Narrow Bottlenecks Affect Populations during Vertical Seed Transmission but not during Leaf Colonization
The effective size of populations (Ne) determines whether selection or genetic drift is the predominant force shaping their genetic structure and evolution. Populations having high Ne adapt faster, as selection acts more intensely, than populations having low Ne, where random effects of genetic drift dominate. Estimating Ne for various steps of plant virus life cycle has been the focus of several studies in the last decade, but no estimates are available for the vertical transmission of plant viruses, although virus seed transmission is economically significant in at least 18% of plant viruses in at least one plant species. Here we study the co-dynamics of two variants of Pea seedborne mosaic virus (PSbMV) colonizing leaves of pea plants (Pisum sativum L.) during the whole flowering period, and their subsequent transmission to plant progeny through seeds. Whereas classical estimators of Ne could be used for leaf infection at the systemic level, as virus variants were equally competitive, dedicated stochastic models were needed to estimate Ne during vertical transmission. Very little genetic drift was observed during the infection of apical leaves, with Ne values ranging from 59 to 216. In contrast, a very drastic genetic drift was observed during vertical transmission, with an average number of infectious virus particles contributing to the infection of a seedling from an infected mother plant close to one. A simple model of vertical transmission, assuming a cumulative action of virus infectious particles and a virus density threshold required for vertical transmission to occur fitted the experimental data very satisfactorily. This study reveals that vertically-transmitted viruses endure bottlenecks as narrow as those imposed by horizontal transmission. These bottlenecks are likely to slow down virus adaptation and could decrease virus fitness and virulence.
Vyšlo v časopise:
Narrow Bottlenecks Affect Populations during Vertical Seed Transmission but not during Leaf Colonization. PLoS Pathog 10(1): e32767. doi:10.1371/journal.ppat.1003833
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1003833
Souhrn
The effective size of populations (Ne) determines whether selection or genetic drift is the predominant force shaping their genetic structure and evolution. Populations having high Ne adapt faster, as selection acts more intensely, than populations having low Ne, where random effects of genetic drift dominate. Estimating Ne for various steps of plant virus life cycle has been the focus of several studies in the last decade, but no estimates are available for the vertical transmission of plant viruses, although virus seed transmission is economically significant in at least 18% of plant viruses in at least one plant species. Here we study the co-dynamics of two variants of Pea seedborne mosaic virus (PSbMV) colonizing leaves of pea plants (Pisum sativum L.) during the whole flowering period, and their subsequent transmission to plant progeny through seeds. Whereas classical estimators of Ne could be used for leaf infection at the systemic level, as virus variants were equally competitive, dedicated stochastic models were needed to estimate Ne during vertical transmission. Very little genetic drift was observed during the infection of apical leaves, with Ne values ranging from 59 to 216. In contrast, a very drastic genetic drift was observed during vertical transmission, with an average number of infectious virus particles contributing to the infection of a seedling from an infected mother plant close to one. A simple model of vertical transmission, assuming a cumulative action of virus infectious particles and a virus density threshold required for vertical transmission to occur fitted the experimental data very satisfactorily. This study reveals that vertically-transmitted viruses endure bottlenecks as narrow as those imposed by horizontal transmission. These bottlenecks are likely to slow down virus adaptation and could decrease virus fitness and virulence.
Zdroje
1. HarrisonBD (1956) The infectivity of extracts made from leaves at intervals after inoculation with viruses. J Gen Microbiol 15: 210–220.
2. MalpicaJ, FraileA, MorenoI, ObiesCI, DrakeJW, et al. (2002) The rate and character of spontaneous mutation in an RNA virus. Genetics 162: 1505–1511.
3. GutiérrezS, MichalakisY, BlancS (2012) Virus population bottlenecks during within-host progression and host-to-host transmission. Curr Opin Virol 2: 1–10.
4. ZwartMP, DaròsJA, ElenaSF (2011) One is enough: In vivo effective population size is dose-dependent for a plant RNA virus. PLoS Pathog 7: e1002122.
5. Wright S (1969) Evolution and the genetics of populations. II. The theory of gene frequencies. Chicago: University of Chicago Press. 520 p.
6. WangJ (2005) Estimation of effective population sizes from data on genetic markers. Phil Trans R Soc B 360: 1395–1409.
