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Multi-targeting of viral RNAs with synthetic trans-acting small interfering RNAs enhances plant antiviral resistance

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Multi-targeting of viral RNAs with synthetic trans-acting small interfering RNAs enhances plant antiviral resistance

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dc.contributor.author CARBONELL, ALBERTO es_ES
dc.contributor.author Lisón, Purificación es_ES
dc.contributor.author Daròs, José-Antonio es_ES
dc.date.accessioned 2021-02-03T04:34:02Z
dc.date.available 2021-02-03T04:34:02Z
dc.date.issued 2019-11 es_ES
dc.identifier.issn 0960-7412 es_ES
dc.identifier.uri http://hdl.handle.net/10251/160607
dc.description.abstract [EN] RNA interference (RNAi)-based tools are used in multiple organisms to induce antiviral resistance through the sequence-specific degradation of target RNAs by complementary small RNAs. In plants, highly specific antiviral RNAi-based tools include artificial microRNAs (amiRNAs) and synthetic trans-acting small interfering RNAs (syn-tasiRNAs). syn-tasiRNAs have emerged as a promising antiviral tool allowing for the multi-targeting of viral RNAs through the simultaneous expression of several syn-tasiRNAs from a single precursor. Here, we compared in tomato plants the effects of an amiRNA construct expressing a single amiRNA and a syn-tasiRNA construct expressing four different syn-tasiRNAs against Tomato spotted wilt virus (TSWV), an economically important pathogen affecting tomato crops worldwide. Most of the syn-tasiRNA lines were resistant to TSWV, whereas the majority of the amiRNA lines were susceptible and accumulated viral progenies with mutations in the amiRNA target site. Only the two amiRNA lines with higher amiRNA accumulation were resistant, whereas resistance in syn-tasiRNA lines was not exclusive of lines with high syn-tasiRNA accumulation. Collectively, these results suggest that syn-tasiRNAs induce enhanced antiviral resistance because of the combined silencing effect of each individual syn-tasiRNA, which minimizes the possibility that the virus simultaneously mutates all different target sites to fully escape each syn-tasiRNA. es_ES
dc.description.sponsorship We thank V. Aragones and E. Moya for invaluable technical assistance. This work was supported by grants from Ministerio de Ciencia, Innovacion y Universidades (MCIU, Spain), Agencia Estatal de Investigacion (AEI, Spain) and Fondo Europeo de Desarrollo Regional (FEDER, European Union) (RTI2018-095118-A-100 and RYC-2017-21648 to A.C.; BIO2017-83184-R to J.-A.D.). es_ES
dc.language Inglés es_ES
dc.publisher Blackwell Publishing es_ES
dc.relation.ispartof The Plant Journal es_ES
dc.rights Reconocimiento (by) es_ES
dc.subject Syn-tasiRNA es_ES
dc.subject Antiviral resistance es_ES
dc.subject AmiRNA es_ES
dc.subject RNA silencing es_ES
dc.subject Solanum lycopersicum es_ES
dc.subject Tomato spotted wilt virus es_ES
dc.subject.classification BIOQUIMICA Y BIOLOGIA MOLECULAR es_ES
dc.title Multi-targeting of viral RNAs with synthetic trans-acting small interfering RNAs enhances plant antiviral resistance es_ES
dc.type Artículo es_ES
dc.identifier.doi 10.1111/tpj.14466 es_ES
dc.relation.projectID info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/BIO2017-83184-R/ES/VIRUS DE PLANTAS: PATOGENOS Y TAMBIEN VECTORES PARA LA PRODUCCION DE PROTEINAS, METABOLITOS, RNAS Y NANOPARTICULAS/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/RTI2018-095118-A-I00/ES/COMPLEJOS ARGONAUTA1 DE PLANTAS: IDENTIFICACION DE SUS COMPONENTES PROTEICOS Y DE RNA, Y AJUSTE FINO DEL SILENCIAMIENTO MEDIANTE SU PROGRAMACION POR PEQUEÑOS RNAS ARTIFICIALES/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/AEI//RYC-2017-21648/ es_ES
