Key importance of small RNA binding for the activity of a GW motif-containing RNA silencing suppressor

dc.contributor.affiliationInstituto Universitario Mixto de Biología Molecular y Celular de Plantas
dc.contributor.authorPerez-Cañamas, Mes_ES
dc.contributor.authorHERNANDEZ FORT, CARMEN
dc.contributor.funderMinisterio de Economía y Competitividades_ES
dc.date.accessioned2016-07-25T11:36:21Z
dc.date.available2016-07-25T11:36:21Z
dc.date.issued2015-01-30
dc.description.abstractBackground: GW/WG motif-containing viral suppressors of RNA silencing (VSRs) have been proposed to act through interaction with Argonaute (AGO) proteins. Results: The activity of a GW motif-containing VSR was found to rely on small RNA binding capability rather than on AGO interaction. Conclusion: Overlapping signals in VSRs may lead to misinterpretation of relevant molecular traits. Significance: Knowing primary target(s) of VSRs is critical for better understanding of the host-virus arms race. Viruses express viral suppressors of RNA silencing (VSRs) to counteract RNA silencing-based host defenses. Although virtually all stages of the antiviral silencing pathway can be inhibited by VSRs, small RNAs (sRNAs) and Argonaute (AGO) proteins seem to be the most frequent targets. Recently, GW/WG motifs of some VSRs have been proposed to dictate their suppressor function by mediating interaction with AGO(s). Here we have studied the VSR encoded by Pelargonium line pattern virus (family Tombusviridae). The results show that p37, the viral coat protein, blocks RNA silencing. Site-directed mutagenesis of some p37 sequence traits, including a conserved GW motif, allowed generation of suppressor-competent and -incompetent molecules and uncoupling of the VSR and particle assembly capacities. The engineered mutants were used to assess the importance of p37 functions for viral infection and the relative contribution of diverse molecular interactions to suppressor activity. Two main conclusions can be drawn: (i) the silencing suppression and encapsidation functions of p37 are both required for systemic Pelargonium line pattern virus infection, and (ii) the suppressor activity of p37 relies on the ability to bind sRNAs rather than on interaction with AGOs. The data also caution against potential misinterpretations of results due to overlap of sequence signals related to distinct protein properties. This is well illustrated by mutation of the GW motif in p37 that concurrently affects nucleolar localization, efficient interaction with AGO1, and sRNA binding capability. These concomitant effects could have been overlooked in other GW motif-containing suppressors, as we exemplify with the orthologous p38 of turnip crinkle virus.es_ES
dc.description.accrualMethodSes_ES
dc.description.bibliographicCitationPerez-Cañamas, M.; Hernandez Fort, C. (2015). Key importance of small RNA binding for the activity of a GW motif-containing RNA silencing suppressor. Journal of Biological Chemistry. 290(5):3106-3120. https://doi.org/10.1074/jbc.M114.593707es_ES
dc.description.issue5es_ES
dc.description.referencesBaulcombe, D. (2005). RNA silencing. Trends in Biochemical Sciences, 30(6), 290-293. doi:10.1016/j.tibs.2005.04.012es_ES
dc.description.referencesPickford, A. S., & Cogoni, C. (2003). RNA-mediated gene silencing. Cellular and Molecular Life Sciences, 60(5), 871-882. doi:10.1007/s00018-003-2245-2es_ES
dc.description.referencesBivalkar-Mehla, S., Vakharia, J., Mehla, R., Abreha, M., Kanwar, J. R., Tikoo, A., & Chauhan, A. (2011). Viral RNA silencing suppressors (RSS): Novel strategy of viruses to ablate the host RNA interference (RNAi) defense system. Virus Research, 155(1), 1-9. doi:10.1016/j.virusres.2010.10.003es_ES
dc.description.referencesDing, S.-W., & Voinnet, O. (2007). Antiviral Immunity Directed by Small RNAs. Cell, 130(3), 413-426. doi:10.1016/j.cell.2007.07.039es_ES
dc.description.referencesLu, R., Maduro, M., Li, F., Li, H. W., Broitman-Maduro, G., Li, W. X., & Ding, S. W. (2005). Animal virus replication and RNAi-mediated antiviral silencing in Caenorhabditis elegans. Nature, 436(7053), 1040-1043. doi:10.1038/nature03870es_ES
