Satellite RNAs interfere with the function of viral RNA silencing suppressors

Frontiers in Plant Science

Volumn 6, Issue APR, 2015, Pages

  Shen, Wan Xia ^a,b   Au, Phil Chi Khang ^b,e   Shi, Bu Jun ^c   Smith, Neil A ^b   Dennis, Elizabeth S ^b   Guo, Hui Shan ^d   Zhou, Chang Yong ^a   Wang, Ming Bo ^b  

^a SOUTHWEST UNIVERSITY   (China)

^b CSIRO   (Australia)

^c UNIVERSITY OF ADELAIDE   (Australia)

^d INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^e UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

microRNA expression; RNA silencing; Satellite RNA; Symptom attenuation; Virus encoded suppressor

Indexed keywords

CUCUMBER MOSAIC VIRUS; NICOTIANA BENTHAMIANA; NICOTIANA TABACUM; TOMBUSVIRUS;

EID: 84934875746     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2015.00281     Document Type: Article

References (55)

1. Aliyari, R., Wu, Q. F., Li, H. W., Wang, X. H., Li, F., Green, L. D., et al. (2008). Mechanism of induction and suppression of antiviral immunity directed by virus-derived small RNAs in Drosophila. Cell Host Microbe 4, 387-397. doi: 10. 1016/j. chom. 2008. 09. 001.
2. Baulcombe, D. C., and Molnar, A. (2004). Crystal structure of p19-a universal suppressor of RNA silencing. Trends Biochem. Sci. 29, 279-281. doi: 10. 1016/j. tibs. 2004. 04. 007.
3. Baulcombe, D. C., Saunders, G. R., Bevan, M. W., Mayo, M. A., and Harrison, B. D. (1986). Expression of biologically-active viral satellite RNA from the nuclear genome of transformed plants. Nature 321, 446-449. doi: 10. 1038/321446a0.
4. 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. doi: 10. 1093/emboj/17. 22. 6739.
5. 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. Gene Dev. 18, 1179-1186. doi: 10. 1101/gad. 1201204.
6. Chen, S., Helliwell, C. A., Wu, L. M., Dennis, E. S., Upadhyaya, N. M., Zhang, R., et al. (2005). A novel T-DNA vector design for selection of transgenic lines with simple transgene integration and stable transgene expression. Funct. Plant Biol. 32, 671-681. doi: 10. 1071/FP05072.
7. Ding, S. W., Shi, B. J., Li, W. X., and Symons, R. H. (1996). An interspecies hybrid RNA virus is significantly more virulent than either parental virus. Proc. Natl. Acad. Sci. U. S. A. 93, 7470-7474. doi: 10. 1073/pnas. 93. 15. 7470.
8. Du, Z. Y., Chen, A. Z., Chen, W. H., Liao, Q. S., Zhang, H. M., Bao, Y. M., et al. (2014). Nuclear-cytoplasmic partitioning of Cucumber mosaic virus protein 2b determines the balance between its roles as a virulence determinant and an RNA-silencing suppressor. J. Virol. 88, 5228-5241. doi: 10. 1128/JVI. 00284-14.
9. Duan, C. G., Fang, Y. Y., Zhou, B. J., Zhao, J. H., Hou, W. N., Zhu, H., et al. (2012). Suppression of Arabidopsis ARGONAUTE1-mediated slicing, transgene-induced RNA silencing, and DNA methylation by distinct domains of the Cucumber mosaic virus 2b protein. Plant Cell 24, 259-274. doi: 10. 1105/tpc. 111. 092718.
10. Ebhardt, H. A., and Unrau, P. J. (2009). Characterizing multiple exogenous and endogenous small RNA populations in parallel with subfemtomolar sensitivity using a streptavidin gel-shift assay. RNA 15, 724-731. doi: 10. 1261/rna. 1235109.
11. Garcia-Arenal, F., and Palukaitis, P. (1999). Structure and functional relationships of satellite RNAs of Cucumber mosaic virus. Curr. Top. Microbiol. 239, 37-63. doi: 10. 1007/978-3-662-09796-0_3.
12. Gerlach, W. L., Llewellyn, D., and Haseloff, J. (1987). Construction of a plant disease resistance gene from the satellite RNA of Tobacco ringspot virus. Nature 328, 802-805. doi: 10. 1038/328802a0.
13. Gonzalez, I., Rakitina, D., Semashko, M., Taliansky, M., Praveen, S., Palukaitis, P., et al. (2012). RNA binding is more critical to the suppression of silencing function of Cucumber mosaic virus 2b protein than nuclear localization. RNA 18, 771-782. doi: 10. 1261/rna. 031260. 111.
14. Hamera, S., Song, X. G., Su, L., Chen, X. Y., and Fang, R. X. (2012). Cucumber mosaic virus suppressor 2b binds to AGO4-related small RNAs and impairs AGO4 activities. Plant J. 69, 104-115. doi: 10. 1111/j. 1365-313X. 2011. 04774. x.
15. 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. doi: 10. 1038/328799a0.
