In planta recognition of a double-stranded RNA synthesis protein complex by a potexviral RNA silencing suppressor

Plant Cell

Volumn 26, Issue 5, 2014, Pages 2168-2183

  Okano, Yukari ^a   Senshu, Hiroko ^a   Hashimoto, Masayoshi ^a   Neriya, Yutaro ^a   Netsu, Osamu ^a   Minato, Nami ^a   Yoshida, Tetsuya ^a   Maejima, Kensaku ^a   Oshima, Kenro ^a   Komatsu, Ken ^a   Yamaji, Yasuyuki ^a   Namba, Shigetou ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84903639084     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.113.120535     Document Type: Article

References (80)

1. Adenot, X., Elmayan, T., Lauressergues, D., Boutet, S., Bouché, N., Gasciolli, V., and Vaucheret, H. (2006). DRB4-dependent TAS3 trans-acting siRNAs control leaf morphology through AGO7. Curr. Biol. 16: 927-932.
2. Allen, E., and Howell, M.D. (2010). miRNAs in the biogenesis of transacting siRNAs in higher plants. Semin. Cell Dev. Biol. 21: 798-804.
3. Allen, E., Xie, Z., Gustafson, A.M., and Carrington, J.C. (2005). MicroRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121: 207-221.
4. Amari, K., Lerich, A., Schmitt-Keichinger, C., Dolja, V.V., and Ritzenthaler, C. (2011). Tubule-guided cell-to-cell movement of a plant virus requires class XI myosin motors. PLoS Pathog. 7: e1002327.
5. Azevedo, J., Garcia, D., Pontier, D., Ohnesorge, S., Yu, A., Garcia, S., Braun, L., Bergdoll, M., Hakimi, M.A., Lagrange, T., and Voinnet, O. (2010). Argonaute quenching and global changes in Dicer homeostasis caused by a pathogen-encoded GW repeat protein. Genes Dev. 24: 904-915.
6. Bartel, D.P. (2004). MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 116: 281-297.
7. Baumberger, N., and Baulcombe, D.C. (2005). Arabidopsis ARGONAUTE1 is an RNA Slicer that selectively recruits microRNAs and short interfering RNAs. Proc. Natl. Acad. Sci. USA 102: 11928-11933.
8. Baumberger, N., Tsai, C.H., Lie, M., Havecker, E., and Baulcombe, D.C. (2007). The Polerovirus silencing suppressor P0 targets ARGONAUTE proteins for degradation. Curr. Biol. 17: 1609-1614.
9. Bayne, E.H., Rakitina, D.V., Morozov, S.Y., and Baulcombe, D.C. (2005). Cell-to-cell movement of potato potexvirus X is dependent on suppression of RNA silencing. Plant J. 44: 471-482.
10. Blevins, T., Rajeswaran, R., Shivaprasad, P.V., Beknazariants, D., Si-Ammour, A., Park, H.S., Vazquez, F., Robertson, D., Meins, F., Jr., Hohn, T., and Pooggin, M.M. (2006). Four plant Dicers mediate viral small RNA biogenesis and DNA virus induced silencing. Nucleic Acids Res. 34: 6233-6246.
11. Bortolamiol, D., Pazhouhandeh, M., Marrocco, K., Genschik, P., and Ziegler-Graff, V. (2007). The Polerovirus F box protein P0 targets ARGONAUTE1 to suppress RNA silencing. Curr. Biol. 17: 1615-1621.
12. 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.
13. Burgyán, J., and Havelda, Z. (2011). Viral suppressors of RNA silencing. Trends Plant Sci. 16: 265-272.
14. Chapman, E.J., Prokhnevsky, A.I., Gopinath, K., Dolja, V.V., and Carrington, J.C. (2004). Viral RNA silencing suppressors inhibit the microRNA pathway at an intermediate step. Genes Dev. 18: 1179-1186.
15. Chen, J., Li, W.X., Xie, D., Peng, J.R., and Ding, S.W. (2004). Viral virulence protein suppresses RNA silencing-mediated defense but upregulates the role of microRNA in host gene expression. Plant Cell 16: 1302-1313.
