Abstract
RNA silencing is a conserved mechanism found ubiquitously in eukaryotic organisms. It has been used to regulate gene expression and development. In addition, RNA silencing serves as an important mechanism in plants’ defense against invasive nucleic acids, such as viruses, transposons, and transgenes. As a counter-defense, most plants, and some animal viruses, encode RNA silencing suppressors to interfere at one or several points of the silencing pathway. In this study, we showed that Pns12 of RGDV (Rice gall dwarf virus) exhibits silencing suppressor activity on the reporter green fluorescent protein in transgenic Nicotiana benthamiana line 16c. Pns12 of RGDV suppressed local silencing induced by sense RNA but had no effect on that induced by dsRNA. Expression of Pns12 also enhanced Potato virus X pathogenicity in N. benthamiana. Collectively, these results suggested that RGDV Pns12 functions as a virus suppressor of RNA silencing, which might target an upstream step of dsRNA formation in the RNA silencing pathway. Furthermore, we showed that Pns12 is localized mainly in the nucleus of N. benthamiana leaf cells.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Ding S W, Voinnet O. Antiviral immunity directed by small RNAs. Cell, 2007, 130: 413–426, 17693253, 10.1016/j.cell.2007.07.039, 1:CAS:528:DC%2BD2sXptlyntLY%3D
Fire A. RNA-triggered gene silencing. Trends Genet, 1999, 15: 358–363, 10461204, 10.1016/S0168-9525(99)01818-1, 1:CAS:528:DyaK1MXltlyms7s%3D
Caplen N J, Fleenor J, Fire A, et al. dsRNA-mediated gene silencing in cultured Drosophila cells: A tissue culture model for the analysis of RNA interference. Gene, 2005, 252: 95–105, 10.1016/S0378-1119(00)00224-9
Caplen N J, Parrish S, Imani F, et al. Specific inhibition of gene expression by small double-stranded RNAs in invertebrate and vertebrate systems. Proc Natl Acad Sci USA, 2001, 98: 9742–9747, 11481446, 10.1073/pnas.171251798, 1:CAS:528:DC%2BD3MXmtlCmsrY%3D
Hammond S M, Bernstein E, Beach D, et al. An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature, 2000, 404: 293–296, 10749213, 10.1038/35005107, 1:CAS:528:DC%2BD3cXit1agtrw%3D
Elbashir S M, Lendeckel W, Tuschl T. RNA interference is mediated by 21- and 22-nucleotide RNAs. Gene Dev, 2001, 15: 188–200, 11157775, 10.1101/gad.862301, 1:CAS:528:DC%2BD3MXhvVOjtbg%3D
Fire A, Xu S Q, Montgomery M K, et al. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature, 1998, 391: 806–811, 9486653, 10.1038/35888, 1:CAS:528:DyaK1cXhtlCju74%3D
Zamore P D. Ancient pathways programmed by small RNAs. Science, 2002, 296: 1265–1269, 12016303, 10.1126/science.1072457, 1:CAS:528:DC%2BD38Xjsl2qt7g%3D
Ding S W. RNA silencing. Curr Opin Biotech, 2000, 11: 152–156, 10753772, 10.1016/S0958-1669(00)00074-4, 1:CAS:528:DC%2BD3cXisFynsrs%3D
Vance V, Vaucheret H. RNA silencing in plants—defense and counterdefense. Science, 2001, 292: 2277–2280, 11423650, 10.1126/science.1061334, 1:CAS:528:DC%2BD3MXks1yrtr8%3D
Ding S W, Li H W, Lu R, et al. RNA silencing: A conserved antiviral immunity of plants and animals. Virus Res, 2004, 102: 109–115, 15068886, 10.1016/j.virusres.2004.01.021, 1:CAS:528:DC%2BD2cXivVKmtL0%3D
Roth B M, Pruss G J, Vance V B. Plant viral suppressors of RNA silencing. Virus Res, 2004, 102: 97–108, 15068885, 10.1016/j.virusres.2004.01.020, 1:CAS:528:DC%2BD2cXivVKmtLw%3D
