1887

Journal of General Virology header logo

Volume 94, Issue 8

Non-structural protein P6 encoded by rice black-streaked dwarf virus is recruited to viral inclusion bodies by binding to the viroplasm matrix protein P9-1 Free

Abstract

Like other members of the family , rice black-streaked dwarf virus (RBSDV, genus ) is thought to replicate and assemble within cytoplasmic viral inclusion bodies, commonly called viroplasms. RBSDV P9-1 is the key protein for the formation of viroplasms, but little is known about the other proteins of the viroplasm or the molecular interactions amongst its components. RBSDV non-structural proteins were screened for their association with P9-1 using a co-immunoprecipitation assay. Only P6 was found to directly interact with P9-1, an interaction that was confirmed by bimolecular fluorescence complementation assay in () cells. Immunoelectron microscopy showed that P6 and P9-1 co-localized in electron-dense inclusion bodies, indicating that P6 is a constituent of the viroplasm. In addition, non-structural protein P5 also localized to viroplasms and interacted with P6. In cells, P6 was diffusely distributed throughout the cytoplasm when expressed alone, but localized to inclusions when co-expressed with P9-1, suggesting that P6 is recruited to viral inclusion bodies by binding to P9-1. P5 localized to the inclusions formed by P9-1 when co-expressed with P6 but did not when P6 was absent, suggesting that P5 is recruited to viroplasms by binding to P6. This study provides a model by which viral non-structural proteins are recruited to RBSDV viroplasms.

  • Received:
  • Accepted:
  • Published Online:
© 2013 SGM
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.051698-0
2013-08-01
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/jgv/94/8/1908.html?itemId=/content/journal/jgv/10.1099/vir.0.051698-0&mimeType=html&fmt=ahah

