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One Is Enough: Effective Population Size Is Dose-Dependent for a Plant RNA Virus


Effective population size (Ne) determines the strength of genetic drift and the frequency of co-infection by multiple genotypes, making it a key factor in viral evolution. Experimental estimates of Ne for different plant viruses have, however, rendered diverging results. The independent action hypothesis (IAH) states that each virion has a probability of infection, and that virions act independent of one another during the infection process. A corollary of IAH is that Ne must be dose dependent. A test of IAH for a plant virus has not been reported yet. Here we perform a test of an IAH infection model using a plant RNA virus, Tobacco etch virus (TEV) variants carrying GFP or mCherry fluorescent markers, in Nicotiana tabacum and Capsicum annuum plants. The number of primary infection foci increased linearly with dose, and was similar to a Poisson distribution. At high doses, primary infection foci containing both genotypes were found at a low frequency (<2%). The probability that a genotype that infected the inoculated leaf would systemically infect that plant was near 1, although in a few rare cases genotypes could be trapped in the inoculated leaf by being physically surrounded by the other genotype. The frequency of mixed-genotype infection could be predicted from the mean number of primary infection foci using the independent-action model. Independent action appears to hold for TEV, and Ne is therefore dose-dependent for this plant RNA virus. The mean number of virions causing systemic infection can be very small, and approaches 1 at low doses. Dose-dependency in TEV suggests that comparison of Ne estimates for different viruses are not very meaningful unless dose effects are taken into consideration.


Vyšlo v časopise: One Is Enough: Effective Population Size Is Dose-Dependent for a Plant RNA Virus. PLoS Pathog 7(7): e32767. doi:10.1371/journal.ppat.1002122
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002122

Souhrn

Effective population size (Ne) determines the strength of genetic drift and the frequency of co-infection by multiple genotypes, making it a key factor in viral evolution. Experimental estimates of Ne for different plant viruses have, however, rendered diverging results. The independent action hypothesis (IAH) states that each virion has a probability of infection, and that virions act independent of one another during the infection process. A corollary of IAH is that Ne must be dose dependent. A test of IAH for a plant virus has not been reported yet. Here we perform a test of an IAH infection model using a plant RNA virus, Tobacco etch virus (TEV) variants carrying GFP or mCherry fluorescent markers, in Nicotiana tabacum and Capsicum annuum plants. The number of primary infection foci increased linearly with dose, and was similar to a Poisson distribution. At high doses, primary infection foci containing both genotypes were found at a low frequency (<2%). The probability that a genotype that infected the inoculated leaf would systemically infect that plant was near 1, although in a few rare cases genotypes could be trapped in the inoculated leaf by being physically surrounded by the other genotype. The frequency of mixed-genotype infection could be predicted from the mean number of primary infection foci using the independent-action model. Independent action appears to hold for TEV, and Ne is therefore dose-dependent for this plant RNA virus. The mean number of virions causing systemic infection can be very small, and approaches 1 at low doses. Dose-dependency in TEV suggests that comparison of Ne estimates for different viruses are not very meaningful unless dose effects are taken into consideration.


Zdroje

1. WrightS 1930 Evolution in Mendelian populations. Genetics 16 97 159

2. NijhuisMBoucherCABSchipperPLeitnerTSchuurmanR 1998 Stochastic processes strongly influence HIV-1 evolution during suboptimal protease-inhibitor therapy. Proc Natl Acad Sci USA 95 14441 14446

3. MoyaAElenaSFBrachoAMirallesRBarrioE 2000 The evolution of RNA viruses: A population genetics view. Proc Natl Acad Sci USA 97 6967 6973

4. ChaoL 1990 Fitness of RNA virus decreased by Muller's Ratchet. Nature 348 454 455

5. de la IglesiaFElenaSF 2007 Fitness declines in Tobacco etch virus upon serial bottleneck transfers. J Virol 81 4941 4947