Voinnet O. Induction and suppression of RNA silencing: Insights from viral infections. Nat Rev Genet, 2005, 6: 206–220, 15703763, 10.1038/nrg1555, 1:CAS:528:DC%2BD2MXhslGjur8%3D
Qi Y J, Zhong X H, Itaya A, et al. Dissecting RNA silencing in protoplasts uncovers novel effects of viral suppressors on the silencing pathway at the cellular level. Nucleic Acids Res, 2004, 32: e179, 15601991, 10.1093/nar/gnh180
Li F, Ding S W. Virus counterdefense: Diverse strategies for evading the RNA-silencing immunity. Annu Rev Microbiol, 2006, 60: 503–531, 16768647, 10.1146/annurev.micro.60.080805.142205, 1:CAS:528:DC%2BD28Xht1Whtb3J
Anandalakshmi R, Pruss G J, Ge X, et al. A viral suppressor of gene silencing in plants. Proc Natl Acad Sci USA, 1998, 95: 13079–13084, 9789044, 10.1073/pnas.95.22.13079, 1:CAS:528:DyaK1cXntFWkurk%3D
Brigneti G, Voinnet O, Li W X, et al. Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana. EMBO J, 1998, 17: 6739–6746, 9822616, 10.1093/emboj/17.22.6739, 1:CAS:528:DyaK1cXnvF2jtLw%3D
Kasschau K D, Carrington J C. A counterdefensive strategy of plant viruses: Suppression of posttranscriptional gene silencing. Cell, 1998, 95: 461–470, 9827799, 10.1016/S0092-8674(00)81614-1, 1:CAS:528:DyaK1cXns1ektro%3D
Lecellier C H, Dunoyer P, Arar K, et al. A cellular microRNA mediates antiviral defense in human cells. Science, 2005, 308: 557–560, 15845854, 10.1126/science.1108784, 1:CAS:528:DC%2BD2MXjtlOjt78%3D
Cao X S, Zhou P, Zhang X M, et al. Identification of an RNA silencing suppressor from a plant double-stranded RNA virus. J Virol, 2005, 79: 13018–13027, 16189004, 10.1128/JVI.79.20.13018-13027.2005, 1:CAS:528:DC%2BD2MXhtFWisbvP
Liu F, Zhao Q, Ruan X, et al. Suppressor of RNA silencing encoded by Rice gall dwarf virus genome segment 11. Chin Sci Bull, 2008, 53: 96–103
Schnettler E, Hemmes H, Goldbach R, et al. The NS3 protein of Rice hoja blanca virus suppresses RNA silencing in mammalian cells. J Gen Virol, 2008, 89: 336–340, 18089758, 10.1099/vir.0.83293-0, 1:CAS:528:DC%2BD1cXns1Wnuw%3D%3D
Xiong R, Wu J, Zhou Y, et al. Characterization and subcellular localization of an RNA silencing suppressor encoded by Rice stripe tenuivirus. Virology, 2009, 387: 29–40, 19251298, 10.1016/j.virol.2009.01.045, 1:CAS:528:DC%2BD1MXkt1Sjs7w%3D
Shi Y, Ryabov E V, Wezel R V, et al. Suppression of local RNA silencing is not sufficient to promote cell-to-cell movement of Turnip crinkle virus in Nicotiana benthamiana. Plant Signal Behav, 2009, 4: 15–22, 19568335, 10.4161/psb.4.1.7573, 1:CAS:528:DC%2BD1MXpsVyqtLg%3D
Zhang L, Wang Z, Wang X, et al. Two virus-encoded RNA silencing suppressors, P14 of Beet necrotic yellow vein virus and S6 of Rice black streak dwarf virus. Chin Sci Bull, 2005, 50: 219–224
Lu R, Folimonov A, Shintaku M, et al. Three distinct suppressors of RNA silencing encoded by a 20-kb viral RNA genome. Proc Natl Acad Sci USA, 2004, 101: 15742–15747, 15505219, 10.1073/pnas.0404940101, 1:CAS:528:DC%2BD2cXhtVWisLnO
Gopal P, Kumar P P, Sinilal B, et al. Differential roles of C4 and beta C1 in mediating suppression of post-transcriptional gene silencing: Evidence for transactivation by the C2 of Bhendi yellow vein mosaic virus, a monopartite begomovirus. Virus Res, 2007, 123: 9–18, 16949698, 10.1016/j.virusres.2006.07.014, 1:CAS:528:DC%2BD28Xht1eku7bN
