1932

Abstract

Multipartite virus genomes are composed of several segments, each packaged in a distinct viral particle. Although this puzzling genome architecture is found in ∼17% of known viral species, its distribution among hosts or among distinct types of genome-composing nucleic acid remains poorly understood. No convincing advantage of multipartitism has been identified, yet the maintenance of genomic integrity appears problematic. Here we review recent studies shedding light on these issues. Multipartite viruses rapidly modify the copy number of each segment/gene from one host species to another, a putative benefit if host switches are common. One multipartite virus functions in a multicellular way: The segments do not all need to be present in the same cell and can functionally complement across cells, maintaining genome integrity within hosts. The genomic integrity maintenance during host-to-host transmission needs further elucidation. These features challenge several virology foundations and could apply to other multicomponent viral systems.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-virology-010220-063346
2020-09-29
2024-04-16
Loading full text...

Full text loading...

/deliver/fulltext/virology/7/1/annurev-virology-010220-063346.html?itemId=/content/journals/10.1146/annurev-virology-010220-063346&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Lucía-Sanz A, Manrubia S. 2017. Multipartite viruses: adaptive trick or evolutionary treat. ? NPJ Syst. Biol. Appl. 3:134Important review on the evolution of multipartite viruses.
    [Google Scholar]
  2. 2. 
    Sicard A, Michalakis Y, Gutiérrez S, Blanc S 2016. The strange lifestyle of multipartite viruses. PLOS Pathogens 12:11e1005819Important review on multipartite viruses with a focus on different steps of their life cycle.
    [Google Scholar]
  3. 3. 
    Liu W, Hajano J-U-D, Wang X 2018. New insights on the transmission mechanism of tenuiviruses by their vector insects. Curr. Opin. Virol. 33:13–17
    [Google Scholar]
  4. 4. 
    Dietzgen RG, Freitas-Astúa J, Chabi-Jesus C, Ramos-González PL, Goodin MM et al. 2018. Dichorhaviruses in their host plants and mite vectors. Adv. Virus Res. 102:119–48
    [Google Scholar]
  5. 5. 
    Leastro MO, Kitajima EW, Silva MS, Resende RO, Freitas-Astúa J 2018. Dissecting the subcellular localization, intracellular trafficking, interactions, membrane association, and topology of citrus leprosis virus C proteins. Front. Plant Sci. 9:1299
    [Google Scholar]
  6. 6. 
    Hu Z, Li G, Li G, Yao Q, Chen K 2013. Bombyx mori bidensovirus: the type species of the new genus Bidensovirus in the new family Bidnaviridae. Chin. Sci. Bull 58:364528–32
    [Google Scholar]
  7. 7. 
    Ladner JT, Wiley MR, Beitzel B, Auguste AJ, Dupuis AP et al. 2016. A multicomponent animal virus isolated from mosquitoes. Cell Host Microbe 20:3357–67
    [Google Scholar]
  8. 8. 
    Wichgers Schreur PJ, Kortekaas J 2016. Single-molecule FISH reveals non-selective packaging of Rift Valley fever virus genome segments. PLOS Pathogens 12:8e1005800
    [Google Scholar]
  9. 9. 
    Gokhale DV, Bald JG. 1987. Relationship between plant virus concentration and infectivity: a ‘growth curve’ model. J. Virol. Methods 18:4225–32
    [Google Scholar]
  10. 10. 
    Brooke CB, Ince WL, Wrammert J, Ahmed R, Wilson PC et al. 2013. Most influenza A virions fail to express at least one essential viral protein. J. Virol. 87:63155–62Founding study revealing the problem of genome integrity in segmented viruses.
    [Google Scholar]
  11. 11. 
    Lister RM. 1966. Possible relationships of virus-specific products of tobacco rattle virus infections. Virology 28:2350–53
    [Google Scholar]
  12. 12. 
    Van Kammen A. 1967. Purification and properties of the components of cowpea mosaic virus. Virology 31:4633–42
    [Google Scholar]
  13. 13. 
    Chu PWG, Helms K. 1988. Novel virus-like particles containing circular single-stranded DNAs associated with subterranean clover stunt disease. Virology 167:138–49
    [Google Scholar]
  14. 14. 
    Hesketh EL, Saunders K, Fisher C, Potze J, Stanley J et al. 2018. The 3.3 Å structure of a plant geminivirus using cryo-EM. Nat. Commun. 9:12369
    [Google Scholar]
  15. 15. 
