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.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Viral populations with reduced adaptation capacity yield viruses that are tissue restricted, and thus attenuated.
“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
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The genetical theory of natural selection
Fisher, R. A. (1930) · doi:10.5962/bhl.title.27468 · Cited by 17,617 · see citing works
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 · see citing works
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 · see citing works
THE EVOLUTIONARY ADVANTAGE OF RECOMBINATION
Felsenstein, J. (1974) · Genetics · doi:10.1093/genetics/78.2.737 · Cited by 1,711 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 1,247 · see citing works
Muller, H. (1932) · American Naturalist · doi:10.1086/280418 · Cited by 1,242 · see citing works
Vignuzzi, M., Stone, J. K., Arnold, J. J., Cameron, C. E., & Andino, R. (2006) · Nature · doi:10.1038/nature04388 · Cited by 1,116 · see citing works
Self-citationTHE GENETICAL THEORY OF NATURAL SELECTION
Wright, S. (1930) · Journal of Heredity · doi:10.1093/oxfordjournals.jhered.a103361 · Cited by 899 · see citing works
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 853 · see citing works
Self-citationThe fate of competing beneficial mutations in an asexual population
Gerrish, P. J., & Lenski, R. E. (1998) · Genetica · doi:10.1023/a:1017067816551 · Cited by 783 · see citing works
The 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 721 · see citing works
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 · see citing works
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 · see citing works
Racaniello, V. R., & Baltimore, D. (1981) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.78.8.4887 · Cited by 555 · see citing works
The fate of competing beneficial mutations in an asexual population.
Gerrish, P. J., & Lenski, R. E. (1998) · PubMed · Cited by 520 · see citing works
The mechanism of RNA recombination in poliovirus
Kirkegaard, K., & Baltimore, D. (1986) · Cell · doi:10.1016/0092-8674(86)90600-8 · Cited by 499 · see citing works
Fitness of RNA virus decreased by Muller’s ratchet
Chao, L. (1990) · Nature · doi:10.1038/348454a0 · Cited by 488 · see citing works
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 · see citing works
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 · see citing works
Pfeiffer, J. K., & Kirkegaard, K. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1232294100 · Cited by 405 · see citing works
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 379 · see citing works
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 · see citing works
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 320 · see citing works
The 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 260 · see citing works
Self-citationHost 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 · see citing works
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 240 · see citing works
Self-citationCooper, T. F. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050225 · Cited by 209 · see citing works
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 194 · see citing works
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 · see citing works
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 · see citing works
The advantage of sex in evolving yeast populations
Zeyl, C., & Bell, G. (1997) · Nature · doi:10.1038/41312 · Cited by 159 · see citing works
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 · see citing works
Lauring, A. S., Acevedo, A., Cooper, S., & Andino, R. (2012) · Cell Host & Microbe · doi:10.1016/j.chom.2012.10.008 · Cited by 135 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