16. Havelda, Z., Hornyik, C., Valoczi, A., and Burgyan, J. (2005). Defective interfering RNA hinders the activity of a Tombusvirus-encoded posttranscriptional gene silencing suppressor. J. Virol. 79, 450-457. doi: 10. 1128/JVI. 79. 1. 450-457. 2005.
17. Hou, W. N., Duan, C. G., Fang, R. X., Zhou, X. Y., and Guo, H. S. (2011). Satellite RNA reduces expression of the 2b suppressor protein resulting in the attenuation of symptoms caused byCucumber mosaic virus infection. Mol. Plant Pathol. 12, 595-605. doi: 10. 1111/j. 1364-3703. 2010. 00696. x.
18. Hu, C. C., Hsu, Y. H., and Lin, N. S. (2009). Satellite RNAs and satellite viruses of plants. Viruses 1, 1325-1350. doi: 10. 3390/v1031325.
19. Ishikawa, A. (2009). The Arabidopsis G-Protein beta-subunit is required for defense response against Agrobacterium tumefaciens. Biosci. Biotechnol. Biochem. 73, 47-52. doi: 10. 1271/bbb. 80449.
20. Jay, F., Wang, Y., Yu, A., Taconnat, L., Pelletier, S., Colot, V., et al. (2011). Misregulation of AUXIN RESPONSE FACTOR 8 underlies the developmental abnormalities caused by three distinct viral silencing suppressors in Arabidopsis. PLoS Pathog 7: e1002035. doi: 10. 1371/journal. ppat. 1002035.
21. Kasschau, K. D., Xie, Z., Allen, E., Llave, C., Chapman, E. J., Krizan, K. A., et al. (2003). P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA function. Dev. Cell 4, 205-217. doi: 10. 1016/S1534-5807(03)00025-X.
22. Lakatos, L., Csorba, T., Pantaleo, V., Chapman, E. J., Carrington, J. C., Liu, Y. P., et al. (2006). Small RNA binding is a common strategy to suppress RNA silencing by several viral suppressors. EMBO J. 25, 2768-2780. doi: 10. 1038/sj. emboj. 7601164.
23. 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. doi: 10. 1111/j. 1365-313X. 2007. 03042. x.
24. Liu, L., and Lomonossoff, G. P. (2002). Agroinfection as a rapid method for propagating Cowpea mosaic virus-based constructs. J. Virol. Methods 105, 343-348. doi: 10. 1016/S0166-0934(02)00121-0.
25. 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. doi: 10. 1105/tpc. 1. 12. 1165.
26. Moriones, E., Diaz, I., Rodriguezcerezo, E., Fraile, A., and Garciaarenal, F. (1992). Differential interactions among strains of Tomato aspermy virus and satellite RNAs of Cucumber mosaic virus. Virology 186, 475-480. doi: 10. 1016/0042-6822(92)90012-E.
27. Ohta, S., Mita, S., Hattori, T., and Nakamura, K. (1990). Construction and expression in Tobacco of a β-Glucuronidase (GUS) reporter gene dontaining an intron within the coding sequence. Plant Cell Physiol. 31, 805-813.
28. Omarov, R., Sparks, K., Smith, L., Zindovic, J., and Scholthof, H. B. (2006). Biological relevance of a stable biochemical interaction between the Tombusvirus-encoded P19 and short interfering RNAs. J. Virol. 80, 3000-3008. doi: 10. 1128/JVI. 80. 6. 3000-3008. 2006.
29. Palukaitis, P., Roossinck, M. J., Dietzgen, R. G., and Francki, R. I. B. (1992). Cucumber mosaic virus. Adv. Virus Res. 41, 281-348. doi: 10. 1016/S0065-3527(08)60039-1.
30. Piazzolla, P., Tousignant, M. E., and Kaper, J. M. (1982). Cucumber mosaic virus-associated RNA 5 IX. The overtaking of viral RNA synthesis by CARNA 5 and dsCARNA 5 in tobacco. Virology122, 147-157. doi: 10. 1016/0042-6822(82)90384-1.
31. Pumplin, N., and Voinnet, O. (2013). RNA silencing suppression by plant pathogens: defence, counter-defence and counter-counter-defence. Nat. Rev. Microbiol. 11, 745-760. doi: 10. 1038/nrmicro3120.
32. Roossinck, M. J., Sleat, D., and Palukaitis, P. (1992). Satellite RNAs of plant viruses: structures and biological effects. Microbiol. Rev. 56, 265-279.
33. Ruiz-Ferrer, V., and Voinnet, O. (2009). Roles of plant small RNAs in biotic stress responses. Annu. Rev. Plant Biol. 60, 485-510. doi: 10. 1146/annurev. arplant. 043008. 092111.
34. Sambrook, J., Fritsch, E., and Maniatis, T. (1989). Molecular-Cloning-A Laboratory Manual, 2nd Edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
35. Shen, W. X., Smith, N. A., Zhou, C. Y., and Wang, M. B. (2014). High-level accumulation of exogenous small RNAs not affecting endogenous small RNA biogenesis and function in plants. J. Integr. Agric. 13, 1017-1023. doi: 10. 1016/S2095-3119(13)60525-0.
