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Dynamics of the Multiplicity of Cellular Infection in a Plant Virus


Recombination, complementation and competition profoundly influence virus evolution and epidemiology. Since viruses are intracellular parasites, the basic parameter determining the potential for such interactions is the multiplicity of cellular infection (cellular MOI), i.e. the number of viral genome units that effectively infect a cell. The cellular MOI values that prevail in host organisms have rarely been investigated, and whether they remain constant or change widely during host invasion is totally unknown. Here, we fill this experimental gap by presenting the first detailed analysis of the dynamics of the cellular MOI during colonization of a host plant by a virus. Our results reveal ample variations between different leaf levels during the course of infection, with values starting close to 2 and increasing up to 13 before decreasing to initial levels in the latest infection stages. By revealing wide dynamic changes throughout a single infection, we here illustrate the existence of complex scenarios where the opportunity for recombination, complementation and competition among viral genomes changes greatly at different infection phases and at different locations within a multi-cellular host.


Vyšlo v časopise: Dynamics of the Multiplicity of Cellular Infection in a Plant Virus. PLoS Pathog 6(9): e32767. doi:10.1371/journal.ppat.1001113
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1001113

Souhrn

Recombination, complementation and competition profoundly influence virus evolution and epidemiology. Since viruses are intracellular parasites, the basic parameter determining the potential for such interactions is the multiplicity of cellular infection (cellular MOI), i.e. the number of viral genome units that effectively infect a cell. The cellular MOI values that prevail in host organisms have rarely been investigated, and whether they remain constant or change widely during host invasion is totally unknown. Here, we fill this experimental gap by presenting the first detailed analysis of the dynamics of the cellular MOI during colonization of a host plant by a virus. Our results reveal ample variations between different leaf levels during the course of infection, with values starting close to 2 and increasing up to 13 before decreasing to initial levels in the latest infection stages. By revealing wide dynamic changes throughout a single infection, we here illustrate the existence of complex scenarios where the opportunity for recombination, complementation and competition among viral genomes changes greatly at different infection phases and at different locations within a multi-cellular host.


Zdroje

1. TurnerPE

ChaoL

1998 Sex and the evolution of intrahost competition in RNA virus phi6. Genetics 150 523 532

2. TurnerPE

ChaoL

1999 Prisoner's dilemma in an RNA virus. Nature 398 441 443

3. TurnerPE

ChaoL

2003 Escape from Prisoner's Dilemma in RNA phage phi6. Am Nat 161 497 505

4. FroissartR

WilkeCO

MontvilleR

RemoldSK

ChaoL

2004 Co-infection weakens selection against epistatic mutations in RNA viruses. Genetics 168 9 19

5. GaoH

FeldmanMW

2009 Complementation and epistasis in viral coinfection dynamics. Genetics 182 251 263

6. OlkkonenVM

BamfordDH

1989 Quantitation of the adsorption and penetration stages of bacteriophage phi 6 infection. Virology 171 229 238

7. TurnerPE

BurchCL

HanleyKA

ChaoL

1999 Hybrid frequencies confirm limit to coinfection in the RNA bacteriophage phi6. J Virol 73 2420 2424

8. BullJC

GodfrayHC

O'ReillyDR

2001 Persistence of an occlusion-negative recombinant nucleopolyhedrovirus in Trichoplusia ni indicates high multiplicity of cellular infection. Appl Environ Microbiol 67 5204 5209

9. Gonzalez-JaraP

FraileA

CantoT

Garcia-ArenalF

2009 The multiplicity of infection of a plant virus varies during colonization of its eukaryotic host. J Virol 83 7487 7494

10. MiyashitaS

KishinoH

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

11. DrakeJW

HollandJJ

1999 Mutation rates among RNA viruses. Proc Natl Acad Sci U S A 96 13910 13913

12. DuffyS

ShackeltonLA

HolmesEC

2008 Rates of evolutionary change in viruses: patterns and determinants. Nat Rev Genet 9 267 276

13. FroissartR

RozeD

UzestM

GalibertL

BlancS

2005 Recombination every day: abundant recombination in a virus during a single multi-cellular host infection. PLoS Biol 3 e89

14. MonsionB

DuborjalH

BlancS

2008 Quantitative Single-letter Sequencing: a method for simultaneously monitoring numerous known allelic variants in single DNA samples. BMC Genomics 9 85

15. MonsionB

FroissartR

MichalakisY

BlancS

2008 Large bottleneck size in Cauliflower Mosaic Virus populations during host plant colonization. PLoS Pathog 4 e1000174

16. KouyosRD

AlthausCL

BonhoefferS

2006 Stochastic or deterministic: what is the effective population size of HIV-1? Trends Microbiol 14 507 511

17. 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

18. YvonM

MonsionB

MartinJP

GutiérrezS

BlancS

2009 PCR-based amplification and analysis of specific viral sequences from individual plant cells. Journal of Virological Methods doi:10.1016/j.jviromet.2009.04.016

19. ShallaTA

SheperdRJ

PetersenLJ

1980 Comparative cytology of nine isolates of cauliflower mosaic virus. Virology 102 381 388

20. DietrichC

MaissE

2003 Fluorescent labelling reveals spatial separation of potyvirus populations in mixed infected Nicotiana benthamiana plants. J Gen Virol 84 2871 2876

21. TakahashiT

Sugawarat

YamatsutaT

IsogaiM

NatsuakiT

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 1206

22. GiritchA

MarillonnetS

EnglerC

van EldikG

BottermanJ

2006 Rapid high-yield expression of full-size IgG antibodies in plants coinfected with noncompeting viral vectors. Proc Natl Acad Sci U S A 103 14701 14706

