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Tempo and mode of plant RNA virus escape from RNA interference-mediated resistance

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Tempo and mode of plant RNA virus escape from RNA interference-mediated resistance

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dc.contributor.author Lafforgue, Guillaume es_ES
dc.contributor.author Martínez García, Fernando es_ES
dc.contributor.author Sardanyes Cayuela, Jose es_ES
dc.contributor.author De la Iglesia Jordán, Francisca es_ES
dc.contributor.author Niu, Qi-Wen es_ES
dc.contributor.author Lin, Shih-Shun es_ES
dc.contributor.author Sole, Ricard V. es_ES
dc.contributor.author Chua, Nam-Hai es_ES
dc.contributor.author Daros Arnau, Jose Antonio es_ES
dc.contributor.author Elena Fito, Santiago Fco es_ES
dc.date.accessioned 2013-12-16T13:44:15Z
dc.date.available 2013-12-16T13:44:15Z
dc.date.issued 2011
dc.identifier.issn 0022-538X
dc.identifier.uri http://hdl.handle.net/10251/34546
dc.description.abstract A biotechnological application of artificial microRNAs (amiRs) is the generation of plants that are resistant to virus infection. This resistance has proven to be highly effective and sequence specific. However, before these transgenic plants can be deployed in the field, it is important to evaluate the likelihood of the emergence of resistance-breaking mutants. Two issues are of particular interest: (i) whether such mutants can arise in nontransgenic plants that may act as reservoirs and (ii) whether a suboptimal expression level of the transgene, resulting in subinhibitory concentrations of the amiR, would favor the emergence of escape mutants. To address the first issue, we experimentally evolved independent lineages of Turnip mosaic virus (TuMV) (family Potyviridae) in fully susceptible wild-type Arabidopsis thaliana plants and then simulated the spillover of the evolving virus to fully resistant A. thaliana transgenic plants. To address the second issue, the evolution phase took place with transgenic plants that expressed the amiR at subinhibitory concentrations. Our results show that TuMV populations replicating in susceptible hosts accumulated resistance-breaking alleles that resulted in the overcoming of the resistance of fully resistant plants. The rate at which resistance was broken was 7 times higher for TuMV populations that experienced subinhibitory concentrations of the antiviral amiR. A molecular characterization of escape alleles showed that they all contained at least one nucleotide substitution in the target sequence, generally a transition of the G-to-A and C-to-U types, with many instances of convergent molecular evolution. To better understand the viral population dynamics taking place within each host, as well as to evaluate relevant population genetic parameters, we performed in silico simulations of the experiments. Together, our results contribute to the rational management of amiR-based antiviral resistance in plants. es_ES
dc.description.sponsorship This work was supported by Human Frontiers Science Program Organization grant RGP12/2008, Generalitat Valenciana grant PROMETEO/2010/019, and CSIC grant 2010TW0015. We also acknowledge support from The Santa Fe Institute. en_EN
dc.language Inglés es_ES
dc.publisher American Society for Microbiology es_ES
dc.relation.ispartof Journal of Virology es_ES
dc.rights Reserva de todos los derechos es_ES
dc.subject Cucumber-mosaic-virus es_ES
dc.subject Antiretroviral resistance es_ES
dc.subject Viral-RNA es_ES
dc.subject Type-1 es_ES
dc.subject Inhibition es_ES
dc.subject Replication es_ES
dc.subject Arabidopsis es_ES
