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

Volumn 23, Issue 4, 2011, Pages 1625-1638

  Wang, Xian Bing ^a   Jovel, Juan ^a   Udomporn, Petchthai ^a,b   Wang, Ying ^a,b   Wu, Qingfa ^a   Li, Wan Xiang ^a   Gasciolli, Virginie ^c   Vaucheret, Herve ^c   Ding, Shou Wei ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b KASETSART UNIVERSITY   (Thailand)

^c INSTITUT JEAN PIERRE BOURGIN   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS THALIANA; CUCUMBER MOSAIC VIRUS; RNA VIRUSES;

EID: 79957761869     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.110.082305     Document Type: Article

References (86)

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. Aliyari, R., Wu, Q., Li, H.W., Wang, X.H., Li, F., Green, L.D., Han, C.S., Li, W.X., and Ding, S.W. (2008). Mechanism of induction and suppression of antiviral immunity directed by virus-derived small RNAs in Drosophila. Cell Host Microbe 4: 387-397.
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. Allen, E., Xie, Z., Gustafson, A.M., Sung, G.H., Spatafora, J.W., and Carrington, J.C. (2004). Evolution of microRNA genes by inverted duplication of target gene sequences in Arabidopsis thaliana. Nat. Genet. 36: 1282-1290.
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. Baumberger, N., and Baulcombe, D.C. (2005). Arabidopsis ARGO-NAUTE1 is an RNA Slicer that selectively recruits microRNAs and short interfering RNAs. Proc. Natl. Acad. Sci. USA 102: 11928-11933.
7. Baumberger, N., Tsai, C.H., Lie, M., Havecker, E., and Baulcombe, D.C. (2007). The Polerovirus silencing suppressor P0 targets ARGO-NAUTE proteins for degradation. Curr. Biol. 17: 1609-1614.
8. 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.
9. 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.
10. Bouché, N., Lauressergues, D., Gasciolli, V., and Vaucheret, H. (2006). An antagonistic function for Arabidopsis DCL2 in development and a new function for DCL4 in generating viral siRNAs. EMBO J. 25: 3347-3356.
11. Boutet, S., Vazquez, F., Liu, J., Béclin, C., Fagard, M., Gratias, A., Morel, J.B., Crété, P., Chen, X., and Vaucheret, H. (2003). Arabi-dopsis HEN1: A genetic link between endogenous miRNA controlling development and siRNA controlling transgene silencing and virus resistance. Curr. Biol. 13: 843-848.
12. 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.
13. Chen, H.M., Chen, L.T., Patel, K., Li, Y.H., Baulcombe, D.C., and Wu, S.H. (2010). 22-Nucleotide RNAs trigger secondary siRNA biogenesis in plants. Proc. Natl. Acad. Sci. USA 107: 15269-15274.
14. 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.
15. Csorba, T., Bovi, A., Dalmay, T., and Burgyán, J. (2007). The p122 subunit of Tobacco Mosaic Virus replicase is a potent silencing suppressor and compromises both small interfering RNA- and micro-RNA-mediated pathways. J. Virol. 81: 11768-11780.
16. Cuperus, J.T., Carbonell, A., Fahlgren, N., Garcia-Ruiz, H., Burke, R.T., Takeda, A., Sullivan, C.M., Gilbert, S.D., Montgomery, T.A., and Carrington, J.C. (2010). Unique functionality of 22-nt miRNAs in triggering RDR6-dependent siRNA biogenesis from target transcripts in Arabidopsis. Nat. Struct. Mol. Biol. 17: 997-1003.
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 trans-gene but not by a virus. Cell 101: 543-553.
18. 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.
19. 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 Arabi-dopsis is associated with drastically reduced accumulation of three classes of viral small interfering RNAs. Plant Cell 19: 2053-2063.
20. Ding, S.W. (2010). RNA-based antiviral immunity. Nat. Rev. Immunol. 10: 632-644.
21. 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.
22. Ding, S.W., and Voinnet, O. (2007). Antiviral immunity directed by small RNAs. Cell 130: 413-426.
23. Donaire, L., Barajas, D., Martínez-García, B., Martínez-Priego, L., Pagán, I., and Llave, C. (2008). Structural and genetic requirements for the biogenesis of tobacco rattle virus-derived small interfering RNAs. J. Virol. 82: 5167-5177.