dc.rights.accessRights Abierto es_ES
dc.contributor.affiliation Universitat Politècnica de València. Departamento de Biotecnología - Departament de Biotecnologia 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 Carbonell, A.; Lisón, P.; Daròs, J. (2019). Multi-targeting of viral RNAs with synthetic trans-acting small interfering RNAs enhances plant antiviral resistance. The Plant Journal. 100(4):720-737. https://doi.org/10.1111/tpj.14466 es_ES
dc.description.accrualMethod S es_ES
dc.relation.publisherversion https://doi.org/10.1111/tpj.14466 es_ES
dc.description.upvformatpinicio 720 es_ES
dc.description.upvformatpfin 737 es_ES
dc.type.version info:eu-repo/semantics/publishedVersion es_ES
dc.description.volume 100 es_ES
dc.description.issue 4 es_ES
dc.identifier.pmid 31350772 es_ES
dc.identifier.pmcid PMC6899541 es_ES
dc.relation.pasarela S\392435 es_ES
dc.contributor.funder European Regional Development Fund es_ES
dc.contributor.funder Agencia Estatal de Investigación es_ES
dc.description.references Ai, T., Zhang, L., Gao, Z., Zhu, C. X., & Guo, X. (2011). Highly efficient virus resistance mediated by artificial microRNAs that target the suppressor of PVX and PVY in plants. Plant Biology, 13(2), 304-316. doi:10.1111/j.1438-8677.2010.00374.x es_ES
dc.description.references Ali, Z., Ali, S., Tashkandi, M., Zaidi, S. S.-A., & Mahfouz, M. M. (2016). CRISPR/Cas9-Mediated Immunity to Geminiviruses: Differential Interference and Evasion. Scientific Reports, 6(1). doi:10.1038/srep26912 es_ES
dc.description.references Berkhout, B., & Das, A. T. (2012). HIV-1 Escape From RNAi Antivirals: Yet Another Houdini Action? Molecular Therapy - Nucleic Acids, 1, e26. doi:10.1038/mtna.2012.22 es_ES
dc.description.references Bishop, K. N., Holmes, R. K., Sheehy, A. M., & Malim, M. H. (2004). APOBEC-Mediated Editing of Viral RNA. Science, 305(5684), 645-645. doi:10.1126/science.1100658 es_ES
dc.description.references Ter Brake, O., Konstantinova, P., Ceylan, M., & Berkhout, B. (2006). Silencing of HIV-1 with RNA Interference: a Multiple shRNA Approach. Molecular Therapy, 14(6), 883-892. doi:10.1016/j.ymthe.2006.07.007 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 Carbonell, A. (2017). Artificial small RNA-based strategies for effective and specific gene silencing in plants. Plant gene silencing: mechanisms and applications, 110-127. doi:10.1079/9781780647678.0110 es_ES
dc.description.references Carbonell, A. (2019). Design and High-Throughput Generation of Artificial Small RNA Constructs for Plants. Plant MicroRNAs, 247-260. doi:10.1007/978-1-4939-9042-9_19 es_ES
dc.description.references Carbonell, A. (2019). Secondary Small Interfering RNA-Based Silencing Tools in Plants: An Update. Frontiers in Plant Science, 10. doi:10.3389/fpls.2019.00687 es_ES
dc.description.references Carbonell, A., & Daròs, J.-A. (2017). Artificial microRNAs and synthetictrans-acting small interfering RNAs interfere with viroid infection. Molecular Plant Pathology, 18(5), 746-753. doi:10.1111/mpp.12529 es_ES
dc.description.references Carbonell, A., & Daròs, J.-A. (2019). Design, Synthesis, and Functional Analysis of Highly Specific Artificial Small RNAs with Antiviral Activity in Plants. Antiviral Resistance in Plants, 231-246. doi:10.1007/978-1-4939-9635-3_13 es_ES
