Satellite RNA reduces expression of the 2b suppressor protein resulting in the attenuation of symptoms caused by Cucumber mosaic virus infection

Molecular Plant Pathology

Volumn 12, Issue 6, 2011, Pages 595-605

  Hou, Wei Na ^a,b   Duan, Cheng Guo ^a   Fang, Rong Xiang ^a   Zhou, Xiao Yang ^b   Guo, Hui Shan ^a  

^a INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^b BEIJING FORESTRY UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

2B PROTEIN, CUCUMBER MOSAIC VIRUS; COMPLEMENTARY DNA; SATELLITE RNA; SMALL INTERFERING RNA; VIRUS PROTEIN;

ARABIDOPSIS; ARTICLE; GENETICS; METABOLISM; MOSAIC VIRUS; PATHOGENICITY; PHYSIOLOGY; PLANT DISEASE; RHIZOBIUM; SUPPRESSOR GENE; TOBACCO; VIROLOGY; VIRUS GENOME;

AGROBACTERIUM; ARABIDOPSIS; CUCUMOVIRUS; DNA, COMPLEMENTARY; GENES, SUPPRESSOR; GENOME, VIRAL; PLANT DISEASES; RNA, SATELLITE; RNA, SMALL INTERFERING; TOBACCO; VIRAL PROTEINS;

ARABIDOPSIS; CUCUMBER MOSAIC VIRUS; CYTOMEGALOVIRUS; NICOTIANA BENTHAMIANA;

EID: 79959937256     PISSN: 14646722     EISSN: 13643703     Source Type: Journal    
DOI: 10.1111/j.1364-3703.2010.00696.x     Document Type: Article

References (42)