24. Dunoyer, P., Himber, C., and Voinnet, O. (2005). DICER-LIKE 4 is required for RNA interference and produces the 21-nucleotide small interfering RNA component of the plant cell-to-cell silencing signal. Nat. Genet. 37: 1356-1360.
25. Elmayan, T., Proux, F., and Vaucheret, H. (2005). Arabidopsis RPA2: A genetic link among transcriptional gene silencing, DNA repair, and DNA replication. Curr. Biol. 15: 1919-1925.
26. Endres, M.W., Gregory, B.D., Gao, Z., Foreman, A.W., Mlotshwa, S., Ge, X., Pruss, G.J., Ecker, J.R., Bowman, L.H., and Vance, V. (2010). Two plant viral suppressors of silencing require the ethylene-inducible host transcription factor RAV2 to block RNA silencing. PLoS Pathog. 6: e1000729.
27. Fusaro, A.F., Matthew, L., Smith, N.A., Curtin, S.J., Dedic-Hagan, J., Ellacott, G.A., Watson, J.M., Wang, M.B., Brosnan, C., Carroll, B.J., and Waterhouse, P.M. (2006). RNA interference-inducing hairpin RNAs in plants act through the viral defence pathway. EMBO Rep. 7: 1168-1175.
28. Galiana-Arnoux, D., Dostert, C., Schneemann, A., Hoffmann, J.A., and Imler, J.L. (2006). Essential function in vivo for Dicer-2 in host defense against RNA viruses in drosophila. Nat. Immunol. 7: 590-597.
29. Garcia-Ruiz, H., Takeda, A., Chapman, E.J., Sullivan, C.M., Fahlgren, N., Brempelis, K.J., and Carrington, J.C. (2010). Arabidopsis RNA-dependent RNA polymerases and dicer-like proteins in antiviral defense and small interfering RNA biogenesis during Turnip Mosaic Virus infection. Plant Cell 22: 481-496.
30. 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.
31. Harvey, J.J., Lewsey, M.G., Patel, K., Westwood, J., Heimstädt, S., Carr, J.P., and Baulcombe, D.C. (2011). An antiviral defense role of AGO2 in plants. PLoS ONE 6: e14639.
32. Havelda, Z., Várallyay, E., Vá lóczi, A., and Burgyán, J. (2008). Plant virus infection-induced persistent host gene downregulation in sys-temically infected leaves. Plant J. 55: 278-288.
33. Hutvágner, G., and Zamore, P.D. (2002). A microRNA in a multiple-turnover RNAi enzyme complex. Science 297: 2056-2060.
34. 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.
35. Langmead, B., Trapnell, C., Pop, M., and Salzberg, S.L. (2009). Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10: R25.
36. Lewsey, M., Surette, M., Robertson, F.C., Ziebell, H., Choi, S.H., Ryu, K.H., Canto, T., Palukaitis, P., Payne, T., Walsh, J.A., and Carr, J.P. (2009). The role of the Cucumber mosaic virus 2b protein in viral movement and symptom induction. Mol. Plant Microbe Interact. 22: 642-654.
37. Lewsey, M.G., Murphy, A.M., Maclean, D., Dalchau, N., Westwood, J.H., Macaulay, K., Bennett, M.H., Moulin, M., Hanke, D.E., Powell, G., Smith, A.G., and Carr, J.P. (2010). Disruption of two defensive signaling pathways by a viral RNA silencing suppressor. Mol. Plant Microbe Interact. 23: 835-845.
38. Li, H.W., Li, W.X., and Ding, S.W. (2002). Induction and suppression of RNA silencing by an animal virus. Science 296: 1319-1321.
39. (-Δ Δ C(T)) Method. Methods 25: 402-408.
40. Llave, C. (2010). Virus-derived small interfering RNAs at the core of plant-virus interactions. Trends Plant Sci. 15: 701-707.
41. Lobbes, D., Rallapalli, G., Schmidt, D.D., Martin, C., and Clarke, J. (2006). SERRATE: A new player on the plant microRNA scene. EMBO Rep. 7: 1052-1058.
42. Lu, R., Maduro, M., Li, F., Li, H.W., Broitman-Maduro, G., Li, W.X., and Ding, S.W. (2005). Animal virus replication and RNAi-mediated antiviral silencing in Caenorhabditis elegans. Nature 436: 1040-1043.