The Hill–Robertson Effect and the Evolution of Recombination
Roze, D., & Barton, N. (2006) · Genetics · doi:10.1534/genetics.106.058586 · Cited by 109 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Self-citationLowry, K., Woodman, A., Cook, J., & Evans, D. J. (2014) · PLoS Pathogens · doi:10.1371/journal.ppat.1004191 · Cited by 78 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 51 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
RNA viruses as complex adaptive systems
Elena, S. F., & Sanjuán, R. (2005) · Biosystems · doi:10.1016/j.biosystems.2005.02.001 · Cited by 20 · see citing works
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 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Sanjuán, R., & Domingo‐Calap, P. (2016) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-016-2299-6 · Cited by 952 · see citing works
The molecular virology of coronaviruses
Hartenian, E., Nandakumar, D., Lari, A., Ly, M., Tucker, J. M., & Glaunsinger, B. A. (2020) · Journal of Biological Chemistry · doi:10.1074/jbc.rev120.013930 · Cited by 513 · see citing works
Independent infections of porcine deltacoronavirus among Haitian children
Lednicky, J. A., Tagliamonte, M. S., White, S. K., Elbadry, M. A., Alam, M. M., Stephenson, C. J., Bonny, T. S., Loeb, J. C., Telisma, T., Chavannes, S., et al. (2021) · Nature · doi:10.1038/s41586-021-04111-z · Cited by 489 · see citing works
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 483 · see citing works
Learning the language of viral evolution and escape
Hie, B., Zhong, E. D., Berger, B., & Bryson, B. (2021) · Science · doi:10.1126/science.abd7331 · Cited by 361 · see citing works
Domingo, E., & Perales, C. (2019) · PLoS Genetics · doi:10.1371/journal.pgen.1008271 · Cited by 330 · see citing works
SARS-CoV-2/COVID-19: Viral Genomics, Epidemiology, Vaccines, and Therapeutic Interventions
Uddin, M. J., Mustafa, F., Rizvi, T. A., Loney, T., Suwaidi, H. S. A., Al-Marzouqi, A. H. H., Kamal‐Eldin, A., Alsabeeha, N. H. M., Adrian, T. E., Stefanini, C., et al. (2020) · Viruses · doi:10.3390/v12050526 · Cited by 314 · see citing works
Engineering the Live-Attenuated Polio Vaccine to Prevent Reversion to Virulence
Yeh, M. T., Bujaki, E., Dolan, P. T., Smith, M., Wahid, R., Konz, J., Weiner, A. J., Bandyopadhyay, A. S., Van Damme, P., De Coster, I., et al. (2020) · Cell Host & Microbe · doi:10.1016/j.chom.2020.04.003 · Cited by 221 · see citing works
Self-citationPicornaviridae—the ever-growing virus family
Zell, R. (2017) · Archives of Virology · doi:10.1007/s00705-017-3614-8 · Cited by 196 · see citing works
Bacteria Facilitate Enteric Virus Co-infection of Mammalian Cells and Promote Genetic Recombination
Erickson, A. K., Jesudhasan, P. R. R., Mayer, M. J., Narbad, A., Winter, S., & Pfeiffer, J. K. (2017) · Cell Host & Microbe · doi:10.1016/j.chom.2017.11.007 · Cited by 187 · see citing works
Mechanisms and Concepts in RNA Virus Population Dynamics and Evolution
Dolan, P., Whitfield, Z. J., & Andino, R. (2018) · Annual Review of Virology · doi:10.1146/annurev-virology-101416-041718 · Cited by 170 · see citing works
Self-citationVariation in Recombination Rate: Adaptive or Not?
Ritz, K. R., Noor, M. A. F., & Singh, N. D. (2017) · Trends in Genetics · doi:10.1016/j.tig.2017.03.003 · Cited by 170 · see citing works
A speed–fidelity trade-off determines the mutation rate and virulence of an RNA virus
Fitzsimmons, W. J., Woods, R. J., McCrone, J. T., Woodman, A., Arnold, J. J., Yennawar, M., Evans, R., Cameron, C. E., & Lauring, A. S. (2018) · PLoS Biology · doi:10.1371/journal.pbio.2006459 · Cited by 132 · see citing works
Petton, B., Destoumieux‐Garzón, D., Pernet, F., Toulza, È., de Lorgeril, J., Dégremont, L., & Mitta, G. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.630343 · Cited by 128 · see citing works