1. Baulcombe, D.C. (2007) Molecular biology. Amplified silencing. Science, 315, 199-200.
2. Brigneti, G., Voinnet, O., Li, W.X., Ji, L.H., Ding, S.W. and Baulcombe, D.C. (1998) Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana. EMBO J. 17, 6739-6746.
3. Dalmay, T., Hamilton, A., Rudd, S., Angell, S. and Baulcombe, D.C. (2000) An RNA-dependent RNA polymerase gene in Arabidopsis is required for posttranscriptional gene silencing mediated by a transgene but not by a virus. Cell, 101, 543-553.
4. Devic, M., Jaegle, M. and Baulcombe, D. (1989) Symptom production on tobacco and tomato is determined by two distinct domains of the satellite RNA of cucumber mosaic virus (strain Y). J. Gen. Virol. 70 (Pt 10), 2765-2774.
5. Diaz-Pendon, J.A., Li, F., Li, W.X. and Ding, S.W. (2007) Suppression of antiviral silencing by cucumber mosaic virus 2b protein in Arabidopsis is associated with drastically reduced accumulation of three classes of viral small interfering RNAs. Plant Cell, 19, 2053-2063.
6. Ding, B., Li, Q., Nguyen, L., Palukaitis, P. and Lucas, W.J. (1995) Cucumber mosaic virus 3a protein potentiates cell-to-cell trafficking of CMV RNA in tobacco plants. Virology, 207, 345-353.
7. Ding, S.W., Anderson, B.J., Haase, H.R. and Symons, R.H. (1994) New overlapping gene encoded by the cucumber mosaic virus genome. Virology, 198, 593-601.
8. Ding, S.W., Li, W.X. and Symons, R.H. (1995) A novel naturally occurring hybrid gene encoded by a plant RNA virus facilitates long distance virus movement. EMBO J. 14, 5762-5772.
9. Du, Q.S., Duan, C.G., Zhang, Z.H., Fang, Y.Y., Fang, R.X., Xie, Q. and Guo, H.S. (2007) DCL4 targets Cucumber mosaic virus satellite RNA at novel secondary structures. J. Virol. 81, 9142-9151.
10. Garcia-Arenal, F., Escriu, F., Aranda, M.A., Alonso-Prados, J.L., Malpica, J.M. and Fraile, A. (2000) Molecular epidemiology of Cucumber mosaic virus and its satellite RNA. Virus Res. 71, 1-8.
11. Gonzalez, I., Martinez, L., Rakitina, D.V., Lewsey, M.G., Atencio, F.A., Llave, C., Kalidina, N.O., Carr, J.P., Palukaitis, P. and Canto, T. (2010) Cucumber mosaic virus 2b protein subcellular targets and interactions: their significance to RNA silencing suppressor activity. Mol. Plant-Microbe Interact. 23, 294-303.
12. Guo, H.S. and Ding, S.W. (2002) A viral protein inhibits the long range signaling activity of the gene silencing signal. EMBO J. 21, 398-407.
13. Hajimorad, M.R., Ghabrial, S.A. and Roossinck, M.J. (2009) De novo emergence of a novel satellite RNA of cucumber mosaic virus following serial passages of the virus derived from RNA transcripts. Arch. Virol. 154, 137-140.
14. Harrison, B.D., Mayo, M.A. and Baulcombe, D.C. (1987) Virus resistance in transgenic plants that express cucumber mosaic virus satellite RNA. Nature, 328, 799-802.
15. Hayes, R.J. and Buck, K.W. (1990) Complete replication of a eukaryotic virus RNA in vitro by a purified RNA-dependent RNA polymerase. Cell, 63, 363-368.
16. Hidaka, S. and Hanada, K. (1994) Structural features unique to a new 405-nucleotide satellite RNA of cucumber mosaic virus inducing tomato necrosis. Virology, 200, 806-808.
17. Jaegle, M., Devic, M., Longstaff, M. and Baulcombe, D. (1990) Cucumber mosaic virus satellite RNA (Y strain): analysis of sequences which affect yellow mosaic symptoms on tobacco. J. Gen. Virol. 71 (Pt 9), 1905-1912.
18. Ji, L.H. and Ding, S.W. (2001) The suppressor of transgene RNA silencing encoded by Cucumber mosaic virus interferes with salicylic acid-mediated virus resistance. Mol. Plant-Microbe Interact. 14, 715-724.
19. Kaper, J.M. (1995) Role of satellites in viral pathogenesis: nested parasitic nucleic acids competing for expression. Viruses Viroids, III, 373-392.
20. Kuwata, S., Masuta, C. and Takanami, Y. (1991) Reciprocal phenotype alterations between two satellite RNAs of cucumber mosaic virus. J. Gen. Virol. 72 (Pt 10), 2385-2389.
21. Lewsey, M., Robertson, F.C., Canto, T., Palukaitis, P. and Carr, J.P. (2007) Selective targeting of miRNA-regulated plant development by a viral counter-silencing protein. Plant J. 50, 240-252.
22. Li, H.W., Lucy, A.P., Guo, H.S., Li, W.X., Ji, L.H., Wong, S.M. and Ding, S.W. (1999) Strong host resistance targeted against a viral suppressor of the plant gene silencing defence mechanism. EMBO J. 18, 2683-2691.