16. Chiu, M.H., Chen, I.H., Baulcombe, D.C., and Tsai, C.H. (2010). The silencing suppressor P25 of Potato virus X interacts with Argonaute1 and mediates its degradation through the proteasome pathway. Mol. Plant Pathol. 11: 641-649.
17. 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.
18. Dalmay, T., Horsefield, R., Braunstein, T.H., and Baulcombe, D.C. (2001). SDE3 encodes an RNA helicase required for post-transcriptional gene silencing in Arabidopsis. EMBO J. 20: 2069-2078.
19. Deleris, A., Gallego-Bartolome, J., Bao, J., Kasschau, K.D., Carrington, J.C., and Voinnet, O. (2006). Hierarchical action and inhibition of plant Dicer-like proteins in antiviral defense. Science 313: 68-71.
20. 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.
21. Ding, S.W., and Voinnet, O. (2007). Antiviral immunity directed by small RNAs. Cell 130: 413-426.
22. Du, Z., Xiao, D., Wu, J., Jia, D., Yuan, Z., Liu, Y., Hu, L., Han, Z., Wei, T., Lin, Q., Wu, Z., and Xie, L. (2011). p2 of rice stripe virus (RSV) interacts with OsSGS3 and is a silencing suppressor. Mol. Plant Pathol. 12: 808-814.
23. Dunoyer, P., Lecellier, C.H., Parizotto, E.A., Himber, C., and Voinnet, O. (2004). Probing the microRNA and small interfering RNA pathways with virus-encoded suppressors of RNA silencing. Plant Cell 16: 1235-1250.
24. Earley, K.W., Haag, J.R., Pontes, O., Opper, K., Juehne, T., Song, K., and Pikaard, C.S. (2006). Gateway-compatible vectors for plant functional genomics and proteomics. Plant J. 45: 616-629.
25. Elmayan, T., Adenot, X., Gissot, L., Lauressergues, D., Gy, I., and Vaucheret, H. (2009). A neomorphic sgs3 allele stabilizing miRNA cleavage products reveals that SGS3 acts as a homodimer. FEBS J. 276: 835-844.
26. Fukunaga, R., and Doudna, J.A. (2009). dsRNA with 59 overhangs contributes to endogenous and antiviral RNA silencing pathways in plants. EMBO J. 28: 545-555.
27. Garcia, D., Garcia, S., Pontier, D., Marchais, A., Renou, J.P., Lagrange, T., and Voinnet, O. (2012). Ago hook and RNA helicase motifs underpin dual roles for SDE3 in antiviral defense and silencing of nonconserved intergenic regions. Mol. Cell 48: 109-120.
28. Garcia-Ruiz, H., Takeda, A., Chapman, E.J., Sullivan, C.M., Fahlgren, N., Brempelis, K.J., and Carrington, J.C. (2010). Arabidopsis RNAdependent RNA polymerases and Dicer-like proteins in antiviral defense and small interfering RNA biogenesis during turnip mosaic virus infection. Plant Cell 22: 481-496.
29. Giner, A., Lakatos, L., García-Chapa, M., López-Moya, J.J., and Burgyán, J. (2010). Viral protein inhibits RISC activity by argonaute binding through conserved WG/GW motifs. PLoS Pathog. 6: e1000996.
30. Glick, E., Zrachya, A., Levy, Y., Mett, A., Gidoni, D., Belausov, E., Citovsky, V., and Gafni, Y. (2008). Interaction with host SGS3 is required for suppression of RNA silencing by tomato yellow leaf curl virus V2 protein. Proc. Natl. Acad. Sci. USA 105: 157-161.
31. Guo, H., Song, X., Xie, C., Huo, Y., Zhang, F., Chen, X., Geng, Y., and Fang, R. (2013). Rice yellow stunt rhabdovirus protein 6 suppresses systemic RNA silencing by blocking RDR6-mediated secondary siRNA synthesis. Mol. Plant Microbe Interact. 26: 927-936.
32. Hagiwara-Komoda, Y., Hirai, K., Mochizuki, A., Nishiguchi, M., Meshi, T., and Ishikawa, M. (2008). Overexpression of a host factor TOM1 inhibits tomato mosaic virus propagation and suppression of RNA silencing. Virology 376: 132-139.