Omura T, Inoue H, Saito Y. Purification and some properties of Rice gall dwarf virus, a new Phytoreovirus. Phytopathology, 1982, 72: 1246–1249, 10.1094/Phyto-72-1246
Xie L H, Lin Q Y, Xie L Y, et al. Rice bunchy stunt virus: A new member of Phytoreovirus. J Fujian Agri Univ, 1996, 25: 312–319
Picton A, Potgieter C, Rey M E. Molecular analysis of six segments of Tobacco leaf enation virus, a novel Phytoreovirus from tobacco. Virus Genes, 2007, 35: 387–393, 17356907, 10.1007/s11262-007-0088-x, 1:CAS:528:DC%2BD2sXnvFeisb4%3D
Katsar C S, Hunter W B, Sinisterra X H. Phytoreovirus-like sequences isolated from glassy-winged sharpshooter salivary glands (Hemiptera: Cicadellidae: Homalodisca vitripennis). Florida Entomol, 2007, 90: 196–203, 10.1653/0015-4040(2007)90[196:PSIFSG]2.0.CO;2, 1:CAS:528:DC%2BD2sXlt1ansro%3D
Wei T, Ichiki-Uehara T, Miyazaki N, et al. Association of Rice gall dwarf virus with microtubules is necessary for viral release from cultured insect vector cells. J Virol, 2009, 83: 10830–10835, 19640979, 10.1128/JVI.01067-09, 1:CAS:528:DC%2BD1MXhtlCltr%2FO
Francki R, Boccardo G. The plant reoviridae. In: The Reoviridae. New York: Plenum Press, 1983. 505–563
Ichimi K, Kikuchi A, Moriyasu Y, et al. Sequence analysis and GTP-binding ability of the minor core protein P5 of Rice gall dwarf virus. Jpn Agr Res Q, 2002, 36: 83–87, 1:CAS:528:DC%2BD38XntF2ju7g%3D
Moriyasu Y, Maruyama-Funatsuki W, Kikuchi A, et al. Molecular analysis of the genome segments S1, S4, S6, S7 and S12 of a Rice gall dwarf virus isolate from Thailand; completion of the genomic sequence. Arch Virol, 2007, 152: 1315–1322, 17426918, 10.1007/s00705-007-0948-7, 1:CAS:528:DC%2BD2sXntVOltL4%3D
Zhang H M, Yang J, Xin X, et al. Molecular characterization of the genome segments S4, S6 and S7 of Rice gall dwarf virus. Arch Virol, 2007a, 152: 1593–1602, 17558539, 10.1007/s00705-007-1004-3, 1:CAS:528:DC%2BD2sXpsFWrsrc%3D
Zhang H M, Xin X, Yang J, et al. Completion of the sequence of Rice gall dwarf virus from Guangxi, China. Arch Virol, 2008, 153: 1737–1741, 18661096, 10.1007/s00705-008-0167-x, 1:CAS:528:DC%2BD1cXhtVejs7jJ
Zhang H M, Yang J, Xin X, et al. Molecular characterization of the largest and smallest genome segments, S1 and S12, of Rice gall dwarf virus. Virus Genes, 2007b, 35: 815–823, 17674177, 10.1007/s11262-007-0142-8, 1:CAS:528:DC%2BD2sXht1agsLzN
Powers J G, Sit T L, Qu F, et al. A versatile assay for the identification of RNA silencing suppressors based on complementation of viral movement. Mol Plant Microbe In, 2008, 21: 879–890, 10.1094/MPMI-21-7-0879, 1:CAS:528:DC%2BD1cXnsVOru7s%3D
Hamilton A J, Voinnet O, Chappell L, et al. Two classes of short interfering RNA in RNA silencing. EMBO J, 2002, 21: 4671–4679, 12198169, 10.1093/emboj/cdf464, 1:CAS:528:DC%2BD38Xms1KmsrY%3D
Goto K, Kanazawa A, Kusaba M, et al. A simple and rapid method to detect plant siRNAs using nonradioactive probes. Plant Mol Biol Rep, 2003, 21: 51–58, 10.1007/BF02773396, 1:CAS:528:DC%2BD3sXlt1Khurk%3D
Li W X, Ding S W. Viral suppressors of RNA silencing. Curr Opin Biotechnol, 2001, 12: 150–154, 11287229, 10.1016/S0958-1669(00)00190-7, 1:CAS:528:DC%2BD3MXjt1Olu7w%3D