Recombination in Enteroviruses, a Multi-Step Modular Evolutionary Process
Muslin, C., Kain, A. M., Bessaud, M., Blondel, B., & Delpeyroux, F. (2019) · Viruses · doi:10.3390/v11090859 · Cited by 127 · see citing works
The Mutational Robustness of Influenza A Virus
Visher, E., Whitefield, S. E., McCrone, J. T., Fitzsimmons, W. J., & Lauring, A. S. (2016) · PLoS Pathogens · doi:10.1371/journal.ppat.1005856 · Cited by 102 · see citing works
Picornaviral polymerase structure, function, and fidelity modulation
Peersen, O. B. (2017) · Virus Research · doi:10.1016/j.virusres.2017.01.026 · Cited by 96 · see citing works
Mechanisms and consequences of positive-strand RNA virus recombination
Bentley, K., & Evans, D. J. (2018) · Journal of General Virology · doi:10.1099/jgv.0.001142 · Cited by 99 · see citing works
Mapping the Evolutionary Potential of RNA Viruses
Dolan, P., Whitfield, Z. J., & Andino, R. (2018) · Cell Host & Microbe · doi:10.1016/j.chom.2018.03.012 · Cited by 91 · see citing works
Self-citationPopulation Diversity and Collective Interactions during Influenza Virus Infection
Brooke, C. B. (2017) · Journal of Virology · doi:10.1128/jvi.01164-17 · Cited by 86 · see citing works
Poliovirus intrahost evolution is required to overcome tissue-specific innate immune responses
Xiao, Y., Dolan, P., Goldstein, E. F., Li, M., Farkov, M., Brodsky, L., & Andino, R. (2017) · Nature Communications · doi:10.1038/s41467-017-00354-5 · Cited by 89 · see citing works
Self-citationColson, P., Fournier, P., Delerce, J., Million, M., Bedotto, M., Houhamdi, L., Yahi, N., Bayette, J., Levasseur, A., Fantini, J., et al. (2022) · Journal of Medical Virology · doi:10.1002/jmv.27789 · Cited by 76 · see citing works
Tohma, K., Lepore, C. J., Martinez, M., Degiuseppe, J. I., Khamrin, P., Saito, M., Mayta, H., Nwaba, A. U. A., Ford-Siltz, L. A., Green, K. Y., et al. (2021) · PLoS Pathogens · doi:10.1371/journal.ppat.1009744 · Cited by 73 · see citing works
Genetic variation in adaptability and pleiotropy in budding yeast
Jerison, E. R., Kryazhimskiy, S., Mitchell, J. K., Bloom, J. S., Kruglyak, L., & Desai, M. M. (2017) · eLife · doi:10.7554/elife.27167 · Cited by 70 · see citing works
Characterizing Transcriptional Regulatory Sequences in Coronaviruses and Their Role in Recombination
Yang, Y., Yan, W., Hall, A. B., & Jiang, X. (2020) · Molecular Biology and Evolution · doi:10.1093/molbev/msaa281 · Cited by 64 · see citing works
Virus population dynamics during infection
Poirier, E. Z., & Vignuzzi, M. (2017) · Current Opinion in Virology · doi:10.1016/j.coviro.2017.03.013 · Cited by 64 · see citing works
Nikolaidis, M., Mimouli, K., Kyriakopoulou, Z., Tsimpidis, M., Tsakogiannis, D., Markoulatos, P., & Amoutzias, G. D. (2018) · Virology · doi:10.1016/j.virol.2018.10.006 · Cited by 64 · see citing works
Recombination in Positive-Strand RNA Viruses
Wang, H., Cui, X., Cai, X., & An, T. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.870759 · Cited by 63 · see citing works
A New Mechanistic Model for Viral Cross Protection and Superinfection Exclusion
Zhang, X., Zhang, S., Guo, Q., Sun, R., Wèi, T., & Qu, F. (2018) · Frontiers in Plant Science · doi:10.3389/fpls.2018.00040 · Cited by 60 · see citing works
Graham, R. L., Deming, D., Deming, M. E., Yount, B. L., & Baric, R. S. (2018) · Communications Biology · doi:10.1038/s42003-018-0175-7 · Cited by 58 · see citing works
Geoghegan, J. L., & Holmes, E. C. (2018) · Genetics · doi:10.1534/genetics.118.301556 · Cited by 56 · see citing works
Brito, B. P., Pauszek, S. J., Hartwig, E. J., Smoliga, G. R., Vu, L. T., Đông, P. V., Stenfeldt, C., Rodrı́guez, L. L., King, D. P., Knowles, N. J., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-24870-6 · Cited by 53 · see citing works