36. 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. doi: 10. 1094/MPMI. 2002. 15. 9. 947.
37. Shimura, H., and Pantaleo, V. (2011). Viral induction and suppression of RNA silencing in plants. Biochim. Biophys. Acta 1809, 601-612. doi: 10. 1016/j. bbagrm. 2011. 04. 005.
38. Shimura, H., Pantaleo, V., Ishihara, T., Myojo, N., Inaba, J., Sueda, K., et al. (2011). A viral satellite RNA induces yellow symptoms on tobacco by targeting a gene involved in chlorophyll biosynthesis using the RNA silencing machinery. PLoS Pathog. 7: e1002021. doi: 10. 1371/journal. ppat. 1002021.
39. Simon, A. E., Roossinck, M. J., and Havelda, Z. (2004). Plant virus satellite and defective interfering RNAs: new paradigms for a new century. Annu. Rev. Phytopathol. 42, 415-437. doi: 10. 1146/annurev. phyto. 42. 040803. 140402.
40. Smith, N. A., Eamens, A. L., and Wang, M. B. (2011). Viral small interfering RNAs target host genes to mediate disease symptoms in plants. PLoS Pathog. 7: e1002022. doi: 10. 1371/journal. ppat. 1002022.
41. 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. doi: 10. 1094/MPMI. 2002. 15. 7. 647.
42. Takanami, Y. (1981). A striking change in symptoms on cucumber mosaic virus-infected tobacco plants induced by a satellite RNA. Virology 109, 120-126. doi: 10. 1016/0042-6822(81)90476-1.
43. Vargason, J. M., Szittya, G., Burgyan, J., and Hall, T. M. (2003). Size selective recognition of siRNA by an RNA silencing suppressor. Cell 115, 779-811. doi: 10. 1016/S0092-8674(03)00984-X.
44. Voinnet, O. (2009). Origin, biogenesis, and activity of plant microRNAs. Cell 136, 669-687. doi: 10. 1016/j. cell. 2009. 01. 046.
45. 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. U. S. A. 96, 14147-14152. doi: 10. 1073/pnas. 96. 24. 14147.
46. Wang, M. B., Bian, X. Y., Wu, L. M., Liu, L. X., Smith, N. A., Isenegger, D., et al. (2004). On the role of RNA silencing in the pathogenicity and evolution of viroids and viral satellites. Proc. Natl. Acad. Sci. U. S. A. 101, 3275-3280. doi: 10. 1073/pnas. 0400104101.
47. Wang, M. B., Helliwell, C. A., Wu, L. M., Waterhouse, P. M., Peacock, W. J., and Dennis, E. S. (2008). Hairpin RNAs derived from RNA polymerase II and polymerase III promoter-directed transgenes are processed differently in plants. RNA 14, 903-913. doi: 10. 1261/rna. 760908.
48. Wang, M. B., and Waterhouse, P. M. (2000). High-efficiency silencing of a beta-glucuronidase gene in rice is correlated with repetitive transgene structure but is independent of DNA methylation. Plant Mol. Biol. 43, 67-82. doi: 10. 1023/A: 1006490331303.
49. Wang, M. B., Wesley, S. V., Finnegan, E. J., Smith, N. A., and Waterhouse, P. M. (2001). Replicating satellite RNA induces sequence-specific DNA methylation and truncated transcripts in plants. RNA 7, 16-28. doi: 10. 1017/S1355838201001224.
50. Wood, C. C., Petrie, J. R., Shrestha, P., Mansour, M. P., Nichols, P. D., Green, A. G., et al. (2009). A leaf-based assay using interchangeable design principles to rapidly assemble multistep recombinant pathways. Plant Biotechnol. J. 7, 914-924. doi: 10. 1111/j. 1467-7652. 2009. 00453. x.
51. Wu, G., and Kaper, J. M. (1995). Competition of viral and satellite RNAs of Cucumber mosaic virus for replication in vitro by viral RNA-dependent RNA polymerase. Res. Virol. 146, 61-67. doi: 10. 1016/0923-2516(96)80590-5.
52. Ye, J., Qua, 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. doi: 10. 1016/j. febslet. 2008. 11. 031.
53. Zamore, P. D. (2001). RNA interference: listening to the sound of silence. Nat. Struct. Biol. 8, 746-750. doi: 10. 1038/nsb0901-746.
54. Zhang, L., Hanada, K., and Palukaitis, P. (1994). Mapping local and systemic symptom determinants of Cucumber mosaic cucumovirus in tobacco. J. Gen. Virol. 75, 3185-3191. doi: 10. 1099/0022-1317-75-11-3185.
55. Zhang, X. R., Yuan, Y. R., Pei, Y., Lin, S. S., Tuschl, T., Patel, D. J., et al. (2006). Cucumber mosaic virus-encoded 2b suppressor inhibits Arabidopsis Argonaute1 cleavage activity to counter plant defense. Gene Dev. 20, 3255-3268. doi: 10. 1101/gad. 1495506.