7. RobertsonA (1961) Inbreeding in artificial selection programmes. Genet Res 2: 189–194.
8. LynchM, ConeryJ, BurgerR (1995) Mutation accumulation and the extinction of small populations. Am Nat 146: 489–518.
9. MouryB, FabreF, SenoussiR (2007) Estimation of the number of virus particles transmitted by an insect vector. Proc Natl Acad Sci U S A 104: 17891–17896.
10. FabreF, MontarryJ, CovilleJ, SenoussiR, SimonV, et al. (2012) Modelling the evolutionary dynamics of viruses within their hosts: A case study using high-throughput sequencing. PLoS Pathog 8: e1002654.
11. BetancourtM, FereresA, FraileA, García-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.
12. SacristánS, DíazM, FraileA, García-ArenalF (2011) Contact transmission of Tobacco mosaic virus: a quantitative analysis of parameters relevant for virus evolution. J Virol 85: 4974–4981.
13. SacristánS, MalpicaJM, FraileA, García-ArenalF (2003) Estimation of population bottlenecks during systemic movement of Tobacco mosaic virus in tobacco plants. J Virol 77: 9906–9911.
14. González-JaraP, FraileA, CantoT, García-ArenalF (2009) The multiplicity of infection of a plant virus varies during colonization of its eukaryotic host. J Virol 83: 7487–7494.
15. MiyashitaS, KishinoH (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.
16. GutiérrezS, YvonM, ThébaudG, MonsionB, MichalakisY, et al. (2010) Dynamics of the multiplicity of cellular infection in a plant virus. PLoS Pathog 6: e1001113.
17. FrenchR, StengerDC (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.
18. BroadbentL (1965) The epidemiology of tomato mosaic XI: Seed-transmission of TMV. Ann Appl Biol 56: 177–205.
19. CouttsBA, PrinceRT, JonesRAC (2009) Quantifying effects of seedborne inoculum on virus spread, yield losses, and seed infection in the Pea seedborne mosaic virus-field pea pathosystem. Phytopathology 99: 1156–1167.
20. JohansenE, EdwardsMC, HamptonRO (1994) Seed transmission of viruses: Current perspectives. Annu Rev Phytopathol 32: 363–386.
21. BorgstrømB, JohansenIE (2001) Mutations in Pea seedborne mosaic virus genome-linked protein VPg alter pathotype-specific virulence in Pisum sativum. Mol Plant-Microbe Interact 14: 707–714.
22. WangD, WoodsRD, CockbainAJ, MauleAJ, BiddleAJ (1993) The susceptibility of pea cultivars to Pea seed-borne mosaic virus infection and seed transmission in the UK. Plant Pathol 42: 42–47.
23. WangD, MauleAJ (1992) Early embryo invasion as a determinant in pea of the seed transmission of Pea seed-borne mosaic virus. J Gen Virol 73: 1615–1620.
24. WrightS (1931) Evolution in Mendelian populations. Genetics 16: 97–159.
25. MonsionB, FroissartR, MichalakisY, BlancS (2008) Large bottleneck size in Cauliflower mosaic virus populations during host plant colonization. PLoS Pathog 4: e1000174.
26. FelsensteinJ (1971) Inbreeding and variance effective numbers in populations with overlapping generations. Genetics 68: 581–597.
27. JohansenIE, DoughertyWG, KellerKE, WangD, HamptonRO (1996) Multiple viral determinants affect seed transmission of Pea seedborne mosaic virus in Pisum sativum. J Gen Virol 77: 3149–3154.
28. JohnsonJB, OmlandKS (2004) Model selection in ecology and evolution. Trends Ecol Evol 19: 101–108.
29. BurnhamKP, AndersonDR (2004) Multimodel Inference: Understanding AIC and BIC Model Selection. Sociol Method Res 33: 261–304.
30. KhelifaM, MasseD, BlancS, DruckerM (2010) Evaluation of the minimal replication time of Cauliflower mosaic virus in different hosts. Virology 396: 238–245.
31. MartinezF, SardanyesJ, ElenaSF (2011) Dynamics of a Plant RNA Virus Intracellular Accumulation: Stamping Machine vs. Geometric Replication. Genetics 188: 637–646.