dc.description.references Carbonell, A., Takeda, A., Fahlgren, N., Johnson, S. C., Cuperus, J. T., & Carrington, J. C. (2014). New Generation of Artificial MicroRNA and Synthetic Trans-Acting Small Interfering RNA Vectors for Efficient Gene Silencing in Arabidopsis. Plant Physiology, 165(1), 15-29. doi:10.1104/pp.113.234989 es_ES
dc.description.references Carbonell, A., Fahlgren, N., Mitchell, S., Cox, K. L., Reilly, K. C., Mockler, T. C., & Carrington, J. C. (2015). Highly specific gene silencing in a monocot species by artificial micro RNA s derived from chimeric mi RNA precursors. The Plant Journal, 82(6), 1061-1075. doi:10.1111/tpj.12835 es_ES
dc.description.references Carbonell, A., López, C., & Daròs, J.-A. (2019). Fast-Forward Identification of Highly Effective Artificial Small RNAs Against Different Tomato spotted wilt virus Isolates. Molecular Plant-Microbe Interactions®, 32(2), 142-156. doi:10.1094/mpmi-05-18-0117-ta es_ES
dc.description.references Bhushan, K. (2018). CRISPR/Cas13a targeting of RNA virus in plants. Plant Cell Reports, 37(12), 1707-1712. doi:10.1007/s00299-018-2297-2 es_ES
dc.description.references Chen, L., Cheng, X., Cai, J., Zhan, L., Wu, X., Liu, Q., & Wu, X. (2016). Multiple virus resistance using artificial trans-acting siRNAs. Journal of Virological Methods, 228, 16-20. doi:10.1016/j.jviromet.2015.11.004 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 Cuperus, J. T., Carbonell, A., Fahlgren, N., Garcia-Ruiz, H., Burke, R. T., Takeda, A., … Carrington, J. C. (2010). Unique functionality of 22-nt miRNAs in triggering RDR6-dependent siRNA biogenesis from target transcripts in Arabidopsis. Nature Structural & Molecular Biology, 17(8), 997-1003. doi:10.1038/nsmb.1866 es_ES
dc.description.references Debreczeni, D. E., López, C., Aramburu, J., Darós, J. A., Soler, S., Galipienso, L., … Rubio, L. (2015). Complete sequence of three different biotypes of tomato spotted wilt virus (wild type, tomato Sw-5 resistance-breaking and pepper Tsw resistance-breaking) from Spain. Archives of Virology, 160(8), 2117-2123. doi:10.1007/s00705-015-2453-8 es_ES
dc.description.references Ding, S.-W. (2010). RNA-based antiviral immunity. Nature Reviews Immunology, 10(9), 632-644. doi:10.1038/nri2824 es_ES
dc.description.references Von Eije, K. J., Brake, O. ter, & Berkhout, B. (2008). 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 Ellul, P., Garcia-Sogo, B., Pineda, B., Ríos, G., Roig, L., & Moreno, V. (2003). The ploidy level of transgenic plants in Agrobacterium-mediated transformation of tomato cotyledons (Lycopersicon esculentum L.Mill.) is genotype and procedure dependent. Theoretical and Applied Genetics, 106(2), 231-238. doi:10.1007/s00122-002-0928-y es_ES
dc.description.references Fahim, M., Millar, A. A., Wood, C. C., & Larkin, P. J. (2011). Resistance to Wheat streak mosaic virus generated by expression of an artificial polycistronic microRNA in wheat. Plant Biotechnology Journal, 10(2), 150-163. doi:10.1111/j.1467-7652.2011.00647.x es_ES
dc.description.references Fahlgren, N., & Carrington, J. C. (2009). miRNA Target Prediction in Plants. Plant MicroRNAs, 51-57. doi:10.1007/978-1-60327-005-2_4 es_ES
dc.description.references Fire, A., Xu, S., Montgomery, M. K., Kostas, S. A., Driver, S. E., & Mello, C. C. (1998). Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature, 391(6669), 806-811. doi:10.1038/35888 es_ES
dc.description.references Gitlin, L., Stone, J. K., & Andino, R. (2005). 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 Khan, M. Z., Amin, I., Hameed, A., & Mansoor, S. (2018). CRISPR–Cas13a: Prospects for Plant Virus Resistance. Trends in Biotechnology, 36(12), 1207-1210. doi:10.1016/j.tibtech.2018.05.005 es_ES