23. Lucy, A.P., Guo, H.S., Li, W.X. and Ding, S.W. (2000) Suppression of post-transcriptional gene silencing by a plant viral protein localized in the nucleus. EMBO J. 19, 1672-1680.
24. Masuta, C. and Takanami, Y. (1989) Determination of sequence and structural requirements for pathogenicity of a cucumber mosaic virus satellite RNA (Y-satRNA). Plant Cell, 1, 1165-1173.
25. Mlotshwa, S., Voinnet, O., Mette, M.F., Matzke, M., Vaucheret, H., Ding, S.W., Pruss, G. and Vance, V.B. (2002) RNA silencing and the mobile silencing signal. Plant Cell, 14 (Suppl), S289-S301.
26. Mourrain, P., Beclin, C., Elmayan, T., Feuerbach, F., Godon, C., Morel, J.B., Jouette, D., Lacombe, A., Nikic, S., Picault, N., Remoue, K., Sanial, M., Vo, T. and Vaucheret, H. (2000) Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell, 101, 533-542.
27. Palukaitis, P. (1988) Pathogenicity regulation by satellite RNAs of cucumber mosaic virus: minor nucleotide sequence changes alter host responses. Mol. Plant-Microbe Interact. 1, 175-181.
28. Palukaitis, P. and Garcia-Arenal, F. (2003) Cucumoviruses. Adv. Virus Res. 62, 241-323.
29. Parizotto, E.A., Dunoyer, P., Rahm, N., Himber, C. and Voinnet, O. (2004) In vivo investigation of the transcription, processing, endonucleolytic activity, and functional relevance of the spatial distribution of a plant miRNA. Genes Dev. 18, 2237-2242.
30. Roossinck, M.J., Sleat, D. and Palukaitis, P. (1992) Satellite RNAs of plant viruses: structures and biological effects. Microbiol. Rev. 56, 265-279.
31. Schwach, F., Vaistij, F.E., Jones, L. and Baulcombe, D.C. (2005) An RNA-dependent RNA polymerase prevents meristem invasion by potato virus X and is required for the activity but not the production of a systemic silencing signal. Plant Physiol. 138, 1842-1852.
32. Schwinghamer, M.W. and Symons, R.H. (1975) Fractionation of cucumber mosaic virus RNA and its translation in a wheat embryo cell-free system. Virology, 63, 252-262.
33. Shi, B.J., Palukaitis, P. and Symons, R.H. (2002) Differential virulence by strains of Cucumber mosaic virus is mediated by the 2b gene. Mol. Plant-Microbe Interact. 15, 947-955.
34. Sleat, D.E. and Palukaitis, P. (1990) Site-directed mutagenesis of a plant viral satellite RNA changes its phenotype from ameliorative to necrogenic. Proc. Natl. Acad. Sci. USA, 87, 2946-2950.
35. Soards, A.J., Murphy, A.M., Palukaitis, P. and Carr, J.P. (2002) Virulence and differential local and systemic spread of cucumber mosaic virus in tobacco are affected by the CMV 2b protein. Mol. Plant-Microbe Interact. 15, 647-653.
36. Vaistij, F.E., Jones, L. and Baulcombe, D.C. (2002) Spreading of RNA targeting and DNA methylation in RNA silencing requires transcription of the target gene and a putative RNA-dependent RNA polymerase. Plant Cell, 14, 857-867.
37. Vance, V. and Vaucheret, H. (2001) RNA silencing in plants-defense and counterdefense. Science, 292, 2277-2280.
38. Wang, X.B., Wu, Q., Ito, T., Cillo, F., Li, W.X., Chen, X., Yu, J.L. and Ding, S.W. (2010) RNAi-mediated viral immunity requires amplification of virus-derived siRNAs in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA, 107, 484-489.
39. Waterworth, H.E., Kaper, J.M. and Tousignant, M.E. (1979) CARNA 5, the small cucumber mosaic virus-dependent replicating RNA, regulates disease expression. Science, 204, 845-847.
40. Yang, S.J., Carter, S.A., Cole, A.B., Cheng, N.H. and Nelson, R.S. (2004) A natural variant of a host RNA-dependent RNA polymerase is associated with increased susceptibility to viruses by Nicotiana benthamiana. Proc. Natl. Acad. Sci. USA, 101, 6297-6302.
41. Ying, X.B., Dong, L., Zhu, H., Duan, C.G., Du, Q.S., Lv, D.Q., Fang, Y.Y., Garcia, J.A., Fang, R.X. and Guo, H.S. (2010) RNA-dependent RNA polymerase 1 from Nicotiana tabacum suppresses RNA silencing and enhances viral infection in Nicotiana benthamiana. Plant Cell, 22, 1358-1372.
42. Zhang, X., Yuan, Y.R., Pei, Y., Lin, S.S., Tuschl, T., Patel, D.J. and Chua, N.H. (2006) Cucumber mosaic virus-encoded 2b suppressor inhibits Arabidopsis Argonaute1 cleavage activity to counter plant defense. Genes Dev. 20, 3255-3268.