33. Hernandez-Pinzon, I., Yelina, N.E., Schwach, F., Studholme, D.J., Baulcombe, D., and Dalmay, T. (2007). SDE5, the putative homologue of a human mRNA export factor, is required for transgene silencing and accumulation of trans-acting endogenous siRNA. Plant J. 50: 140-148.
34. Himber, C., Dunoyer, P., Moissiard, G., Ritzenthaler, C., and Voinnet, O. (2003). Transitivity-dependent and-independent cellto-cell movement of RNA silencing. EMBO J. 22: 4523-4533.
35. Himeno, M., Maejima, K., Komatsu, K., Ozeki, J., Hashimoto, M., Kagiwada, S., Yamaji, Y., and Namba, S. (2010). Significantly low level of small RNA accumulation derived from an encapsidated mycovirus with dsRNA genome. Virology 396: 69-75.
36. Jauvion, V., Elmayan, T., and Vaucheret, H. (2010). The conserved RNA trafficking proteins HPR1 and TEX1 are involved in the production of endogenous and exogenous small interfering RNA in Arabidopsis. Plant Cell 22: 2697-2709.
37. Jouannet, V., Moreno, A.B., Elmayan, T., Vaucheret, H., Crespi, M.D., and Maizel, A. (2012). Cytoplasmic Arabidopsis AGO7 accumulates in membrane-associated siRNA bodies and is required for ta-siRNA biogenesis. EMBO J. 31: 1704-1713.
38. Kalantidis, K., Schumacher, H.T., Alexiadis, T., and Helm, J.M. (2008). RNA silencing movement in plants. Biol. Cell 100: 13-26.
39. Kalinina, N.O., Rakitina, D.V., Solovyev, A.G., Schiemann, J., and Morozov, S.Y. (2002). RNA helicase activity of the plant virus movement proteins encoded by the first gene of the triple gene block. Virology 296: 321-329.
40. Kasschau, K.D., Xie, Z., Allen, E., Llave, C., Chapman, E.J., Krizan, K.A., and Carrington, J.C. (2003). P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA function. Dev. Cell 4: 205-217.
41. Komatsu, K., Hashimoto, M., Ozeki, J., Yamaji, Y., Maejima, K., Senshu, H., Himeno, M., Okano, Y., Kagiwada, S., and Namba, S. (2010). Viral-induced systemic necrosis in plants involves both programmed cell death and the inhibition of viral multiplication, which are regulated by independent pathways. Mol. Plant Microbe Interact. 23: 283-293.
42. Kumakura, N., Takeda, A., Fujioka, Y., Motose, H., Takano, R., and Watanabe, Y. (2009). SGS3 and RDR6 interact and colocalize in cytoplasmic SGS3/RDR6-bodies. FEBS Lett. 583: 1261-1266.
43. Lakatos, L., Csorba, T., Pantaleo, V., Chapman, E.J., Carrington, J.C., Liu, Y.P., Dolja, V.V., Calvino, L.F., López-Moya, J.J., and Burgyán, J. (2006). Small RNA binding is a common strategy to suppress RNA silencing by several viral suppressors. EMBO J. 25: 2768-2780.
44. Leshchiner, A.D., Minina, E.A., Rakitina, D.V., Vishnichenko, V.K., Solovyev, A.G., Morozov, S.Y., and Kalinina, N.O. (2008). Oligomerization of the potato virus X 25-kD movement protein. Biochemistry (Mosc.) 73: 50-55.
45. Liu, X., and Gorovsky, M.A. (1993). Mapping the 59 and 39 ends of Tetrahymena thermophila mRNAs using RNA ligase mediated amplification of cDNA ends (RLM-RACE). Nucleic Acids Res. 21: 4954-4960.
46. Lu, R., Folimonov, A., Shintaku, M., Li, W.X., Falk, B.W., Dawson, W.O., and Ding, S.W. (2004). Three distinct suppressors of RNA silencing encoded by a 20-kb viral RNA genome. Proc. Natl. Acad. Sci. USA 101: 15742-15747.
47. Mérai, Z., Kerényi, Z., Kertész, 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.
48. Moissiard, G., Parizotto, E.A., Himber, C., and Voinnet, O. (2007). Transitivity in Arabidopsis can be primed, requires the redundant action of the antiviral Dicer-like 4 and Dicer-like 2, and is compromised by viral-encoded suppressor proteins. RNA 13: 1268-1278.