dc.description.referencesSegers, G. C., Zhang, X., Deng, F., Sun, Q., & Nuss, D. L. (2007). Evidence that RNA silencing functions as an antiviral defense mechanism in fungi. Proceedings of the National Academy of Sciences, 104(31), 12902-12906. doi:10.1073/pnas.0702500104es_ES
dc.description.referencesWang, X.-H., Aliyari, R., Li, W.-X., Li, H.-W., Kim, K., Carthew, R., … Ding, S.-W. (2006). RNA Interference Directs Innate Immunity Against Viruses in Adult Drosophila. Science, 312(5772), 452-454. doi:10.1126/science.1125694es_ES
dc.description.referencesWu, Q., Wang, X., & Ding, S.-W. (2010). Viral Suppressors of RNA-Based Viral Immunity: Host Targets. Cell Host & Microbe, 8(1), 12-15. doi:10.1016/j.chom.2010.06.009es_ES
dc.description.referencesDing, S.-W. (2010). RNA-based antiviral immunity. Nature Reviews Immunology, 10(9), 632-644. doi:10.1038/nri2824es_ES
dc.description.referencesBaumberger, N., & Baulcombe, D. C. (2005). Arabidopsis ARGONAUTE1 is an RNA Slicer that selectively recruits microRNAs and short interfering RNAs. Proceedings of the National Academy of Sciences, 102(33), 11928-11933. doi:10.1073/pnas.0505461102es_ES
dc.description.referencesQi, Y., Denli, A. M., & Hannon, G. J. (2005). Biochemical Specialization within Arabidopsis RNA Silencing Pathways. Molecular Cell, 19(3), 421-428. doi:10.1016/j.molcel.2005.06.014es_ES
dc.description.referencesVaucheret, H. (2008). Plant ARGONAUTES. Trends in Plant Science, 13(7), 350-358. doi:10.1016/j.tplants.2008.04.007es_ES
dc.description.referencesGhildiyal, M., & Zamore, P. D. (2009). Small silencing RNAs: an expanding universe. Nature Reviews Genetics, 10(2), 94-108. doi:10.1038/nrg2504es_ES
dc.description.referencesLipardi, C., Wei, Q., & Paterson, B. M. (2001). RNAi as Random Degradative PCR. Cell, 107(3), 297-307. doi:10.1016/s0092-8674(01)00537-2es_ES
dc.description.referencesMoissiard, G., Parizotto, E. A., Himber, C., & 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(8), 1268-1278. doi:10.1261/rna.541307es_ES
dc.description.referencesDeleris, A., Gallego-Bartolome, J., Bao, J., Kasschau, K. D., Carrington, J. C., & Voinnet, O. (2006). Hierarchical Action and Inhibition of Plant Dicer-Like Proteins in Antiviral Defense. Science, 313(5783), 68-71. doi:10.1126/science.1128214es_ES
dc.description.referencesGarcia-Ruiz, H., Takeda, A., Chapman, E. J., Sullivan, C. M., Fahlgren, N., Brempelis, K. J., & 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. The Plant Cell, 22(2), 481-496. doi:10.1105/tpc.109.073056es_ES
dc.description.referencesHarvey, J. J. W., Lewsey, M. G., Patel, K., Westwood, J., Heimstädt, S., Carr, J. P., & Baulcombe, D. C. (2011). An Antiviral Defense Role of AGO2 in Plants. PLoS ONE, 6(1), e14639. doi:10.1371/journal.pone.0014639es_ES
dc.description.referencesJaubert, M., Bhattacharjee, S., Mello, A. F. S., Perry, K. L., & Moffett, P. (2011). ARGONAUTE2 Mediates RNA-Silencing Antiviral Defenses against Potato virus X in Arabidopsis. Plant Physiology, 156(3), 1556-1564. doi:10.1104/pp.111.178012es_ES
dc.description.referencesQu, F., Ye, X., & Morris, T. J. (2008). Arabidopsis DRB4, AGO1, AGO7, and RDR6 participate in a DCL4-initiated antiviral RNA silencing pathway negatively regulated by DCL1. Proceedings of the National Academy of Sciences, 105(38), 14732-14737. doi:10.1073/pnas.0805760105es_ES
dc.description.referencesScholthof, H. B., Alvarado, V. Y., Vega-Arreguin, J. C., Ciomperlik, J., Odokonyero, D., Brosseau, C., … Moffett, P. (2011). Identification of an ARGONAUTE for Antiviral RNA Silencing in Nicotiana benthamiana. Plant Physiology, 156(3), 1548-1555. doi:10.1104/pp.111.178764es_ES
dc.description.referencesWang, X.-B., Jovel, J., Udomporn, P., Wang, Y., Wu, Q., Li, W.-X., … 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. The Plant Cell, 23(4), 1625-1638. doi:10.1105/tpc.110.082305es_ES
dc.description.referencesLi, F., & Ding, S.-W. (2006). Virus Counterdefense: Diverse Strategies for Evading the RNA-Silencing Immunity. Annual Review of Microbiology, 60(1), 503-531. doi:10.1146/annurev.micro.60.080805.142205es_ES
dc.description.referencesAlvarado, V., & Scholthof, H. B. (2009). Plant responses against invasive nucleic acids: RNA silencing and its suppression by plant viral pathogens. Seminars in Cell & Developmental Biology, 20(9), 1032-1040. doi:10.1016/j.semcdb.2009.06.001es_ES
