Cucumber mosaic virus suppressor 2b binds to AGO4-related small RNAs and impairs AGO4 activities

Plant Journal

Volumn 69, Issue 1, 2012, Pages 104-115

  Hamera, Sadia ^a,b,c   Song, Xiaoguang ^a,b,c   Su, Lei ^a,b   Chen, Xiaoying ^a,b   Fang, Rongxiang ^a,b  

^a INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^b National Plant Gene Research Center   (China)

^c UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

AGO4; cucumber mosaic virus (CMV); repeat associated siRNA; RNA directed DNA methylation (RdDM); small RNA binding; viral suppressor of RNA silencing

Indexed keywords

AGO4; CUCUMBER MOSAIC VIRUS; REPEAT-ASSOCIATED SIRNA; RNA-DIRECTED DNA METHYLATION (RDDM); SMALL RNA; VIRAL SUPPRESSOR OF RNA SILENCING;

ALKYLATION; METHYLATION; VIRUSES;

RNA;

ADENOSINE; AGO4 PROTEIN, ARABIDOPSIS; ARABIDOPSIS PROTEIN; ARGONAUTE PROTEIN; MICRORNA; SMALL INTERFERING RNA; VIRUS PROTEIN;

ARABIDOPSIS; ARTICLE; DNA METHYLATION; GENETICS; HOST PATHOGEN INTERACTION; METABOLISM; MOSAIC VIRUS; NUCLEOTIDE REPEAT; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; TRANSGENIC PLANT; VIROLOGY;

ADENOSINE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; ARGONAUTE PROTEINS; CUCUMOVIRUS; DNA METHYLATION; HOST-PATHOGEN INTERACTIONS; MICRORNAS; PLANTS, GENETICALLY MODIFIED; PROTEIN STRUCTURE, TERTIARY; REPETITIVE SEQUENCES, NUCLEIC ACID; RNA, SMALL INTERFERING; VIRAL PROTEINS;

ARABIDOPSIS; CUCUMBER MOSAIC VIRUS;

EID: 84355162862     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2011.04774.x     Document Type: Article

References (40)