References

  1. Afrikanova I., Fabbretti E., Miozzo M. C., Burrone O. R. 1998; Rotavirus NSP5 phosphorylation is up-regulated by interaction with NSP2. J Gen Virol 79:2679–2686[PubMed]
     [Google Scholar]
  2. Akita F., Higashiura A., Shimizu T., Pu Y., Suzuki M., Uehara-Ichiki T., Sasaya T., Kanamaru S., Arisaka F.& other authors ( 2012; Crystallographic analysis reveals octamerization of viroplasm matrix protein P9-1 of rice black streaked dwarf virus. J Virol 86:746–756 [View Article][PubMed]
     [Google Scholar]
  3. Arnold M. M., Murray K. E., Nibert M. L. 2008; Formation of the factory matrix is an important, though not a sufficient function of nonstructural protein μNS during reovirus infection. Virology 375:412–423 [View Article][PubMed]
     [Google Scholar]
  4. Attoui H., Mertens P. P. C., Becnel J., Belaganahalli S., Bergoin M., Brussaard C. P., Chappell J. D., Ciarlet M., del Vas M.& other authors ( 2011; The family Reoviridae . In Virus Taxonomy: Ninth Report of the International Committee for the Taxonomy of Viruses pp. 541–637 Edited by King A. M. Q., Adams M. J., Castens E. B., Lefkowitz E. J. New York: Elsevier Academic Press;
     [Google Scholar]
  5. Bai F. W., Yan J., Qu Z. C., Zhang H. W., Xu J., Ye M. M., Shen D. L. 2002; Phylogenetic analysis reveals that a dwarfing disease on different cereal crops in China is due to rice black streaked dwarf virus (RBSDV). Virus Genes 25:201–206 [View Article][PubMed]
     [Google Scholar]
  6. Becker M. M., Goral M. I., Hazelton P. R., Baer G. S., Rodgers S. E., Brown E. G., Coombs K. M., Dermody T. S. 2001; Reovirus σNS protein is required for nucleation of viral assembly complexes and formation of viral inclusions. J Virol 75:1459–1475 [View Article][PubMed]
     [Google Scholar]
  7. Becker M. M., Peters T. R., Dermody T. S. 2003; Reovirus σNS and μNS proteins form cytoplasmic inclusion structures in the absence of viral infection. J Virol 77:5948–5963 [View Article][PubMed]
     [Google Scholar]
  8. Broering T. J., Kim J., Miller C. L., Piggott C. D., Dinoso J. B., Nibert M. L., Parker J. S. 2004; Reovirus nonstructural protein μNS recruits viral core surface proteins and entering core particles to factory-like inclusions. J Virol 78:1882–1892 [View Article][PubMed]
     [Google Scholar]
  9. Contin R., Arnoldi F., Campagna M., Burrone O. R. 2010; Rotavirus NSP5 orchestrates recruitment of viroplasmic proteins. J Gen Virol 91:1782–1793 [View Article][PubMed]
     [Google Scholar]
  10. Fabbretti E., Afrikanova I., Vascotto F., Burrone O. R. 1999; Two non-structural rotavirus proteins, NSP2 and NSP5, form viroplasm-like structures in vivo . J Gen Virol 80:333–339[PubMed]
     [Google Scholar]
  11. Fang S., Yu J., Feng J., Han C., Li D., Liu Y. 2001; Identification of rice black-streaked dwarf fijivirus in maize with rough dwarf disease in China. Arch Virol 146:167–170 [View Article][PubMed]
     [Google Scholar]
  12. Gillian A. L., Schmechel S. C., Livny J., Schiff L. A., Nibert M. L. 2000; Reovirus protein sigmaNS binds in multiple copies to single-stranded RNA and shares properties with single-stranded DNA binding proteins. J Virol 74:5939–5948 [View Article][PubMed]
     [Google Scholar]
  13. Hu C. D., Kerppola T. K. 2003; Simultaneous visualization of multiple protein interactions in living cells using multicolor fluorescence complementation analysis. Nat Biotechnol 21:539–545 [View Article][PubMed]
     [Google Scholar]
  14. Isogai M., Uyeda I., Lee B. C. 1998a; Detection and assignment of proteins encoded by rice black streaked dwarf fijivirus S7, S8, S9 and S10. J Gen Virol 79:1487–1494[PubMed]
     [Google Scholar]
  15. Isogai M., Uyeda I., Lindsten K. 1998b; Taxonomic characteristics of fijiviruses based on nucleotide sequences of the oat sterile dwarf virus genome. J Gen Virol 79:1479–1485[PubMed]
     [Google Scholar]
  16. Jia D., Chen H., Zheng A., Chen Q., Liu Q., Xie L., Wu Z., Wei T. 2012; Development of an insect vector cell culture and RNA interference system to investigate the functional role of fijivirus replication protein. J Virol 86:5800–5807 [View Article][PubMed]
     [Google Scholar]
  17. Kattoura M. D., Clapp L. L., Patton J. T. 1992; The rotavirus nonstructural protein, NS35, possesses RNA-binding activity in vitro and in vivo . Virology 191:698–708 [View Article][PubMed]
     [Google Scholar]
  18. Li J., Xue J., Zhang H. M., Yang J., Lv M. F., Xie L., Meng Y., Li P. P., Chen J. P. 2013; Interactions between the P6 and P5-1 proteins of southern rice black-streaked dwarf fijivirus in yeast and plant cells. Arch Virol (Epub ahead of print) [View Article][PubMed]
     [Google Scholar]
  19. Liu H., Wei C., Zhong Y., Li Y. 2007a; Rice black-streaked dwarf virus minor core protein P8 is a nuclear dimeric protein and represses transcription in tobacco protoplasts. FEBS Lett 581:2534–2540 [View Article][PubMed]
     [Google Scholar]
  20. Liu H., Wei C., Zhong Y., Li Y. 2007b; Rice black-streaked dwarf virus outer capsid protein P10 has self-interactions and forms oligomeric complexes in solution. Virus Res 127:34–42 [View Article][PubMed]
     [Google Scholar]
  21. Liu Y., Jia D., Chen H., Chen Q., Xie L., Wu Z., Wei T. 2011; The P7-1 protein of southern rice black-streaked dwarf virus, a fijivirus, induces the formation of tubular structures in insect cells. Arch Virol 156:1729–1736 [View Article][PubMed]
     [Google Scholar]
  22. Maroniche G. A., Mongelli V. C., Peralta A. V., Distéfano A. J., Llauger G., Taboga O. A., Hopp E. H., del Vas M. 2010; Functional and biochemical properties of Mal de Río Cuarto virus (Fijivirus, Reoviridae) P9-1 viroplasm protein show further similarities to animal reovirus counterparts. Virus Res 152:96–103 [View Article][PubMed]