23. LeisnerSM

TurgeonR

HowellSH

1993 Effects of host plant development and genetic determinants on the long-distance movement of cauliflower mosaic virus in Arabidopsis. Plant Cell 5 191 202

24. LoveAJ

YunBW

LavalV

LoakeGJ

MilnerJJ

2005 Cauliflower mosaic virus, a compatible pathogen of Arabidopsis, engages three distinct defense-signaling pathways and activates rapid systemic generation of reactive oxygen species. Plant Physiol 139 935 948

25. LoveAJ

LavalV

GeriC

LairdJ

TomosAD

2007 Components of Arabidopsis defense- and ethylene-signaling pathways regulate susceptibility to Cauliflower mosaic virus by restricting long-distance movement. Mol Plant Microbe Interact 20 659 670

26. ChaoL

TranTT

TranTT

1997 The advantage of sex in the RNA virus Phi6. Genetics 147 953 959

27. FisherRA

1930 The Genetical Theory of Natural Selection. Oxford Oxford University Press

28. MullerHJ

1964 The relation of recombination to mutational advance. Mutat Res 106 2 9

29. HuangAS

1973 Defective interfering viruses. Annu Rev Microbiol 27 101 117

30. PerraultJ

1981 Origin and replication of defective interfering particles. Curr Top Microbiol Immunol 93 151 207

31. RouxL

SimonAE

HollandJJ

1991 Effects of defective interfering viruses on virus replication and pathogenesis in vitro and in vivo. Adv Virus Res 40 181 211

32. Garcia-ArriazaJ

ManrubiaSC

TojaM

DomingoE

EscarmisC

2004 Evolutionary transition toward defective RNAs that are infectious by complementation. J Virol 78 11678 11685

33. FroissartR

MichalakisY

BlancS

2002 Helper component-transcomplementation in the vector transmission of plant viruse. Phytopathology 92 576 579

34. DruckerM

FroissartR

HebrardE

UzestM

RavallecM

2002 Intracellular distribution of viral gene products regulates a complex mechanism of cauliflower mosaic virus acquisition by its aphid vector. Proc Natl Acad Sci U S A 99 2422 2427

35. MartinièreA

GarganiD

UzestM

LautredouN

BlancS

2009 A Role for Plant Microtubules in the Formation of Transmission-specific inclusion bodies of Cauliflower mosaic virus. Plant J 58 135 146

36. LoveAJ

LairdJ

HoltJ

HamiltonAJ

SadanandomA

2007 Cauliflower mosaic virus protein P6 is a suppressor of RNA silencing. J Gen Virol 88 3439 3444

37. HaasG

AzevedoJ

MoissiardG

GeldreichA

HimberC

2008 Nuclear import of CaMV P6 is required for infection and suppression of the RNA silencing factor DRB4. Embo J 27 2102 2112

38. JungA

MaierR

VartanianJP

BocharovG

JungV

2002 Multiply infected spleen cells in HIV patients. Nature 418 144

39. LevyDN

AldrovandiGM

KutschO

ShawGM

2004 Dynamics of HIV-1 recombination in its natural target cells. Proceedings of the National Academy of Sciences of the United States of America 101 4204 4209

40. DivekiZ

SalankiK

BalazsE

2002 Limited utility of blue fluorescent protein (BFP) in monitoring plant virus movement. Biochimie 84 997 1002

41. HullR

PlaskittA

1970 Electron microscopy on the behavior of two strains of alfalfa mosaic virus in mixed infections. Virology 42 773 776

42. TakeshitaM

ShigemuneN

KikuharaK

FuruyaN

TakanamiY

2004 Spatial analysis for exclusive interactions between subgroups I and II of Cucumber mosaic virus in cowpea. Virology 328 45 51

43. KennedyJS

DayMF

EastopVF

1962 A conspectus of aphids as vectors of plant viruses. London Commonwealth Inst. Entomol 114

44. FranckA

GuilleyH

JonardJ

RichardsK

HirthL

1980 Nucleotide sequence of cauliflower mosaic virus DNA. Cell 21 285 294

45. HullR

ShepherdRJ

1976 The coat proteins of cauliflower mosaic virus. Virology 70 217 220

46. BrissonN

PaszkowskiJ

PenswickJR

GronenbornB

HohnT

1984 Expression of a bacterial gene in plants by using a viral vector. Nature 310 511 514

47. De ZoetenGA

PenswickJR

HorisbergerMA

AhlP

SchultzeM

1989 The expression, localization, and effect of human interferon in plants. Virology 172 213 222

48. ImlauA

TruernitE

SauerN

1999 Cell-to-cell and long-distance trafficking of the green fluorescent protein in the phloem and symplastic unloading of the protein into sink tissues. Plant Cell 11 309 322

49. ChenCC

ChenTC

RajaJA

ChangCA

ChenLW

2007 Effectiveness and stability of heterologous proteins expressed in plants by Turnip mosaic virus vector at five different insertion sites. Virus Res 130 210 227

50. RabindranS

DawsonWO

2001 Assessment of recombinants that arise from the use of a TMV-based transient expression vector. Virology 284 182 189

51. Team RDC 2004 R: A Language and Environment for Statistical Computing. Vienna R Foundation for Statistical Computing

52. LeisnerSM

TurgeonR

HowellSH

1992 Long distance movement of cauliflower mosaic virus in infected turnip plants. Molec Plant-microbe interactions 5 41 47

53. MartiniereA

GarganiD

UzestM

LautredouN

BlancS

2009 A role for plant microtubules in the formation of transmission-specific inclusion bodies of Cauliflower mosaic virus. Plant J 58 135 146

54. MorenoA

HebrardE

UzestM

BlancS

FereresA

2005 A single amino acid position in the helper component of cauliflower mosaic virus can change the spectrum of transmitting vector species. J Virol 79 13587 13593

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Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

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