Chinese Bulletin of Botany ›› 2012, Vol. 47 ›› Issue (4): 395-404.doi: 10.3724/SP.J.1259.2012.00395

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The Movement Protein of Barley Yellow Dwarf Virus is a Suppressor of RNA Silencing

Yongmei Shen, Guofu Liu, Jijun Yang, Xiaohui Huo, Xuesong Cao*   

  1. School of Life Sciences, Liaocheng University, Liaocheng 252059, China
  • Received:2011-10-28 Revised:2012-03-30 Online:2012-07-26 Published:2012-07-01
  • Contact: Xuesong Cao E-mail:darlingshen@163.com

Abstract: The genome of barley yellow dwarf virus (BYDV), a member of the Luteoviridae family, contains 6 open reading frames (ORFs). We cloned the 6 ORFs into plasmid of pWEIMING101 and electroporated them into Agrobacterium tumefaciens for transient coexpression of BYDV ORFs and GFP in Nicotiana benthamiana line 16c, a transgenic GFP plant. Northern blot analysis revealed the movement protein (MP) encoded by BYDV-PAV ORF4 as a suppressor of both local and systemic GFP RNA silencing and RNA silencing triggered by double-stranded GFP RNA. The fluorescent intensity was associated with steady state levels of GFP mRNAs and its degradation product of siRNAs. The nuclear localization signal in the N terminus of the MP and amino acid 5 and 6 were the functional domain and motif, respectively, essential for inhibiting RNA silencing. Transient expression of BYDV-MP alone in infiltrated tissue resulted in cell death.

