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Within-host Evolution of Segments Ratio for the Tripartite Genome of Alfalfa Mosaic Virus

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Within-host Evolution of Segments Ratio for the Tripartite Genome of Alfalfa Mosaic Virus

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dc.contributor.author Wu, Beilei es_ES
dc.contributor.author Zwart, Mark P. es_ES
dc.contributor.author Sanchez Navarro, Jesus Angel es_ES
dc.contributor.author Elena Fito, Santiago Fco es_ES
dc.date.accessioned 2018-07-26T07:05:09Z
dc.date.available 2018-07-26T07:05:09Z
dc.date.issued 2017 es_ES
dc.identifier.issn 2045-2322 es_ES
dc.identifier.uri http://hdl.handle.net/10251/106293
dc.description.abstract [EN] The existence of multipartite viruses is an intriguing mystery in evolutionary virology. Several hypotheses suggest benefits that should outweigh the costs of a reduced transmission efficiency and of segregation of coadapted genes associated with encapsidating each segment into a different particle. Advantages range from increasing genome size despite high mutation rates, faster replication, more efficient selection resulting from reassortment during mixed infections, better regulation of gene expression, or enhanced virion stability and cell-to-cell movement. However, support for these hypotheses is scarce. Here we report experiments testing whether an evolutionary stable equilibrium exists for the three genomic RNAs of Alfalfa mosaic virus (AMV). Starting infections with different segment combinations, we found that the relative abundance of each segment evolves towards a constant ratio. Population genetic analyses show that the segment ratio at this equilibrium is determined by frequency-dependent selection. Replication of RNAs 1 and 2 was coupled and collaborative, whereas the replication of RNA 3 interfered with the replication of the other two. We found that the equilibrium solution is slightly different for the total amounts of RNA produced and encapsidated, suggesting that competition exists between all RNAs during encapsidation. Finally, we found that the observed equilibrium appears to be host-species dependent. es_ES
dc.description.sponsorship We thank Francisca de la Iglesia, Paula Agudo and Lorena Corachan for their dedication and expert technical assistance. This project was funded in part by grants BFU2015-65037P from the Spanish Ministry of Economy and Competitiveness-FEDER, PROMETEOII/2014/021 from Generalitat Valenciana and EvoEvo (ICT610427) from the European Commission 7th Framework Program to S.F.E. The China Scholarship Council and the Chinese Academy of Agricultural Sciences provided funding to B.W. es_ES
dc.language Inglés es_ES
dc.publisher Nature Publishing Group es_ES
dc.relation.ispartof Scientific Reports es_ES
dc.rights Reconocimiento (by) es_ES
dc.title Within-host Evolution of Segments Ratio for the Tripartite Genome of Alfalfa Mosaic Virus es_ES
dc.type Artículo es_ES
dc.identifier.doi 10.1038/s41598-017-05335-8 es_ES
dc.relation.projectID info:eu-repo/grantAgreement/GVA//PROMETEOII%2F2014%2F021/ES/Comparative systems biology of host-virus interactions/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/EC/FP7/610427/EU/Evolution of Evolution/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/MINECO//BFU2015-65037-P/ES/EVOLUCION DE VIRUS EN HUESPEDES CON SUSCEPTIBILIDAD VARIABLE: CONSECUENCIAS EN EFICACIA Y VIRULENCIA DE CAMBIOS EN LAS REDES INTERACTOMICAS DE PROTEINAS VIRUS-HUESPED/ 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 Wu, B.; Zwart, MP.; Sanchez Navarro, JA.; Elena Fito, SF. (2017). Within-host Evolution of Segments Ratio for the Tripartite Genome of Alfalfa Mosaic Virus. Scientific Reports. 7. https://doi.org/10.1038/s41598-017-05335-8 es_ES
dc.description.accrualMethod S es_ES
