, Italy

    Mariella M. Finetti-Sialer

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  1. Samira Rabieifaradonbeh
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  2. Alireza Afsharifar
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  3. Mariella M. Finetti-Sialer
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Correspondence to Mariella M. Finetti-Sialer.

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Accession numbers

GenBank accession numbers MH509194, MH509195, MH509196, and MH509197 were assigned to BYSMV_ P3 gene, BYSMV_ P6 gene, BYSMV_ Pp gene, and BYSMV_ P9 gene respectively.

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Rabieifaradonbeh, S., Afsharifar, A. & Finetti-Sialer, M.M. Molecular and functional characterization of the barley yellow striate mosaic virus genes encoding phosphoprotein, P3, P6 and P9. Eur J Plant Pathol 161, 107–121 (2021). https://doi.org/10.1007/s10658-021-02307-7

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