1. Agorio, A., and, Vera, P., (2007) ARGONAUTE4 is required for resistance to Pseudomonas syringae in Arabidopsis. Plant Cell, 19, 3778-3790.
2. Bhattacharjee, S., Zamora, A., Azhar, M.T., Sacco, M.A., Lambert, L.H., and, Moffett, P., (2009) Virus resistance induced by NB-LRR proteins involves Argonaute4-dependent translational control. Plant J. 58, 940-951.
3. Buchmann, R.C., Asad, S., Wolf, J.N., Mohannath, G., and, Bisaro, D.M., (2009) Geminivirus AL2 and L2 proteins suppress transcriptional gene silencing and cause genome-wide reductions in cytosine methylation. J. Virol. 83, 5005-5013.
4. Calabrese, J.M., and, Sharp, P.A., (2006) Characterization of the short RNAs bound by the P19 suppressor of RNA silencing in mouse embryonic stem cells. RNA 12, 2092-2102. (Pubitemid 44865957)
5. Chan, S.W., Zilberman, D., Xie, Z., Johansen, L.K., Carrington, J.C., and, Jacobsen, S.E., (2004) RNA silencing genes control de novo DNA methylation. Science, 303, 1336. (Pubitemid 38269419)
6. Chen, H.Y., Yang, J., Lin, C., and, Yuan, Y.A., (2008) Structural basis for RNA-silencing suppression by Tomato aspermy virus protein 2b. EMBO Rep. 9, 754-760.
7. Chinnusamy, V., and, Zhu, J.K., (2009) RNA-directed DNA methylation and demethylation in plants. Sci. China C. Life Sci. 52, 331-343.
8. Clough, S.J., and, Bent, A.F., (1998) Floral dip: a simplified method for Agrobacterium mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
9. 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.
10. El-Shami, M., Pontier, D., Lahmy, S., Braun, L., Picart, C., Vega, D., Hakimi, M.A., Jacobsen, S.E., Cooke, R., and, Lagrange, T., (2007) Reiterated WG/GW motifs form functionally and evolutionarily conserved ARGONAUTE-binding platforms in RNAi-related components. Genes Dev. 21, 2539-2544. (Pubitemid 47607665)
11. Gonzalez, I., Martinez, L., Rakitina, D.V., Lewsey, M.G., Atencio, F.A., Llave, C., Kalinina, 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. Goto, K., Kobori, T., Kosaka, Y., Natsuaki, T., and, Masuta, C., (2007) Characterization of silencing suppressor 2b of cucumber mosaic virus based on examination of its small RNA-binding abilities. Plant Cell Physiol. 48, 1050-1060. (Pubitemid 47216635)
13. 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.
14. Havecker, E.R., Wallbridge, L.M., Hardcastle, T.J., Bush, M.S., Kelly, K.A., Dunn, R.M., Schwach, F., Doonan, J.H., and, Baulcombe, D.C., (2010) The Arabidopsis RNA-directed DNA methylation argonautes functionally diverge based on their expression and interaction with target loci. Plant Cell, 22, 321-334.
15. Hu, C.D., Chinenov, Y., and, Kerppola, T.K., (2002) Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation. Mol. Cell 9, 789-798. (Pubitemid 34454889)
16. Jacobsen, S.E., and, Meyerowitz, E.M., (1997) Hypermethylated SUPERMAN epigenetic alleles in arabidopsis. Science, 277, 1100-1103. (Pubitemid 27371632)
17. Lakatos, L., Szittya, G., Silhavy, D., and, Burgyan, J., (2004) Molecular mechanism of RNA silencing suppression mediated by p19 protein of tombusviruses. EMBO J. 23, 876-884. (Pubitemid 38418754)
18. Lakatos, L., Csorba, T., Pantaleo, V., Chapman, E.J., Carrington, J.C., Liu, Y.P., Dolja, V.V., Calvino, L.F., Lopez-Moya, J.J., and, Burgyan, J., (2006) Small RNA binding is a common strategy to suppress RNA silencing by several viral suppressors. EMBO J. 25, 2768-2780. (Pubitemid 43980384)
19. 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. (Pubitemid 46624133)
20. Li, C.F., Pontes, O., El-Shami, M., Henderson, I.R., Bernatavichute, Y.V., Chan, S.W., Lagrange, T., Pikaard, C.S., and, Jacobsen, S.E., (2006) An ARGONAUTE4-containing nuclear processing center colocalized with Cajal bodies in Arabidopsis thaliana. Cell, 126, 93-106.
21. 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. (Pubitemid 30182173)
22. Merai, Z., Kerenyi, Z., Kertesz, S., Magna, M., Lakatos, L., and, Silhavy, D., (2006) Double-stranded RNA binding may be a general plant RNA viral strategy to suppress RNA silencing. J. Virol. 80, 5747-5756. (Pubitemid 43849153)
23. Mi, S., Cai, T., Hu, Y., et al. (2008) Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5′ terminal nucleotide. Cell, 133, 116-127.
24. Molnar, A., Melnyk, C., and, Baulcombe, D.C., (2011) Silencing signals in plants: a long journey for small RNAs. Genome Biol. 12, 215.
25. Mourrain, P., Beclin, C., Elmayan, T., et al. (2000) Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell, 101, 533-542.
26. Qi, Y., Denli, A.M., and, Hannon, G.J., (2005) Biochemical specialization within Arabidopsis RNA silencing pathways. Mol. Cell 19, 421-428. (Pubitemid 41074895)
27. Qi, Y., He, X., Wang, X.J., Kohany, O., Jurka, J., and, Hannon, G.J., (2006) Distinct catalytic and non-catalytic roles of ARGONAUTE4 in RNA-directed DNA methylation. Nature, 443, 1008-1012. (Pubitemid 44646179)
28. Qu, J., Ye, J., and, Fang, R., (2007) Artificial microRNA-mediated virus resistance in plants. J. Virol. 81, 6690-6699. (Pubitemid 46878073)
29. Rogers, S.O., and, Bendich, A.J., (1985) Extraction of DNA from milligram amounts of fresh, herbarium and mummified plant tissues. Plant Mol. Biol. 5, 69-76.
30. 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. (Pubitemid 35180978)
31. Vargason, J.M., Szittya, G., Burgyan, J., and, Hall, T.M., (2003) Size selective recognition of siRNA by an RNA silencing suppressor. Cell, 115, 799-811. (Pubitemid 38058493)
32. Waadt, R., Schmidt, L.K., Lohse, M., Hashimoto, K., Bock, R., and, Kudla, J., (2008) Multicolor bimolecular fluorescence complementation reveals simultaneous formation of alternative CBL/CIPK complexes in planta. Plant J. 56, 505-516.
33. Wu, Q., Wang, X., and, Ding, S.W., (2010) Viral suppressors of RNA-based viral immunity: host targets. Cell Host Microbe, 8, 12-15.
34. Xie, Z., Johansen, L.K., Gustafson, A.M., Kasschau, K.D., Lellis, A.D., Zilberman, D., Jacobsen, S.E., and, Carrington, J.C., (2004) Genetic and functional diversification of small RNA pathways in plants. PLoS Biol. 2, E104.
35. Ye, K., and, Patel, D.J., (2005) RNA silencing suppressor p21 of Beet yellows virus forms an RNA binding octameric ring structure. Structure, 13, 1375-1384. (Pubitemid 41262104)
36. Ye, J., Qu, J., Zhang, J.F., Geng, Y.F., and, Fang, R.X., (2009) A critical domain of the Cucumber mosaic virus 2b protein for RNA silencing suppressor activity. FEBS Lett. 583, 101-106.
37. 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. (Pubitemid 44904848)
38. Zheng, B., Wang, Z., Li, S., Yu, B., Liu, J.Y., and, Chen, X., (2009) Intergenic transcription by RNA polymerase II coordinates Pol IV and Pol V in siRNA-directed transcriptional gene silencing in Arabidopsis. Genes Dev. 23, 2850-2860.
39. Zilberman, D., Cao, X., and, Jacobsen, S.E., (2003) ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science, 299, 716-719. (Pubitemid 36159488)
40. Zuker, M., (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31, 3406-3415. (Pubitemid 37442169)