dc.relation.publisherversion https://doi.org/10.1038/s41598-017-05335-8 es_ES
dc.type.version info:eu-repo/semantics/publishedVersion es_ES
dc.description.volume 7 es_ES
dc.identifier.pmid 28694514 en_EN
dc.identifier.pmcid PMC5504059 en_EN
dc.relation.pasarela S\356545 es_ES
dc.contributor.funder Ministerio de Economía y Competitividad es_ES
dc.contributor.funder Generalitat Valenciana es_ES
dc.description.references Crosland, W. J. & Crozier, R. H. Myrmecia pilosula, an ant with only one pair of chromosomes. Science 231, 1278 (1986). es_ES
dc.description.references Grubben, G. J. H. & Denton, O. A. Plant Resources of Tropical Africa 2. Vegetables. (PROTA Foundation/Backhuys Publishers, 2004). es_ES
dc.description.references Allers, T. & Mevarech, A. Archaeal genetics – the third way. Nat. Rev. Genet. 6, 58–73 (2005). es_ES
dc.description.references Gronenborn, B. Nanoviruses: genome organization and protein function. Vet. Microbiol. 98, 103–109 (2004). es_ES
dc.description.references Jaspars, E. M. Plant viruses with a multipartite genome. Adv. Virus Res. 19, 37–149 (1974). es_ES
dc.description.references Sicard, A., Michalakis, Y., Gutiérrez, S. & Blanc, S. The strange lifestyle of multipartite viruses. PLoS Pathog. 12, e1005819 (2016). es_ES
dc.description.references Hayakawa, T. et al. Analysis of proteins encoded in the bipartite genome of a new type of parvo-like virus isolated from silkworm – structural protein with DNA polymerase motif. Virus Res. 66, 101–108 (2000). es_ES
dc.description.references Ladner, J. T. et al. A multicomponent animal virus isolated from mosquitoes. Cell Host Microb. 20, 357–367 (2016). es_ES
dc.description.references Iranzo, J. & Manrubia, S. C. Evolutionary dynamics of genome segmentation in multipartite viruses. Proc. R. Soc. B. 279, 3812–3819 (2012). es_ES
dc.description.references Escriu, F., Fraile, A. & García-Arenal, F. Constraints to genetic exchange support gene coadaptation in a tripartite RNA virus. PLoS Pathog. 3, e8 (2007). es_ES
dc.description.references Pressing, J. & Reanney, D. C. Divided genomes and intrinsic noise. J. Mol. Evol. 20, 135–146 (1984). es_ES
dc.description.references Nee, S. The evolution of multicompartimental genomes in viruses. J. Mol. Evol. 25, 277–281 (1987). es_ES
dc.description.references Chao, L. Evolution of sex in RNA viruses. J. Theor. Biol. 133, 99–112 (1988). es_ES
dc.description.references Chao, L. Levels of selection, evolution of sex in RNA viruses, and the origin of life. J. Theor. Biol. 153, 229–246 (1991). es_ES
dc.description.references Miralles, R., Gerrish, P. J., Moya, A. & Elena, S. F. Clonal interference and the evolution of RNA viruses. Science 285, 1745–1747 (1999). es_ES
dc.description.references Ojosnegros, S. et al. Viral genome segmentation can result from a trade-off between genetic content and particle stability. PLoS Genet. 7, e1001344 (2011). es_ES
dc.description.references Gilbertson, R. L., Sudarshana, M., Jiang, H., Rojas, M. R. & Lucas, W. J. Limitations on Geminivirus genome size imposed by plasmodesmata and virus-encoded movement proteins: insights into DNA trafficking. Plant Cell. 15, 2578–2591 (2003). es_ES
dc.description.references Sicard, A. et al. Gene copy number is differentially regulated in a multipartite virus. Nat. Commun. 4, 2248 (2013). es_ES
dc.description.references Allison, R. F., Janda, M. & Ahlquist, P. Infectious in vitro transcripts from Cowpea chlorotic mottle virus cDNA clones and exchange of individual RNA components with Brome mosaic virus. J. Virol. 62, 3581–3588 (1988). es_ES
dc.description.references Ahlquist, P., French, R., Janda, M. & Loesch-Fries, S. Multicomponent RNA plant virus infection derived from cloned viral cDNA. Proc. Natl. Acad. Sci. USA 81, 7066–7070 (1984). es_ES
