Modelling the Evolutionary Dynamics of Viruses within Their Hosts: A Case Study Using High-Throughput Sequencing
Uncovering how natural selection and genetic drift shape the evolutionary dynamics of virus populations within their hosts can pave the way to a better understanding of virus emergence. Mathematical models already play a leading role in these studies and are intended to predict future emergences. Here, using high-throughput sequencing, we analyzed the within-host population dynamics of four Potato virus Y (PVY) variants differing at most by two substitutions involved in pathogenicity properties. Model selection procedures were used to compare experimental results to six hypotheses regarding competitiveness and intensity of genetic drift experienced by viruses during host plant colonization. Results indicated that the frequencies of variants were well described using Lotka-Volterra models where the competition coefficients βij exerted by variant j on variant i are equal to their fitness ratio, rj/ri. Statistical inference allowed the estimation of the effect of each mutation on fitness, revealing slight (s = −0.45%) and high (s = −13.2%) fitness costs and a negative epistasis between them. Results also indicated that only 1 to 4 infectious units initiated the population of one apical leaf. The between-host variances of the variant frequencies were described using Dirichlet-multinomial distributions whose scale parameters, closely related to the fixation index FST, were shown to vary with time. The genetic differentiation of virus populations among plants increased from 0 to 10 days post-inoculation and then decreased until 35 days. Overall, this study showed that mathematical models can accurately describe both selection and genetic drift processes shaping the evolutionary dynamics of viruses within their hosts.
Vyšlo v časopise:
Modelling the Evolutionary Dynamics of Viruses within Their Hosts: A Case Study Using High-Throughput Sequencing. PLoS Pathog 8(4): e32767. doi:10.1371/journal.ppat.1002654
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1002654
Souhrn
Uncovering how natural selection and genetic drift shape the evolutionary dynamics of virus populations within their hosts can pave the way to a better understanding of virus emergence. Mathematical models already play a leading role in these studies and are intended to predict future emergences. Here, using high-throughput sequencing, we analyzed the within-host population dynamics of four Potato virus Y (PVY) variants differing at most by two substitutions involved in pathogenicity properties. Model selection procedures were used to compare experimental results to six hypotheses regarding competitiveness and intensity of genetic drift experienced by viruses during host plant colonization. Results indicated that the frequencies of variants were well described using Lotka-Volterra models where the competition coefficients βij exerted by variant j on variant i are equal to their fitness ratio, rj/ri. Statistical inference allowed the estimation of the effect of each mutation on fitness, revealing slight (s = −0.45%) and high (s = −13.2%) fitness costs and a negative epistasis between them. Results also indicated that only 1 to 4 infectious units initiated the population of one apical leaf. The between-host variances of the variant frequencies were described using Dirichlet-multinomial distributions whose scale parameters, closely related to the fixation index FST, were shown to vary with time. The genetic differentiation of virus populations among plants increased from 0 to 10 days post-inoculation and then decreased until 35 days. Overall, this study showed that mathematical models can accurately describe both selection and genetic drift processes shaping the evolutionary dynamics of viruses within their hosts.
Zdroje
1. AndersonPKCunninghamAAPatelNGMoralesFJEpsteinPR 2004 Emerging infectious diseases of plants: Pathogen pollution, climate change and agrotechnology drivers. Trends Ecol Evol 19 535 544
2. HolmesEC 2009 The evolutionary genetics of emerging viruses. Annu Rev Ecol Evol Syst 40 353 372
3. JonesRAC 2009 Plant virus emergence and evolution: Origins, new encounter scenarios, factors driving emergence, effects of changing world conditions, and prospects for control. Virus Res 141 113 130
4. ElenaSFBedhommeSCarrascoPCuevasJMde la IglesiaF 2011 The evolutionary genetics of emerging plant RNA viruses. Mol Plant Microbe Interact 24 287 293
5. HolmesECDrummondAJ 2007 The evolutionary genetics of viral emergence. ChildsJEMacKenzieJSRichtJA Wildlife and emerging zoonotic diseases: The biology, circumstances and consequences of cross-species transmission Verlag Berlin Heidelberg Springer 51 66
6. zur WieschPAKouyosREngelstädterJRegoesRRBonhoefferS 2011 Population biological principles of drug-resistance evolution in infectious diseases. Lancet Infect Dis 11 236 247
7. GómezPRodríguez-HernándezAMMouryBArandaMA 2009 Genetic resistance for the sustainable control of plant virus diseases: Breeding, mechanisms and durability. Eur J Plant Pathol 125 1 22
