1932

Abstract

Natural selection acts on cellular organisms by ensuring the genes responsible for an advantageous phenotype consistently reap the phenotypic advantage. This is possible because reproductive cells of these organisms are almost always haploid, separating the beneficial gene from its rival allele at every generation. How natural selection acts on plus-strand RNA viruses is unclear because these viruses frequently load host cells with numerous genome copies and replicate thousands of progeny genomes in each cell. Recent studies suggest that these viruses encode the Bottleneck, Isolate, Amplify, Select (BIAS) mechanism that blocks all but a few viral genome copies from replication, thus creating the environment in which the bottleneck-escaping viral genome copies are isolated from each other, allowing natural selection to reward beneficial mutations and purge lethal errors. This BIAS mechanism also blocks the genomes of highly homologous superinfecting viruses, thus explaining cellular-level superinfection exclusion.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-virology-100520-114758
2022-09-29
2024-06-25
Loading full text...

Full text loading...

/deliver/fulltext/virology/9/1/annurev-virology-100520-114758.html?itemId=/content/journals/10.1146/annurev-virology-100520-114758&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Dawkins R. 1989. The Selfish Gene Oxford, UK: Oxford Univ. Press
    [Google Scholar]
  2. 2.
    Cook LM, Grant BS, Saccheri IJ, Mallet J. 2012. Selective bird predation on the peppered moth: the last experiment of Michael Majerus. Biol. Lett. 8:609–12
    [Crossref] [Google Scholar]
  3. 3.
    Robinson PS, Coorens THH, Palles C, Mitchell E, Abascal F et al. 2021. Increased somatic mutation burdens in normal human cells due to defective DNA polymerases. Nat. Genet. 53:1434–42
    [Crossref] [Google Scholar]
  4. 4.
    Schulte MB, Draghi JA, Plotkin JB, Andino R. 2015. Experimentally guided models reveal replication principles that shape the mutation distribution of RNA viruses. eLife 4:e03753
    [Crossref] [Google Scholar]
  5. 5.
    Kang L, He G, Sharp AK, Wang X, Brown AM et al. 2021. A selective sweep in the Spike gene has driven SARS-CoV-2 human adaptation. Cell 184:4392–400.e4
    [Crossref] [Google Scholar]
  6. 6.
    Zhang X-F, Sun R, Guo Q, Zhang S, Meulia T et al. 2017. A self-perpetuating repressive state of a viral replication protein blocks superinfection by the same virus. PLOS Pathog 13:e1006253
    [Crossref] [Google Scholar]
  7. 7.
    Zhang X-F, Zhang S, Guo Q, Sun R, Wei T, Qu F. 2018. A new mechanistic model for viral cross protection and superinfection exclusion. Front. Plant Sci. 9:40
    [Crossref] [Google Scholar]
  8. 8.
    Qu F, Zheng L, Zhang S, Sun R, Slot J, Miyashita S. 2020. Bottleneck, Isolate, Amplify, Select (BIAS) as a mechanistic framework for intracellular population dynamics of positive-sense RNA viruses. Virus Evol 6:2veaa086
    [Crossref] [Google Scholar]
  9. 9.
    Sanjuán R. 2017. Collective infectious units in viruses. Trends Microbiol 25:402–12
    [Crossref] [Google Scholar]
  10. 10.
    White KA, Skuzeski JM, Li W, Wei N, Morris TJ 1995. Immunodetection, expression strategy and complementation of turnip crinkle virus p28 and p88 replication components. Virology 211:525–34
    [Crossref] [Google Scholar]
  11. 11.
    Buck KW. 1999. Replication of tobacco mosaic virus RNA. Philos. Trans. R. Soc. B 354:613–27
    [Crossref] [Google Scholar]
  12. 12.
    Schaller T, Appel N, Koutsoudakis G, Kallis S, Lohmann V et al. 2007. Analysis of hepatitis C virus superinfection exclusion by using novel fluorochrome gene-tagged viral genomes. J. Virol. 81:4591–603
    [Crossref] [Google Scholar]
  13. 13.
    Zou G, Zhang B, Lim P-Y, Yuan Z, Bernard KA, Shi P-Y. 2009. Exclusion of West Nile virus superinfection through RNA replication. J. Virol. 83:11765–76
    [Crossref] [Google Scholar]
  14. 14.
    Tscherne DM, Evans MJ, von Hahn T, Jones CT, Stamataki Z et al. 2007. Superinfection exclusion in cells infected with hepatitis C virus. J. Virol. 81:3693–703
    [Crossref] [Google Scholar]
  15. 15.
    Tscherne DM, Evans MJ, MacDonald MR, Rice CM. 2008. Transdominant inhibition of bovine viral diarrhea virus entry. J. Virol. 82:2427–36
    [Crossref] [Google Scholar]
  16. 16.