    Chou Y, Vafabakhsh R, Doğanay S, Gao Q, Ha T, Palese P 2012. One influenza virus particle packages eight unique viral RNAs as shown by FISH analysis. PNAS 109:239101–6
    [Google Scholar]
  16. 16. 
    Pressing J, Reanney DC. 1984. Divided genomes and intrinsic noise. J. Mol. Evol. 20:2135–46
    [Google Scholar]
  17. 17. 
    Nee S. 1987. The evolution of multicompartmental genomes in viruses. J. Mol. Evol. 25:4277–81
    [Google Scholar]
  18. 18. 
    Nee S, Maynard Smith J 1990. The evolutionary biology of molecular parasites. Parasitology 100:S1S5–5
    [Google Scholar]
  19. 19. 
    Szathmáry E. 1992. Natural selection and dynamical coexistence of defective and complementing virus segments. J. Theor. Biol. 157:3383–406
    [Google Scholar]
  20. 20. 
    Szathmáry E. 1992. Viral sex, levels of selection, and the origin of life. J. Theor. Biol. 159:199–109
    [Google Scholar]
  21. 21. 
    Zwart MP, Elena SF. 2015. Matters of size: genetic bottlenecks in virus infection and their potential impact on evolution. Annu. Rev. Virol. 2:161–79Reviews concepts and results on virus bottleneck sizes and MOI.
    [Google Scholar]
  22. 22. 
    Zhang Y-J, Wu Z-X, Holme P, Yang K-C 2019. Advantage of being multicomponent and spatial: multipartite viruses colonize structured populations with lower thresholds. Phys. Rev. Lett. 123:13138101
    [Google Scholar]
  23. 23. 
    Varsani A, Lefeuvre P, Roumagnac P, Martin D 2018. Notes on recombination and reassortment in multipartite/segmented viruses. Curr. Opin. Virol. 33:156–66Reviews observations in recombination and reassortment in segmented and multipartite viruses.
    [Google Scholar]
  24. 24. 
    Lefkowitz EJ, Adams MJ, Davison AJ, Siddell SG, Simmonds P 2015. Virus Taxonomy: The Classification and Nomenclature of Viruses. The Online 10th Report of the International Committee on Taxonomy of Viruses. London: ICTV https://talk.ictvonline.org/ictv-reports/ictv_online_report/
  25. 25. 
    Lucía-Sanz A, Aguirre J, Manrubia S 2018. Theoretical approaches to disclosing the emergence and adaptive advantages of multipartite viruses. Curr. Opin. Virol. 33:89–95
    [Google Scholar]
  26. 26. 
    Chao L. 1991. Levels of selection, evolution of sex in RNA viruses, and the origin of life. J. Theor. Biol. 153:2229–46
    [Google Scholar]
  27. 27. 
    Chao L. 1988. Evolution of sex in RNA viruses. J. Theor. Biol. 133:199–112
    [Google Scholar]
  28. 28. 
    Nee S. 1989. On the evolution of sex in RNA viruses. J. Theor. Biol. 138:3407–12
    [Google Scholar]
  29. 29. 
    Ojosnegros S, García-Arriaza J, Escarmís C, Manrubia SC, Perales C et al. 2011. Viral genome segmentation can result from a trade-off between genetic content and particle stability. PLOS Genet 7:3e1001344Only empirical paper exploring the potential advantages of multipartite variants.
    [Google Scholar]
  30. 30. 
    Garcia-Arriaza J, Manrubia SC, Toja M, Domingo E, Escarmis C 2004. Evolutionary transition toward defective RNAs that are infectious by complementation. J. Virol. 78:11678–85
    [Google Scholar]
  31. 31. 
    Valdano E, Manrubia S, Gómez S, Arenas A 2019. Endemicity and prevalence of multipartite viruses under heterogeneous between-host transmission. PLOS Comput. Biol. 15:3e1006876
    [Google Scholar]
  32. 32. 
    Iranzo J, Manrubia SC. 2012. Evolutionary dynamics of genome segmentation in multipartite viruses. Proc. Biol. Sci. 279:17433812–19Theoretical investigation of the parameter range favoring multipartitism depending on the number of segments.
    [Google Scholar]
  33. 33. 