Emergence and widespread circulation of a recombinant SARS-CoV-2 lineage in North America
Gutiérrez, B., Castelán-Sánchez, H. G., Cândido, D. D. S., Jackson, B., Fleishon, S., Houzet, R., Ruis, C., Delaye, L., Faria, N. R., Rambaut, A., et al. (2022) · Cell Host & Microbe · doi:10.1016/j.chom.2022.06.010 · Cited by 52 · see citing works
Liu, F., Huang, Y., Wang, Q., & Shan, H. (2020) · Viruses · doi:10.3390/v12030283 · Cited by 51 · see citing works
Bessaud, M., Joffret, M., Blondel, B., & Delpeyroux, F. (2016) · Scientific Reports · doi:10.1038/srep38831 · Cited by 48 · see citing works
Dissemination of Internal Ribosomal Entry Sites (IRES) Between Viruses by Horizontal Gene Transfer
Arhab, Y., Bulakhov, A. G., Pestova, T. V., & Hellen, C. U. T. (2020) · Viruses · doi:10.3390/v12060612 · Cited by 45 · see citing works
Evolutionary implications of SARS-CoV-2 vaccination for the future design of vaccination strategies
Rouzine, I. M., & Rozhnova, G. (2023) · Communications Medicine · doi:10.1038/s43856-023-00320-x · Cited by 47 · see citing works
Self-citationRNA recombination at Chikungunya virus 3'UTR as an evolutionary mechanism that provides adaptability
Filomatori, C. V., Bardossy, E. S., Merwaiss, F., Suzuki, Y., Henrion-Lacritick, A., Saleh, M., & Alvarez, D. E. (2019) · PLoS Pathogens · doi:10.1371/journal.ppat.1007706 · Cited by 46 · see citing works
Dynamics of West Nile virus evolution in mosquito vectors
Grubaugh, N. D., & Ebel, G. D. (2016) · Current Opinion in Virology · doi:10.1016/j.coviro.2016.09.007 · Cited by 45 · see citing works
Li, C., Wang, H., Shi, J., Yang, D., Zhou, G., Chang, J., Cameron, C. E., Woodman, A., & Li, Y. (2019) · Journal of Virology · doi:10.1128/jvi.00576-19 · Cited by 45 · see citing works
Cui, X., Xia, D., Huang, X., Sun, Y., Shī, M., Zhang, J., Li, G., Yang, Y., Wang, H., Cai, X., et al. (2022) · Microbiology Spectrum · doi:10.1128/spectrum.02934-22 · Cited by 42 · see citing works
Brennan, J. W., & Sun, Y. (2024) · mBio · doi:10.1128/mbio.00692-24 · Cited by 42 · see citing works
RNA Virus Fidelity Mutants: A Useful Tool for Evolutionary Biology or a Complex Challenge?
Kautz, T. F., & Forrester, N. L. (2018) · Viruses · doi:10.3390/v10110600 · Cited by 42 · see citing works
Poliovirus Polymerase Leu420 Facilitates RNA Recombination and Ribavirin Resistance
Kempf, B. J., Peersen, O. B., & Barton, D. J. (2016) · Journal of Virology · doi:10.1128/jvi.00078-16 · Cited by 41 · see citing works
Evolutionary and Structural Overview of Human Picornavirus Capsid Antibody Evasion
Cifuente, J. O., & Moratorio, G. (2019) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2019.00283 · Cited by 38 · see citing works
Ribosomal control in RNA virus-infected cells
Wang, X., Zhu, J., Zhang, D., & Liu, G. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.1026887 · Cited by 37 · see citing works
Emergency Services of Viral RNAs: Repair and Remodeling
Agol, V. I., & Gmyl, A. P. (2018) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00067-17 · Cited by 34 · see citing works
Honey Bee Virus Transmission via Hive Products
Schittny, D., Yañez, O., & Neumann, P. (2020) · Veterinary Sciences · doi:10.3390/vetsci7030096 · Cited by 36 · see citing works
Ngangas, S. T., Bisseux, M., Jugie, G., Lambert, C., Cohen, R., Werner, A., Archimbaud, C., Henquell, C., Mirand, A., & Bailly, J. (2022) · Viruses · doi:10.3390/v14051078 · Cited by 33 · see citing works
Changes in the EV-A71 Genome through Recombination and Spontaneous Mutations: Impact on Virulence
Mandary, M. B., & Poh, C. L. (2018) · Viruses · doi:10.3390/v10060320 · Cited by 33 · see citing works
Rangel, M. A., Dolan, P., Taguwa, S., Xiao, Y., Andino, R., & Frydman, J. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2304667120 · Cited by 33 · see citing works