dc.subject Mutations es_ES
dc.subject Efficient es_ES
dc.subject Transcription es_ES
dc.title Tempo and mode of plant RNA virus escape from RNA interference-mediated resistance es_ES
dc.type Artículo es_ES
dc.identifier.doi 10.1128/JVI.05326-11
dc.relation.projectID info:eu-repo/grantAgreement/HFSP//RGP0012%2F2008/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/GVA//PROMETEO%2F2010%2F019/ES/Implicaciones evolutivas de la supresión del silenciamiento del RNA por parte de proteína virales/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/CSIC//2010TW0015/ES/Evaluation of the durability of artificial microRNA-mediated strategies for plant resistance to RNA viruses/ es_ES
dc.rights.accessRights Abierto es_ES
dc.contributor.affiliation Universitat Politècnica de València. Instituto Universitario Mixto de Biología Molecular y Celular de Plantas - Institut Universitari Mixt de Biologia Molecular i Cel·lular de Plantes es_ES
dc.description.bibliographicCitation Lafforgue, G.; Martínez García, F.; Sardanyes Cayuela, J.; De La Iglesia Jordán, F.; Niu, Q.; Lin, S.; Sole, RV.... (2011). Tempo and mode of plant RNA virus escape from RNA interference-mediated resistance. Journal of Virology. 85(19):9686-9695. https://doi.org/10.1128/JVI.05326-11 es_ES
dc.description.accrualMethod S es_ES
dc.relation.publisherversion http://dx.doi.org/10.1128/JVI.05326-11 es_ES
dc.description.upvformatpinicio 9686 es_ES
dc.description.upvformatpfin 9695 es_ES
dc.type.version info:eu-repo/semantics/publishedVersion es_ES
dc.description.volume 85 es_ES
dc.description.issue 19 es_ES
dc.relation.senia 216049
dc.identifier.pmid 21775453 en_EN
dc.identifier.pmcid PMC3196453 en_EN
dc.contributor.funder Human Frontier Science Program Organization es_ES
dc.contributor.funder Generalitat Valenciana es_ES
dc.contributor.funder Consejo Superior de Investigaciones Científicas; National Science Council of Taiwan es_ES
dc.contributor.funder Santa Fe Institute es_ES
dc.description.references Ali, A., Li, H., Schneider, W. L., Sherman, D. J., Gray, S., Smith, D., & Roossinck, M. J. (2006). Analysis of Genetic Bottlenecks during Horizontal Transmission of Cucumber Mosaic Virus. Journal of Virology, 80(17), 8345-8350. doi:10.1128/jvi.00568-06 es_ES
dc.description.references Betancourt, M., Fereres, A., Fraile, A., & Garcia-Arenal, F. (2008). Estimation of the Effective Number of Founders That Initiate an Infection after Aphid Transmission of a Multipartite Plant Virus. Journal of Virology, 82(24), 12416-12421. doi:10.1128/jvi.01542-08 es_ES
dc.description.references Bishop, K. N. (2004). APOBEC-Mediated Editing of Viral RNA. Science, 305(5684), 645-645. doi:10.1126/science.1100658 es_ES
dc.description.references Boden, D., Pusch, O., Lee, F., Tucker, L., & Ramratnam, B. (2003). Human Immunodeficiency Virus Type 1 Escape from RNA Interference. Journal of Virology, 77(21), 11531-11535. doi:10.1128/jvi.77.21.11531-11535.2003 es_ES
dc.description.references Boucher, C. A. B., O’Sullivan, E., Mulder, J. W., Ramautarsing, C., Kellam, P., Darby, G., … Larder, B. A. (1992). Ordered Appearance of Zidovudine Resistance Mutations during Treatment of 18 Human Immunodeficiency Virus-Positive Subjects. Journal of Infectious Diseases, 165(1), 105-110. doi:10.1093/infdis/165.1.105 es_ES
dc.description.references Boyes, D. C. (2001). Growth Stage-Based Phenotypic Analysis of Arabidopsis: A Model for High Throughput Functional Genomics in Plants. THE PLANT CELL ONLINE, 13(7), 1499-1510. doi:10.1105/tpc.13.7.1499 es_ES