dc.description.referencesQu, F., & Morris, T. J. (2005). Suppressors of RNA silencing encoded by plant viruses and their role in viral infections. FEBS Letters, 579(26), 5958-5964. doi:10.1016/j.febslet.2005.08.041es_ES
dc.description.referencesMangwende, T., Wang, M.-L., Borth, W., Hu, J., Moore, P. H., Mirkov, T. E., & Albert, H. H. (2009). The P0 gene of Sugarcane yellow leaf virus encodes an RNA silencing suppressor with unique activities. Virology, 384(1), 38-50. doi:10.1016/j.virol.2008.10.034es_ES
dc.description.referencesMartinez-Turino, S., & Hernandez, C. (2009). Inhibition of RNA silencing by the coat protein of Pelargonium flower break virus: distinctions from closely related suppressors. Journal of General Virology, 90(2), 519-525. doi:10.1099/vir.0.006098-0es_ES
dc.description.referencesSenshu, H., Ozeki, J., Komatsu, K., Hashimoto, M., Hatada, K., Aoyama, M., … Namba, S. (2009). Variability in the level of RNA silencing suppression caused by triple gene block protein 1 (TGBp1) from various potexviruses during infection. Journal of General Virology, 90(4), 1014-1024. doi:10.1099/vir.0.008243-0es_ES
dc.description.referencesCuellar, W. J., Tairo, F., Kreuze, J. F., & Valkonen, J. P. T. (2008). Analysis of gene content in sweet potato chlorotic stunt virus RNA1 reveals the presence of the p22 RNA silencing suppressor in only a few isolates: implications for viral evolution and synergism. Journal of General Virology, 89(2), 573-582. doi:10.1099/vir.0.83471-0es_ES
dc.description.referencesMarques, N. T., Costa, Â. A., Lopes, D., Silva, G., & Nolasco, G. (2012). Comparing p20’s RNA silencing suppressing activity among five phylogenetic groups of Citrus Tristeza virus. European Journal of Plant Pathology, 133(1), 229-235. doi:10.1007/s10658-011-9877-0es_ES
dc.description.referencesBurgyán, J., & Havelda, Z. (2011). Viral suppressors of RNA silencing. Trends in Plant Science, 16(5), 265-272. doi:10.1016/j.tplants.2011.02.010es_ES
dc.description.referencesPumplin, N., & Voinnet, O. (2013). RNA silencing suppression by plant pathogens: defence, counter-defence and counter-counter-defence. Nature Reviews Microbiology, 11(11), 745-760. doi:10.1038/nrmicro3120es_ES
dc.description.referencesVargason, J. M., Szittya, G., Burgyán, J., & Hall, T. M. T. (2003). Size Selective Recognition of siRNA by an RNA Silencing Suppressor. Cell, 115(7), 799-811. doi:10.1016/s0092-8674(03)00984-xes_ES
dc.description.referencesYe, K., Malinina, L., & Patel, D. J. (2003). Recognition of small interfering RNA by a viral suppressor of RNA silencing. Nature, 426(6968), 874-878. doi:10.1038/nature02213es_ES
dc.description.referencesCsorba, T., Bovi, A., Dalmay, T., & Burgyan, J. (2007). The p122 Subunit of Tobacco Mosaic Virus Replicase Is a Potent Silencing Suppressor and Compromises both Small Interfering RNA- and MicroRNA-Mediated Pathways. Journal of Virology, 81(21), 11768-11780. doi:10.1128/jvi.01230-07es_ES
dc.description.referencesHemmes, H., Lakatos, L., Goldbach, R., Burgyan, J., & Prins, M. (2007). The NS3 protein of Rice hoja blanca tenuivirus suppresses RNA silencing in plant and insect hosts by efficiently binding both siRNAs and miRNAs. RNA, 13(7), 1079-1089. doi:10.1261/rna.444007es_ES
dc.description.referencesLakatos, L., Csorba, T., Pantaleo, V., Chapman, E. J., Carrington, J. C., Liu, Y.-P., … Burgyán, J. (2006). Small RNA binding is a common strategy to suppress RNA silencing by several viral suppressors. The EMBO Journal, 25(12), 2768-2780. doi:10.1038/sj.emboj.7601164es_ES
dc.description.referencesMerai, Z., Kerenyi, Z., Kertesz, S., Magna, M., Lakatos, L., & Silhavy, D. (2006). Double-Stranded RNA Binding May Be a General Plant RNA Viral Strategy To Suppress RNA Silencing. Journal of Virology, 80(12), 5747-5756. doi:10.1128/jvi.01963-05es_ES
dc.description.referencesChao, J. A., Lee, J. H., Chapados, B. R., Debler, E. W., Schneemann, A., & Williamson, J. R. (2005). Dual modes of RNA-silencing suppression by Flock House virus protein B2. Nature Structural & Molecular Biology, 12(11), 952-957. doi:10.1038/nsmb1005es_ES
