Skip to main content

Advertisement

Log in

RNA silencing suppressor Pns11 of rice gall dwarf virus induces virus-like symptoms in transgenic rice

  • Original Article
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

Transgenic rice (Oryza sativa) plants expressing the Pns11 protein of rice gall dwarf virus (RGDV) displayed multiple abnormal phenotypes, some of which were highly reminiscent of the symptoms observed in RGDV-infected rice. Further analysis indicated that the apparent alterations in plant growth and morphology were correlated with the expression levels of microRNA160, microRNA162, microRNA167, microRNA168, and the microRNA target OsARF8. Especially, the striking dwarfing phenotype depended on the high expression level of microRNA167. By analogy to other categories of plant viruses, the RNA silencing suppressors encoded by plant dsRNA viruses function as pathogenicity determinants. These findings significantly deepen our current mechanistic understanding of the RNA silencing suppressor (VSR) encoded by a dsRNA virus and provide additional evidence that interference with microRNA expression is a VSR function utilized by a diverse range of viruses.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Boccardo G, Milne RG, Disthaporn S, Chettanachit D, Putta M (1985) Morphology and nucleic acid of rice gall dwarf virus. Intervirology 23:167–171

    Article  PubMed  CAS  Google Scholar 

  2. Bonnet E, Wuyts J, Rouze P, Van de Peer Y (2004) Detection of 91 potential conserved plant microRNAs in Arabidopsis thaliana and Oryza sativa identifies important target genes. Proc Natl Acad Sci USA 101:11511–11516

    Article  PubMed  CAS  Google Scholar 

  3. Burgyan J, Havelda Z (2011) Viral suppressors of RNA silencing. Trends Plant Sci 16:265–272

    Article  PubMed  CAS  Google Scholar 

  4. Cao X, Zhou P, Zhang X, Zhu S, Zhong X, Xiao Q, Ding B, Li Y (2005) Identification of an RNA silencing suppressor from a plant double-stranded RNA virus. J Virol 79:13018–13027

    Article  PubMed  CAS  Google Scholar 

  5. Carthew RW, Sontheimer EJ (2009) Origins and mechanisms of miRNAs and siRNAs. Cell 136:642–655

    Article  PubMed  CAS  Google Scholar 

  6. Chapman EJ, Prokhnevsky AI, Gopinath K, Dolja VV, Carrington JC (2004) Viral RNA silencing suppressors inhibit the microRNA pathway at an intermediate step. Genes Dev 18:1179–1186

    Article  PubMed  CAS  Google Scholar 

  7. Cui X, Tao X, Xie Y, Fauquet CM, Zhou X (2004) A DNAbeta associated with tomato yellow leaf curl China virus is required for symptom induction. J Virol 78:13966–13974

    Article  PubMed  CAS  Google Scholar 

  8. Cui X, Li G, Wang D, Hu D, Zhou X (2005) A Begomovirus DNAbeta-encoded protein binds DNA, functions as a suppressor of RNA silencing, and targets the cell nucleus. J Virol 79:10764–10775

    Article  PubMed  CAS  Google Scholar 

  9. Ding SW, Voinnet O (2007) Antiviral immunity directed by small RNAs. Cell 130:413–426

    Article  PubMed  CAS  Google Scholar 

  10. Dunoyer P, Lecellier CH, Parizotto EA, Himber C, Voinnet O (2004) Probing the microRNA and small interfering RNA pathways with virus-encoded suppressors of RNA silencing. Plant Cell 16:1235–1250

    Article  PubMed  CAS  Google Scholar 

  11. Fan HZ, Zhang SG, He XZ, Xie SD, Liu CZ, Zhou LG, Zhu D, Liu XR (1983) Rice gall dwarf - A new virus disease epidemic in the west of Guangdong province of South China. Acta Phytopathologica Sinica 4:1–6

    Google Scholar 

  12. Fujioka T, Kaneko F, Kazama T, Suwabe K, Suzuki G, Makino A, Mae T, Endo M, Kawagishi-Kobayashi M, Watanabe M (2008) Identification of small RNAs in late developmental stage of rice anthers. Genes Genet Syst 83:281–284