8. FabreFRousseauEMailleretLMouryB 2012 Durable strategies to deploy plant resistance in agricultural landscapes. New Phytol 193 1064 1075
9. García-ArenalFFraileAMalpicaJM 2001 Variability and genetic structure of plant virus populations. Annu Rev Phytopathol 39 157 186
10. SanjuánR 2010 Mutational fitness effects in RNA and single-stranded DNA viruses: Common patterns revealed by site-directed mutagenesis studies. Phil Trans R Soc B 365 1975 1982
11. WrightS 1931 Evolution in Mendelian populations. Genetics 16 97 159
12. HallJSFrenchRHeinGLMorrisTJStengerDC 2001 Three distinct mechanisms facilitate genetic isolation of sympatric wheat streak mosaic virus lineages. Virology 282 230 236
13. SacristánSMalpicaJMFraileAGarcía-ArenalF 2003 Estimation of population bottlenecks during systemic movement of Tobacco mosaic virus in tobacco plants. J Virol 77 9906 9911
14. MonsionBFroissartRMichalakisYBlancS 2008 Large bottleneck size in Cauliflower mosaic virus populations during host plant colonization. PLoS Pathog 4 e1000174
15. GutiérrezSYvonMThébaudGMonsionBMichalakisY 2010 Dynamics of the multiplicity of cellular infection in a plant virus. PLoS Pathog 6 e1001113
16. ZwartMPDaròsJAElenaSF 2011 One is enough: In vivo effective population size is dose-dependent for a plant RNA virus. PLoS Pathog 7 e1002122
17. CarrascoPde la IglesiaFElenaSF 2007 Distribution of fitness and virulence effects caused by single-nucleotide substitutions in Tobacco etch virus. J Virol 81 12979 12984
18. JanzacBMontarryJPalloixANavaudOMouryB 2010 A point mutation in the polymerase of Potato virus Y confers virulence toward the Pvr4 resistance of pepper and a high competitiveness cost in susceptible cultivar. Mol Plant Microbe Interact 23 823 830
19. FraileAPagánIAnastasioGSáezEGarcía-ArenalF 2011 Rapid genetic diversification and high fitness penalties associated with pathogenicity evolution in a plant virus. Mol Biol Evol 28 1425 1437
20. AymeVPetit-PierreJSoucheSPalloixAMouryB 2007 Molecular dissection of the Potato virus Y VPg virulence factor reveals complex adaptations to the pvr2 resistance allelic series in pepper. J Gen Virol 88 1594 1601
21. BrockhurstMAColegraveNRozenDE 2011 Next-generation sequencing as a tool to study microbial evolution. Mol Ecol 20 972 980
22. MouryBMorelCJohansenEGuilbaudLSoucheS 2004 Mutations in Potato virus Y genome-linked protein determine virulence toward recessive resistances in Capsicum annuum and Lycopersicon hirsutum. Mol Plant Microbe Interact 17 322 329
23. AymeVSoucheSCarantaCJacquemondMChadoeufJ 2006 Different mutations in the genome-linked protein VPg of Potato virus Y confer virulence on the pvr23 resistance in pepper. Mol Plant Microbe Interact 19 557 563
24. HuseSMHuberJAMorrisonHGSoginMLWelchDM 2007 Accuracy and quality of massively parallel DNA pyrosequencing. Genome Biol 8 R143
25. BulmerM 1994 Theoretical evolutionary ecology Sunderland, MA Sinauer 352
26. KitakadoTKitadaSKishinoHSkaugHJ 2006 An integrated-likelihood method for estimating genetic differentiation between populations. Genetics 173 2073 2082
27. SanjuánRNebotMRChiricoNManskyLMBelshawR 2010 Viral mutation rates. J Virol 84 9733 9748
28. González-JaraPFraileACantoTGarcía-ArenalF 2009 The multiplicity of infection of a plant virus varies during colonization of its eukaryotic host. J Virol 83 7487 7494
29. 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
30. FrenchRStrengerDC 2005 Population structure within lineages of Wheat streak mosaic virus derived from a common founding event exhibits stochastic variation inconsistent with the deterministic quasi-species model. Virology 343 179 189
31. TurgeonR 1989 The sink-source transition in leaves. Annu Rev Plant Physiol Plant Mol Biol 40 119 138
32. VuorinenALKelloniemiJValkonenJPT 2011 Why do viruses need phloem for systemic invasion of plants. Plant Sci 181 355 363
33. WeinreichDMWatsonRAChaoLHarrisonR 2005 Perspective: Sign epistasis and genetic constraint on evolutionary trajectories. Evolution 59 1165 1174
34. RhodesTDNikolaitchikOChenJPowellDHuWS 2005 Genetic recombination of Human immunodeficiency virus type 1 in one round of viral replication: effects of genetic distance, target cells, accessory genes, and lack of high negative interference in crossover events. J Virol 79 1666 1677
35. SoléRVFerrerRGonzález-GarcíaIQuerJDomingoE 1999 Red queen dynamics, competition and critical points in a model of RNA virus quasispecies. J Theor Biol 198 47 59
36. EigenMMcCaskillJSchusterP 1988 Molecular quasi-species. J Phys Chem 92 6881 6891
37. FabreFBruchouCPalloixAMouryB 2009 Key determinants of resistance durability to plant viruses: Insights from a model linking within- and between-host dynamics. Virus Res 141 140 149
38. MideoNAlizonSDayT 2008 Linking within- and between-host dynamics in the evolutionary epidemiology of infectious diseases. Trends Ecol Evol 23 511 517
39. JegerMJSealSEVan den BoschF 2006 Evolutionary epidemiology of plant virus disease. ThreshJMMaramoroschKShatkinAJ Plant virus epidemiology San Diego Academic Press 163 203
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
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