dc.description.referencesMerai, Z., Kerenyi, Z., Molnar, A., Barta, E., Valoczi, A., Bisztray, G., … Silhavy, D. (2005). Aureusvirus P14 Is an Efficient RNA Silencing Suppressor That Binds Double-Stranded RNAs without Size Specificity. Journal of Virology, 79(11), 7217-7226. doi:10.1128/jvi.79.11.7217-7226.2005es_ES
dc.description.referencesHaas, G., Azevedo, J., Moissiard, G., Geldreich, A., Himber, C., Bureau, M., … Voinnet, O. (2008). Nuclear import of CaMV P6 is required for infection and suppression of the RNA silencing factor DRB4. The EMBO Journal, 27(15), 2102-2112. doi:10.1038/emboj.2008.129es_ES
dc.description.referencesZhang, X., Yuan, Y.-R., Pei, Y., Lin, S.-S., Tuschl, T., Patel, D. J., & Chua, N.-H. (2006). Cucumber mosaic virus-encoded 2b suppressor inhibits Arabidopsis Argonaute1 cleavage activity to counter plant defense. Genes & Development, 20(23), 3255-3268. doi:10.1101/gad.1495506es_ES
dc.description.referencesBaumberger, N., Tsai, C.-H., Lie, M., Havecker, E., & Baulcombe, D. C. (2007). The Polerovirus Silencing Suppressor P0 Targets ARGONAUTE Proteins for Degradation. Current Biology, 17(18), 1609-1614. doi:10.1016/j.cub.2007.08.039es_ES
dc.description.referencesBortolamiol, D., Pazhouhandeh, M., Marrocco, K., Genschik, P., & Ziegler-Graff, V. (2007). The Polerovirus F Box Protein P0 Targets ARGONAUTE1 to Suppress RNA Silencing. Current Biology, 17(18), 1615-1621. doi:10.1016/j.cub.2007.07.061es_ES
dc.description.referencesCsorba, T., Lózsa, R., Hutvágner, G., & Burgyán, J. (2010). Polerovirus protein P0 prevents the assembly of small RNA-containing RISC complexes and leads to degradation of ARGONAUTE1. The Plant Journal, 62(3), 463-472. doi:10.1111/j.1365-313x.2010.04163.xes_ES
dc.description.referencesAzevedo, J., Garcia, D., Pontier, D., Ohnesorge, S., Yu, A., Garcia, S., … Voinnet, O. (2010). Argonaute quenching and global changes in Dicer homeostasis caused by a pathogen-encoded GW repeat protein. Genes & Development, 24(9), 904-915. doi:10.1101/gad.1908710es_ES
dc.description.referencesGiner, A., Lakatos, L., García-Chapa, M., López-Moya, J. J., & Burgyán, J. (2010). Viral Protein Inhibits RISC Activity by Argonaute Binding through Conserved WG/GW Motifs. PLoS Pathogens, 6(7), e1000996. doi:10.1371/journal.ppat.1000996es_ES
dc.description.referencesEl-Shami, M., Pontier, D., Lahmy, S., Braun, L., Picart, C., Vega, D., … Lagrange, T. (2007). Reiterated WG/GW motifs form functionally and evolutionarily conserved ARGONAUTE-binding platforms in RNAi-related components. Genes & Development, 21(20), 2539-2544. doi:10.1101/gad.451207es_ES
dc.description.referencesRochon D. Lommel S. Martelli G. P. Rubino L. Russo M. (2012) Family Tombusvirdae . in Ninth Report of the International Committee on Taxonomy of Viruses, pp. 1111–1138, Elsevier Academic Press, San Diego, CAes_ES
dc.description.referencesCasta�o, A., & Hern�ndez, C. (2005). Complete nucleotide sequence and genome organization of Pelargonium line pattern virus and its relationship with the family Tombusviridae. Archives of Virology, 150(5), 949-965. doi:10.1007/s00705-004-0464-yes_ES
dc.description.referencesCastaño, A., Ruiz, L., & Hernández, C. (2009). Insights into the translational regulation of biologically active open reading frames of Pelargonium line pattern virus. Virology, 386(2), 417-426. doi:10.1016/j.virol.2009.01.017es_ES
dc.description.referencesKinard, G., & Jordan, R. (2002). GENOME ORGANIZATION OF PELARGONIUM CHLOROTIC RING PATTERN VIRUS: FURTHER IMPLICATIONS FOR TOMBUSVIRIDAE TAXONOMY. Acta Horticulturae, (568), 17-27. doi:10.17660/actahortic.2002.568.1es_ES
dc.description.referencesQu, F., Ren, T., & Morris, T. J. (2003). The Coat Protein of Turnip Crinkle Virus Suppresses Posttranscriptional Gene Silencing at an Early Initiation Step. Journal of Virology, 77(1), 511-522. doi:10.1128/jvi.77.1.511-522.2003es_ES
dc.description.referencesMeng, C. (2006). Host-induced avirulence of hibiscus chlorotic ringspot virus mutants correlates with reduced gene-silencing suppression activity. Journal of General Virology, 87(2), 451-459. doi:10.1099/vir.0.81578-0es_ES
dc.description.referencesVoinnet, O., Pinto, Y. M., & Baulcombe, D. C. (1999). Suppression of gene silencing: A general strategy used by diverse DNA and RNA viruses of plants. Proceedings of the National Academy of Sciences, 96(24), 14147-14152. doi:10.1073/pnas.96.24.14147es_ES