    Webster B, Ott M, Greene WC. 2013. Evasion of superinfection exclusion and elimination of primary viral RNA by an adapted strain of hepatitis C virus. J. Virol. 87:13354–69
    [Crossref] [Google Scholar]
  17. 17.
    Ali A, Li H, Schneider WL, Sherman DJ, Gray S et al. 2006. Analysis of genetic bottlenecks during horizontal transmission of Cucumber mosaic virus. J. Virol. 80:8345–50
    [Crossref] [Google Scholar]
  18. 18.
    Moury B, Fabre F, Senoussi R. 2007. Estimation of the number of virus articles transmitted by an insect vector. PNAS 104:17891–96
    [Crossref] [Google Scholar]
  19. 19.
    Pathak KB, Nagy PD. 2009. Defective interfering RNAs: foes of viruses and friends of virologists. Viruses 1:895–919
    [Crossref] [Google Scholar]
  20. 20.
    Martinez F, Sardanyes J, Elena SF, Daros J-A. 2011. Dynamics of a plant RNA virus intracellular accumulation: stamping machine versus geometric replication. Genetics 188:637–46
    [Crossref] [Google Scholar]
  21. 21.
    Domingo E, Perales C. 2019. Viral quasispecies. PLOS Genet 15:e1008271
    [Crossref] [Google Scholar]
  22. 22.
    Lauring AS, Andino R. 2010. Quasispecies theory and the behavior of RNA viruses. PLOS Pathog 6:e1001005
    [Crossref] [Google Scholar]
  23. 23.
    McKinney HH. 1929. Mosaic diseases in the Canary Islands, West Africa, and Gibraltar. J. Agric. Res. 39:557–78
    [Google Scholar]
  24. 24.
    Ziebell H, Carr JP. 2010. Cross-protection: a century of mystery. Adv. Virus Res. 76:211–64
    [Crossref] [Google Scholar]
  25. 25.
    Baulcombe D. 2004. RNA silencing in plants. Nature 431:356–63
    [Crossref] [Google Scholar]
  26. 26.
    Ziebell H, Payne T, Berry JO, Walsh JA, Carr JP. 2007. A cucumber mosaic virus mutant lacking the 2b counter-defence protein gene provides protection against wild-type strains. J. Gen. Virol. 88:2862–71
    [Crossref] [Google Scholar]
  27. 27.
    Zhang X-F, Guo J, Zhang X, Meulia T, Paul P et al. 2015. Random plant viral variants attain temporal advantages during systemic infections and in turn resist other variants of the same virus. Sci. Rep. 5:15346
    [Crossref] [Google Scholar]
  28. 28.
    Folimonova SY. 2012. Superinfection exclusion is an active virus-controlled function that requires a specific viral protein. J. Virol. 86:5554–61
    [Crossref] [Google Scholar]
  29. 29.
    Folimonova SY. 2013. Developing an understanding of cross-protection by Citrus tristeza virus. Front. Microbiol. 4:76
    [Crossref] [Google Scholar]
  30. 30.
    Sacristán S, Malpica JM, Fraile A, García-Arenal F. 2003. Estimation of population bottlenecks during systemic movement of Tobacco mosaic virus in tobacco plants. J. Virol. 77:9906–11
    [Crossref] [Google Scholar]
  31. 31.
    Li H, Roossinck MJ. 2004. Genetic bottlenecks reduce population variation in an experimental RNA virus population. J. Virol. 78:10582–87
    [Crossref] [Google Scholar]
  32. 32.
    Hall JS, French R, Hein GL, Morris TJ, Stenger DC. 2001. Three distinct mechanisms facilitate genetic isolation of sympatric wheat streak mosaic virus lineages. Virology 282:230–36
    [Crossref] [Google Scholar]
  33. 33.
    Dietrich C, Maiss E. 2003. Fluorescent labelling reveals spatial separation of potyvirus populations in mixed infected Nicotiana benthamiana plants. J. Gen. Virol. 84:2871–76
    [Crossref] [Google Scholar]
  34. 34.
    French R, Stenger DC. 2003. Evolution of wheat streak mosaic virus: Dynamics of population growth within plants may explain limited variation. Annu. Rev. Phytopathol. 41:199–214
    [Crossref] [Google Scholar]
  35. 35.
    Zwart MP, Daròs J-A, Elena SF. 2011. One is enough: In vivo effective population size is dose-dependent for a plant RNA virus. PLOS Pathog 7:e1002122
    [Crossref] [Google Scholar]
  36. 36.