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Azevedo J, Garcia D, Pontier D, Ohnesorge S, Yu A, Garcia S, Braun L, Bergdoll M, Hakimi MA, Lagrange T (2010). Argonaute quenching and global changes in Dicer homeostasis caused by a pathogen-encoded GW repeat protein. Genes & Dev 24, 904-915.
Baulcombe D (2004). RNA silencing in plants. Nature 431, 356–363.
Baumberger N, Tsai CH, Lie M, Havecker E, Baulcombe D (2007). The polerovirus silencing suppressor P0 targets ARGONAUTE proteins for degradation. Curr Biol 17, 1609–1614.
Bernstein E, Caudy AA, Hammond SM, Hannon GJ (2001). Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409, 363–366.
Bortolamiol D, Pazhouhandeh M, Marocco K, Genschick P, Ziegler-Graff V (2007). The polerovirus F Box protein P0 target ARGONAUTE1 to suppress RNA silencing. Curr Biol 17, 1615–1621.
Brigneti G, Voinnet O, Li WX, Ji LH, Ding SW, Baulcombe DC (1988). Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana. EMBO J 17, 6739-6746.
Cao XS, Zhou P, Zhang XM, Zhu SF, Zhong XH, Xiao Q, Ding B, Li Y (2005) . Identification of an RNA silencing suppressor from a plant double-stranded RNA virus. Journal of Virololgy 79(20), 13018-13027.
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.
Chay CA, Gunasinge UB, Dinesh-Kumar SP (1996). Aphid transmission and systemic plant infection determinants of Barley Yellow Dwarf Luteovirus-PAV are contained in the coat protein readthrough domain and 17-kDa protein, respectively. Virology 219, 57-65.
Cui Xiaofeng, Li Guixin, Wang Daowen, Hu Dongwei, Zhou Xueping (2005). A Begomovirus DNA -Encoded Protein Binds DNA, Functions as a Suppressor of RNA Silencing, and Targets the Cell Nucleus. Virololgy, 79(16), 10764–10775.
Ding SW, Voinnet O (2007). Antiviral Immunity Directed by Small RNAs. Cell 130, 413–426.
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.
Dunover P, Schott G, Himber C, Meyer D, Takeda A, Carrington JC, Voinnet O (2010). Small RNA duplexes funcition as mobile silencing signals between plant cells. Science 328, 912-915.
Fire A et al. (1998). Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391, 806–811.
Ghazala W, Waltermann A, Pilot R, Winter S, Varrelmann M (2008). Functional characterization and subcellular localization of the 16K cysteine-rich suppressor of gene silencing protein of tobacco rattle virus. General Virology 89, 1748–1758.
Hamilton A, Voinnet O, Chappell L, Baulcombe D (2002). Two classes of short interfering RNA in RNA silencing. EMBO J 21, 4671–4679.
Hammond SM, Bernstein E, Beach D, Hannon GJ (2000). An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cell extracts. Nature 404, 293–296.
Himber C, Dunoyer P, Moissiard G, Ritzenthaler C, Voinnet O (2003). Transitivity-dependent and -independent cell-to-cell movement of RNA silencing. EMBO J 22, 4523–4533.
Hull R (2001). Matthews’Plant Virology, 4th edn. San Diego: Academic Press.
Kasschau KD, Carrington JC(1998). A counterdefensive strategy of plant viruses. cell 95, 461-470.
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, 205–21.
Lakatos L, Csorba T, Pantaleo V, Chapman EJ, Carrington JC, Liu YP (2006). Small RNA binding is a common strategy to suppress RNA silencing by several viral suppressors. EMBO J 25, 2768–80.
Li WX, Ding SW (2001). Viral suppressors of RNA silencing. Curr.Opinion Biotech 12, 150–154.
Liu H, Reavy B, Swanson M, MacFarlane SA (2002). Functional replacement of the tobacco rattle virus cysteine-rich rotein by pathogenicity proteins from unrelated plant viruses.Virology 298, 232-239.
Liu Y, Sun B, Wang XF, Zheng ChL, Zhou GH (2007). Three digoxigenin-labeled cDNA probes for speci?c detection of the natural population of Barley yellow dwarf viruses in China by dot-blot hybridization. Journal of Virological Methods 145, 22–29.
Llave C, Kasschau KD, Carrington JC (2000). Proc Natl Acad Sci USA 97, 13401-13406.
Mayo MA, Ziegler-Graff V (1996). Molecular biology of Luteoviruses. Advances in Virus Reaserch 46, 413-460.
Martín-Hernández A, Baulcombe DC. (2008). Tobacco Rattle Virus 16-Kilodalton Protein Encodes a Suppressor of RNA Silencing That Allows Transient Viral Entry in Meristems. Journal of virology 82 (8), 4064–4071.
Meister G, Landthaler M, Patkaniowska A, Dorsett Y, Teng G, Tuschl T (2004). Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol Cell 15, 185–197.
Miller AW and Rasochová L (1997). Barley yellow dwarf viruses. Annu. Rev. Phytopathol 35, 167–90.
Miller WA, Liu S, Beckett R (2002). Barley yellow dwarf virus:Luteoviridae or Tombusviridae? Mol Plant Pathol 3, 177–183.
Molnar A, Melnyk CW, Bassett A, Hardcastle TJ, Dunn R, Baulcombe DC (2010). Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science 328, 872-875.
Nass PH, Domier LL, Jacstys BP (1998). In situ localization of barley yellow dwarf virus-PAV 17-kDa protein and nucleic acids in oats. Phytopathology 88, 1031-1039.
Palauqui JC, Vaucheret H (1998). Transgenes are dispensible for the RNA degradation step of co-suppression. Proc Natl Acad Sci USA 95, 9675–9680.
Pazhouhandeh M, Dieterle M, Marrocco K, Lechner E, Berry B, Brault V, Hemmer O, Kretsch T, Richards KE, Genschik P, Ziegler-Graff V (2006). F-box-like domainin the polerovirus protein P0 is required for silencing suppressor function. Proc Natl Acad Sci USA 103, 1994–1999.
Scholthof HB (2001). Molecular plant–microbe interactions that cut the mustard. Plant Physiol 127, 1476–83.
Silhavy D, Molnar A, Lucioli A, Szittya G, Hornyik C, Tavazza M, Burgyan J (2002). A viral protein suppresses RNA silencing and binds silencing-generated, 21- to 25-nucleotide double-stranded RNAs. EMBO J 21, 3070–3080.
Tolia NH, Joshua-Tor L (2007). Slicer and the argonautes. Nat Chem Biol 3, 36-43.
Vargason JM, Szittya G, Burgyan J, Tanaka Hall TM (2003). Size selective recognition of siRNA by an RNA silencing suppressor. Cell 115, 799–811.
Voinnet O (2005). Induction and suppression of RNA silencing:insights from viral infections. Nat Rev Genet 6, 206-220.
Voinnet O, Lederer C, Baulcombe DC (2000). A viral movement protein prevents spread of the gene silencing signal in Nicotiana benthamiana. Cell 103, 157-167.
Voinnet O, Pinto VM, Baulcombe DC (1999). Suppression of gene silencing. Proc Natl Acad Sci USA 96, 14147-14152.
Voinnet O, Vain P, Angell S, Baulcombe DC (1998). Systemic spread of sequence-specific transgene RNA degradation in plants is initiated by localized introduction of ectopic promoterless DNA. Cell 95, 177-187.
Xia ZL, Wang Y, Du ZhQ, Li JM, Richard Y.Zhao, Wang DW (2008). Apotential nuclear envelope-targeting domain and an arginine-rich RNA binding element identified in the putative movement protein of the GAV strain of Barley yellow dwarf virus. Functional Plant Biology 35(1), 40-50.
Xiong RY, Wu JX, Zhou YJ, Zhou XP (2009). Characterization and subcellular localization of an RNA silencing suppressor encoded by Rice stripe tenuivirus. Virology 387, 29–40.
Zamore PD, Tuschl T, Sharp PA, Bartel DP (2000). RNAi: Double-stranded RNA directs the ATP-dependent cleavage of mRNA at 21 to 23 nucleotide intervals. Cell 101, 25–33.
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