6. BergstromCTMcElhanyPRealLA 1999 Transmission bottlenecks as determinants of virulence in rapidly evolving pathogens. Proc Natl Acad Sci USA 96 5095 5100

7. ZwartMPHemerikLCoryJSde VisserJBianchiF 2009 An experimental test of the independent action hypothesis in virus-insect pathosystems. Proc R Soc B 276 2233 2242

8. FroissartRRozeDUzestMGalibertLBlancS 2005 Recombination every day: Abundant recombination in a virus during a single multi-cellular host infection. PLoS Biol 3 389 395

9. VignuzziMStoneJKArnoldJJCameronCEAndinoR 2006 Quasispecies diversity determines pathogenesis through cooperative interactions in a viral population. Nature 439 344 348

10. ZwartMPvan der WerfWvan OersMMHemerikLvan LentJMV 2009 Mixed infections and the competitive fitness of faster-acting genetically modified viruses. Evol Appl 2 209 221

11. MartinSElenaSF 2009 Application of game theory to the interaction between plant viruses during mixed infections. J Gen Virol 90 2815 2820

12. TaylorDRZeylCCookeE 2002 Conflicting levels of selection in the accumulation of mitochondrial defects in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 99 3690 3694

13. ZwartMPvan der WerfWGeorgievskaLvan OersMMVlakJM 2010 Mixed-genotype infections of Trichoplusia ni larvae with Autographa californica multicapsid nucleopolyhedrovirus: Speed of action and persistence of a recombinant in serial passage. Biol Control 52 77 83

14. DruettHA 1952 Bacterial invasion. Nature 170 288 288

15. FurumotoWAMickeyR 1967 A mathematical model for infectivity-dilution curve of Tobacco mosiac virus - experimental tests. Virology 32 224 233

16. FurumotoWAMickeyR 1967 A mathematical model for infectivity-dilution curve of Tobacco mosaic virus - theoretical considerations. Virology 32 216 223

17. BaldJG 1937 The use of numbers of infections for comparing the concentration of plant virus suspensions I. Dilution experiments with purified suspensions. Ann Appl Biol 24 33 55

18. García-ArenalFFraileA 2011 Population dynamics and genetics of plant infection by viruses. CarantaCArandaMATepferMLópez-MoyaJJ Recent advances in plant virology Norfolk, UK Caister Academic Press 263 281

19. WatsonMA 1972 Transmission of plant viruses by aphids. KadoCIAgrawalHO Principles and techniques in plant virology New York Van Nostrand Reinhold Co 131 167

20. GomezPSempereRNElenaSFArandaMA 2009 Mixed infections of Pepino mosaic virus strains modulate the evolutionary dynamics of this emergent virus. J Virol 83 12378 12387

21. HammondJLecoqHRaccahB 1999 Epidemiological risks from mixed virus infections and transgenic plants expressing viral genes. Adv Vir Res 54 189 314

22. Lopez-FerberMSimonOWilliamsTCaballeroP 2003 Defective or effective? Mutualistic interactions between virus genotypes. Proc R Soc B 270 2249 2255

23. ClavijoGWilliamsTMunozDCaballeroPLopez-FerberM 2010 Mixed genotype transmission bodies and virions contribute to the maintenance of diversity in an insect virus. Proc R Soc B 277 943 951

24. BennettCW 1953 Interactions between viruses and virus strains. Adv Vir Res 1 39 67

25. MouryBFabreFSenoussiR 2007 Estimation of the number of virus particles transmitted by an insect vector. Proc Natl Acad Sci USA 104 17891 17896

26. AliALiHYSchneiderWLShermanDJGrayS 2006 Analysis of genetic bottlenecks during horizontal transmission of Cucumber mosaic virus. J Virol 80 8345 8350

27. BetancourtMFereresAFraileAGarcia-ArenalF 2008 Estimation of the effective number of founders that initiate an infection after aphid transmission of a multipartite plant virus. J Virol 82 12416 12421