dc.description.references Khan, M. Z., Haider, S., Mansoor, S., & Amin, I. (2019). Targeting Plant ssDNA Viruses with Engineered Miniature CRISPR-Cas14a. Trends in Biotechnology, 37(8), 800-804. doi:10.1016/j.tibtech.2019.03.015 es_ES
dc.description.references Kis, A., Tholt, G., Ivanics, M., Várallyay, É., Jenes, B., & Havelda, Z. (2015). Polycistronic artificial miRNA-mediated resistance toWheat dwarf virusin barley is highly efficient at low temperature. Molecular Plant Pathology, 17(3), 427-437. doi:10.1111/mpp.12291 es_ES
dc.description.references KUNG, Y.-J., LIN, S.-S., HUANG, Y.-L., CHEN, T.-C., HARISH, S. S., CHUA, N.-H., & YEH, S.-D. (2011). Multiple artificial microRNAs targeting conserved motifs of the replicase gene confer robust transgenic resistance to negative-sense single-stranded RNA plant virus. Molecular Plant Pathology, 13(3), 303-317. doi:10.1111/j.1364-3703.2011.00747.x es_ES
dc.description.references Lafforgue, G., Martinez, F., Sardanyes, J., de la Iglesia, F., Niu, Q.-W., Lin, S.-S., … Elena, S. F. (2011). Tempo and Mode of Plant RNA Virus Escape from RNA Interference-Mediated Resistance. Journal of Virology, 85(19), 9686-9695. doi:10.1128/jvi.05326-11 es_ES
dc.description.references Lafforgue, G., Martinez, F., Niu, Q.-W., Chua, N.-H., Daros, J.-A., & Elena, S. F. (2013). Improving the Effectiveness of Artificial MicroRNA (amiR)-Mediated Resistance against Turnip Mosaic Virus by Combining Two amiRs or by Targeting Highly Conserved Viral Genomic Regions. Journal of Virology, 87(14), 8254-8256. doi:10.1128/jvi.00914-13 es_ES
dc.description.references Levanova, A., & Poranen, M. M. (2018). RNA Interference as a Prospective Tool for the Control of Human Viral Infections. Frontiers in Microbiology, 9. doi:10.3389/fmicb.2018.02151 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 Liu, Q., Wang, F., & Axtell, M. J. (2014). Analysis of Complementarity Requirements for Plant MicroRNA Targeting Using a Nicotiana benthamiana Quantitative Transient Assay  . The Plant Cell, 26(2), 741-753. doi:10.1105/tpc.113.120972 es_ES
dc.description.references Llave, C., Xie, Z., Kasschau, K. D., & Carrington, J. C. (2002). Cleavage of Scarecrow-like mRNA Targets Directed by a Class of Arabidopsis miRNA. Science, 297(5589), 2053-2056. doi:10.1126/science.1076311 es_ES
dc.description.references Mahas, A., & Mahfouz, M. (2018). Engineering virus resistance via CRISPR–Cas systems. Current Opinion in Virology, 32, 1-8. doi:10.1016/j.coviro.2018.06.002 es_ES
dc.description.references Martínez, F., Lafforgue, G., Morelli, M. J., González-Candelas, F., Chua, N.-H., Daròs, J.-A., & Elena, S. F. (2012). Ultradeep Sequencing Analysis of Population Dynamics of Virus Escape Mutants in RNAi-Mediated Resistant Plants. Molecular Biology and Evolution, 29(11), 3297-3307. doi:10.1093/molbev/mss135 es_ES
dc.description.references Mehta, D., Stürchler, A., Anjanappa, R. B., Zaidi, S. S.-A., Hirsch-Hoffmann, M., Gruissem, W., & Vanderschuren, H. (2019). Linking CRISPR-Cas9 interference in cassava to the evolution of editing-resistant geminiviruses. Genome Biology, 20(1). doi:10.1186/s13059-019-1678-3 es_ES
dc.description.references Mitter, N., Zhai, Y., Bai, A. X., Chua, K., Eid, S., Constantin, M., … Pappu, H. R. (2016). Evaluation and identification of candidate genes for artificial microRNA-mediated resistance to tomato spotted wilt virus. Virus Research, 211, 151-158. doi:10.1016/j.virusres.2015.10.003 es_ES