dc.description.referencesTakeda, A., Tsukuda, M., Mizumoto, H., Okamoto, K., Kaido, M., Mise, K., & Okuno, T. (2005). A plant RNA virus suppresses RNA silencing through viral RNA replication. The EMBO Journal, 24(17), 3147-3157. doi:10.1038/sj.emboj.7600776es_ES
dc.description.referencesPowers, J. G., Sit, T. L., Heinsohn, C., George, C. G., Kim, K.-H., & Lommel, S. A. (2008). The Red clover necrotic mosaic virus RNA-2 encoded movement protein is a second suppressor of RNA silencing. Virology, 381(2), 277-286. doi:10.1016/j.virol.2008.09.004es_ES
dc.description.referencesKnoester, M., van Loon, L. C., van den Heuvel, J., Hennig, J., Bol, J. F., & Linthorst, H. J. M. (1998). Ethylene-insensitive tobacco lacks nonhost resistance against soil-borne fungi. Proceedings of the National Academy of Sciences, 95(4), 1933-1937. doi:10.1073/pnas.95.4.1933es_ES
dc.description.referencesSambrock J. Fritsch E. F. Maniatis T. (2001) Molecular Cloning: A Laboratory Manual, 3rd Ed., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NYes_ES
dc.description.referencesPowers, J. G., Sit, T. L., Qu, F., Morris, T. J., Kim, K.-H., & Lommel, S. A. (2008). A Versatile Assay for the Identification of RNA Silencing Suppressors Based on Complementation of Viral Movement. Molecular Plant-Microbe Interactions, 21(7), 879-890. doi:10.1094/mpmi-21-7-0879es_ES
dc.description.referencesGonzález, I., Martínez, L., Rakitina, D. V., Lewsey, M. G., Atencio, F. A., Llave, C., … Canto, T. (2010). Cucumber Mosaic Virus 2b Protein Subcellular Targets and Interactions: Their Significance to RNA Silencing Suppressor Activity. Molecular Plant-Microbe Interactions, 23(3), 294-303. doi:10.1094/mpmi-23-3-0294es_ES
dc.description.referencesKim, S. H., MacFarlane, S., Kalinina, N. O., Rakitina, D. V., Ryabov, E. V., Gillespie, T., … Taliansky, M. (2007). Interaction of a plant virus-encoded protein with the major nucleolar protein fibrillarin is required for systemic virus infection. Proceedings of the National Academy of Sciences, 104(26), 11115-11120. doi:10.1073/pnas.0704632104es_ES
dc.description.referencesVerwoerd, T. C., Dekker, B. M. M., & Hoekema, A. (1989). A small-scale procedure for the rapid isolation of plant RNAs. Nucleic Acids Research, 17(6), 2362-2362. doi:10.1093/nar/17.6.2362es_ES
dc.description.referencesIvars, P., Alonso, M., Borja, M., & Hernández, C. (2004). Development of a Non-radioactive Dot-blot Hybridisation Assay for the Detection of Pelargonium Flower Break Virus and Pelargonium line Pattern Virus. European Journal of Plant Pathology, 110(3), 275-283. doi:10.1023/b:ejpp.0000019798.87567.22es_ES
dc.description.referencesMartínez-Turiño, S., & Hernández, C. (2011). A membrane-associated movement protein of Pelargonium flower break virus shows RNA-binding activity and contains a biologically relevant leucine zipper-like motif. Virology, 413(2), 310-319. doi:10.1016/j.virol.2011.03.001es_ES
dc.description.referencesJohansen, L. K., & Carrington, J. C. (2001). Silencing on the Spot. Induction and Suppression of RNA Silencing in the Agrobacterium-Mediated Transient Expression System. Plant Physiology, 126(3), 930-938. doi:10.1104/pp.126.3.930es_ES
dc.description.referencesChen, H.-Y., Yang, J., Lin, C., & Yuan, Y. A. (2008). Structural basis for RNA-silencing suppression by Tomato aspermy virus protein 2b. EMBO reports, 9(8), 754-760. doi:10.1038/embor.2008.118es_ES
dc.description.referencesVaewhongs, A. A., & Lommel, S. A. (1995). Virion Formation Is Required for the Long-Distance Movement of Red Clover Necrotic Mosaic Virus in Movement Protein Transgenic Plants. Virology, 212(2), 607-613. doi:10.1006/viro.1995.1518es_ES
dc.description.referencesCao, M., Ye, X., Willie, K., Lin, J., Zhang, X., Redinbaugh, M. G., … Qu, F. (2010). The Capsid Protein of Turnip Crinkle Virus Overcomes Two Separate Defense Barriers To Facilitate Systemic Movement of the Virus in Arabidopsis. Journal of Virology, 84(15), 7793-7802. doi:10.1128/jvi.02643-09es_ES
