Inhibition of 3′ modification of small RNAs in virus-infected plants require spatial and temporal co-expression of small RNAs and viral silencing-suppressor proteins

Nucleic Acids Research

Volumn 36, Issue 12, 2008, Pages 4099-4107

  Lózsa, Rita ^a   Csorba, Tibor ^a   Lakatos, Lóránt ^a   Burgyán, József ^a  

^a SZENT ISTVÁN UNIVERSITY   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

METHYLTRANSFERASE; MICRORNA; PLANT RNA; PROTEIN; PROTEIN P19; SMALL INTERFERING RNA; VIRAL SILENCING SUPPRESSOR PROTEIN; CYSTEINE PROTEINASE; HC PRO PROTEIN, POTYVIRUS; HC-PRO PROTEIN, POTYVIRUS; RNA BINDING PROTEIN; VIRUS PROTEIN; VIRUS RNA;

ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; CYTOPLASM; GENE EXPRESSION; GENE SILENCING; IN VIVO STUDY; NONHUMAN; PLANT; PLANT VIRUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN RNA BINDING; RNA DEGRADATION; RNA METHYLATION; VIRAL PLANT DISEASE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PLANT DISEASE; POTYVIRUS; RNA INTERFERENCE; TOBACCO; TOMBUSVIRUS; VIROLOGY;

CARNATION ITALIAN RINGSPOT VIRUS; NICOTIANA BENTHAMIANA; TOBACCO ETCH VIRUS;

CYSTEINE ENDOPEPTIDASES; CYTOPLASM; GENE EXPRESSION REGULATION, PLANT; GENE EXPRESSION REGULATION, VIRAL; MICRORNAS; PLANT DISEASES; POTYVIRUS; RNA INTERFERENCE; RNA, PLANT; RNA, SMALL INTERFERING; RNA, VIRAL; RNA-BINDING PROTEINS; TOBACCO; TOMBUSVIRUS; VIRAL PROTEINS;

EID: 47249134724     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkn365     Document Type: Article

References (45)