dc.description.references Brodersen, P., Sakvarelidze-Achard, L., Bruun-Rasmussen, M., Dunoyer, P., Yamamoto, Y. Y., Sieburth, L., & Voinnet, O. (2008). Widespread Translational Inhibition by Plant miRNAs and siRNAs. Science, 320(5880), 1185-1190. doi:10.1126/science.1159151 es_ES
dc.description.references Burch, C. L., Guyader, S., Samarov, D., & Shen, H. (2007). Experimental Estimate of the Abundance and Effects of Nearly Neutral Mutations in the RNA Virus ϕ6. Genetics, 176(1), 467-476. doi:10.1534/genetics.106.067199 es_ES
dc.description.references Chen, C. C., Chao, C. H., Chen, C. C., Yeh, S. D., Tsai, H. T., & Chang, C. A. (2003). Identification ofTurnip mosaic virusIsolates Causing Yellow Stripe and Spot on Calla Lily. Plant Disease, 87(8), 901-905. doi:10.1094/pdis.2003.87.8.901 es_ES
dc.description.references Chen, Y.-K., Lohuis, D., Goldbach, R., & Prins, M. (2004). High frequency induction of RNA-mediated resistance against Cucumber mosaic virus using inverted repeat constructs. Molecular Breeding, 14(3), 215-226. doi:10.1023/b:molb.0000047769.82881.f5 es_ES
dc.description.references Coburn, G. A., & Cullen, B. R. (2002). Potent and Specific Inhibition of Human Immunodeficiency Virus Type 1 Replication by RNA Interference. Journal of Virology, 76(18), 9225-9231. doi:10.1128/jvi.76.18.9225-9231.2002 es_ES
dc.description.references Conticello, S. G., Thomas, C. J. F., Petersen-Mahrt, S. K., & Neuberger, M. S. (2004). Evolution of the AID/APOBEC Family of Polynucleotide (Deoxy)cytidine Deaminases. Molecular Biology and Evolution, 22(2), 367-377. doi:10.1093/molbev/msi026 es_ES
dc.description.references Couce, A., & Blázquez, J. (2009). Side effects of antibiotics on genetic variability. FEMS Microbiology Reviews, 33(3), 531-538. doi:10.1111/j.1574-6976.2009.00165.x es_ES
dc.description.references Cullen, B. R. (2006). Role and Mechanism of Action of the APOBEC3 Family of Antiretroviral Resistance Factors. Journal of Virology, 80(3), 1067-1076. doi:10.1128/jvi.80.3.1067-1076.2006 es_ES
dc.description.references Das, A. T., Brummelkamp, T. R., Westerhout, E. M., Vink, M., Madiredjo, M., Bernards, R., & Berkhout, B. (2004). Human Immunodeficiency Virus Type 1 Escapes from RNA Interference-Mediated Inhibition. Journal of Virology, 78(5), 2601-2605. doi:10.1128/jvi.78.5.2601-2605.2004 es_ES
dc.description.references Nicola-Negri, E. D., Brunetti, A., Tavazza, M., & Ilardi, V. (2005). Hairpin RNA-Mediated Silencing of Plum pox virus P1 and HC-Pro Genes for Efficient and Predictable Resistance to the Virus. Transgenic Research, 14(6), 989-994. doi:10.1007/s11248-005-1773-y es_ES
dc.description.references Elbashir, S. M. (2001). Functional anatomy of siRNAs for mediating efficient RNAi in Drosophila melanogaster embryo lysate. The EMBO Journal, 20(23), 6877-6888. doi:10.1093/emboj/20.23.6877 es_ES
dc.description.references Elena, S. F., Solé, R. V., & Sardanyés, J. (2010). Simple genomes, complex interactions: Epistasis in RNA virus. Chaos: An Interdisciplinary Journal of Nonlinear Science, 20(2), 026106. doi:10.1063/1.3449300 es_ES
dc.description.references García-Arenal, F., & McDonald, B. A. (2003). An Analysis of the Durability of Resistance to Plant Viruses. Phytopathology, 93(8), 941-952. doi:10.1094/phyto.2003.93.8.941 es_ES
dc.description.references Ge, Q., McManus, M. T., Nguyen, T., Shen, C.-H., Sharp, P. A., Eisen, H. N., & Chen, J. (2003). RNA interference of influenza virus production by directly targeting mRNA for degradation and indirectly inhibiting all viral RNA transcription. Proceedings of the National Academy of Sciences, 100(5), 2718-2723. doi:10.1073/pnas.0437841100 es_ES