Self-citationPicornavirus RNA Recombination Counteracts Error Catastrophe
Kempf, B. J., Watkins, C. L., Peersen, O. B., & Barton, D. J. (2019) · Journal of Virology · doi:10.1128/jvi.00652-19 · Cited by 29 · see citing works
Mastrodomenico, V., Esin, J. J., Graham, M. L., Tate, P. M., Hawkins, G. M., Sandler, Z. J., Rademacher, D. J., Kicmal, T., Dial, C. N., & Mounce, B. C. (2019) · Journal of Virology · doi:10.1128/jvi.00530-19 · Cited by 30 · see citing works
Genomic evidence for divergent co-infections of co-circulating SARS-CoV-2 lineages
Zhou, H., Cheng, Y., Xu, L. S., Li, J.-Y., Tao, C., Ji, C., Han, N., Yang, R., Wu, H. M., Li, Y., et al. (2022) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2022.07.042 · Cited by 29 · see citing works
Homologous recombination is an intrinsic defense against antiviral RNA interference
Aguado, L. C., Jordan, T. X., Hsieh, E., Blanco-Melo, D., Heard, J. R., Panis, M., Vignuzzi, M., & tenOever, B. R. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1810229115 · Cited by 27 · see citing works
From RNA World to SARS-CoV-2: The Edited Story of RNA Viral Evolution
Kockler, Z. W., & Gordenin, D. A. (2021) · Cells · doi:10.3390/cells10061557 · Cited by 24 · see citing works
Bradley, C. C., Wang, C., Gordon, A. J. E., Wen, A. X., Luna, P. N., Cooke, M. B., Kohrn, B. F., Kennedy, S. R., Avadhanula, V., Piedra, P. A., et al. (2024) · Nature Microbiology · doi:10.1038/s41564-024-01655-4 · Cited by 26 · see citing works
Tagliamonte, M. S., Abid, N., Borocci, S., Sangiovanni, E., Ostrov, D. A., Pond, S. L. K., Salemi, M., Chillemi, G., & Mavian, C. N. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms22010080 · Cited by 24 · see citing works
Induced intra- and intermolecular template switching as a therapeutic mechanism against RNA viruses
Janissen, R., Woodman, A., Shengjuler, D., Vallet, T., Lee, K.-M., Kuijpers, L., Moustafa, I. M., Fitzgerald, F., Huang, P.-N., Perkins, A. L., et al. (2021) · Molecular Cell · doi:10.1016/j.molcel.2021.10.003 · Cited by 23 · see citing works
A proofreading-impaired herpesvirus generates populations with quasispecies-like structure
Trimpert, J., Groenke, N., Kunec, D., Eschke, K., He, S., McMahon, D. P., & Osterrieder, N. (2019) · Nature Microbiology · doi:10.1038/s41564-019-0547-x · Cited by 23 · see citing works
Delmotte, J., Chaparro, C., Galinier, R., de Lorgeril, J., Petton, B., Stenger, P., Vidal‐Dupiol, J., Destoumieux‐Garzón, D., Gueguen, Y., Montagnani, C., et al. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.01579 · Cited by 22 · see citing works
Impact of Cultivated Hosts on the Recombination of Cucumber Mosaic Virus
Ouedraogo, R. S., Pita, J. S., Somda, I., Traoré, O., & Roossinck, M. J. (2019) · Journal of Virology · doi:10.1128/jvi.01770-18 · Cited by 22 · see citing works
Genetic Characterization and Molecular Evolution of Urban Seoul Virus in Southern China
Su, Q., Chen, Y., Li, M., Ma, J., Wang, B., Luo, J., & He, H. (2019) · Viruses · doi:10.3390/v11121137 · Cited by 21 · see citing works
The advantage of recombination when selection is acting at many genetic Loci
Hickey, D. A., & Golding, G. B. (2018) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2018.01.018 · Cited by 21 · see citing works
Bentley, K., Alnaji, F. G., Woodford, L., Jones, S., Woodman, A., & Evans, D. J. (2021) · PLoS Pathogens · doi:10.1371/journal.ppat.1009676 · Cited by 22 · see citing works
Burel, E., Colson, P., Lagier, J., Levasseur, A., Bedotto, M., Lavrard, P., Fournier, P., Scola, B. L., & Raoult, D. (2022) · Viruses · doi:10.3390/v14061266 · Cited by 20 · see citing works
Kasahara‐Kamiie, M., Kagawa, M., Shiokawa, M., Sunaga, F., Fukase, Y., Aihara, N., Shiga, T., Kamiie, J., Aoki, H., & Nagai, M. (2021) · Transboundary and Emerging Diseases · doi:10.1111/tbed.14149 · Cited by 19 · see citing works
