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Magnitude and sign epistasis among deleterious mutations in a positive-sense plant RNA virus

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Magnitude and sign epistasis among deleterious mutations in a positive-sense plant RNA virus

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dc.contributor.author Lalic, Jasna es_ES
dc.contributor.author Elena Fito, Santiago Fco es_ES
dc.date.accessioned 2016-10-31T12:38:33Z
dc.date.available 2016-10-31T12:38:33Z
dc.date.issued 2012-08
dc.identifier.issn 0018-067X
dc.identifier.uri http://hdl.handle.net/10251/72998
dc.description.abstract How epistatic interactions between mutations determine the genetic architecture of fitness is of central importance in evolution. The study of epistasis is particularly interesting for RNA viruses because of their genomic compactness, lack of genetic redundancy, and apparent low complexity. Moreover, interactions between mutations in viral genomes determine traits such as resistance to antiviral drugs, virulence and host range. In this study we generated 53 Tobacco etch potyvirus genotypes carrying pairs of single-nucleotide substitutions and measured their separated and combined deleterious fitness effects. We found that up to 38% of pairs had significant epistasis for fitness, including both positive and negative deviations from the null hypothesis of multiplicative effects. Interestingly, the sign of epistasis was correlated with viral protein-protein interactions in a model network, being predominantly positive between linked pairs of proteins and negative between unlinked ones. Furthermore, 55% of significant interactions were cases of reciprocal sign epistasis (RSE), indicating that adaptive landscapes for RNA viruses maybe highly rugged. Finally, we found that the magnitude of epistasis correlated negatively with the average effect of mutations. Overall, our results are in good agreement to those previously reported for other viruses and further consolidate the view that positive epistasis is the norm for small and compact genomes that lack genetic robustness. Heredity (2012) 109, 71-77; doi: 10.1038/hdy.2012.15; published online 11 April 2012 es_ES
dc.description.sponsorship We thank Francisca de la Iglesia and Angels Prosper for their excellent technical assistance, Stephanie Bedhomme and Mark P Zwart for the discussion and Mario A Fares for statistical advice. Jose A Daros generously gifted us the pMTEV plasmid. This research was supported by the Spanish Ministry of Science and Innovation grant BFU2009-06993 to SFE. JL was supported by the JAE program from CSIC. en_EN
dc.language Inglés es_ES
dc.publisher Nature Publishing Group es_ES
dc.relation.ispartof Heredity es_ES
dc.rights Reserva de todos los derechos es_ES
dc.subject Epistasis es_ES
dc.subject Fitness landscapes es_ES
dc.subject Genome architecture es_ES
dc.subject Virus evolution es_ES
dc.title Magnitude and sign epistasis among deleterious mutations in a positive-sense plant RNA virus es_ES
dc.type Artículo es_ES
dc.identifier.doi 10.1038/hdy.2012.15
dc.relation.projectID info:eu-repo/grantAgreement/MICINN//BFU2009-06993/ES/Biologia Evolutiva Y De Sistemas De La Emergencia De Fitovirus De Rna/ es_ES
dc.rights.accessRights Cerrado 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 Lalic, J.; Elena Fito, SF. (2012). Magnitude and sign epistasis among deleterious mutations in a positive-sense plant RNA virus. Heredity. 109(2):71-77. https://doi.org/10.1038/hdy.2012.15 es_ES
dc.description.accrualMethod S es_ES
dc.relation.publisherversion http://dx.doi.org/10.1038/hdy.2012.15 es_ES
dc.description.upvformatpinicio 71 es_ES
dc.description.upvformatpfin 77 es_ES
dc.type.version info:eu-repo/semantics/publishedVersion es_ES
dc.description.volume 109 es_ES
dc.description.issue 2 es_ES
dc.relation.senia 232201 es_ES
dc.contributor.funder Ministerio de Ciencia e Innovación es_ES
dc.contributor.funder Consejo Superior de Investigaciones Científicas es_ES
dc.description.references Bagheri HC, Wagner GP (2004). Evolution of dominance in metabolic pathways. Genetics 168: 1716–1735. es_ES
dc.description.references Bedoya LC, Daròs JA (2010). Stability of Tobacco etch virus infectious clones in plasmid vectors. Virus Res 149: 234–240. es_ES
dc.description.references Bershtein S, Segal M, Bekerman R, Tokuriki N, Tawfik DS (2006). Robustness-epistasis link shapes the fitness landscape of a randomly drifting protein. Nature 444: 929–932. es_ES
dc.description.references Betancourt AJ (2010). Lack of evidence for sign epistasis between beneficial mutations in an RNA bacteriophage. J Mol Evol 71: 437–443. es_ES
dc.description.references Bonhoeffer S, Chappey C, Parkin NT, Whitcomb JM, Petropoulos CJ (2004). Evidence for positive epistasis in HIV-1. Science 306: 1547–1550. es_ES
dc.description.references Burch CL, Chao L (2004). Epistasis and its relationship to canalization in the RNA virus φ6. Genetics 167: 559–567. es_ES
dc.description.references Carrasco P, Daròs JA, Agudelo-Romero P, Elena SF (2007a). A real-time RT-PCR assay for quantifying the fitness of Tobacco etch virus in competition experiments. J Virol Meth 139: 181–188. es_ES
dc.description.references Carrasco P, de la Iglesia F, Elena SF (2007b). Distribution of fitness and virulence effects caused by single-nucleotide substitutions in Tobacco etch virus. J Virol 81: 12979–12984. es_ES
dc.description.references Cong M, Heneine W, García-Lerma JG (2007). The fitness cost of mutations associated with Human immunodeficiency virus type 1 drug resistance is modulated by mutational interactions. J Virol 81: 3037–3041. es_ES
dc.description.references Coyne JA (1992). Genetics and speciation. Nature 355: 511–515. es_ES
dc.description.references Crow JF, Kimura M (1970) An Introduction to Population Genetics Theory. Harper and Row New York. es_ES
dc.description.references Da Silva J, Coetzer M, Nedellec R, Pastore C, Mosier DE (2010). Fitness epistasis and constraints on adaptation in a Human immunodeficiency virus type 1 protein region. Genetics 185: 293–303. es_ES
dc.description.references Desai MM, Weissman D, Feldman MW (2007). Evolution can favor antagonistic epistasis. Genetics 177: 1001–1010. es_ES
dc.description.references De la Iglesia F, Elena SF (2007). Fitness declines in Tobacco etch virus upon serial bottleneck transfers. J Virol 81: 4941–4947. es_ES
dc.description.references De Visser JAGM, Elena SF (2007). The evolution of sex: empirical insights into the roles of epistasis and drift. Nat Rev Genet 8: 139–149. es_ES
dc.description.references De Visser JAGM, Hermisson J, Wagner GP, Ancel-Meyers L, Bagheri-Chaichian H, Blanchard JL et al. (2003). Perspective: Evolution and detection of genetic robustness. Evolution 57: 1959–1972. es_ES
dc.description.references De Visser JAGM, Cooper TF, Elena SF (2011). The causes of epistasis. Proc R Soc B 10: 3617–3624. es_ES
dc.description.references Edlund JA, Adami C (2004). Evolution of robustness in digital organisms. Artif Life 10: 167–179. es_ES
dc.description.references Elena SF (1999). Little evidence for synergism among deleterious mutations in a nonsegmented RNA virus. J Mol Evol 49: 703–707. es_ES
dc.description.references Elena SF, Solé RV, Sardanyés J (2010). Simple genomes, complex interactions: epistasis in RNA virus. Chaos 20: 026106. es_ES
dc.description.references Franke J, Klözer A, de Visser JAGM, Krug J (2011). Evolutionary accessibility of mutational pathways. PLoS Comp Biol 7: e1002134. es_ES
dc.description.references Killcoyne S, Carter GW, Smith J, Boyle J (2009). Cytoscape: a community-based framework for network modeling. Meth Mol Biol 563: 219–239. es_ES
dc.description.references Kondrashov AS (1994). Muller’s ratchet under epistatic selection. Genetics 136: 1469–1473. es_ES
dc.description.references Kondrashov AS, Crow JF (1991). Haploidy or diploidy: which is better. Nature 351: 314–315. es_ES
dc.description.references Kondrashov FA, Kondrashov AS (2001). Multidimensional epistasis and the disadvantage of sex. Proc Natl Acad Sci USA 98: 12089–12092. es_ES
dc.description.references Kouyos RD, Silander OK, Bonhoeffer S (2007). Epistasis between deleterious mutations and the evolution of recombination. Trends Ecol Evol 6: 308–315. es_ES
dc.description.references Kvitek DJ, Sherlock G (2011). Reciprocal sign epistasis between frequently experimentally evolved adaptive mutations causes a rugged fitness landscape. PLoS Genet 7: e1002056. es_ES
dc.description.references Macía J, Solé RV, Elena SF (2012). The causes of epistasis in genetic networks. Evolution 66: 586–596. es_ES
dc.description.references Maisnier-Patin S, Berg OG, Lijas L, Andersson DI (2002). Compensatory adaptation to the deleterious effect of antibiotic resistance in Salmonella typhimurium. Mol Microbiol 46: 355–366. es_ES
dc.description.references Martínez JP, Bocharov G, Ignatovich A, Reiter J, Dittmar MT, Wain-Hobson S et al. (2011). Fitness ranking of individual mutants drives patterns of epistatic interactions in HIV-1. PLoS ONE 6: e18375. es_ES
dc.description.references Martínez-Picado J, Martínez MA (2009). HIV-1 reverse transcriptase inhibitor resistance mutations and fitness: a view from the clinic and ex vivo. Virus Res 134: 104–123. es_ES
dc.description.references Molla A, Korneyeve M, Gao Q, Vasavanonda S, Schipper PJ, Mo HM et al. (1996). Ordered accumulation of mutations in HIV protease confers resistance to ritonavir. Nat Med 2: 760–766. es_ES
dc.description.references Parera M, Pérez-Álvarez N, Clotet B, Martínez MA (2009). Epistasis among deleterious mutations in the HIV-1 protease. J Mol Biol 392: 243–250. es_ES
dc.description.references Pepin KM, Wichman HA (2007). Variable epistatic effects between mutations at host recognition sites in φX174. Evolution 67: 1710–1724. es_ES
dc.description.references Pfaffl MV (2004). Quantification strategies in real-time PCR. In Bustin SA ed A-Z of Quantitative PCR, International University Line. La Jolla USA. pp 87–112. es_ES
dc.description.references Phillips PC (2008). Epistasis – the essential role of gene interactions in the structure and evolution of genetic systems. Nat Rev Genet 9: 855–867. es_ES
dc.description.references Poelwijk FJ, Kiviet DJ, Weinreich DM, Tans SJ (2007). Empirical fitness landscapes reveal accessible evolutionary paths. Nature 445: 383–386. es_ES
dc.description.references Poelwijk FJ, Tanase-Nicola S, Kiviet DJ, Tans SJ (2011). Reciprocal sign epistasis is a necessary condition for multi-peaked fitness landscapes. J Theor Biol 272: 141–144. es_ES
dc.description.references Poon AFY, Chao L (2006). Functional origins of fitness effect-sizes of compensatory mutations in the DNA bacteriophage φX174. Evolution 60: 2032–2043. es_ES
dc.description.references Proulx SR, Phillips PC (2005). The opportunity for canalization and the evolution of genetic networks. Am Nat 165: 147–162. es_ES
dc.description.references Remold SK, Lenski RE (2004). Pervasive joint influence of epistasis and plasticity on mutational effects in Escherichia coli. Nat Genet 36: 423 426. es_ES
dc.description.references Rice WR (1989). Analyzing tables of statistical tests. Evolution 43: 223–225. es_ES
dc.description.references Rodrigo G, Carrera J, Ruiz-Ferrer V, Del Toro FJ, Llave C, Voinnet O et al. (2011). Characterization of the Arabidopsis thaliana interactome targeted by viruses. Santa Fe Institute Working Paper 11-10-049. es_ES
dc.description.references Rokyta DR, Joyce P, Caudle B, Miller C, Beisel CJ, Wichman HA (2011). Epistasis between beneficial mutations and the phenotype-to-fitness map for a ssDNA virus. PLoS Genet 7: e1002075. es_ES
dc.description.references Salverda MLM, Dellus E, Gorter FA, Debets AJM, Van der Oost J, Hoekstra RF et al. (2011). Initial mutations direct alternative pathways of protein evolution. PLoS Genet 7: e1001321. es_ES
dc.description.references Sanjuán R (2006). Quantifying antagonistic epistasis in a multifunctional RNA secondary structure of the Rous sarcoma virus. J Gen Virol 87: 1595–1602. es_ES
dc.description.references Sanjuán R, Elena SF (2006). Epistasis correlates to genomic complexity. Proc Natl Acad Sci USA 103: 14402–14405. es_ES
dc.description.references Sanjuán R, Forment J, Elena SF (2006). In silico predicted robustness of viroids RNA secondary structure. II. Interaction between mutation pairs. Mol Biol Evol 23: 2123–2130. es_ES
dc.description.references Sanjuán R, Moya A, Elena SF (2004). The contribution of epistasis to the architecture of fitness in an RNA virus. Proc Natl Acad Sci USA 101: 15376–15379. es_ES
dc.description.references Sanjuán R, Nebot MR (2008). A network model for the correlation between epistasis and genomic complexity. PLoS ONE 3: e2663. es_ES
dc.description.references Schrag SJ, Perrot V, Levin BR (1997). Adaptation to the fitness cost of antibiotic resistance in E. coli. Proc R Soc B 264: 1287–1291. es_ES
dc.description.references Van Opijnen T, Boerlijst MC, Berkhout B (2006). Effects of random mutations in the Human immunodeficiency virus type 1 transcriptional promoter on viral fitness in different host cell environments. J Virol 80: 6678–6685. es_ES
dc.description.references Weinreich DM (2005). The rank ordering of genotypic fitness values predicts genetic constraints on natural selection on landscapes lacking sign epistasis. Genetics 171: 1397–1405. es_ES
dc.description.references Weinreich DM, Delaney NF, DePristo MA, Hartl DL (2006). Darwinian evolution can follow only very few mutational paths to fitter proteins. Science 312: 111–114. es_ES
dc.description.references Weinreich DM, Watson RA, Chao L (2005). Perspective: sign epistasis and genetic constraint on evolutionary trajectories. Evolution 59: 1165–1174. es_ES
dc.description.references Welch JJ, Waxman D (2005). The nk model and population genetics. J Theor Biol 234: 329–340. es_ES
dc.description.references Wilke CO, Adami C (2001). Interaction between directional epistasis and average mutational effects. Proc R Soc B 298: 1469–1474. es_ES
dc.description.references Wilke CO, Lenski RE, Adami C (2003). Compensatory mutations cause excess of antagonistic epistasis in RNA secondary structure folding. BMC Evol Biol 3: 1–14. es_ES
dc.description.references Withlock MC, Phillips PC, Moore FBG, Tonsor SJ (1995). Multiple fitness peaks and epistasis. Annu Rev Ecol Evol Syst 26: 601–629. es_ES
dc.description.references You L, Yin J (2002). Dependence of epistasis on environment and mutation severity as revealed by in silico mutagenesis of phage T7. Genetics 160: 1273–1281. es_ES


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