1887

Abstract

Rice ragged stunt virus (RRSV), an oryzavirus, is transmitted by brown planthopper in a persistent propagative manner. In this study, sequential infection of RRSV in the internal organs of its insect vector after ingestion of virus was investigated by immunofluorescence microscopy. RRSV was first detected in the epithelial cells of the midgut, from where it proceeded to the visceral muscles surrounding the midgut, then throughout the visceral muscles of the midgut and hindgut, and finally into the salivary glands. Viroplasms, the sites of virus replication and assembly of progeny virions, were formed in the midgut epithelium, visceral muscles and salivary glands of infected insects and contained the non-structural protein Pns10 of RRSV, which appeared to be the major constituent of the viroplasms. Viroplasm-like structures formed in non-host insect cells following expression of Pns10 in a baculovirus system, suggesting that the viroplasms observed in RRSV-infected cells were composed basically of Pns10. RNA interference induced by ingestion of dsRNA from the gene of RRSV strongly inhibited such viroplasm formation, preventing efficient virus infection and spread in its insect vectors. These results show that Pns10 of RRSV is essential for viroplasm formation and virus replication in the vector insect.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.042424-0
2012-10-01
2024-05-13
Loading full text...

Full text loading...

/deliver/fulltext/jgv/93/10/2299.html?itemId=/content/journal/jgv/10.1099/vir.0.042424-0&mimeType=html&fmt=ahah