    Article  PubMed  CAS  Google Scholar 

  13. Hiei Y, Ohta S, Komari T, Kumashiro T (1994) Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J 6:271–282

    Article  PubMed  CAS  Google Scholar 

  14. Jameson PE, Clarke SF (2002) Hormone-virus interactions in plants. Crit Rev Plant Sci 21:205–228

    Article  CAS  Google Scholar 

  15. Jay F, Wang Y, Yu A, Taconnat L, Pelletier S, Colot V, Renou JP, Voinnet O (2011) Misregulation of auxin response factor 8 underlies the developmental abnormalities caused by three distinct viral silencing suppressors in Arabidopsis. PLoS Pathog 7:e1002035

    Article  PubMed  CAS  Google Scholar 

  16. Jover-Gil S, Candela H, Ponce MR (2005) Plant microRNAs and development. Int J Dev Biol 49:733–744

    Article  PubMed  CAS  Google Scholar 

  17. Kalmykova AI, Klenov MS, Gvozdev VA (2005) Argonaute protein PIWI controls mobilization of retrotransposons in the Drosophila male germline. Nucleic Acids Res 33:2052–2059

    Article  PubMed  CAS  Google Scholar 

  18. Kasschau KD, Xie Z, Allen E, Llave C, Chapman EJ, Krizan KA, Carrington JC (2003) P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA function. Dev Cell 4:205–217

    Article  PubMed  CAS  Google Scholar 

  19. Kurihara Y, Takashi Y, Watanabe Y (2006) The interaction between DCL1 and HYL1 is important for efficient and precise processing of pri-miRNA in plant microRNA biogenesis. RNA 12:206–212

    Article  PubMed  CAS  Google Scholar 

  20. Li F, Ding SW (2006) Virus counterdefense: diverse strategies for evading the RNA-silencing immunity. Annu Rev Microbiol 60:503–531

    Article  PubMed  CAS  Google Scholar 

  21. Liu B, Li P, Li X, Liu C, Cao S, Chu C, Cao X (2005) Loss of function of OsDCL1 affects microRNA accumulation and causes developmental defects in rice. Plant Physiol 139:296–305

    Article  PubMed  CAS  Google Scholar 

  22. Liu FX, Zhao Q, Ruan XL, He YW, Li HP (2008) Suppressor of RNA silencing encoded by rice gall dwarf virus genome segment 11. Chinese Sci Bull 3:362–369

    Article  Google Scholar 

  23. Liu PP, Montgomery TA, Fahlgren N, Kasschau KD, Nonogaki H, Carrington JC (2007) Repression of auxin response factor 10 by microRNA160 is critical for seed germination and post-germination stages. Plant J 52:133–146

    Article  PubMed  CAS  Google Scholar 

  24. Liu Q, Feng Y, Zhu Z (2009) Dicer-like (DCL) proteins in plants. Funct Integr Genomics 9:277–286

    Article  PubMed  CAS  Google Scholar 

  25. Lu YH, Zhang JF, Xiong RY, Xu QF, Zhou YJ (2011) Identification of an RNA silencing suppressor encoded by southern rice black-streaked dwarf virus S6. Scientia Agricultura Sinica 14:2909–2917

    Google Scholar 

  26. Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325

    Article  PubMed  CAS  Google Scholar 

  27. Omura T, Yan J, Zhong B, Wada M, Zhu Y, Tomaru M, Maruyama W, Kikuchi A, Watanabe Y, Kimura I, Hibino H (1998) The P2 protein of rice dwarf phytoreovirus is required for adsorption of the virus to cells of the insect vector. J Virol 72:9370–9373

    PubMed  CAS  Google Scholar 

  28. Omura T, Yan J (1999) Role of outer capsid proteins in transmission of Phytoreovirus by insect vectors. Adv Virus Res 54:15–43

    Article  PubMed  CAS  Google Scholar 

  29. Palatnik JF, Allen E, Wu X, Schommer C, Schwab R, Carrington JC, Weigel D (2003) Control of leaf morphogenesis by microRNAs. Nature 425:257–263

    Article  PubMed  CAS  Google Scholar 

  30. Park W, Li J, Song R, Messing J, Chen X (2002) Carpel factory, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr Biol 12:1484–1495

    Article  PubMed  CAS  Google Scholar 

  31. Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP (2002) MicroRNAs in plants. Genes Dev 16:1616–1626

    Article  PubMed  CAS  Google Scholar 

  32. Ren B, Guo Y, Gao F, Zhou P, Wu F, Meng Z, Wei C, Li Y (2010) Multiple functions of rice dwarf phytoreovirus Pns10 in suppressing systemic RNA silencing. J Virol 84:12914–12923

    Article  PubMed  CAS  Google Scholar 

  33. Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP (2002) Prediction of plant microRNA targets. Cell 110:513–520