dc.description.referencesValli, A., Dujovny, G., & Garcia, J. A. (2007). Protease Activity, Self Interaction, and Small Interfering RNA Binding of the Silencing Suppressor P1b from Cucumber Vein Yellowing Ipomovirus. Journal of Virology, 82(2), 974-986. doi:10.1128/jvi.01664-07es_ES
dc.description.referencesTakeda, A., Sugiyama, K., Nagano, H., Mori, M., Kaido, M., Mise, K., … Okuno, T. (2002). Identification of a novel RNA silencing suppressor, NSs protein of Tomato spotted wilt virus. FEBS Letters, 532(1-2), 75-79. doi:10.1016/s0014-5793(02)03632-3es_ES
dc.description.referencesLucy, A. P. (2000). Suppression of post-transcriptional gene silencing by a plant viral protein localized in the nucleus. The EMBO Journal, 19(7), 1672-1680. doi:10.1093/emboj/19.7.1672es_ES
dc.description.referencesWang, Y. (2004). Functional analysis of the Cucumber mosaic virus 2b protein: pathogenicity and nuclear localization. Journal of General Virology, 85(10), 3135-3147. doi:10.1099/vir.0.80250-0es_ES
dc.description.referencesXu, A., Zhao, Z., Chen, W., Zhang, H., Liao, Q., Chen, J., … Du, Z. (2013). Self-interaction of the cucumber mosaic virus 2b protein plays a vital role in the suppression of RNA silencing and the induction of viral symptoms. Molecular Plant Pathology, 14(8), 803-812. doi:10.1111/mpp.12051es_ES
dc.description.referencesHamera, S., Song, X., Su, L., Chen, X., & Fang, R. (2011). Cucumber mosaic virus suppressor 2b binds to AGO4-related small RNAs and impairs AGO4 activities. The Plant Journal, 69(1), 104-115. doi:10.1111/j.1365-313x.2011.04774.xes_ES
dc.description.referencesThomas, C. L., Leh, V., Lederer, C., & Maule, A. J. (2003). Turnip crinkle virus coat protein mediates suppression of RNA silencing in nicotiana benthamiana. Virology, 306(1), 33-41. doi:10.1016/s0042-6822(02)00018-1es_ES
dc.description.referencesGonzalez, I., Rakitina, D., Semashko, M., Taliansky, M., Praveen, S., Palukaitis, P., … Canto, T. (2012). RNA binding is more critical to the suppression of silencing function of Cucumber mosaic virus 2b protein than nuclear localization. RNA, 18(4), 771-782. doi:10.1261/rna.031260.111es_ES
dc.description.referencesChiba, S., Hleibieh, K., Delbianco, A., Klein, E., Ratti, C., Ziegler-Graff, V., … Gilmer, D. (2013). The Benyvirus RNA Silencing Suppressor Is Essential for Long-Distance Movement, Requires Both Zinc-Finger and NoLS Basic Residues but Not a Nucleolar Localization for Its Silencing-Suppression Activity. Molecular Plant-Microbe Interactions, 26(2), 168-181. doi:10.1094/mpmi-06-12-0142-res_ES
dc.description.referencesRuiz-Ruiz, S., Soler, N., Sánchez-Navarro, J., Fagoaga, C., López, C., Navarro, L., … Flores, R. (2013). Citrus tristeza virus p23: Determinants for Nucleolar Localization and Their Influence on Suppression of RNA Silencing and Pathogenesis. Molecular Plant-Microbe Interactions, 26(3), 306-318. doi:10.1094/mpmi-08-12-0201-res_ES
dc.description.referencesBRAGG, J. N., & JACKSON, A. O. (2004). The C-terminal region of the Barley stripe mosaic virusgammab protein participates in homologous interactions and is required for suppression of RNA silencing. Molecular Plant Pathology, 5(5), 465-481. doi:10.1111/j.1364-3703.2004.00246.xes_ES
dc.description.referencesDuan, C.-G., Fang, Y.-Y., Zhou, B.-J., Zhao, J.-H., Hou, W.-N., Zhu, H., … Guo, H.-S. (2012). Suppression of Arabidopsis ARGONAUTE1-Mediated Slicing, Transgene-Induced RNA Silencing, and DNA Methylation by Distinct Domains of the Cucumber mosaic virus 2b Protein. The Plant Cell, 24(1), 259-274. doi:10.1105/tpc.111.092718es_ES
dc.description.referencesVogler, H., Akbergenov, R., Shivaprasad, P. V., Dang, V., Fasler, M., Kwon, M.-O., … Heinlein, M. (2007). Modification of Small RNAs Associated with Suppression of RNA Silencing by Tobamovirus Replicase Protein. Journal of Virology, 81(19), 10379-10388. doi:10.1128/jvi.00727-07es_ES
dc.description.referencesEndres, M. W., Gregory, B. D., Gao, Z., Foreman, A. W., Mlotshwa, S., Ge, X., … Vance, V. (2010). Two Plant Viral Suppressors of Silencing Require the Ethylene-Inducible Host Transcription Factor RAV2 to Block RNA Silencing. PLoS Pathogens, 6(1), e1000729. doi:10.1371/journal.ppat.1000729es_ES
dc.description.referencesDalmay, T. (1992). Replication and Movement of a Coat Protein Mutant of Cymbidium Ringspot Tombusvirus. Molecular Plant-Microbe Interactions, 5(5), 379. doi:10.1094/mpmi-5-379es_ES