49. Montgomery, T.A., Howell, M.D., Cuperus, J.T., Li, D., Hansen, J.E., Alexander, A.L., Chapman, E.J., Fahlgren, N., Allen, E., and Carrington, J.C. (2008a). Specificity of ARGONAUTE7-miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation. Cell 133: 128-141.
50. Montgomery, T.A., Yoo, S.J., Fahlgren, N., Gilbert, S.D., Howell, M.D., Sullivan, C.M., Alexander, A., Nguyen, G., Allen, E., Ahn, J. H., and Carrington, J.C. (2008b). AGO1-miR173 complex initiates phased siRNA formation in plants. Proc. Natl. Acad. Sci. USA 105: 20055-20062.
51. Morel, J.B., Godon, C., Mourrain, P., Béclin, C., Boutet, S., Feuerbach, F., Proux, F., and Vaucheret, H. (2002). Fertile hypomorphic ARGONAUTE (ago1) mutants impaired in post-transcriptional gene silencing and virus resistance. Plant Cell 14: 629-639.
52. Morozov, S.Y., and Solovyev, A.G. (2003). Triple gene block: Modular design of a multifunctional machine for plant virus movement. J. Gen. Virol. 84: 1351-1366.
53. Nakazawa, Y., Hiraguri, A., Moriyama, H., and Fukuhara, T. (2007). The dsRNA-binding protein DRB4 interacts with the Dicer-like protein DCL4 in vivo and functions in the trans-acting siRNA pathway. Plant Mol. Biol. 63: 777-785.
54. Nishikiori, M., Dohi, K., Mori, M., Meshi, T., Naito, S., and Ishikawa, M. (2006). Membrane-bound tomato mosaic virus replication proteins participate in RNA synthesis and are associated with host proteins in a pattern distinct from those that are not membrane bound. J. Virol. 80: 8459-8468.
55. Peragine, A., Yoshikawa, M., Wu, G., Albrecht, H.L., and Poethig, R.S. (2004). SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNAs in Arabidopsis. Genes Dev. 18: 2368-2379.
56. Rajagopalan, R., Vaucheret, H., Trejo, J., and Bartel, D.P. (2006). A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev. 20: 3407-3425.
57. 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.
58. Senshu, H., Ozeki, J., Komatsu, K., Hashimoto, M., Hatada, K., Aoyama, M., Kagiwada, S., Yamaji, Y., and Namba, S. (2009). Variability in the level of RNA silencing suppression caused by triple gene block protein 1 (TGBp1) from various potexviruses during infection. J. Gen. Virol. 90: 1014-1024.
59. Senshu, H., Yamaji, Y., Minato, N., Shiraishi, T., Maejima, K., Hashimoto, M., Miura, C., Neriya, Y., and Namba, S. (2011). A dual strategy for the suppression of host antiviral silencing: Two distinct suppressors for viral replication and viral movement encoded by potato virus M. J. Virol. 85: 10269-10278.
60. Shivaprasad, P.V., Rajeswaran, R., Blevins, T., Schoelz, J., Meins, F., Jr., Hohn, T., and Pooggin, M.M. (2008). The CaMV transactivator/ viroplasmin interferes with RDR6-dependent trans-acting and secondary siRNA pathways in Arabidopsis. Nucleic Acids Res. 36: 5896-5909.
61. Takeda, A., Sugiyama, K., Nagano, H., Mori, M., Kaido, M., Mise, K., Tsuda, S., and Okuno, T. (2002). Identification of a novel RNA silencing suppressor, NSs protein of Tomato spotted wilt virus. FEBS Lett. 532: 75-79.
62. Tilsner, J., Linnik, O., Wright, K.M., Bell, K., Roberts, A.G., Lacomme, C., Santa Cruz, S., and Oparka, K.J. (2012). The TGB1 movement protein of Potato virus X reorganizes actin and endomembranes into the X-body, a viral replication factory. Plant Physiol. 158: 1359-1370.