Wahid, R., Mercer, L. D., León, T. D., DeAntonio, R., Sáez‐Llorens, X., Macadam, A. J., Chumakov, K., Strating, J. R. P. M., Koel, B. F., Konopka‐Anstadt, J. L., et al. (2022) · The Lancet Microbe · doi:10.1016/s2666-5247(22)00254-3 · Cited by 18 · see citing works
Self-citationCellular and Natural Viral Engineering in Cognition-Based Evolution
Miller, W. B., Reber, A. S., Marshall, P., & Baluška, F. (2023) · Communicative & Integrative Biology · doi:10.1080/19420889.2023.2196145 · Cited by 18 · see citing works
Enterovirus B types cause severe infection in infants aged 0–3 months
Yang, X., Duan, L., Zhan, W., Tang, Y., Liang, L., Xie, J. L., & Luo, M. (2023) · Virology Journal · doi:10.1186/s12985-023-01965-9 · Cited by 16 · see citing works
Park, J.-H., & Lee, C. (2020) · Archives of Virology · doi:10.1007/s00705-020-04767-4 · Cited by 16 · see citing works
Characterization of Viral Populations by Using Circular Sequencing
Whitfield, Z. J., & Andino, R. (2016) · Journal of Virology · doi:10.1128/jvi.00804-14 · Cited by 15 · see citing works
Self-citationKim, H.-J., Aponte-Diaz, D., Sotoudegan, M. S., Shengjuler, D., Arnold, J. J., & Cameron, C. E. (2023) · PLoS Biology · doi:10.1371/journal.pbio.3001693 · Cited by 12 · see citing works
Devaux, C. A., Pontarotti, P., Levasseur, A., Colson, P., & Raoult, D. (2024) · Frontiers in Public Health · doi:10.3389/fpubh.2023.1284337 · Cited by 16 · see citing works
Insular Microbiogeography: Three Pathogens as Exemplars
Kaufman, J. H., Elkins, C. A., Davis, M., Weis, A. M., Huang, B. C., Mammel, M. K., Patel, I. R., Beck, K. L., Edlund, S. B., Chambliss, D. D., et al. (2019) · Current Issues in Molecular Biology · doi:10.21775/cimb.036.089 · Cited by 14 · see citing works
Self-citationEvaluation of recombination detection methods for viral sequencing
Jaya, F. R., Brito, B. P., & Darling, A. E. (2023) · Virus Evolution · doi:10.1093/ve/vead066 · Cited by 12 · see citing works
A Low Fidelity Virus Shows Increased Recombination during the Removal of an Alphavirus Reporter Gene
Kautz, T. F., Jaworski, E. A., Routh, A. L., & Forrester, N. L. (2020) · Viruses · doi:10.3390/v12060660 · Cited by 11 · see citing works
Interactions among microorganisms open up a new world for anti‐infectious therapy
Zhang, Y., Zhang, H., Xu, T., Zeng, L., Liu, F., Huang, X., & Liu, Q. (2022) · FEBS Journal · doi:10.1111/febs.16705 · Cited by 12 · see citing works
Steinberg, A. P., Silander, O., & Kussell, E. L. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2206945119 · Cited by 11 · see citing works
Sensors for surveillance of RNA viruses: a One Health perspective
Chen, Y., Wang, P., Zhang, F., Dai, H., Jiao, X.-Y., Wang, X., Yu, Q., Kang, M., Su, S., & Wang, D. (2024) · The Lancet Microbe · doi:10.1016/j.lanmic.2024.101029 · Cited by 11 · see citing works
Spatial Virome Analysis of Zanthoxylum armatum Trees Affected With the Flower Yellowing Disease
Cao, M., Zhang, S., Liao, R., Wang, X., Xuan, Z., Zhan, B., Li, Z., Zhang, J., Du, X., Tang, Z., et al. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.702210 · Cited by 11 · see citing works
Epistasis detectably alters correlations between genomic sites in a narrow parameter window
Pedruzzi, G., & Rouzine, I. M. (2019) · PLoS ONE · doi:10.1371/journal.pone.0214036 · Cited by 11 · see citing works
Self-citationFurusawa, Y., Yamada, S., Lopes, T. J. D. S., Dutta, J., Khan, Z., Kriti, D., van Bakel, H., & Kawaoka, Y. (2019) · mBio · doi:10.1128/mbio.01794-19 · Cited by 10 · see citing works
Kovalev, N., Pogany, J., & Nagy, P. D. (2019) · Journal of Virology · doi:10.1128/jvi.01015-19 · Cited by 10 · see citing works
SARS-CoV-2 and human retroelements: a case for molecular mimicry?