1. Matzke,M., Aufsatz,W., Kanno,T., Daxinger,L., Papp,I., Mette,M.F. and Matzke,A.J. (2004) Genetic analysis of RNA-mediated transcriptional gene silencing. Biochim. Biophys. Acta, 1677, 129-141.
2. Ding,S.W. and Voinnet,O. (2007) Antiviral immunity directed by small RNAs. Cell, 130, 413-426.
3. Carrington,J.C. and Ambros,V. (2003) Role of microRNAs in plant and animal development. Science, 301, 336-338.
4. Bartel,D.P. (2004) MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell, 116, 281-297.
5. Rand,T.A., Petersen,S., Du,F. and Wang,X. (2005) Argonaute2 cleaves the anti-guide strand of siRNA during RISC activation. Cell, 123 621-629.
6. Matranga,C., Tomari,Y., Shin,C., Bartel,D.P. and Zamore,P.D. (2005) Passenger-strand cleavage facilitates assembly of siRNA into Ago2-containing RNAi enzyme complexes. Cell, 123, 607-620.
7. Baulcombe,D.C. (2007) Molecular biology. Amplified silencing. Science 315, 199-200.
8. Pak,J. and Fire,A. (2007) Distinct populations of primary and secondary effectors during RNAi in C. elegans. Science, 315, 241-244.
9. Yu,B., Yang,Z., Li,J., Minakhina,S., Yang,M., Padgett,R.W., Steward,R. and Chen,X. (2005) Methylation as a crucial step in plant microRNA biogenesis. Science, 307, 932-935.
10. Park,W., Li,J., Song,R., Messing,J. and Chen,X. (2002) CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr. Biol., 12, 1484-1495.
11. Li,J., Yang,Z., Yu,B., Liu,J. and Chen,X. (2005) Methylation protects miRNAs and siRNAs from a 3′-end uridylation activity in Arabidopsis. Curr. Biol., 15, 1501-1507.
12. Houwing,S., Kamminga,L.M., Berezikov,E., Cronembold,D., Girard,A., van den Elst,H., Filippov,D.V., Blaser,H., Raz,E., Moens,C.B. et al. (2007) A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in Zebrafish. Cell, 129, 69-82.
13. Tomari,Y., Du,T. and Zamore,P.D. (2007) Sorting of Drosophila small silencing RNAs. Cell, 130, 299-308.
14. Saito,K., Sakaguchi,Y., Suzuki,T., Siomi,H. and Siomi,M.C. (2007) Pimet, the Drosophila homolog of HEN1, mediates 2′-O-methylation of Piwi- interacting RNAs at their 3′ ends. Genes Dev., 21, 1603-1608.
15. Kirino,Y. and Mourelatos,Z. (2007) The mouse homolog of HEN1 is a potential methylase for Piwi-interacting RNAs. RNA, 13, 1397-1401.
16. Silhavy,D. and Burgyan,J. (2004) Effects and side-effects of viral RNA silencing suppressors on short RNAs. Trends Plant Sci., 9, 76-83.
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.
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.
19. 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.
20. Csorba,T., Bovi,A., Dalmay,T. and Burgyan,J. (2007) The p122 subunit of Tobacco mosaic virus replicase is a potent silencing suppressor and compromises both siRNA and miRNA mediated pathways. J. Virol., 81, 11768-11780.
21. 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.
22. Pazhouhandeh,M., Dieterle,M., Marrocco,K., Lechner,E., Berry,B., Brault,V., Hemmer,O., Kretsch,T., Richards,K.E., Genschik,P. et al. (2006) F-box-like domain in the polerovirus protein P0 is required for silencing suppressor function. Proc. Natl Acad. Sci. USA, 103, 1994-1999.
23. 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.
24. 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.
25. 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.
26. Yu,B., Chapman,E.J., Yang,Z., Carrington,J.C. and Chen,X. (2006) Transgenically expressed viral RNA silencing suppressors interfere with microRNA methylation in Arabidopsis. FEBS Lett., 580, 3117-3120.
27. Akbergenov,R., Si-Ammour,A., Blevins,T., Amin,I., Kutter,C., Vanderschuren,H., Zhang,P., Gruissem,W., Meins,F. Jr, Hohn,T. et al. (2006) Molecular characterization of geminivirus-derived small RNAs in different plant species. Nucleic Acids Res., 34, 462-471.
28. Vogler,H., Akbergenov,R., Shivaprasad,P.V., Dang,V., Fasler,M., Kwon,M.O., Zhanybekova,S., Hohn,T. and Heinlein,M. (2007) Modification of small RNAs associated with suppression of RNA silencing by tobamovirus replicase protein. J Virol., 81, 10379-10388.
29. Ebhardt,H.A., Thi,E.P., Wang,M.B. and Unrau,P.J. (2005) Extensive 3′ modification of plant small RNAs is modulated by helper component-proteinase expression. Proc. Natl Acad. Sci. USA, 102 13398-13403.
30. Vargason,J., Szittya,G., Burgyan,J. and Hall,T.M. (2003) Size selective recognition of siRNA by an RNA silencing suppressor. Cell, 115 799-811.
31. Zamore,P.D., Tuschl,T., Sharp,P.A. and Bartel,D.P. (2000) RNAi: double-stranded RNA directs the ATP-dependent cleavage of mRNA at 21 to 23 nucleotide intervals. Cell, 101, 25-33.
32. Vaucheret,H., Mallory,A.C. and Bartel,D.P. (2006) AGO1 homeostasis entails coexpression of MIR168 and AGO1 and preferential stabilization of miR168 by AGO1. Mol. Cell, 22, 129-136.
33. 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.
34. Papp,I., Mette,M.F., Aufsatz,W., Daxinger,L., Schauer,S.E., Ray,A., van der Winden,J., Matzke,M. and Matzke,A.J. (2003) Evidence for nuclear processing of plant micro RNA and short interfering RNA precursors. Plant Physiol., 132, 1382-1390.
35. 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.
36. Valoczi,A., Hornyik,C., Varga,N., Burgyan,J., Kauppinen,S. and Havelda,Z. (2004) Sensitive and specific detection of microRNAs by northern blot analysis using LNA-modified oligonucleotide probes. Nucleic Acids Res., 32, e175.
37. Kurihara,Y. and Watanabe,Y. (2004) Arabidopsis micro-RNA biogenesis through Dicer-like 1 protein functions. Proc. Natl Acad. Sci. USA, 101, 12753-12758.
38. Park,M.Y., Wu,G., Gonzalez-Sulser,A., Vaucheret,H. and Poethig,R.S. (2005) Nuclear processing and export of microRNAs in Arabidopsis. Proc. Natl Acad. Sci. USA, 102, 3691-3696.
39. 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.
40. Molnar,A., Csorba,T., Lakatos,L., Varallyay,E., Lacomme,C. and Burgyan,J. (2005) Plant virus-derived small interfering RNAs originate predominantly from highly structured single-stranded viral RNAs. J. Virol., 79, 7812-7818.
41. Burgyan,J., Rubino,L. and Russo,M. (1996) The 5′-terminal region of a tombusvirus genome determines the origin of multivesicular bodies. J. Gen. Virol., 77, 1967-1974.
42. Schaad,M.C., Jensen,P.E. and Carrington,J.C. (1997) Formation of plant RNA virus replication complexes on membranes: Role of an endoplasmic reticulum-targeted viral protein. EMBO J., 16, 4049-4059.
43. Fang,Y. and Spector,D.L. (2007) Identification of nuclear dicing bodies containing proteins for MicroRNA biogenesis in living Arabidopsis plants. Curr. Biol., 17, 1-6.
44. Qi,Y., Denli,A.M. and Hannon,G.J. (2005) Biochemical specialization within Arabidopsis RNA silencing pathways. Mol. Cell, 19, 421-428.
45. Chellappan,P., Vanitharani,R. and Fauquet,C.M. (2005) MicroRNA-binding viral protein interferes with Arabidopsis development. Proc. Natl Acad. Sci. USA, 102, 10381-10386.