dc.description.references Hajimorad, M. R., Kurath, G., Randles, J. W. & Francki, R. I. B. Change in phenotype and encapsidated RNA segments of an isolate of Alfalfa mosaic virus: an influence of host passage. J. Gen. Virol. 72, 2885–2893 (1991). es_ES
dc.description.references Dzianott, A. & Bujarski, J. J. Infection and RNA recombination of Brome mosaic virus. Arabidopsis thaliana. Virology 318, 482–492 (2004). es_ES
dc.description.references French, R. & Ahlquist, P. Intercistronic as well as terminal sequences are required for efficient amplification of Brome mosaic virus RNA3. J. Virol. 61, 1457–1465 (1987). es_ES
dc.description.references French, R. & Ahlquist, P. Characterization and engineering of sequences controlling in vivo synthesis of Brome mosaic virus subgenomic RNA. J. Virol. 62, 2411–2420 (1988). es_ES
dc.description.references Pacha, R. F., Allison, R. F. & Ahlquist, P. cis-Acting sequences required for in vivo amplification of genomic RNA3 are organized differently in related bromoviruses. Virology 174, 436–443 (1990). es_ES
dc.description.references Traynor, P., Young, B. M. & Ahlquist, P. Deletion analysis of Brome mosaic virus 2a protein: effects on RNA replication and systemic spread. J. Virol. 65, 2807–2815 (1991). es_ES
dc.description.references Pacha, R. F. & Ahlquist, P. Use of Bromovirus RNA3 hybrids to study template specificity in viral RNA amplification. J. Virol. 65, 3693–3703 (1991). es_ES
dc.description.references Bol, J. F. Alfalfa mosaic virus: coat protein-dependent initiation of infection. Mol. Plant Pathol. 4, 1–8 (2003). es_ES
dc.description.references Tromas, N., Zwart, M. P., Lafforgue, G. & Elena, S. F. Within-host spatiotemporal dynamics of plant virus infection at the cellular level. PLoS Genet. 10, e1004186 (2014). es_ES
dc.description.references Melnyk, C. W., Molnar, A. & Baulcombe, D. C. Intercellular and systemic movement of RNA silencing signals. EMBO J. 30, 3553–3563 (2011). es_ES
dc.description.references Cuevas, J. M., Willemsen, A., Hillung, J., Zwart, M. P. & Elena, S. F. Temporal dynamics of intrahost molecular evolution for a plant RNA virus. Mol. Biol. Evol. 32, 1132–1147 (2015). es_ES
dc.description.references Ayala, F. J. & Campbell, C. A. Frequency-dependent selection. Annu. Rev. Ecol. Syst. 5, 115–138 (1974). es_ES
dc.description.references Van Dun, C. M., Van Vloten-Doting, L. & Bol, J. F. Expression of Alfalfa mosaic virus cDNA1 and 2 in transgenic tobacco plants. Virology 163, 572–578 (1988). es_ES
dc.description.references Ni, P., Vaughan, R. C., Tragesser, B., Hoover, H. & Kao, C. C. The plant host can affect the encapsidation of Brome mosaic virus (BMV) RNA: BMV virions are surprisingly heterogeneous. J. Mol. Biol. 426, 1061–1076 (2014). es_ES
dc.description.references Hayes, R. J. & Buck, K. W. Complete replication of a eukaryotic virus-RNA in vitro by a purified RNA-dependent RNA-polymerase. Cell 63, 363–368 (1990). es_ES
dc.description.references Kao, C. C., Quadt, R., Hershberger, R. P. & Ahlquist, P. Brome mosaic virus RNA replication proteins 1a and 2a form a complex in vitro. J. Virol. 66, 6322–6329 (1992). es_ES
dc.description.references Quadt, R., Kao, C. C., Browning, K. S., Hershberger, R. P. & Ahlquist, P. Characterization of a host protein associated with Brome mosaic virus RNA-dependent RNA-polymerase. Proc. Natl. Acad. USA 90, 1498–1502 (1993). es_ES
dc.description.references Neeleman, L., Olsthoorn, R. C. L., Linthorst, H. J. M. & Bol, J. F. Translation of a nonpolyadenylated viral RNA is enhanced by binding of viral coat protein or polyadenylation of the RNA. Proc. Natl. Acad. Sci. USA 98, 14286–14291 (2001). es_ES
dc.description.references Olsthoorn, R. C., Mertens, S., Brederode, F. T. & Bol, J. F. A conformational switch at the 3′ end of a plant virus RNA regulates viral replication. EMBO J. 18, 4856–4864 (1999). es_ES