Koch, B. (2022) · BMC Genomic Data · doi:10.1186/s12863-022-01040-2 · Cited by 10 · see citing works
Natural recombination of equine hepacivirus subtype 1 within the NS5A and NS5B genes
Lu, G., Ou, J., Sun, Y., Wu, L., Xu, H., Zhang, G., & Li, S. (2019) · Virology · doi:10.1016/j.virol.2019.05.006 · Cited by 10 · see citing works
Watkins, C. L., Kempf, B. J., Beaucourt, S. M., Barton, D. J., & Peersen, O. B. (2020) · Journal of Biological Chemistry · doi:10.1074/jbc.ra120.013906 · Cited by 10 · see citing works
A review of the recombination events, mechanisms and consequences of Coxsackievirus A6
Wang, Z., & Wen, H. (2024) · Infectious Medicine · doi:10.1016/j.imj.2024.100115 · Cited by 9 · see citing works
An Evolutionary Model of Progression to AIDS
Rouzine, I. M. (2020) · Microorganisms · doi:10.3390/microorganisms8111714 · Cited by 9 · see citing works
Self-citationLiu, F., Wang, Q., Huang, Y., Wang, N., Zhang, Y., & Shan, H. (2020) · Frontiers in Veterinary Science · doi:10.3389/fvets.2020.600796 · Cited by 9 · see citing works
Emergence of a novel recombinant of CV-A5 in HFMD epidemics in Xiangyang, China
Yu, Y., Luo, Z., Jin, W.-P., Mai, J., Qian, S., Lu, J., Wei, Z., Meng, S., Wang, Z., Guan, X., et al. (2021) · BMC Medical Genomics · doi:10.1186/s12920-021-01107-6 · Cited by 9 · see citing works
IDbSV: An Open-Access Repository for Monitoring SARS-CoV-2 Variations and Evolution
Essabbar, A., Kartti, S., Alouane, T., Hakmi, M., Belyamani, L., & Ibrahimi, A. (2021) · Frontiers in Medicine · doi:10.3389/fmed.2021.765249 · Cited by 8 · see citing works
Tavakoli, A., Lotfı, F. H., Lotfi, M., Bayati, M., Seif, M., Salesi, M., Emadi, M., Keshavarz, K., & Delavari, S. (2023) · PubMed Central · doi:10.30476/ijms.2022.94615.2598 · Cited by 8 · see citing works
Wang, Z., & Pei, W. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1331981 · Cited by 8 · see citing works
Genetic recombination of poliovirus facilitates subversion of host barriers to infectionPreprint
Acevedo, A., Woodman, A., Arnold, J. J., Yeh, M. T., Evans, D., Cameron, C. E., & Andino, R. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/273060 · Cited by 8 · see citing works
Self-citationKITAMURA, K., & Shimizu, H. (2022) · Japanese Journal of Infectious Diseases · doi:10.7883/yoken.jjid.2022.312 · Cited by 7 · see citing works
An Extended Primer Grip of Picornavirus Polymerase Facilitates Sexual RNA Replication Mechanisms
Kempf, B. J., Watkins, C. L., Peersen, O. B., & Barton, D. J. (2020) · Journal of Virology · doi:10.1128/jvi.00835-20 · Cited by 7 · see citing works
Sekiguchi, Y., Nagata, A., Sunaga, F., Oi, T., Imai, R., Madarame, H., Katayama, Y., Oba, M., Okabayashi, T., Misawa, N., et al. (2020) · Archives of Virology · doi:10.1007/s00705-020-04816-y · Cited by 7 · see citing works
Induced copy-back RNA synthesis as a novel therapeutic mechanism against RNA virusesPreprint
Janissen, R., Woodman, A., Lee, K.-M., Moustafa, I. M., Fitzgerald, F., Huang, P.-N., Kuijpers, L., Perkins, A. L., Harki, D. A., Arnold, J. J., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.02.12.946558 · Cited by 7 · see citing works
Molecular basis of RNA recombination in the 3′UTR of chikungunya virus genome
Bardossy, E. S., Volpe, S., Suzuki, Y., Merwaiss, F., Faraj, S. E., Montes, M. R., Saleh, M., Alvarez, D. E., & Filomatori, C. V. (2024) · Nucleic Acids Research · doi:10.1093/nar/gkae650 · Cited by 6 · see citing works
- 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 › Cardiology and Cardiovascular Medicine › 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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review