     [Google Scholar]
  23. Maroniche G. A., Mongelli V. C., Llauger G., Alfonso V., Taboga O., del Vas M. 2012; In vivo subcellular localization of Mal de Río Cuarto virus (MRCV) non-structural proteins in insect cells reveals their putative functions. Virology 430:81–89 [View Article][PubMed]
     [Google Scholar]
  24. Netherton C., Moffat K., Brooks E., Wileman T. 2007; A guide to viral inclusions, membrane rearrangements, factories, and viroplasm produced during virus replication. Adv Virus Res 70:101–182 [View Article][PubMed]
     [Google Scholar]
  25. Patton J. T., Silvestri L. S., Tortorici M. A., Vasquez-Del Carpio R., Taraporewala Z. F. 2006; Rotavirus genome replication and morphogenesis: role of the viroplasm. Curr Top Microbiol Immunol 309:169–187 [View Article][PubMed]
     [Google Scholar]
  26. Roy P., Noad R. 2006; Bluetongue virus assembly and morphogenesis. Curr Top Microbiol Immunol 309:87–116 [View Article][PubMed]
     [Google Scholar]
  27. Shikata E., Kitagawa Y. 1977; Rice black-streaked dwarf virus: its properties, morphology and intracellular localization. Virology 77:826–842 [View Article][PubMed]
     [Google Scholar]
  28. Sun L., Suzuki N. 2008; Intragenic rearrangements of a mycoreovirus induced by the multifunctional protein p29 encoded by the prototypic hypovirus CHV1-EP713. RNA 14:2557–2571 [View Article][PubMed]
     [Google Scholar]
  29. Sun L., Andika I. B., Kondo H., Chen J. 2013; Identification of the amino acid residues and domains in the cysteine-rich protein of Chinese wheat mosaic virus that are important for RNA silencing suppression and subcellular localization. Mol Plant Pathol 14:265–278 [View Article][PubMed]
     [Google Scholar]
  30. Supyani S., Hillman B. I., Suzuki N. 2007; Baculovirus expression of the 11 mycoreovirus-1 genome segments and identification of the guanylyltransferase-encoding segment. J Gen Virol 88:342–350 [View Article][PubMed]
     [Google Scholar]
  31. Thomas C. P., Booth T. F., Roy P. 1990; Synthesis of bluetongue virus-encoded phosphoprotein and formation of inclusion bodies by recombinant baculovirus in insect cells: it binds the single-stranded RNA species. J Gen Virol 71:2073–2083 [View Article][PubMed]
     [Google Scholar]
  32. Touris-Otero F., Martínez-Costas J., Vakharia V. N., Benavente J. 2004a; Avian reovirus nonstructural protein µNS forms viroplasm-like inclusions and recruits protein sigmaNS to these structures. Virology 319:94–106 [View Article][PubMed]
     [Google Scholar]
  33. Tourís-Otero F., Cortez-San Martín M., Martínez-Costas J., Benavente J. 2004b; Avian reovirus morphogenesis occurs within viral factories and begins with the selective recruitment of σNS and λA to µNS inclusions. J Mol Biol 341:361–374 [View Article][PubMed]
     [Google Scholar]
  34. Wang Z. H., Fang S. G., Xu J. L., Sun L. Y., Li D. W., Yu J. L. 2003; Sequence analysis of the complete genome of rice black-streaked dwarf virus isolated from maize with rough dwarf disease. Virus Genes 27:163–168 [View Article][PubMed]
     [Google Scholar]
  35. Wang Q., Tao T., Zhang Y., Wu W., Li D., Yu J., Han C. 2011; Rice black-streaked dwarf virus P6 self-interacts to form punctate, viroplasm-like structures in the cytoplasm and recruits viroplasm-associated protein P9-1. Virol J 8:24 [View Article][PubMed]
     [Google Scholar]
  36. Wei T., Shimizu T., Hagiwara K., Kikuchi A., Moriyasu Y., Suzuki N., Chen H., Omura T. 2006; Pns12 protein of rice dwarf virus is essential for formation of viroplasms and nucleation of viral-assembly complexes. J Gen Virol 87:429–438 [View Article][PubMed]
     [Google Scholar]
  37. Xiong R., Wu J., Zhou Y., Zhou X. 2008; Identification of a movement protein of the tenuivirus rice stripe virus. J Virol 82:12304–12311 [View Article][PubMed]
     [Google Scholar]
  38. Xu H., Li Y., Mao Z., Li Y., Wu Z., Qu L., An C., Ming X., Schiemann J.& other authors ( 1998; Rice dwarf phytoreovirus segment S11 encodes a nucleic acid binding protein. Virology 240:267–272 [View Article][PubMed]
     [Google Scholar]
  39. Zhang H. M., Chen J. P., Adams M. J. 2001; Molecular characterisation of segments 1 to 6 of rice black-streaked dwarf virus from China provides the complete genome. Arch Virol 146:2331–2339 [View Article][PubMed]
     [Google Scholar]
  40. Zhang L., Wang Z., Wang X., Li D., Han C., Zhai Y., Yu J. 2005; Two virus-encoded RNA silencing suppressors, P14 of Beet necrotic yellow vein virus and S6 of Rice black streak dwarf virus. Chin Sci Bull 50:305–310 [View Article]
     [Google Scholar]
  41. Zhang C., Liu Y., Liu L., Lou Z., Zhang H., Miao H., Hu X., Pang Y., Qiu B. 2008; Rice black streaked dwarf virus P9-1, an α-helical protein, self-interacts and forms viroplasms in vivo. J Gen Virol 89:1770–1776 [View Article][PubMed]
     [Google Scholar]
  42. Zhao Y., Thomas C., Bremer C., Roy P. 1994; Deletion and mutational analyses of bluetongue virus NS2 protein indicate that the amino but not the carboxy terminus of the protein is critical for RNA-protein interactions. J Virol 68:2179–2185[PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.051698-0
Loading
Non-structural protein P6 encoded by rice black-streaked dwarf virus is recruited to viral inclusion bodies by binding to the viroplasm matrix protein P9-1
J. Gen. Virol. 94, 1908 (2013); https://doi.org/10.1099/vir.0.051698-0
/content/journal/jgv/10.1099/vir.0.051698-0
/content/journal/jgv/10.1099/vir.0.051698-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error