1887

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.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.051698-0
2013-08-01
2019-10-16
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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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). [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [PubMed]
    [Google Scholar]
  26. Roy P., Noad R.. ( 2006; ). Bluetongue virus assembly and morphogenesis. . Curr Top Microbiol Immunol 309:, 87–116. [CrossRef] [PubMed]
    [Google Scholar]
  27. Shikata E., Kitagawa Y.. ( 1977; ). Rice black-streaked dwarf virus: its properties, morphology and intracellular localization. . Virology 77:, 826–842. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef] [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. [CrossRef]
    [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. [CrossRef] [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
/content/journal/jgv/10.1099/vir.0.051698-0
Loading

Data & Media loading...

Supplements

Supplementary material 

PDF

Supplementary material 

PDF

Most Cited This Month

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