    Sicard A, Yvon M, Timchenko T, Gronenborn B, Michalakis Y et al. 2013. Gene copy number is differentially regulated in a multipartite virus. Nat. Commun. 4:2248First paper demonstrating the existence of the genome formula in multipartite viruses.
    [Google Scholar]
  34. 34. 
    Wu B, Zwart MP, Sánchez-Navarro JA, Elena SF 2017. Within-host evolution of segments ratio for the tripartite genome of Alfalfa mosaic virus. Sci. Rep 7:15004
    [Google Scholar]
  35. 35. 
    Hu Z, Zhang X, Liu W, Zhou Q, Zhang Q et al. 2016. Genome segments accumulate with different frequencies in Bombyxmoribidensovirus. J. Basic Microbiol 56:121338–43
    [Google Scholar]
  36. 36. 
    Gallet R, Fabre F, Thébaud G, Sofonea MT, Sicard A et al. 2018. Small bottleneck size in a highly multipartite virus during a complete infection cycle. J. Virol. 92:14e00139-18
    [Google Scholar]
  37. 37. 
    Sicard A, Pirolles E, Gallet R, Vernerey M-S, Yvon M et al. 2019. A multicellular way of life for a multipartite virus. eLife 8:e43599First paper demonstrating a supracellular way of life for a multipartite virus.
    [Google Scholar]
  38. 38. 
    Sanjuán R, Thoulouze M-I. 2019. Why viruses sometimes disperse in groups. Virus Evol 5:1vez014
    [Google Scholar]
  39. 39. 
    Dall'Ara M, Ratti C, Bouzoubaa SE, Gilmer D 2016. Ins and outs of multipartite positive-strand RNA plant viruses: packaging versus systemic spread. Viruses 8:8228
    [Google Scholar]
  40. 40. 
    Gilmer D, Ratti C, Michel F 2018. Long-distance movement of helical multipartite phytoviruses: keep connected or die. Curr. Opin. Virol. 33:120–28
    [Google Scholar]
  41. 41. 
    Betancourt M, Fereres A, Fraile A, García-Arenal F 2008. Estimation of the effective number of founders that initiate an infection after aphid transmission of a multipartite plant virus. J. Virol. 82:2412416–21First paper estimating the bottleneck size in a multipartite virus.
    [Google Scholar]
  42. 42. 
    Schwinghamer MW, Nicholas AH, Schilg MA 2009. Three aphid vectors of faba bean (Viciafaba) viruses in northern New South Wales and occurrence of Acyrthosiphonpisum-transmitted isolates of Soybean dwarf virus.Australas. . Plant Pathol 38:3262–69
    [Google Scholar]
  43. 43. 
    Gronenborn B. 2004. Nanoviruses: genome organisation and protein function. Vet. Microbiol. 98:2103–9
    [Google Scholar]
  44. 44. 
    Mossop DW, Francki RIB. 1978. Survival of a satellite RNA in vivo and its dependence on cucumber mosaic virus for replication. Virology 86:2562–66
    [Google Scholar]
  45. 45. 
    Mossop DW, Francki RIB. 1979. The stability of satellite viral RNAs in vivo and in vitro. . Virology 94:2243–53
    [Google Scholar]
  46. 46. 
    Timchenko T. 2006. Infectivity of nanovirus DNAs: induction of disease by cloned genome components of Fababean necrotic yellows virus. J. Gen. . Virol 87:61735–43
    [Google Scholar]
  47. 47. 
    Grigoras I, Vetten H-J, Commandeur U, Ziebell H, Gronenborn B, Timchenko T 2018. Nanovirus DNA-N encodes a protein mandatory for aphid transmission. Virology 522:281–91
    [Google Scholar]
  48. 48. 
    Michalakis Y, Blanc S. 2018. Editorial overview: multicomponent viral systems. Curr. Opin. Virol. 33:vi–ix
    [Google Scholar]
  49. 49. 
    Borodavka A, Desselberger U, Patton JT 2018. Genome packaging in multi-segmented dsRNA viruses: distinct mechanisms with similar outcomes. Curr. Opin. Virol. 33:106–12
    [Google Scholar]
  50. 50. 
    Hutchinson EC, von Kirchbach JC, Gog JR, Digard P 2010. Genome packaging in influenza A virus. J. Gen. Virol. 91:2313–28
    [Google Scholar]
  51. 51. 