28. HallJSFrenchRHeinGLMorrisTJStengerDC 2001 Three distinct mechanisms facilitate genetic isolation of sympatric Wheat streak mosaic virus lineages. Virology 282 230 236

29. FrenchRStengerDC 2003 Evolution of Wheat streak mosaic virus: Dynamics of population growth within plants may explain limited variation. Ann Rev Phytopathol 41 199 214

30. SacristanSMalpicaJMFraileAGarcia-ArenalF 2003 Estimation of population bottlenecks during systemic movement of Tobacco mosaic virus in tobacco plants. J Virol 77 9906 9911

31. LiHYRoossinckMJ 2004 Genetic bottlenecks reduce population variation in an experimental RNA virus population. J Virol 78 10582 10587

32. ElenaSFBedhommeSCarrascoPCuevasJMde la IglesiaF 2011 The evolutionary genetics of emerging plant RNA viruses. Mol Plant Microbe In 24 287 293

33. MonsionBFroissartRMichalakisYBlancS 2008 Large bottleneck size in Cauliflower mosaic virus populations during host plant colonization. PloS Pathog 4 7

34. BedoyaLCDarosJA 2010 Stability of Tobacco etch virus infectious clones in plasmid vectors. Vir Res 149 234 240

35. ShanerNCCampbellRESteinbachPAGiepmansBNPalmerAE 2004 Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 22 1567 1572

36. FurumotoWAMickeyR 1970 Mathematical analyses of interference phenomenon of Tobacco mosiac virus - theoretical considerations. Virology 40 316 321

37. KleczkowskiA 1949 The transformation of local lesion counts for statistical analysis. Ann Appl Biol 36 139 152

38. KleczkowskiA 1950 Interpreting relationships between the concentrations of plant viruses and numbers of local lesions. J Gen Microbiol 4 53 69

39. Ben-AmiFRegoesRREbertD 2008 A quantitative test of the relationship between parasite dose and infection probability across different host–parasite combinations. Proc R Soc B 275 853 859

40. RidoutMSFenlonJSHughesPR 1993 A generalized one-hit model for bioassays of insect viruses. Biometrics 49 1136 1141

41. DieuBTMZwartMPVlakJM 2010 Can VNTRs be used to study genetic variation within white spot syndrome virus isolates? J Fish Dis 33 689 693

42. RegoesRRHottingerJWSygnarskiLEbertD 2003 The infection rate of Daphnia magna by Pasteuria ramosa conforms with the mass-action principle. Epidemiol Infect 131 957 966

43. ShallaTA 1964 Assembly and aggregation of Tobacco mosaic virus in Tomato leaflets. J Cell Biol 21 253 264

44. MiyashitaSKishinoH 2010 Estimation of the size of genetic bottlenecks in cell-to-cell movement of Soil-borne wheat mosaic virus and the possible role of the bottlenecks in speeding up selection of variations in trans-acting genes or elements. J Virol 84 1828 1837

45. CodonerFMDarosJASoleRVElenaSF 2006 The fittest versus the flattest: Experimental confirmation of the quasispecies effect with subviral pathogens. PLoS Pathog 2 1187 1193

46. BedoyaLMartinezFRubioLDarosJA 2010 Simultaneous equimolar expression of multiple proteins in plants from a disarmed potyvirus vector. J Biotechnol 150 268 275

47. CarrascoPDarosJAAgudelo-RomeroPElenaSF 2007 A real-time RT-PCR assay for quantifying the fitness of Tobacco etch virus in competition experiments. J Virol Meth 139 181 188

48. SanchezFMartinez-HerreraDAguilarIPonzF 1998 Infectivity of Turnip mosaic potyvirus cDNA clones and transcripts on the systemic host Arabidopsis thaliana and local lesion hosts. Vir Res 55 207 219

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Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

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