    Tatineni S, French R. 2016. The coat protein and NIa protease of two Potyviridae family members independently confer superinfection exclusion. J. Virol. 90:10886–905
    [Crossref] [Google Scholar]
  37. 37.
    Zhou X, Sun K, Zhou X, Jackson AO, Li Z 2019. The matrix protein of a plant rhabdovirus mediates superinfection exclusion by inhibiting viral transcription. J. Virol. 93:e00680–19
    [Google Scholar]
  38. 38.
    Tromas N, Zwart MP, Lafforgue G, Elena SF. 2014. Within-host spatiotemporal dynamics of plant virus infection at the cellular level. PLOS Genet 10:e1004186
    [Crossref] [Google Scholar]
  39. 39.
    Takahashi T, Sugawara T, Yamatsuta T, Isogai M, Natsuaki T, Yoshikawa N. 2007. Analysis of the spatial distribution of identical and two distinct virus populations differently labeled with cyan and yellow fluorescent proteins in coinfected plants. Phytopathology 97:1200–6
    [Crossref] [Google Scholar]
  40. 40.
    Grubaugh ND, Weger-Lucarelli J, Murrieta RA, Fauver JR, Garcia-Luna SM et al. 2016. Genetic drift during systemic arbovirus infection of mosquito vectors leads to decreased relative fitness during host switching. Cell Host Microbe 19:481–92
    [Crossref] [Google Scholar]
  41. 41.
    Ciota AT, Ehrbar DJ, Van Slyke GA, Payne AF, Willsey GG et al. 2012. Quantification of intrahost bottlenecks of West Nile virus in Culex pipiens mosquitoes using an artificial mutant swarm. Infect. Genet. Evol. 12:557–64
    [Crossref] [Google Scholar]
  42. 42.
    Frost SDW, Dumaurier M-J, Wain-Hobson S, Brown AJL 2001. Genetic drift and within-host metapopulation dynamics of HIV-1 infection. PNAS 98:6975–80
    [Crossref] [Google Scholar]
  43. 43.
    Leeks A, Sanjuán R, West SA. 2019. The evolution of collective infectious units in viruses. Virus Res 265:94–101
    [Crossref] [Google Scholar]
  44. 44.
    Chen P, Hübner W, Spinelli MA, Chen BK. 2007. Predominant mode of human immunodeficiency virus transfer between T cells is mediated by sustained Env-dependent neutralization-resistant virological synapses. J. Virol. 81:12582–95
    [Crossref] [Google Scholar]
  45. 45.
    Hübner W, McNerney GP, Chen P, Dale BM, Gordon RE et al. 2009. Quantitative 3D video microscopy of HIV transfer across T cell virological synapses. Science 323:1743–47
    [Crossref] [Google Scholar]
  46. 46.
    Del Portillo A, Tripodi J, Najfeld V, Wodarz D, Levy DN, Chen BK. 2011. Multiploid inheritance of HIV-1 during cell-to-cell infection. J. Virol. 85:7169–76
    [Crossref] [Google Scholar]
  47. 47.
    Iwami S, Takeuchi JS, Nakaoka S, Mammano F, Clavel F et al. 2015. Cell-to-cell infection by HIV contributes over half of virus infection. eLife 4:e08150
    [Crossref] [Google Scholar]
  48. 48.
    Law KM, Komarova NL, Yewdall AW, Lee RK, Herrera OL et al. 2016. In vivo HIV-1 cell-to-cell transmission promotes multicopy micro-compartmentalized infection. Cell Rep 15:2771–83
    [Crossref] [Google Scholar]
  49. 49.
    Robinson SM, Tsueng G, Sin J, Mangale V, Rahawi S et al. 2014. Coxsackievirus B exits the host cell in shed microvesicles displaying autophagosomal markers. PLOS Pathog 10:e1004045
    [Crossref] [Google Scholar]
  50. 50.
    Chen Y-H, Du W, Hagemeijer MC, Takvorian PM, Pau C et al. 2015. Phosphatidylserine vesicles enable efficient en bloc transmission of enteroviruses. Cell 160:619–30
    [Crossref] [Google Scholar]
  51. 51.
    Cifuentes-Muñoz N, Dutch RE, Cattaneo R. 2018. Direct cell-to-cell transmission of respiratory viruses: the fast lanes. PLOS Pathog 14:e1007015
    [Crossref] [Google Scholar]
  52. 52.
    Martinez MG, Kielian M. 2016. Intercellular extensions are induced by the alphavirus structural proteins and mediate virus transmission. PLOS Pathog 12:e1006061
    [Crossref] [Google Scholar]
  53. 53.
    Feng Z, Hensley L, McKnight KL, Hu F, Madden V et al. 2013. A pathogenic picornavirus acquires an envelope by hijacking cellular membranes. Nature 496:367–71
    [Crossref] [Google Scholar]
  54. 54.