63. Várallyay, E., Válóczi, A., Agyi, A., Burgyán, J., and Havelda, Z. (2010). Plant virus-mediated induction of miR168 is associated with repression of ARGONAUTE1 accumulation. EMBO J. 29: 3507-3519.
64. Vargason, J.M., Szittya, G., Burgyán, J., and Hall, T.M. (2003). Size selective recognition of siRNA by an RNA silencing suppressor. Cell 115: 799-811.
65. Vaucheret, H. (2006). Post-transcriptional small RNA pathways in plants: Mechanisms and regulations. Genes Dev. 20: 759-771.
66. Vazquez, F., Vaucheret, H., Rajagopalan, R., Lepers, C., Gasciolli, V., Mallory, A.C., Hilbert, J.L., Bartel, D.P., and Crété, P. (2004). Endogenous trans-acting siRNAs regulate the accumulation of Arabidopsis mRNAs. Mol. Cell 16: 69-79.
67. Voinnet, O., and Baulcombe, D.C. (1997). Systemic signalling in gene silencing. Nature 389: 553.
68. Voinnet, O., Lederer, C., and Baulcombe, D.C. (2000). A viral movement protein prevents spread of the gene silencing signal in Nicotiana benthamiana. Cell 103: 157-167.
69. Voinnet, O., Pinto, Y.M., and Baulcombe, D.C. (1999). Suppression of gene silencing: A general strategy used by diverse DNA and RNA viruses of plants. Proc. Natl. Acad. Sci. USA 96: 14147-14152.
70. Voinnet, O., Vain, P., Angell, S., and Baulcombe, D.C. (1998). Systemic spread of sequence-specific transgene RNA degradation in plants is initiated by localized introduction of ectopic promoterless DNA. Cell 95: 177-187.
71. Wang, X.B., Jovel, J., Udomporn, P., Wang, Y., Wu, Q., Li, W.X., Gasciolli, V., Vaucheret, H., and Ding, S.W. (2011). The 21-nucleotide, but not 22-nucleotide, viral secondary small interfering RNAs direct potent antiviral defense by two cooperative argonautes in Arabidopsis thaliana. Plant Cell 23: 1625-1638.
72. Xie, Z., Allen, E., Wilken, A., and Carrington, J.C. (2005). DICERLIKE 4 functions in trans-acting small interfering RNA biogenesis and vegetative phase change in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 102: 12984-12989.
73. Yaegashi, H., Takahashi, T., Isogai, M., Kobori, T., Ohki, S., and Yoshikawa, N. (2007). Apple chlorotic leaf spot virus 50 kDa movement protein acts as a suppressor of systemic silencing without interfering with local silencing in Nicotiana benthamiana. J. Gen. Virol. 88: 316-324.
74. Yamaji, Y., Kobayashi, T., Hamada, K., Sakurai, K., Yoshii, A., Suzuki, M., Namba, S., and Hibi, T. (2006). In vivo interaction between Tobacco mosaic virus RNA-dependent RNA polymerase and host translation elongation factor 1A. Virology 347: 100-108.
75. Yamaji, Y., et al. (2012). Lectin-mediated resistance impairs plant virus infection at the cellular level. Plant Cell 24: 778-793.
76. Ye, K., Malinina, L., and Patel, D.J. (2003). Recognition of small interfering RNA by a viral suppressor of RNA silencing. Nature 426: 874-878.
77. Yoshikawa, M., Iki, T., Tsutsui, Y., Miyashita, K., Poethig, R.S., Habu, Y., and Ishikawa, M. (2013). 39 fragment of miR173-programmed RISC-cleaved RNA is protected from degradation in a complex with RISC and SGS3. Proc. Natl. Acad. Sci. USA 110: 4117-4122.
78. Yoshikawa, M., Peragine, A., Park, M.Y., and Poethig, R.S. (2005). A pathway for the biogenesis of trans-acting siRNAs in Arabidopsis. Genes Dev. 19: 2164-2175.
79. 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.
80. Zheng, Q., Ryvkin, P., Li, F., Dragomir, I., Valladares, O., Yang, J., Cao, K., Wang, L.S., and Gregory, B.D. (2010). Genome-wide double-stranded RNA sequencing reveals the functional significance of base-paired RNAs in Arabidopsis. PLoS Genet. 6: e1001141.