    Article  PubMed  CAS  Google Scholar 

  34. Siddiqui SA, Sarmiento C, Truve E, Lehto H, Lehto K (2008) Phenotypes and functional effects caused by various viral RNA silencing suppressors in transgenic Nicotiana benthamiana and N. tabacum. Mol Plant Microbe Interact 21:178–187

    Article  PubMed  CAS  Google Scholar 

  35. Stav R, Hendelman A, Buxdorf K, Arazi T (2010) Transgenic expression of tomato bushy stunt virus silencing suppressor P19 via the pOp/LhG4 transactivation system induces viral-like symptoms in tomato. Virus Genes 40:119–129

    Article  PubMed  CAS  Google Scholar 

  36. Tomari Y, Zamore PD (2005) Perspective: machines for RNAi. Genes Dev 19:517–529

    Article  PubMed  CAS  Google Scholar 

  37. Varallyay E, Valoczi A, Agyi A, Burgyan J, Havelda Z (2010) Plant virus-mediated induction of miR168 is associated with repression of Argonaute1 accumulation. EMBO J 29:3507–3519

    Article  PubMed  CAS  Google Scholar 

  38. Voinnet O (2005) Induction and suppression of RNA silencing: insights from viral infections. Nat Rev Genet 6:206–220

    Article  PubMed  CAS  Google Scholar 

  39. Wang XB, Zhang LD, Li DW, Han CG, Yu JL (2005) Approaches of research on RNA silencing suppressors encoded by plant viruses. J China Agric Univ 4:31–38

    Google Scholar 

  40. Wei Y, Chen ZH, Chen GX, Xiong LZ, Wu CY (2011) Study of overexpressing miRNA167a to regulate the architecture in Oryza sativa. Mol Plant Breed 4:390–396

    Google Scholar 

  41. Wang WJ, Liu T, Guo L, Liu CM (2011) SLC/AGO1 coordinates cell division and expansion in Arabidopsis. Chin Bull Bot 4:370–378

    Google Scholar 

  42. Wu J, Du Z, Wang C, Cai L, Hu M, Lin Q, Wu Z, Li Y, Xie L (2010) Identification of Pns6, a putative movement protein of RRSV, as a silencing suppressor. Virol J 7:335

    Article  PubMed  Google Scholar 

  43. Wu J, Wang C, Du Z, Cai L, Hu M, Wu Z, Li Y, Xie L (2011) Identification of Pns12 as the second silencing suppressor of rice gall dwarf virus. Sci China Life Sci 54:201–208

    Article  PubMed  CAS  Google Scholar 

  44. Xiong R, Wu J, Zhou Y, Zhou X (2009) Characterization and subcellular localization of an RNA silencing suppressor encoded by rice stripe tenuivirus. Virology 387:29–40

    Article  PubMed  CAS  Google Scholar 

  45. Yang JH, Han SJ, Yoon EK, Lee WS (2006) Evidence of an auxin signal pathway, microRNA167-ARF8-GH3, and its response to exogenous auxin in cultured rice cells. Nucleic Acids Res 34:1892–1899

    Article  PubMed  CAS  Google Scholar 

  46. Zambon RA, Vakharia VN, Wu LP (2006) RNAi is an antiviral immune response against a dsRNA virus in Drosophila melanogaster. Cell Microbiol 8:880–889

    Article  PubMed  CAS  Google Scholar 

  47. Zhou P, Ren B, Zhang XM, Wang Y, Wei CH, Li Y (2010) Stable expression of rice dwarf virus Pns10 suppresses the post-transcriptional gene silencing in transgenic Nicotiana benthamiana plants. Acta Virol 54:99–104

    Article  PubMed  CAS  Google Scholar 

  48. Zhu S, Gao F, Cao X, Chen M, Ye G, Wei C, Li Y (2005) The rice dwarf virus P2 protein interacts with ent-kaurene oxidases in vivo, leading to reduced biosynthesis of gibberellins and rice dwarf symptoms. Plant Physiol 139:1935–1945

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowlegments

This study was supported in part by grants from the National Natural Science Foundation of China (Grant Nos. 30370929 and 30671358).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hua-Ping Li.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Shen, WJ., Ruan, XL., Li, XS. et al. RNA silencing suppressor Pns11 of rice gall dwarf virus induces virus-like symptoms in transgenic rice. Arch Virol 157, 1531–1539 (2012). https://doi.org/10.1007/s00705-012-1339-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-012-1339-2

Keywords

Navigation