dc.description.references Montgomery, T. A., Howell, M. D., Cuperus, J. T., Li, D., Hansen, J. E., Alexander, A. L., … Carrington, J. C. (2008). Specificity of ARGONAUTE7-miR390 Interaction and Dual Functionality in TAS3 Trans-Acting siRNA Formation. Cell, 133(1), 128-141. doi:10.1016/j.cell.2008.02.033 es_ES
dc.description.references Montgomery, T. A., Yoo, S. J., Fahlgren, N., Gilbert, S. D., Howell, M. D., Sullivan, C. M., … Carrington, J. C. (2008). AGO1-miR173 complex initiates phased siRNA formation in plants. Proceedings of the National Academy of Sciences, 105(51), 20055-20062. doi:10.1073/pnas.0810241105 es_ES
dc.description.references Nishitsuji, H., Kohara, M., Kannagi, M., & Masuda, T. (2006). Effective Suppression of Human Immunodeficiency Virus Type 1 through a Combination of Short- or Long-Hairpin RNAs Targeting Essential Sequences for Retroviral Integration. Journal of Virology, 80(15), 7658-7666. doi:10.1128/jvi.00078-06 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 Presloid, J., & Novella, I. (2015). RNA Viruses and RNAi: Quasispecies Implications for Viral Escape. Viruses, 7(6), 3226-3240. doi:10.3390/v7062768 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 SCHOLTHOF, K.-B. G., ADKINS, S., CZOSNEK, H., PALUKAITIS, P., JACQUOT, E., HOHN, T., … FOSTER, G. D. (2011). Top 10 plant viruses in molecular plant pathology. Molecular Plant Pathology, 12(9), 938-954. doi:10.1111/j.1364-3703.2011.00752.x es_ES
dc.description.references Schwab, R., Palatnik, J. F., Riester, M., Schommer, C., Schmid, M., & Weigel, D. (2005). Specific Effects of MicroRNAs on the Plant Transcriptome. Developmental Cell, 8(4), 517-527. doi:10.1016/j.devcel.2005.01.018 es_ES
dc.description.references Shah, P. S., Pham, N. P., & Schaffer, D. V. (2012). HIV Develops Indirect Cross-resistance to Combinatorial RNAi Targeting Two Distinct and Spatially Distant Sites. Molecular Therapy, 20(4), 840-848. doi:10.1038/mt.2012.3 es_ES
dc.description.references Simón-Mateo, C., & García, J. A. (2006). MicroRNA-Guided Processing Impairs Plum Pox Virus Replication, but the Virus Readily Evolves To Escape This Silencing Mechanism. Journal of Virology, 80(5), 2429-2436. doi:10.1128/jvi.80.5.2429-2436.2006 es_ES
dc.description.references Tashkandi, M., Ali, Z., Aljedaani, F., Shami, A., & Mahfouz, M. M. (2018). Engineering resistance against Tomato yellow leaf curl virus via the CRISPR/Cas9 system in tomato. Plant Signaling & Behavior, 13(10), e1525996. doi:10.1080/15592324.2018.1525996 es_ES
dc.description.references Turina, M., Kormelink, R., & Resende, R. O. (2016). Resistance to Tospoviruses in Vegetable Crops: Epidemiological and Molecular Aspects. Annual Review of Phytopathology, 54(1), 347-371. doi:10.1146/annurev-phyto-080615-095843 es_ES
dc.description.references Wang, G., Zhao, N., Berkhout, B., & Das, A. T. (2016). CRISPR-Cas9 Can Inhibit HIV-1 Replication but NHEJ Repair Facilitates Virus Escape. Molecular Therapy, 24(3), 522-526. doi:10.1038/mt.2016.24 es_ES
dc.description.references Wang, Z., Pan, Q., Gendron, P., Zhu, W., Guo, F., Cen, S., … Liang, C. (2016). CRISPR/Cas9-Derived Mutations Both Inhibit HIV-1 Replication and Accelerate Viral Escape. Cell Reports, 15(3), 481-489. doi:10.1016/j.celrep.2016.03.042 es_ES
dc.description.references Yoder, K. E., & Bundschuh, R. (2016). Host Double Strand Break Repair Generates HIV-1 Strains Resistant to CRISPR/Cas9. Scientific Reports, 6(1). doi:10.1038/srep29530 es_ES
dc.description.references Zhang, Z. J. (2014). Artificial trans-acting small interfering RNA: a tool for plant biology study and crop improvements. Planta, 239(6), 1139-1146. doi:10.1007/s00425-014-2054-x es_ES


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