    Santiana M, Ghosh S, Ho BA, Rajasekaran V, Du W-L et al. 2018. Vesicle-cloaked virus clusters are optimal units for inter-organismal viral transmission. Cell Host Microbe 24:208–20.e8
    [Crossref] [Google Scholar]
  55. 55.
    Miyashita S, Ishibashi K, Kishino H, Ishikawa M. 2015. Viruses roll the dice: The stochastic behavior of viral genome molecules accelerates viral adaptation at the cell and tissue levels. PLOS Biol 13:e1002094
    [Crossref] [Google Scholar]
  56. 56.
    Guo Q, Zhang S, Sun R, Yao X, Zhang X-F et al. 2020. Superinfection exclusion by p28 of turnip crinkle virus is separable from its replication function. Mol. Plant-Microbe Interact. 33:364–75
    [Crossref] [Google Scholar]
  57. 57.
    Qu F, Ren T, Morris TJ. 2003. The coat protein of Turnip crinkle virus suppresses posttranscriptional gene silencing at an early initiation step. J. Virol. 77:511–22
    [Crossref] [Google Scholar]
  58. 58.
    Hull R, Covey SN, Dale P. 2000. Genetically modified plants and the 35S promoter: assessing the risks and enhancing the debate. Microb. Ecol. Health Dis. 12:1–5
    [Crossref] [Google Scholar]
  59. 59.
    Cabantous S, Terwilliger TC, Waldo GS. 2005. Protein tagging and detection with engineered self-assembling fragments of green fluorescent protein. Nat. Biotechnol. 23:102–7
    [Crossref] [Google Scholar]
  60. 60.
    Cabantous S, Waldo GS. 2006. In vivo and in vitro protein solubility assays using split GFP. Nat. Methods 3:845–54
    [Crossref] [Google Scholar]
  61. 61.
    Novak JE, Kirkegaard K. 1994. Coupling between genome translation and replication in an RNA virus. Genes Dev 8:1726–37
    [Crossref] [Google Scholar]
  62. 62.
    Okamoto K, Nagano H, Iwakawa H, Mizumoto H, Takeda A et al. 2008. cis-Preferential requirement of a −1 frameshift product p88 for the replication of Red clover necrotic mosaic virus RNA1. Virology 375:205–12
    [Crossref] [Google Scholar]
  63. 63.
    Kawamura-Nagaya K, Ishibashi K, Huang Y-P, Miyashita S, Ishikawa M. 2014. Replication protein of tobacco mosaic virus cotranslationally binds the 5′ untranslated region of genomic RNA to enable viral replication. PNAS 111:E1620–28
    [Crossref] [Google Scholar]
  64. 64.
    Yi G, Gopinath K, Kao CC. 2007. Selective repression of translation by the brome mosaic virus 1a RNA replication protein. J. Virol. 81:1601–9
    [Crossref] [Google Scholar]
  65. 65.
    Lin J, Guo J, Finer J, Dorrance AE, Redinbaugh MG, Qu F. 2014. The Bean pod mottle virus RNA2-encoded 58-kilodalton protein P58 is required in cis for RNA2 accumulation. J. Virol. 88:3213–22
    [Crossref] [Google Scholar]
  66. 66.
    Brese RL, Gonzalez-Perez MP, Koch M, O'Connell O, Luzuriaga K et al. 2018. Ultradeep single-molecule real-time sequencing of HIV envelope reveals complete compartmentalization of highly macrophage-tropic R5 proviral variants in brain and CXCR4-using variants in immune and peripheral tissues. J. Neurovirol. 24:439–53
    [Crossref] [Google Scholar]
  67. 67.
    Russell AB, Elshina E, Kowalsky JR, te Velthuis AJW, Bloom JD. 2019. Single-cell virus sequencing of influenza infections that trigger innate immunity. J. Virol. 93:e00500–19
    [Crossref] [Google Scholar]
  68. 68.
    Yamashita T, Takeda H, Takai A, Arasawa S, Nakamura F et al. 2020. Single-molecular real-time deep sequencing reveals the dynamics of multi-drug resistant haplotypes and structural variations in the hepatitis C virus genome. Sci. Rep. 10:2651
    [Crossref] [Google Scholar]
  69. 69.
    Roberts AG, Cruz SS, Roberts IM, Prior DAM, Turgeon R, Oparka KJ. 1997. Phloem unloading in sink leaves of Nicotiana benthamiana: comparison of a fluorescent solute with a fluorescent virus. Plant Cell 9:1381–96
    [Crossref] [Google Scholar]
/content/journals/10.1146/annurev-virology-100520-114758
Loading
/content/journals/10.1146/annurev-virology-100520-114758
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error