32. JridiC, MartinJF, Marie-JeanneV, LabonneG, BlancS (2006) Distinct viral populations differentiate and evolve independently in a single perennial host plant. J Virol 80: 2349–2357.
33. GutiérrezS, YvonM, PirollesE, GarzoE, FereresA, et al. (2012) Circulating Virus Load Determines the Size of Bottlenecks in Viral Populations Progressing within a Host. PLoS Pathog 8 (11) e1003009.
34. VerhofstedeC, DemecheleerE, De CabooterN, GaillardP, MwanyumbaF, et al. (2003) Diversity of the human immunodeficiency virus type 1 (HIV-1) env sequence after vertical transmission in mother-child pairs infected with HIV-1 subtype A. J Virol 77: 3050–3057.
35. SamleeratT, BraibantM, JourdainG, MoreauA, Ngo-Giang-HuongN, et al. (2008) Characteristics of HIV type 1 (HIV-1) glycoprotein 120 env sequences in mother-infant pairs infected with HIV-1 subtype CRF01_AE. J Infect Dis 198: 868–876.
36. RussellES, KwiekJJ, KeysJ, BartonK, MwapasaV, et al. (2011) The genetic bottleneck in vertical transmission of subtype C HIV-1 is not driven by selection of especially neutralization-resistant virus from the maternal viral population. J Virol 85: 8253–8262.
37. SimmonsHE, DunhamJP, ZinnKE, MunkvoldGP, HolmesEC (2013) Zucchini yellow mosaic virus (ZYMV, Potyvirus): Vertical transmission, seed infection and cryptic infections. Virus Res 176: 259–264.
38. RobertsIM, WangD, ThomasCL, MauleAJ (2003) Pea seed-borne mosaic virus seed transmission exploits novel symplastic pathways to infect the pea embryo and is, in part, dependent upon chance. Protoplasma 222: 31–43.
39. WangD, MauleAJ (1994) A model for seed transmission of a plant virus: Genetic and structural analyses of pea embryo invasion by Pea seed-borne mosaic virus. Plant Cell 6: 777–787.
40. DietrichC, MaissE (2003) Fluorescent labelling reveals spatial separation of potyvirus populations in mixed infected Nicotiana benthamiana plants. J Gen Virol 84: 2871–2876.
41. CarrascoP, de la IglesiaF, ElenaSF (2007) Distribution of fitness and virulence effects caused by single-nucleotide substitutions in tobacco etch virus. J Virol 81: 12979–12984.
42. LafforgueG, TromasN, ElenaSF, ZwartMP (2012) Dynamics of the Establishment of Systemic Potyvirus Infection: Independent yet Cumulative Action of Primary Infection Sites. J Virol 86: 12912–12922.
43. EwaldPW (1987) Transmission Modes and Evolution of the Parasitism-Mutualism Continuum. Ann N Y Acad Sci 503: 295–306.
44. BergstromCT, McElhanyP, RealLA (1999) Transmission bottlenecks as determinants of virulence in rapidly evolving pathogens. Proc Natl Acad Sci U S A 96: 5095–5100.
45. LigatLS, RandlesJW (1993) An eclipse of Pea seed-borne mosaic virus in vegetative tissue of pea following repeated transmission through the seed. Ann Appl Biol 122: 39–47.
46. StewartAD, LogsdonJM, KelleyS (2005) An empirical study of the evolution of virulence under both horizontal and vertical transmission. Ecology 59: 730–739.
47. GallitelliD (2000) The ecology of Cucumber mosaic virus and sustainable agriculture. Virus Res 71: 9–21.
48. AliA, KobayashiM (2010) Seed transmission of Cucumber mosaic virus in pepper. J Virol Methods 163: 234–237.
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2014 Číslo 1
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
Najčítanejšie v tomto čísle
- Human and Plant Fungal Pathogens: The Role of Secondary Metabolites
- Lyme Disease: Call for a “Manhattan Project” to Combat the Epidemic
- Murine Gammaherpesvirus M2 Protein Induction of IRF4 via the NFAT Pathway Leads to IL-10 Expression in B Cells
- Origin, Migration Routes and Worldwide Population Genetic Structure of the Wheat Yellow Rust Pathogen f.sp.