dc.description.references Yi, G., Letteney, E., Kim, C. H. & Kao, C. C. Brome mosaic virus capsid protein regulates accumulation of viral replication proteins by binding to the replicase assembly RNA element. RNA 15, 615–626 (2009). es_ES
dc.description.references Mileyko, Y., Jon, R. I. & Weitz, J. S. Small-scale copy number variation and large-scale changes in gene expression. Proc. Natl. Acad. Sci. USA 105, 16659–16664 (2008). es_ES
dc.description.references Radhakrishnan, A. & Green, R. Connections underlying translation and mRNA stability. J. Mol. Biol. 428, 3558–3564 (2016). es_ES
dc.description.references Bol, J. F. Replication of alfamo- and ilarviruses: role of the coat protein. Annu. Rev. Phytopathol. 43, 39–62 (2005). es_ES
dc.description.references Van Rossum, C. M. A., García, M. L. & Bol, J. F. Accumulation of Alfalfa mosaic virus RNAs 1 and 2 requires the encoded proteins in cis. J. Virol. 70, 5100–5105 (1996). es_ES
dc.description.references Vlot, A. C., Laros, S. M. & Bol, J. F. Coordinate replication of Alfalfa mosaic virus RNAs 1 and 2 involves cis- and trans-acting functions of the encoded helicase-like and polymerase-like domains. J. Virol. 77, 10790–10798 (2003). es_ES
dc.description.references Vlot, A. C. & Bol, J. F. The 5′ untranslated region of Alfalfa mosaic virus RNA 1 is involved in negative-strand RNA synthesis. J. Virol. 77, 11284–11289 (2003). es_ES
dc.description.references Schwartz, M. et al. A positive-strand RNA virus replication complex parallels form and function of retrovirus capsids. Mol. Cell 9, 505–514 (2002). es_ES
dc.description.references Yi, G. & Kao, C. cis- and trans-acting functions of Brome mosaic virus protein 1a in genomic RNA 1 replication. J. Virol. 82, 3045–3053 (2008). es_ES
dc.description.references Janda, M. & Ahlquist, P. RNA-dependent replication, transcription, and persistence of Brome mosaic virus RNA replicons in S. cerevisiae. Cell 72, 961–970 (1993). es_ES
dc.description.references Aparicio, F. & Pallás, V. The coat protein if Alfalfa mosaic virus interacts and interferes with the transcriptional activity of the bHLH transcription factor ILR3 promoting salicylic-dependent defense signaling response. Mol. Plant Pathol. 18, 173–186 (2017). es_ES
dc.description.references Jaspars, E. M. J. Interaction of Alfalfa mosaic virus nucleic acid and protein In Molecular Plant Virology (ed. Davies, J. W.) 155–225 (CRC Press, 1985). es_ES
dc.description.references Ansel-McKinney, P. & Gehrke, L. RNA determinants of a specific RNA-coat protein peptide interaction in Alfalfa mosaic virus: conservation of homologous features in ilarvirus RNAs. J. Mol. Biol. 278, 767–785 (1998). es_ES
dc.description.references Krab, I. M., Caldwell, C., Gallie, D. R. & Bol, J. F. Coat protein enhances translational efficiency of Alfalfa mosaic virus RNAs and interacts with the eIF4G component of initiation factor eIF4F. J. Gen. Virol. 86, 1841–1849 (2005). es_ES
dc.description.references Neeleman, L., Linthorst, H. J. M. & Bol, J. F. Efficient translation of alfamovirus RNAs requires the binding of coat protein dimers to the 3′ termini of the viral RNAs. J. Gen. Virol. 85, 231–240 (2004). es_ES
dc.description.references Herránz, M. C., Pallás, V. & Aparicio, F. Multifunctional roles for the N-terminal basic motif of Alfalfa mosaic virus coat protein: nucleolar/cytoplasmic shuttling, modulation of RNA-binding activity, and virion formation. Mol. Plant Microbe Interact. 25, 1093–1103 (2012). es_ES
dc.description.references Neeleman, L. & Bol, J. F. Cis-acting functions of Alfalfa mosaic virus proteins involved in replication and encapsidation of viral RNA. Virology 254, 324–333 (1999). es_ES
dc.description.references Van Vloten-Doting, L. & Jaspars, E. M. Uncoating of Alfalfa mosaic virus by its own RNA. Virology 48, 699–708 (1972). es_ES


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