Temporal dynamics of intrahost molecular evolution for a plant RNA virus

Molecular Biology and Evolution

Volumn 32, Issue 5, 2015, Pages 1132-1147

  Cuevas, José M ^a   Willemsen, Anouk ^a   Hillung, Julia ^a   Zwart, Mark P ^a   Elena, Santiago F ^a,b  

^a UNIVERSITAT POLITÈCNICA DE VALÈNCIA   (Spain)

^b SANTA FE INSTITUTE   (United States)

Author keywords

adaptation; evolution of virulence; experimental evolution; next generation sequencing; population dynamics; Potyvirus; virus evolution

Indexed keywords

PLANT RNA;

ADAPTATION; ARTICLE; DIRECTIONAL SELECTION; DIVERSIFYING SELECTION; DYNAMICS; GENETIC DRIFT; GENETIC VARIABILITY; MOLECULAR EVOLUTION; NEXT GENERATION SEQUENCING; NONHUMAN; PLANT LEAF; PLANT VIRUS; POPULATION DYNAMICS; RNA VIRUS; TOBACCO ETCH POLYVIRUS; VIRAL PLANT DISEASE; VIRUS LOAD; VIRUS VIRULENCE; BIOLOGICAL MODEL; COMPUTER SIMULATION; GENETICS; HOST PARASITE INTERACTION; MUTATION; PATHOGENICITY; POPULATION GENETICS; POTYVIRUS; TOBACCO; VIROLOGY;

NICOTIANA TABACUM; POTYVIRUS; RNA VIRUSES; TOBACCO ETCH VIRUS;

COMPUTER SIMULATION; EVOLUTION, MOLECULAR; GENETIC DRIFT; GENETIC VARIATION; GENETICS, POPULATION; HOST-PARASITE INTERACTIONS; MODELS, GENETIC; MUTATION; PLANT VIRUSES; POTYVIRUS; RNA VIRUSES; TOBACCO;

EID: 84929650722     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msv028     Document Type: Article

References (75)

1. Agudelo-Romero P, De la Iglesia F, Elena SF. (2008). The pleiotropic cost of host-specialization in tobacco etch potyvirus. Infect Genet Evol. 8: 806-814
2. Azevedo RB, Lohaus R, Srinivasan S, Dang KK, Burch CL. (2006). Sexual reproduction selects for robustness and negative epistasis in artificial gene networks. Nature 440: 87-90
3. Barrick JE, Lenski RE. (2013). Genome dynamics during experimental evolution. Nat Rev Genet. 14: 827-839
4. Bedhomme S, Elena SF. (2011). Virus infection suppresses Nicotiana benthamiana adaptive phenotypic plasticity. PLoS One 6: e17275
5. Bedhomme S, Lafforgue G, Elena SF. (2012). Multihost experimental evolution of a plant RNA virus reveals local adaptation and host-specific mutations. Mol Biol Evol. 29: 1481-1492
6. Bedoya LC, Darós JA. (2010). Stability of Tobacco etch virus infectious clones in plasmid vectors. Virus Res. 149: 234-240
7. Betancourt M, Fraile A, García-Arenal F. (2011). Cucumber mosaic virus satellite RNAs that induce similar symptoms in melon plants show large differences in fitness. J Gen Virol. 92: 1930-1938
8. Bonhoeffer S, Chappey C, Parkin NT, Whitcomb JM, Petropoulos CJ. (2004). Evidence for positive epistasis in HIV-1. Science 306: 1547-1550
9. Bordería AV, Elena SF. (2002). r-and K-selection in experimental populations of Vesicular stomatitis virus. Infect Genet Evol. 2: 137-143
10. Bull JJ, Badgett MR, Wichman HA, Huelsenbeck JP, Hillis DM, Gulati A, Ho C, Molineux IJ. (1997). Exceptional convergent evolution in a virus. Genetics 147: 1497-1507
11. Burch CL, Chao L. (2000). Evolvability of an RNA virus is determined by its mutational neighborhood. Nature 406: 625-628
12. Burch CL, Chao L. (2004). Epistasis and its relationship to canalization in the RNA virus f6. Genetics 167: 559-567
13. Cabanilles L, Arribas M, Lázaro E. (2013). Evolution at increased error rate leads to the coexistence of multiple adaptive pathways in an RNA virus. BMC Evol Biol. 13: 11
14. Carrasco P, Darós JA, Agudelo-Romero P, Elena SF. (2007). A real-time RTPCR assay for quantifying the fitness of Tobacco etch virus in competition experiments. J Virol Methods. 139: 181-188
15. Carrasco P, De la Iglesia F, Elena SF. (2007). Distribution of fitness and virulence effects caused by single-nucleotide substitutions in Tobacco etch virus. J Virol. 81: 12979-12984
16. Carrington JC, Haldeman R, Dolja VV, Restrepo-Hartwig MA. (1993). Internal cleavage and trans-proteolytic activities of the VPg-proteinase (NIa) of tobacco etch potyvirus in vivo. J Virol. 67: 6995-7000
17. Chung BY, Miller WA, Atkins JF, Firth AE. (2008). An overlapping essential gene in the Potyviridae. Proc Natl Acad Sci USA. 105: 5897-5902
18. Codoñer FM, Darós JA, Solé RV, Elena SF. (2006). The fittest versus the flattest: experimental confirmation of the quasispecies effect with subviral pathogens. PLoS Pathog. 2: e136
19. Cuevas JM, Elena SF, Moya A. (2002). Molecular basis of adaptive convergence in experimental populations of RNA viruses. Genetics 162: 533-542
20. Cui X, Wei T, Chowda-Reddy RV, Sun G, Wang A. (2010). The Tobacco etch virus P3 protein forms mobile inclusions via the early secretory pathway and traffics along actin microfilaments. Virology 397: 56-63
21. Domingo E. (1999). Quasispecies. In: Granoff A, Webster RG, editors. Encyclopedia of virology. London: Academic Press. p. 1431-1436
22. Doumayrou J, Avellan A, Froissart R, Michalakis Y. (2012). An experimental test of the transmission-virulence trade-off hypothesis in a plant virus. Evolution 67: 477-486
23. Duffy S, Shackelton LA, Holmes EC. (2008). Rates of evolutionary change in viruses: patterns and determinants. Nat Rev Genet. 9: 267-276
24. Dunham JP, Simmons HE, Holmes EC, Stephenson AG. (2014). Analysis of viral (Zucchini yellow mosaic virus) genetic diversity during systemic movement through a Cucurbita pepo vine. Virus Res. 191: 172-179
25. Eigen M. (1971). Selforganization of matter and the evolution of biological macromolecules. Naturwissenschaften 58: 465-523
26. Eigen M. (1996). On the nature of virus quasispecies. Trends Microbiol. 4: 216-218
27. Elena SF, Carrasco P, Darós JA, Sanjuán R. (2006). Mechanisms of genetic robustness in RNA viruses. EMBO Rep. 7: 168-173
28. Elena SF, González-Candelas F, Novella IS, Duarte EA, Clarke DK, Domingo E, Holland JJ, Moya A. (1996). Evolution of fitness in experimental populations of Vesicular stomatitis virus. Genetics 142: 673-679
29. Elena SF, Sanjuán R. (2007). Virus evolution: insights from an experimental approach. Annu Rev Ecol Evol Syst. 38: 27-52
30. Gutiérrez S, Yvon M, Pirolles E, Garzo E, Fereres A, Michalakis Y, Blanc S. (2012). