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RNA Recombination Enhances Adaptability and Is Required for Virus Spread and Virulence
Open accessAbstract
Mutation and recombination are central processes driving microbial evolution. A high mutation rate fuels adaptation but also generates deleterious mutations. Recombination between two different genomes may resolve this paradox, alleviating effects of clonal interference and purging deleterious mutations. Here we demonstrate that recombination significantly accelerates adaptation and evolution during acute virus infection. We identified a poliovirus recombination determinant within the virus polymerase, mutation of which reduces recombination rates without altering replication fidelity. By generating a panel of variants with distinct mutation rates and recombination ability, we demonstrate that recombination is essential to enrich the population in beneficial mutations and purge it from deleterious mutations. The concerted activities of mutation and recombination are key to virus spread and virulence in infected animals. These findings inform a mathematical model to demonstrate that poliovirus adapts most rapidly at an optimal mutation rate determined by the trade-off between selection and accumulation of detrimental mutations.
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“Indeed, viral populations with reduced adaptation capacity yield viruses that are tissue restricted, and thus attenuated (Xiao et al., 2017a, Xiao et al., 2016).”
From Engineering the Live-Attenuated Polio Vaccine to Prevent Reversion to Virulence (2020) · cites this paper as Xiao et al., 2016
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Citations
Cites
The genetical theory of natural selection
Fisher, R. A. (1930) · doi:10.5962/bhl.title.27468 · Cited by 17,617
The relation of recombination to mutational advance
Muller, H. J. (1964) · Mutation Research · doi:10.1016/0027-5107(64)90047-8 · Cited by 2,512
The effect of linkage on limits to artificial selection
Hill, W. G., & Robertson, A. (1966) · Genetical Research · doi:10.1017/s0016672300010156 · Cited by 1,823
THE EVOLUTIONARY ADVANTAGE OF RECOMBINATION
Felsenstein, J. (1974) · Genetics · doi:10.1093/genetics/78.2.737 · Cited by 1,711
The effect of linkage on limits to artificial selection
Hill, W. G., & Robertson, A. (2007) · Genetics Research · doi:10.1017/s001667230800949x · Cited by 1,562
RNA VIRUS MUTATIONS AND FITNESS FOR SURVIVAL
Domingo, E., & Holland, J. J. (1997) · Annual Review of Microbiology · doi:10.1146/annurev.micro.51.1.151 · Cited by 1,514
Rapid Evolution of RNA Genomes
Holland, J. J., Spindler, K. R., Horodyski, F. M., Grabau, E. A., Nichol, S. T., & VandePol, S. (1982) · Science · doi:10.1126/science.7041255 · Cited by 1,478
Sanjuán, R., Nebot, M. R., Chirico, N., Mansky, L. M., & Belshaw, R. D. (2010) · Journal of Virology · doi:10.1128/jvi.00694-10 · Cited by 1,313
Muller, H. (1932) · American Naturalist · doi:10.1086/280418 · Cited by 1,242
Vignuzzi, M., Stone, J. K., Arnold, J. J., Cameron, C. E., & Andino, R. (2006) · Nature · doi:10.1038/nature04388 · Cited by 1,116
Self-citationTHE GENETICAL THEORY OF NATURAL SELECTION
Wright, S. (1930) · Journal of Heredity · doi:10.1093/oxfordjournals.jhered.a103361 · Cited by 904
The fate of competing beneficial mutations in an asexual population
Gerrish, P. J., & Lenski, R. E. (1998) · Genetica · doi:10.1023/a:1017067816551 · Cited by 895
RNA virus error catastrophe: Direct molecular test by using ribavirin
Crotty, S., Cameron, C. E., & Andino, R. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.111085598 · Cited by 844
Self-citationThe fate of competing beneficial mutations in an asexual population
Gerrish, P. J., & Lenski, R. E. (1998) · Contemporary issues in genetics and evolution · doi:10.1007/978-94-011-5210-5_12 · Cited by 747
Rapid Evolution Of RNA Viruses
Steinhauer, D. A., & Holland, J. J. (1987) · Annual Review of Microbiology · doi:10.1146/annurev.mi.41.100187.002205 · Cited by 598
Evolutionary aspects of recombination in RNA viruses
Worobey, M., & Holmes, E. C. (1999) · Journal of General Virology · doi:10.1099/0022-1317-80-10-2535 · Cited by 556
Racaniello, V. R., & Baltimore, D. (1981) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.78.8.4887 · Cited by 550
The fate of competing beneficial mutations in an asexual population.
Gerrish, P. J., & Lenski, R. E. (1998) · PubMed · Cited by 520
The mechanism of RNA recombination in poliovirus
Kirkegaard, K., & Baltimore, D. (1986) · Cell · doi:10.1016/0092-8674(86)90600-8 · Cited by 499
Fitness of RNA virus decreased by Muller’s ratchet
Chao, L. (1990) · Nature · doi:10.1038/348454a0 · Cited by 488
Basic concepts in RNA virus evolution
Domingo, E., Escarmı́s, C., Sevilla, N., Moyá, A., Elena, S. F., Quer, J., Novella, I. S., & Holland, J. J. (1996) · The FASEB Journal · doi:10.1096/fasebj.10.8.8666162 · Cited by 448
Lack of evidence for proofreading mechanisms associated with an RNA virus polymerase
Steinhauer, D. A., Domingo, E., & Holland, J. J. (1992) · Gene · doi:10.1016/0378-1119(92)90216-c · Cited by 415
Pfeiffer, J. K., & Kirkegaard, K. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1232294100 · Cited by 405
Mutational and fitness landscapes of an RNA virus revealed through population sequencing
Acevedo, A., Brodsky, L., & Andino, R. (2013) · Nature · doi:10.1038/nature12861 · Cited by 389
Self-citationRapid fitness losses in mammalian RNA virus clones due to Muller’s ratchet
Duarte, E., Clarke, D., Moya, A., Domingo, E., & Holland, J. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.13.6015 · Cited by 331
Adaptive Value of High Mutation Rates of RNA Viruses: Separating Causes from Consequences
Elena, S. F., & Sanjuán, R. (2005) · Journal of Virology · doi:10.1128/jvi.79.18.11555-11558.2005 · Cited by 329
Host and virus determinants of picornavirus pathogenesis and tropism
Whitton, J. L., Cornell, C. T., & Feuer, R. (2005) · Nature Reviews Microbiology · doi:10.1038/nrmicro1284 · Cited by 249
Distribution of fixed beneficial mutations and the rate of adaptation in asexual populations
Good, B. H., Rouzine, I. M., Balick, D. J., Hallatschek, O., & Desai, M. M. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1119910109 · Cited by 242
Self-citationThe solitary wave of asexual evolution
Rouzine, I. M., Wakeley, J., & Coffin, J. M. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.242719299 · Cited by 240
Self-citationCooper, T. F. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050225 · Cited by 209
The Evolutionary Genetics of Emerging Viruses
Holmes, E. C. (2009) · Annual Review of Ecology Evolution and Systematics · doi:10.1146/annurev.ecolsys.110308.120248 · Cited by 200
The traveling-wave approach to asexual evolution: Muller's ratchet and speed of adaptation
Rouzine, I. M., Brunet, É., & Wilke, C. O. (2007) · Theoretical Population Biology · doi:10.1016/j.tpb.2007.10.004 · Cited by 175
Self-citationRNA-RNA Recombination in Plant Virus Replication and Evolution
Sztuba-Solińska, J., Urbanowicz, A., Figlerowicz, M., & Bujarski, J. J. (2011) · Annual Review of Phytopathology · doi:10.1146/annurev-phyto-072910-095351 · Cited by 167
The advantage of sex in evolving yeast populations
Zeyl, C., & Bell, G. (1997) · Nature · doi:10.1038/41312 · Cited by 159
The red queen reigns in the kingdom of RNA viruses.
Clarke, D. K., Duarte, E. A., Elena, S. F., Moyá, A., Domingo, E., & Holland, J. J. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.11.4821 · Cited by 157
Lauring, A. S., Acevedo, A., Cooper, S., & Andino, R. (2012) · Cell Host & Microbe · doi:10.1016/j.chom.2012.10.008 · Cited by 143
Self-citationThe Effect of Deleterious Alleles on Adaptation in Asexual Populations
Johnson, T., & Barton, N. (2002) · Genetics · doi:10.1093/genetics/162.1.395 · Cited by 126
Rate of Adaptation in Large Sexual Populations
Neher, R. A., Shraiman, B. I., & Fisher, D. S. (2009) · Genetics · doi:10.1534/genetics.109.109009 · Cited by 115
Dynamic Mutation–Selection Balance as an Evolutionary Attractor
Goyal, S., Balick, D. J., Jerison, E. R., Neher, R. A., Shraiman, B. I., & Desai, M. M. (2012) · Genetics · doi:10.1534/genetics.112.141291 · Cited by 112
The Hill–Robertson Effect and the Evolution of Recombination
Roze, D., & Barton, N. (2006) · Genetics · doi:10.1534/genetics.106.058586 · Cited by 109
Batorsky, R., Kearney, M. F., Palmer, S., Maldarelli, F. M., Rouzine, I. M., & Coffin, J. M. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1102036108 · Cited by 105
Self-citationLibrary preparation for highly accurate population sequencing of RNA viruses
Acevedo, A., & Andino, R. (2014) · Nature Protocols · doi:10.1038/nprot.2014.118 · Cited by 100
Self-citationClune, J., Misevic, D., Ofria, C., Lenski, R. E., Elena, S. F., & Sanjuán, R. (2008) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000187 · Cited by 97
RNA Virus Population Diversity, an Optimum for Maximal Fitness and Virulence
Korboukh, V. K., Lee, C. A., Acevedo, A., Vignuzzi, M., Xiao, Y., Arnold, J. J., Hemperly, S., Graci, J. D., August, A., Andino, R., et al. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.592303 · Cited by 96
Self-citationClune, J., Misevic, D., Ofria, C., Lenski, R. E., Elena, S. F., & Sanjuán, R. (2013) · Genetic and Evolutionary Computation Conference Companion (GECCO Companion) · doi:10.1145/2464576.2464597 · Cited by 90
Evolution of Human Immunodeficiency Virus Under Selection and Weak Recombination
Rouzine, I. M., & Coffin, J. M. (2005) · Genetics · doi:10.1534/genetics.104.029926 · Cited by 85
Self-citationLowry, K., Woodman, A., Cook, J., & Evans, D. J. (2014) · PLoS Pathogens · doi:10.1371/journal.ppat.1004191 · Cited by 80
Crotty, S., Hix, L. M., Sigal, L. J., & Andino, R. (2002) · Journal of General Virology · doi:10.1099/0022-1317-83-7-1707 · Cited by 74
Self-citationStructure and function analysis of the poliovirus cis-acting replication element (CRE)
Goodfellow, I., KERRIGAN, D., & Evans, D. J. (2003) · RNA · doi:10.1261/rna.2950603 · Cited by 74
Molecular Mechanisms of Poliovirus Variation and Evolution
Agol, V. I. (2006) · Current Topics in Microbiology and Immunology · doi:10.1007/3-540-26397-7_8 · Cited by 73
Identification and Manipulation of the Molecular Determinants Influencing Poliovirus Recombination
Runckel, C., Westesson, O., Andino, R., & DeRisi, J. L. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003164 · Cited by 61
Self-citationCosts and Benefits of Mutational Robustness in RNA Viruses
Stern, A., Bianco, S., Yeh, M. T., Wright, C., Butcher, K. D., Tang, C., Nielsen, R., & Andino, R. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.07.011 · Cited by 52
Self-citationThe Role of Advantageous Mutations in Enhancing the Evolution of a Recombination Modifier
Hartfield, M., Otto, S. P., & Keightley, P. D. (2010) · Genetics · doi:10.1534/genetics.109.112920 · Cited by 47
Multi-site adaptation in the presence of infrequent recombination
Rouzine, I. M., & Coffin, J. M. (2010) · Theoretical Population Biology · doi:10.1016/j.tpb.2010.02.001 · Cited by 39
Self-citationGenomic mutation rates that neutralize adaptive evolution and natural selection
Gerrish, P. J., Colato, A., & Sniegowski, P. (2013) · Journal of The Royal Society Interface · doi:10.1098/rsif.2013.0329 · Cited by 29
RNA viruses as complex adaptive systems
Elena, S. F., & Sanjuán, R. (2005) · Biosystems · doi:10.1016/j.biosystems.2005.02.001 · Cited by 20
Rapid Adaptive Amplification of Preexisting Variation in an RNA Virus
Dutta, R. N., Rouzine, I. M., Smith, S. D., Wilke, C. O., & Novella, I. S. (2008) · Journal of Virology · doi:10.1128/jvi.02446-07 · Cited by 17
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Independent infections of porcine deltacoronavirus among Haitian children
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The life cycle of non-polio enteroviruses and how to target it
Baggen, J., Thibaut, H. J., Strating, J. R. P. M., & van Kuppeveld, F. J. M. (2018) · Nature Reviews Microbiology · doi:10.1038/s41579-018-0005-4 · Cited by 500
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Metadata
- Authors
- Xiao, Y., Rouzine, I. M., Bianco, S., Acevedo, A., Goldstein, E. F., Farkov, M., Brodsky, L., & Andino, R.
- Affiliations
- University of California, San Francisco (US)
- IBM Research - Almaden (US)
- University of Haifa (IL)
- Corresponding author
- Andino, Raul
- Venue
- Cell Host & Microbe
- Publisher
- Elsevier BV
- Published
- 2016-04
- Volume
- 19
- Issue
- 4
- Pages
- 493-503
- ISSN
- 1931-3128 (ISSN-L)
- PMC
- PMC4840895
- OpenAlex
- W2335860311
- Cited by
- 157
- References
- 57
- Citations by year
- 2026: 10 · 2025: 10 · 2024: 14 · 2023: 19 · 2022: 13 · 2021: 17 · 2020: 20 · 2019: 16 · 2018: 21 · 2017: 11 · 2016: 6
- FWCI
- 14.53
- Type
- journal article
- Language
- en
- Update notices
- erratum (2017-09-13)
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell Host & Microbe (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- NIH (R01, AI36178, AI40085, P01 AI091575)
- University of California
- DoD-DARPA
- Irvin “Tack” Kuntz
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Health Sciences › Medicine › Infectious Diseases › Viral Infections and Immunology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
- Keywords
- RNA recombination, poliovirus, viral adaptation, mutation rate, deleterious mutations, clonal interference, purging of deleterious mutations, viral virulence, viral spread, acute viral infection
- MeSH terms
- Adaptation, Physiological, Animals, Humans, Poliomyelitis, Recombination, Genetic, DNA-Directed RNA Polymerases, RNA, Viral, Selection, Genetic, Viral Proteins, Virulence, Virus Replication, Poliovirus, Evolution, Molecular
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