dc.description.references Gitlin, L., Stone, J. K., & Andino, R. (2004). Poliovirus Escape from RNA Interference: Short Interfering RNA-Target Recognition and Implications for Therapeutic Approaches. Journal of Virology, 79(2), 1027-1035. doi:10.1128/jvi.79.2.1027-1035.2005 es_ES
dc.description.references Guo, H.-S., Xie, Q., Fei, J.-F., & Chua, N.-H. (2005). MicroRNA Directs mRNA Cleavage of the Transcription Factor NAC1 to Downregulate Auxin Signals for Arabidopsis Lateral Root Development. The Plant Cell, 17(5), 1376-1386. doi:10.1105/tpc.105.030841 es_ES
dc.description.references Hamilton, A. J. (1999). A Species of Small Antisense RNA in Posttranscriptional Gene Silencing in Plants. Science, 286(5441), 950-952. doi:10.1126/science.286.5441.950 es_ES
dc.description.references Haydon, D., Knowles, N., & McCauley, J. (1998). Virus Genes, 16(3), 253-266. doi:10.1023/a:1008018403582 es_ES
dc.description.references Jridi, C., Martin, J.-F., Marie-Jeanne, V., Labonne, G., & Blanc, S. (2006). Distinct Viral Populations Differentiate and Evolve Independently in a Single Perennial Host Plant. Journal of Virology, 80(5), 2349-2357. doi:10.1128/jvi.80.5.2349-2357.2006 es_ES
dc.description.references Kalantidis, K., Psaradakis, S., Tabler, M., & Tsagris, M. (2002). The Occurrence of CMV-Specific Short RNAs in Transgenic Tobacco Expressing Virus-Derived Double-Stranded RNA is Indicative of Resistance to the Virus. Molecular Plant-Microbe Interactions, 15(8), 826-833. doi:10.1094/mpmi.2002.15.8.826 es_ES
dc.description.references Kronke, J., Kittler, R., Buchholz, F., Windisch, M. P., Pietschmann, T., Bartenschlager, R., & Frese, M. (2004). Alternative Approaches for Efficient Inhibition of Hepatitis C Virus RNA Replication by Small Interfering RNAs. Journal of Virology, 78(7), 3436-3446. doi:10.1128/jvi.78.7.3436-3446.2004 es_ES
dc.description.references Lin, S.-S., Wu, H.-W., Elena, S. F., Chen, K.-C., Niu, Q.-W., Yeh, S.-D., … Chua, N.-H. (2009). Molecular Evolution of a Viral Non-Coding Sequence under the Selective Pressure of amiRNA-Mediated Silencing. PLoS Pathogens, 5(2), e1000312. doi:10.1371/journal.ppat.1000312 es_ES
dc.description.references Lindbo, J. A., & Dougherty, W. G. (2005). Plant Pathology and RNAi: A Brief History. Annual Review of Phytopathology, 43(1), 191-204. doi:10.1146/annurev.phyto.43.040204.140228 es_ES
dc.description.references Marin, J., & Sole, R. V. (1999). Macroevolutionary algorithms: a new optimization method on fitness landscapes. IEEE Transactions on Evolutionary Computation, 3(4), 272-286. doi:10.1109/4235.797970 es_ES
dc.description.references Martinez-Picado, J., DePasquale, M. P., Kartsonis, N., Hanna, G. J., Wong, J., Finzi, D., … D’Aquila, R. T. (2000). Antiretroviral resistance during successful therapy of HIV type 1 infection. Proceedings of the National Academy of Sciences, 97(20), 10948-10953. doi:10.1073/pnas.97.20.10948 es_ES
dc.description.references Missiou, A., Kalantidis, K., Boutla, A., Tzortzakaki, S., Tabler, M., & Tsagris, M. (2004). Generation of transgenic potato plants highly resistant to potato virus Y (PVY) through RNA silencing. Molecular Breeding, 14(2), 185-197. doi:10.1023/b:molb.0000038006.32812.52 es_ES
dc.description.references Moury, B., Fabre, F., & Senoussi, R. (2007). Estimation of the number of virus particles transmitted by an insect vector. Proceedings of the National Academy of Sciences, 104(45), 17891-17896. doi:10.1073/pnas.0702739104 es_ES
dc.description.references Niu, Q.-W., Lin, S.-S., Reyes, J. L., Chen, K.-C., Wu, H.-W., Yeh, S.-D., & Chua, N.-H. (2006). Expression of artificial microRNAs in transgenic Arabidopsis thaliana confers virus resistance. Nature Biotechnology, 24(11), 1420-1428. doi:10.1038/nbt1255 es_ES