43. Lu, R., Yigit, E., Li, W.X., and Ding, S.W. (2009). An RIG-I-Like RNA helicase mediates antiviral RNAi downstream of viral siRNA biogenesis in Caenorhabditis elegans. PLoS Pathog. 5: e1000286.
44. Mallory, A.C., Hinze, A., Tucker, M.R., Bouché, N., Gasciolli, V., Elmayan, T., Lauressergues, D., Jauvion, V., Vaucheret, H., and Laux, T. (2009). Redundant and specific roles of the ARGONAUTE proteins AGO1 and ZLL in development and small RNA-directed gene silencing. PLoS Genet. 5: e1000646.
45. Mallory, A.C., and Vaucheret, H. (2009). ARGONAUTE 1 homeostasis invokes the coordinate action of the microRNA and siRNA pathways. EMBO Rep. 10: 521-526.
46. Matzke, M., Kanno, T., Daxinger, L., Huettel, B., and Matzke, A.J. (2009). RNA-mediated chromatin-based silencing in plants. Curr. Opin. Cell Biol. 21: 367-376.
47. Mi, S., et al. (2008). Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 59 terminal nucleotide. Cell 133: 116-127.
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. Moissiard, G., and Voinnet, O. (2006). RNA silencing of host transcripts by cauliflower mosaic virus requires coordinated action of the four Arabidopsis Dicer-like proteins. Proc. Natl. Acad. Sci. USA 103: 19593-19598.
50. 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. (2008). Specificity of ARGONAUTE7-miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation. Cell 133: 128-141.
51. Morel, J.-B., Godon, C., Mourrain, P., Béclin, C., Boutet, S., Feuerbach, F., Proux, F., and Vaucheret, H. (2002). Fertile hypomorphic ARGO-NAUTE (ago1) mutants impaired in post-transcriptional gene silencing and virus resistance. Plant Cell 14: 629-639.
52. Mourrain, P., et al. (2000). Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell 101: 533-542.
53. Omarov, R.T., Ciomperlik, J.J., and Scholthof, H.B. (2007). RNAi-associated ssRNA-specific ribonucleases in Tombusvirus P19 mutant-infected plants and evidence for a discrete siRNA-containing effector complex. Proc. Natl. Acad. Sci. USA 104: 1714-1719.
54. Pantaleo, V., Szittya, G., and Burgyán, J. (2007). Molecular bases of viral RNA targeting by viral small interfering RNA-programmed RISC. J. Virol. 81: 3797-3806.
55. Qu, F. (2010). Antiviral role of plant-encoded RNA-dependent RNA polymerases revisited with deep sequencing of small interfering RNAs of virus origin. Mol. Plant Microbe Interact. 23: 1248-1252.
56. Qu, F., Ye, X., Hou, G., Sato, S., Clemente, T.E., and Morris, T.J. (2005). RDR6 has a broad-spectrum but temperature-dependent antiviral defense role in Nicotiana benthamiana. J. Virol. 79: 15209-15217.
57. Qu, F., Ye, X., and Morris, T.J. (2008). Arabidopsis DRB4, AGO1, AGO7, and RDR6 participate in a DCL4-initiated antiviral RNA silencing pathway negatively regulated by DCL1. Proc. Natl. Acad. Sci. USA 105: 14732-14737.
58. Rhoades, M.W., Reinhart, B.J., Lim, L.P., Burge, C.B., Bartel, B., and Bartel, D.P. (2002). Prediction of plant microRNA targets. Cell 110: 513-520.
59. Schott, D.H., Cureton, D.K., Whelan, S.P., and Hunter, C.P. (2005). An antiviral role for the RNA interference machinery in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 102: 18420-18424.
60. Schubert, S., Rothe, D., Werk, D., Grunert, H.P., Zeichhardt, H., Erdmann, V.A., and Kurreck, J. (2007). Strand-specific silencing of a picornavirus by RNA interference: Evidence for the superiority of plus-strand specific siRNAs. Antiviral Res. 73: 197-205.
61. 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.
62. 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.
63. Sun, Q., Choi, G.H., and Nuss, D.L. (2009). A single Argonaute gene is required for induction of RNA silencing antiviral defense and promotes viral RNA recombination. Proc. Natl. Acad. Sci. USA 106: 17927-17932.