    Brooke CB. 2017. Population diversity and collective interactions during influenza virus infection. J. Virol. 91:22e01164-17
    [Google Scholar]
  52. 52. 
    Jacobs NT, Onuoha NO, Antia A, Steel J, Antia R, Lowen AC 2019. Incomplete influenza A virus genomes occur frequently but are readily complemented during localized viral spread. Nat. Commun. 10:13526
    [Google Scholar]
  53. 53. 
    Diefenbacher M, Sun J, Brooke CB 2018. The parts are greater than the whole: the role of semi-infectious particles in influenza A virus biology. Curr. Opin. Virol. 33:42–46
    [Google Scholar]
  54. 54. 
    Nakatsu S, Sagara H, Sakai-Tagawa Y, Sugaya N, Noda T, Kawaoka Y 2016. Complete and incomplete genome packaging of influenza A and B viruses. mBio 7:5e01248-16
    [Google Scholar]
  55. 55. 
    Vignuzzi M, López CB. 2019. Defective viral genomes are key drivers of the virus-host interaction. Nat. Microbiol. 4:7107587
    [Google Scholar]
  56. 56. 
    Gnanasekaran P, Chakraborty S. 2018. Biology of viral satellites and their role in pathogenesis. Curr. Opin. Virol. 33:96–105
    [Google Scholar]
  57. 57. 
    Wichgers Schreur PJ, Kormelink R, Kortekaas J 2018. Genome packaging of the Bunyavirales.Curr.Opin. . Virol 33:151–55
    [Google Scholar]
  58. 58. 
    Luque D, Rivas G, Alfonso C, Carrascosa JL, Rodriguez JF, Caston JR 2009. Infectious bursal disease virus is an icosahedral polyploid dsRNA virus. PNAS 106:72148–52
    [Google Scholar]
  59. 59. 
    Chaturvedi S, Rao A. 2018. Molecular and biological factors regulating the genome packaging in single-strand positive-sense tripartite RNA plant viruses. Curr. Opin. Virol. 33:113–19
    [Google Scholar]
  60. 60. 
    Basnayake VR, Sit TL, Lommel SA 2006. The genomic RNA packaging scheme of Red clover necrotic mosaic virus. . Virology 345:2532–39
    [Google Scholar]
  61. 61. 
    Basnayake VR, Sit TL, Lommel SA 2009. The Red clover necrotic mosaic virus origin of assembly is delimited to the RNA-2 trans-activator. Virology 384:1169–78
    [Google Scholar]
  62. 62. 
    Newburn LR, White KA. 2019. Trans-acting RNA–RNA interactions in segmented RNA viruses. Viruses 11:8751
    [Google Scholar]
  63. 63. 
    Woith E, Fuhrmann G, Melzig MF 2019. Extracellular vesicles—connecting kingdoms. Int. J. Mol. Sci. 20:225695
    [Google Scholar]
  64. 64. 
    Drab M, Stopar D, Kralj-Iglič V, Iglič A 2019. Inception mechanisms of tunneling nanotubes. Cells 8:6626
    [Google Scholar]
  65. 65. 
    Gill S, Catchpole R, Forterre P 2019. Extracellular membrane vesicles in the three domains of life and beyond. FEMS Microbiol. Rev. 43:3273–303
    [Google Scholar]
  66. 66. 
    Rezelj VV, Levi LI, Vignuzzi M 2018. The defective component of viral populations. Curr. Opin. Virol. 33:74–80
    [Google Scholar]
  67. 67. 
    Pavithra BS, Govin K, Renuka HM, Krishnareddy M, Jalali S et al. 2019. Characterization of cucumber mosaic virus infecting coleus (Plectranthusbarbatus) in Karnataka. VirusDisease 30:3403–12
    [Google Scholar]
  68. 68. 
    Elde NC, Child SJ, Eickbush MT, Kitzman JO, Rogers KS et al. 2012. Poxviruses deploy genomic accordions to adapt rapidly against host antiviral defenses. Cell 150:4831–41
    [Google Scholar]
  69. 69. 
    Bayer A, Brennan G, Geballe AP 2018. Adaptation by copy number variation in monopartite viruses. Curr. Opin. Virol. 33:7–12
    [Google Scholar]
/content/journals/10.1146/annurev-virology-010220-063346
Loading
/content/journals/10.1146/annurev-virology-010220-063346
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