dc.description.references Qu, J., Ye, J., & Fang, R. (2007). Artificial MicroRNA-Mediated Virus Resistance in Plants. Journal of Virology, 81(12), 6690-6699. doi:10.1128/jvi.02457-06 es_ES
dc.description.references Sabariegos, R., Gimenez-Barcons, M., Tapia, N., Clotet, B., & Martinez, M. A. (2005). Sequence Homology Required by Human Immunodeficiency Virus Type 1 To Escape from Short Interfering RNAs. Journal of Virology, 80(2), 571-577. doi:10.1128/jvi.80.2.571-577.2006 es_ES
dc.description.references Sanjuán, R., Agudelo-Romero, P., & Elena, S. F. (2009). Upper-limit mutation rate estimation for a plant RNA virus. Biology Letters, 5(3), 394-396. doi:10.1098/rsbl.2008.0762 es_ES
dc.description.references Sardanyes, J., Sole, R. V., & Elena, S. F. (2009). Replication Mode and Landscape Topology Differentially Affect RNA Virus Mutational Load and Robustness. Journal of Virology, 83(23), 12579-12589. doi:10.1128/jvi.00767-09 es_ES
dc.description.references Tromas, N., & Elena, S. F. (2010). The Rate and Spectrum of Spontaneous Mutations in a Plant RNA Virus. Genetics, 185(3), 983-989. doi:10.1534/genetics.110.115915 es_ES
dc.description.references Turturo, C., Friscina, A., Gaubert, S., Jacquemond, M., Thompson, J. R., & Tepfer, M. (2008). Evaluation of potential risks associated with recombination in transgenic plants expressing viral sequences. Journal of General Virology, 89(1), 327-335. doi:10.1099/vir.0.83339-0 es_ES
dc.description.references Varkonyi-Gasic, E., Wu, R., Wood, M., Walton, E. F., & Hellens, R. P. (2007). Protocol: a highly sensitive RT-PCR method for detection and quantification of microRNAs. Plant Methods, 3(1), 12. doi:10.1186/1746-4811-3-12 es_ES
dc.description.references Vaucheret, H. (2004). The action of ARGONAUTE1 in the miRNA pathway and its regulation by the miRNA pathway are crucial for plant development. Genes & Development, 18(10), 1187-1197. doi:10.1101/gad.1201404 es_ES
dc.description.references Vincenzetti, S., Cambi, A., Neuhard, J., Schnorr, K., Grelloni, M., & Vita, A. (1999). Cloning, Expression, and Purification of Cytidine Deaminase fromArabidopsis thaliana. Protein Expression and Purification, 15(1), 8-15. doi:10.1006/prep.1998.0959 es_ES
dc.description.references Von Eije, K. J., Brake, O. t., & Berkhout, B. (2007). Human Immunodeficiency Virus Type 1 Escape Is Restricted When Conserved Genome Sequences Are Targeted by RNA Interference. Journal of Virology, 82(6), 2895-2903. doi:10.1128/jvi.02035-07 es_ES
dc.description.references Wang, M.-B., Abbott, D. C., & Waterhouse, P. M. (2000). A single copy of a virus-derived transgene encoding hairpin RNA gives immunity to barley yellow dwarf virus. Molecular Plant Pathology, 1(6), 347-356. doi:10.1046/j.1364-3703.2000.00038.x es_ES
dc.description.references Warthmann, N., Chen, H., Ossowski, S., Weigel, D., & Hervé, P. (2008). Highly Specific Gene Silencing by Artificial miRNAs in Rice. PLoS ONE, 3(3), e1829. doi:10.1371/journal.pone.0001829 es_ES
dc.description.references Westerhout, E. M., & Berkhout, B. (2007). A systematic analysis of the effect of target RNA structure on RNA interference. Nucleic Acids Research, 35(13), 4322-4330. doi:10.1093/nar/gkm437 es_ES
dc.description.references Westerhout, E. M. (2005). HIV-1 can escape from RNA interference by evolving an alternative structure in its RNA genome. Nucleic Acids Research, 33(2), 796-804. doi:10.1093/nar/gki220 es_ES
dc.description.references Wichman, H. A. (1999). Different Trajectories of Parallel Evolution During Viral Adaptation. Science, 285(5426), 422-424. doi:10.1126/science.285.5426.422 es_ES


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