dc.description.referencesHacker, D. L., Petty, I. T. D., Wei, N., & Morris, T. J. (1992). Turnip crinkle virus genes required for RNA replication and virus movement. Virology, 186(1), 1-8. doi:10.1016/0042-6822(92)90055-tes_ES
dc.description.referencesMoln√°r, A., Burgy√°n, J., Havelda, Z., Dalmay, T., & Szutorisz, H. (1997). Complete nucleotide sequence of tobacco necrosis virus strain DH and genes required for RNA replication and virus movement. Journal of General Virology, 78(6), 1235-1239. doi:10.1099/0022-1317-78-6-1235es_ES
dc.description.referencesReade, R., Miller, J., Robbins, M., Xiang, Y., & Rochon, D. (2003). Molecular analysis of the cucumber leaf spot virus genome. Virus Research, 91(2), 171-179. doi:10.1016/s0168-1702(02)00251-4es_ES
dc.description.referencesRubino, L., & Russo, M. (1997). Molecular analysis of the pothos latent virus genome. Journal of General Virology, 78(6), 1219-1226. doi:10.1099/0022-1317-78-6-1219es_ES
dc.description.referencesSit, T. L., Johnston, J. C., Ter Borg, M. G., Frison, E., McLean, M. A., & Rochon, D. (1995). Mutational analysis of the cucumber necrosis virus coat protein gene. Virology, 206(1), 38-48. doi:10.1016/s0042-6822(95)80017-4es_ES
dc.description.referencesBrigneti, G. (1998). Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana. The EMBO Journal, 17(22), 6739-6746. doi:10.1093/emboj/17.22.6739es_ES
dc.description.referencesJay, F., Wang, Y., Yu, A., Taconnat, L., Pelletier, S., Colot, V., … Voinnet, O. (2011). Misregulation of AUXIN RESPONSE FACTOR 8 Underlies the Developmental Abnormalities Caused by Three Distinct Viral Silencing Suppressors in Arabidopsis. PLoS Pathogens, 7(5), e1002035. doi:10.1371/journal.ppat.1002035es_ES
dc.description.referencesKasschau, K. D., Xie, Z., Allen, E., Llave, C., Chapman, E. J., Krizan, K. A., & Carrington, J. C. (2003). P1/HC-Pro, a Viral Suppressor of RNA Silencing, Interferes with Arabidopsis Development and miRNA Function. Developmental Cell, 4(2), 205-217. doi:10.1016/s1534-5807(03)00025-xes_ES
dc.description.referencesAlonso, M., & Borja, M. (2005). High incidence of Pelargonium line pattern virus infecting asymptomatic Pelargonium spp. in Spain. European Journal of Plant Pathology, 112(2), 95-100. doi:10.1007/s10658-005-0803-1es_ES
dc.description.sponsorshipThis work was supported by Grant BFU2012-36095 from the Ministerio de Economia y Competitividad (MINECO, Spain) ( to C. H.).en_EN
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dc.identifier.doi10.1074/jbc.M114.593707
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dc.languageIngléses_ES
dc.publisherAmerican Society for Biochemistry and Molecular Biologyes_ES
dc.relation.ispartofJournal of Biological Chemistryes_ES
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dc.relation.references10.1016/j.tibs.2005.04.012es_ES
dc.relation.references10.1007/s00018-003-2245-2es_ES
dc.relation.references10.1016/j.virusres.2010.10.003es_ES
dc.relation.references10.1016/j.cell.2007.07.039es_ES
dc.relation.references10.1038/nature03870es_ES
dc.relation.references10.1073/pnas.0702500104es_ES
dc.relation.references10.1126/science.1125694es_ES
dc.relation.references10.1016/j.chom.2010.06.009es_ES
dc.relation.references10.1038/nri2824es_ES
dc.relation.references10.1073/pnas.0505461102es_ES
dc.relation.references10.1016/j.molcel.2005.06.014es_ES
dc.relation.references10.1016/j.tplants.2008.04.007es_ES
dc.relation.references10.1038/nrg2504es_ES
dc.relation.references10.1016/S0092-8674(01)00537-2es_ES
dc.relation.references10.1261/rna.541307es_ES
dc.relation.references10.1126/science.1128214es_ES
dc.relation.references10.1105/tpc.109.073056es_ES
dc.relation.references10.1371/journal.pone.0014639es_ES
dc.relation.references10.1104/pp.111.178012es_ES
dc.relation.references10.1073/pnas.0805760105es_ES
dc.relation.references10.1104/pp.111.178764es_ES
dc.relation.references10.1105/tpc.110.082305es_ES
dc.relation.references10.1146/annurev.micro.60.080805.142205es_ES
dc.relation.references10.1016/j.semcdb.2009.06.001es_ES
dc.relation.references10.1016/j.febslet.2005.08.041es_ES
dc.relation.references10.1016/j.virol.2008.10.034es_ES