Chen J, Li W X, Xie D, et al. Viral virulence protein suppresses RNA silencing-mediated defense but upregulates the role of microRNA in host gene expression. Plant Cell, 2004, 16: 1302–1313, 15100397, 10.1105/tpc.018986, 1:CAS:528:DC%2BD2cXktlOqtr4%3D
Voinnet O, Lederer C, Baulcombe D C. A viral movement protein prevents spread of the gene silencing signal in Nicotiana benthamiana. Cell, 2000, 103: 157–167, 11051555, 10.1016/S0092-8674(00)00095-7, 1:CAS:528:DC%2BD3cXnt1yqur8%3D
Pruss G, Ge X, Shi X M, et al. Plant viral synergism: The potyviral genome encodes a broad-range pathogenicity enhancer that transactivates replication of heterologous viruses. Plant Cell, 1997, 9: 859–868, 9212462, 10.1105/tpc.9.6.859, 1:CAS:528:DyaK2sXktFClsr0%3D
Waterhouse P M, Helliwell C A. Exploring plant genomes by RNA-induced gene silencing. Nat Rev Genet, 2003, 4: 29–38, 12509751, 10.1038/nrg982, 1:CAS:528:DC%2BD38XpvVent7k%3D
Cui X, Li G, Wang D, et al. A Begomovirus DNAbeta-encoded protein binds DNA, functions as a suppressor of RNA silencing, and targets the cell nucleus. J Virol, 2005, 79: 10764–10775, 16051868, 10.1128/JVI.79.16.10764-10775.2005, 1:CAS:528:DC%2BD2MXntFCqsLs%3D
Li H W, Li W X, Ding S W. Induction and suppression of RNA silencing by an animal virus. Science, 2002, 296: 1319–1321, 12016316, 10.1126/science.1070948, 1:CAS:528:DC%2BD38Xjsl2qurg%3D
Lucy A P, Guo H S, Li W X, et al. Suppression of post-transcriptional gene silencing by a plant viral protein localized in the nucleus. EMBO J, 2000, 19: 1672–1680, 10747034, 10.1093/emboj/19.7.1672, 1:CAS:528:DC%2BD3cXislymtL0%3D
Zhang X R, Yuan Y R, Pei Y, et al. Cucumber mosaic virus-encoded 2b suppressor inhibits Arabidopsis Argonaute1 cleavage activity to counter plant defense. Gene Dev, 2006, 20: 3255–3268, 17158744, 10.1101/gad.1495506, 1:CAS:528:DC%2BD28XhtlSmt7jN
Wang Y Z, Tzfira T, Gaba V, et al. Functional analysis of the Cucumber mosaic virus 2b protein: Pathogenicity and nuclear localization. J Gen Virol, 2004, 85: 3135–3147, 15448377, 10.1099/vir.0.80250-0, 1:CAS:528:DC%2BD2cXosV2gt7Y%3D
van Wezel R, Liu H T, Tien P, et al. Gene C2 of the monopartite geminivirus Tomato yellow leaf curl virus-China encodes a pathogenicity determinant that is localized in the nucleus. Mol Plant Microbe In, 2001, 14: 1125–1128, 10.1094/MPMI.2001.14.9.1125
Dong X L, van Wezel R, Stanley J, et al. Functional characterization of the nuclear localization signal for a suppressor of posttranscriptional gene silencing. J Virol, 2003, 77: 7026–7033, 12768021, 10.1128/JVI.77.12.7026-7033.2003, 1:CAS:528:DC%2BD3sXksFGhs7Y%3D
Author information
Authors and Affiliations
Corresponding authors
Additional information
This article is published with open access at Springerlink.com
Rights and permissions
Open Access This is an open access article distributed under the terms of the Creative Commons Attribution Noncommercial License (https://creativecommons.org/licenses/by-nc/2.0), which permits any noncommercial use, distribution, and reproduction in any medium, provided the original author(s) and source are credited.
About this article
Cite this article
Wu, J., Wang, C., Du, Z. et al. Identification of Pns12 as the second silencing suppressor of Rice gall dwarf virus. Sci. China Life Sci. 54, 201–208 (2011). https://doi.org/10.1007/s11427-011-4142-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11427-011-4142-5