64. Szittya, G., Moxon, S., Pantaleo, V., Toth, G., Rusholme Pilcher, R.L., Moulton, V., Burgyan, J., and Dalmay, T. (2010). Structural and functional analysis of viral siRNAs. PLoS Pathog. 6: e1000838.
65. Takeda, A., Iwasaki, S., Watanabe, T., Utsumi, M., and Watanabe, Y. (2008). The mechanism selecting the guide strand from small RNA duplexes is different among argonaute proteins. Plant Cell Physiol. 49: 493-500.
66. Vaistij, F.E., and Jones, L. (2009). Compromised virus-induced gene silencing in RDR6-deficient plants. Plant Physiol. 149: 1399-1407.
67. van Rij, R.P., Saleh, M.C., Berry, B., Foo, C., Houk, A., Antoniewski, C., and Andino, R. (2006). The RNA silencing endonuclease Argo-naute 2 mediates specific antiviral immunity in Drosophila mela-nogaster. Genes Dev. 20: 2985-2995.
68. 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.
69. Vaucheret, H. (2008). Plant ARGONAUTES. Trends Plant Sci. 13: 350-358.
70. Vaucheret, H., Vazquez, F., Crété, P., and Bartel, D.P. (2004). The action of ARGONAUTE1 in the miRNA pathway and its regulation by the miRNA pathway are crucial for plant development. Genes Dev. 18: 1187-1197.
71. 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 Arabi-dopsis mRNAs. Mol. Cell 16: 69-79.
72. Voinnet, O. (2008). Use, tolerance and avoidance of amplified RNA silencing by plants. Trends Plant Sci. 13: 317-328.
73. 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.
74. Wang, X.H., Aliyari, R., Li, W.X., Li, H.W., Kim, K., Carthew, R., Atkinson, P., and Ding, S.W. (2006). RNA interference directs innate immunity against viruses in adult Drosophila. Science 312: 452-454.
75. Wilkins, C., Dishongh, R., Moore, S.C., Whitt, M.A., Chow, M., and Machaca, K. (2005). RNA interference is an antiviral defense mechanism in Caenorhabditis elegans. Nature 436: 1044-1047.
76. Wu, Q., Luo, Y., Lu, R., Lau, N., Lai, E.C., Li, W.X., and Ding, S.W. (2010). Virus discovery by deep sequencing and assembly of virus-derived small silencing RNAs. Proc. Natl. Acad. Sci. USA 107: 1606-1611.
77. Xie, Z., Allen, E., Wilken, A., and Carrington, J.C. (2005). DICER-LIKE 4 functions in trans-acting small interfering RNA biogenesis and vegetative phase change in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 102: 12984-12989.
78. Xie, Z., Fan, B., Chen, C., and Chen, Z. (2001). An important role of an inducible RNA-dependent RNA polymerase in plant antiviral defense. Proc. Natl. Acad. Sci. USA 98: 6516-6521.
79. 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.
80. Xie, Z., Kasschau, K.D., and Carrington, J.C. (2003). Negative feedback regulation of Dicer-Like1 in Arabidopsis by microRNA-guided mRNA degradation. Curr. Biol. 13: 784-789.
81. 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.
82. Yigit, E., Batista, P.J., Bei, Y., Pang, K.M., Chen, C.C., Tolia, N.H., Joshua-Tor, L., Mitani, S., Simard, M.J., and Mello, C.C. (2006). Analysis of the C. elegans Argonaute family reveals that distinct Argonautes act sequentially during RNAi. Cell 127: 747-757.
83. Zambon, R.A., Vakharia, V.N., and Wu, L.P. (2006). RNAi is an antiviral immune response against a dsRNA virus in Drosophila melanogaster. Cell. Microbiol. 8: 880-889.
84. Zhang, X., Segers, G.C., Sun, Q., Deng, F., and Nuss, D.L. (2008). Characterization of hypovirus-derived small RNAs generated in the chestnut blight fungus by an inducible DCL-2-dependent pathway. J. Virol. 82: 2613-2619.
85. 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.
86. Zheng, X., Zhu, J., Kapoor, A., and Zhu, J.K. (2007). Role of Arab-idopsis AGO6 in siRNA accumulation, DNA methylation and tran-scriptional gene silencing. EMBO J. 26: 1691-1701.