dc.relation.references10.1099/vir.0.006098-0es_ES
dc.relation.references10.1099/vir.0.008243-0es_ES
dc.relation.references10.1099/vir.0.83471-0es_ES
dc.relation.references10.1007/s10658-011-9877-0es_ES
dc.relation.references10.1016/j.tplants.2011.02.010es_ES
dc.relation.references10.1038/nrmicro3120es_ES
dc.relation.references10.1016/S0092-8674(03)00984-Xes_ES
dc.relation.references10.1038/nature02213es_ES
dc.relation.references10.1128/JVI.01230-07es_ES
dc.relation.references10.1261/rna.444007es_ES
dc.relation.references10.1038/sj.emboj.7601164es_ES
dc.relation.references10.1128/JVI.01963-05es_ES
dc.relation.references10.1038/nsmb1005es_ES
dc.relation.references10.1128/JVI.79.11.7217-7226.2005es_ES
dc.relation.references10.1038/emboj.2008.129es_ES
dc.relation.references10.1101/gad.1495506es_ES
dc.relation.references10.1016/j.cub.2007.08.039es_ES
dc.relation.references10.1016/j.cub.2007.07.061es_ES
dc.relation.references10.1111/j.1365-313X.2010.04163.xes_ES
dc.relation.references10.1101/gad.1908710es_ES
dc.relation.references10.1371/journal.ppat.1000996es_ES
dc.relation.references10.1101/gad.451207es_ES
dc.relation.references10.1007/s00705-004-0464-yes_ES
dc.relation.references10.1016/j.virol.2009.01.017es_ES
dc.relation.references10.17660/ActaHortic.2002.568.1es_ES
dc.relation.references10.1128/JVI.77.1.511-522.2003es_ES
dc.relation.references10.1099/vir.0.81578-0es_ES
dc.relation.references10.1073/pnas.96.24.14147es_ES
dc.relation.references10.1038/sj.emboj.7600776es_ES
dc.relation.references10.1016/j.virol.2008.09.004es_ES
dc.relation.references10.1073/pnas.95.4.1933es_ES
dc.relation.references10.1094/MPMI-21-7-0879es_ES
dc.relation.references10.1094/MPMI-23-3-0294es_ES
dc.relation.references10.1073/pnas.0704632104es_ES
dc.relation.references10.1093/nar/17.6.2362es_ES
dc.relation.references10.1023/B:EJPP.0000019798.87567.22es_ES
dc.relation.references10.1016/j.virol.2011.03.001es_ES
dc.relation.references10.1104/pp.126.3.930es_ES
dc.relation.references10.1038/embor.2008.118es_ES
dc.relation.references10.1006/viro.1995.1518es_ES
dc.relation.references10.1128/JVI.02643-09es_ES
dc.relation.references10.1128/JVI.01664-07es_ES
dc.relation.references10.1016/S0014-5793(02)03632-3es_ES
dc.relation.references10.1093/emboj/19.7.1672es_ES
dc.relation.references10.1099/vir.0.80250-0es_ES
dc.relation.references10.1111/mpp.12051es_ES
dc.relation.references10.1111/j.1365-313X.2011.04774.xes_ES
dc.relation.references10.1016/S0042-6822(02)00018-1es_ES
dc.relation.references10.1261/rna.031260.111es_ES
dc.relation.references10.1094/MPMI-06-12-0142-Res_ES
dc.relation.references10.1094/MPMI-08-12-0201-Res_ES
dc.relation.references10.1111/j.1364-3703.2004.00246.xes_ES
dc.relation.references10.1105/tpc.111.092718es_ES
dc.relation.references10.1128/JVI.00727-07es_ES
dc.relation.references10.1371/journal.ppat.1000729es_ES
dc.relation.references10.1094/MPMI-5-379es_ES
dc.relation.references10.1016/0042-6822(92)90055-Tes_ES
dc.relation.references10.1099/0022-1317-78-6-1235es_ES
dc.relation.references10.1016/S0168-1702(02)00251-4es_ES
dc.relation.references10.1099/0022-1317-78-6-1219es_ES
dc.relation.references10.1016/S0042-6822(95)80017-4es_ES
dc.relation.references10.1093/emboj/17.22.6739es_ES
dc.relation.references10.1371/journal.ppat.1002035es_ES
dc.relation.references10.1016/S1534-5807(03)00025-Xes_ES
dc.relation.references10.1007/s10658-005-0803-1es_ES
dc.relation.senia305708es_ES
dc.rightsReserva de todos los derechoses_ES
dc.rights.accessRightsAbiertoes_ES
dc.subjectArgonautees_ES
dc.subjectHost-Pathogen Interactiones_ES
dc.subjectNucleoluses_ES
dc.subjectPlant Viruses_ES
dc.subjectRNA Viruses_ES
dc.subjectGWes_ES
dc.subjectWG Motifses_ES
dc.subjectPelargonium Line Pattern Viruses_ES
dc.subjectCoat Proteines_ES
dc.subjectsRNA Bindinges_ES
dc.subjectViral Suppressor of RNA Silencinges_ES
dc.titleKey importance of small RNA binding for the activity of a GW motif-containing RNA silencing suppressores_ES
dc.typeArtículoes_ES
dc.type.versioninfo:eu-repo/semantics/publishedVersiones_ES
dspace.entity.typePublication
person.identifier256951
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upv.uuidad15a9f1-62aa-49fb-aafb-e4399bb4413ees_ES

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