References

  1. Akita F., Miyazaki N., Hibino H., Shimizu T., Higashiura A., Uehara-Ichiki T., Sasaya T., Tsukihara T., Nakagawa A.other authors 2011; Viroplasm matrix protein Pns9 from rice gall dwarf virus forms an octameric cylindrical structure. J Gen Virol 92:2214–2221 [View Article][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. Boccardo G., Milne R. G. 1984 Plant Reovirus Group. CMI/AAB Descriptions of Plant Viruses no. 294 Kew, UK: Commonwealth Microbiology Institute/Association of Applied Biology;
    [Google Scholar]
  4. Chen J., Zhang D., Yao Q., Zhang J., Dong X., Tian H., Chen J., Zhang W. 2010; Feeding-based RNA interference of a trehalose phosphate synthase gene in the brown planthopper, Nilaparvata lugens. Insect Mol Biol 19:777–786 [View Article][PubMed]
    [Google Scholar]
  5. Chen H., Chen Q., Omura T., Uehara-Ichiki T., Wei T. 2011; Sequential infection of Rice dwarf virus in the internal organs of its insect vector after ingestion of virus. Virus Res 160:389–394 [View Article][PubMed]
    [Google Scholar]
  6. 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]
  7. Fire A., Xu S., Montgomery M. K., Kostas S. A., Driver S. E., Mello C. C. 1998; Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806–811 [View Article][PubMed]
    [Google Scholar]
  8. Hagiwara K., Minobe Y., Nozu Y., Hibino H., Kimura I., Omura T. 1986; Component proteins and structures of rice ragged stunt virus. J Gen Virol 67:1711–1715 [View Article]
    [Google Scholar]
  9. Hibino H. 1996; Biology and epidemiology of rice viruses. Annu Rev Phytopathol 34:249–274 [View Article][PubMed]
    [Google Scholar]
  10. Hibino H., Roechan M., Suoarisman S., Tantera D. M. 1977; A virus disease of rice (kerdil hampa) transmitted by brown planthopper, Nilaparvata lugens Stål, in Indonesia. Contr Centr Res Inst Agric Bogor 35:1–15
    [Google Scholar]
  11. Hibino H., Saleh N., Roechan M. 1979; Reovirus-like particles associated with rice ragged stunt diseased rice and insect vector cells. Ann Phytopath Soc Japan 45:228–239 [View Article]
    [Google Scholar]
  12. Hoang A. T., Zhang H.-M., Yang J., Chen J.-P., Hébrard E., Zhou G.-H., Vinh V. N., Cheng J.-A. 2011; Identification, characterization, and distribution of Southern rice black-streaked dwarf virus in Vietnam. Plant Dis 95:1063–1069 [View Article]
    [Google Scholar]
  13. Hogenhout S. A., Ammar D., Whitfield A. E., Redinbaugh M. G. 2008; Insect vector interactions with persistently transmitted viruses. Annu Rev Phytopathol 46:327–359 [View Article][PubMed]
    [Google Scholar]
  14. 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]
  15. Jiang X. F., Jayaram H., Kumar M., Ludtke S. J., Estes M. K., Prasad B. V. V. 2006; Cryoelectron microscopy structures of rotavirus NSP2–NSP5 and NSP2–RNA complexes: implications for genome replication. J Virol 80:10829–10835 [View Article][PubMed]
    [Google Scholar]
  16. Kumar M., Jayaram H., Vasquez-Del Carpio R., Jiang X., Taraporewala Z. F., Jacobson R. H., Patton J. T., Prasad B. V. V. 2007; Crystallographic and biochemical analysis of rotavirus NSP2 with nucleotides reveals a nucleoside diphosphate kinase-like activity. J Virol 81:12272–12284 [View Article][PubMed]
    [Google Scholar]
  17. Li J., Chen Q., Lin Y., Jiang T., Wu G., Hua H. 2011; RNA interference in Nilaparvata lugens (Homoptera: Delphacidae) based on dsRNA ingestion. Pest Manag Sci 67:852–859 [View Article][PubMed]
    [Google Scholar]
  18. 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]
  19. 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]
  20. Miyazaki N., Uehara-Ichiki T., Xing L., Bergman L., Higashiura A., Nakagawa A., Omura T., Cheng R. H. 2008; Structural evolution of Reoviridae revealed by Oryzavirus in acquiring the second capsid shell. J Virol 82:11344–11353 [View Article][PubMed]
    [Google Scholar]
  21. Shimizu T., Yoshii M., Wei T., Hirochika H., Omura T. 2009; Silencing by RNAi of the gene for Pns12, a viroplasm matrix protein of Rice dwarf virus, results in strong resistance of transgenic rice plants to the virus. Plant Biotechnol J 7:24–32 [View Article][PubMed]
    [Google Scholar]
  22. Shimizu T., Nakazono-Nagaoka E., Akita F., Uehara-Ichiki T., Omura T., Sasaya T. 2011; Immunity to Rice black streaked dwarf virus, a plant reovirus, can be achieved in rice plants by RNA silencing against the gene for the viroplasm component protein. Virus Res 160:400–403 [View Article][PubMed]
    [Google Scholar]
  23. Shimizu T., Nakazono-Nagaoka E., Akita F., Wei T., Sasaya T., Omura T., Uehara-Ichiki T. 2012; Hairpin RNA derived from the gene for Pns9, a viroplasm matrix protein of Rice gall dwarf virus, confers strong resistance to virus infection in transgenic rice plants. J Biotechnol 157:421–427 [View Article][PubMed]
    [Google Scholar]
  24. Silvestri L. S., Taraporewala Z. F., Patton J. T. 2004; Rotavirus replication: plus-sense templates for double-stranded RNA synthesis are made in viroplasms. J Virol 78:7763–7774 [View Article][PubMed]
    [Google Scholar]
  25. Spear A., Sisterson M. S., Stenger D. C. 2012; Reovirus genomes from plant-feeding insects represent a newly discovered lineage within the family Reoviridae. Virus Res 163:503–511 [View Article][PubMed]
    [Google Scholar]
  26. Spinelli S., Campanacci V., Blangy S., Moineau S., Tegoni M., Cambillau C. 2006; Modular structure of the receptor binding proteins of Lactococcus lactis phages. The RBP structure of the temperate phage TP901-1. J Biol Chem 281:14256–14262 [View Article][PubMed]
    [Google Scholar]
  27. 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]
  28. Takahashi Y., Omura T., Shohara K., Tsuchizaki T. 1991; Comparison of four serological methods for practical detection of ten viruses of rice in plants and insects. Plant Dis 75:458–461 [View Article]
    [Google Scholar]
  29. Tsai J., Perrier J. L. 1996; Morphology of the digestive and reproductive systems of Dalbulus maidis and Graminella nigrifrons (Homoptera: Cicadellidae). Fla Entomol 79:563–567 [View Article]
    [Google Scholar]
  30. Upadhyaya N. M., Zinkowsky E., Li Z., Kositratana W., Waterhouse P. M. 1996; The Mr 43K major capsid protein of rice ragged stunt oryzavirus is a post-translationally processed product of a Mr 67,348 polypeptide encoded by genome segment 8. Arch Virol 141:1689–1701 [View Article][PubMed]
    [Google Scholar]
  31. Upadhyaya N. M., Ramm K., Gellatly J. A., Li Z., Kositratana W., Waterhouse P. M. 1997; Rice ragged stunt oryzavirus genome segments S7 and S10 encode non-structural proteins of Mr 68,025 (Pns7) and Mr 32,364 (Pns10). Arch Virol 142:1719–1726 [View Article][PubMed]
    [Google Scholar]
  32. Upadhyaya N. M., Ramm K., Gellatly J. A., Li Z., Kositratana W., Waterhouse P. M. 1998; Rice ragged stunt oryzavirus genome segment S4 could encode an RNA dependent RNA polymerase and a second protein of unknown function. Arch Virol 143:1815–1822 [View Article][PubMed]
    [Google Scholar]
  33. Vasquez-Del Carpio R., Gonzalez-Nilo F. D., Riadi G., Taraporewala Z. F., Patton J. T. 2006; Histidine triad-like motif of the rotavirus NSP2 octamer mediates both RTPase and NTPase activities. J Mol Biol 362:539–554 [View Article][PubMed]
    [Google Scholar]
  34. Wei T., Kikuchi A., Moriyasu Y., Suzuki N., Shimizu T., Hagiwara K., Chen H., Takahashi M., Ichiki-Uehara T., Omura T. 2006a; The spread of Rice dwarf virus among cells of its insect vector exploits virus-induced tubular structures. J Virol 80:8593–8602 [View Article][PubMed]
    [Google Scholar]
  35. Wei T., Shimizu T., Hagiwara K., Kikuchi A., Moriyasu Y., Suzuki N., Chen H., Omura T. 2006b; 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]
  36. Wu J., Du Z., Wang C., Cai L., Hu M., Lin Q., Wu Z., Li Y., Xie L. 2010a; Identification of Pns6, a putative movement protein of RRSV, as a silencing suppressor. Virol J 7:335 [View Article][PubMed]
    [Google Scholar]
  37. Wu Z., Wu J., Adkins S., Xie L., Li W. 2010b; Rice ragged stunt virus segment S6-encoded nonstructural protein Pns6 complements cell-to-cell movement of Tobacco mosaic virus-based chimeric virus. Virus Res 152:176–179 [View Article][PubMed]
    [Google Scholar]
  38. Zhou G. Y., Lu X. B., Lu H. J., Lei J. L., Chen S. X., Gong Z. X. 1999; Rice ragged stunt oryzavirus: role of the viral spike protein in transmission by the insect vector. Ann Appl Biol 135:573–578 [View Article]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.042424-0
Loading
/content/journal/jgv/10.1099/vir.0.042424-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
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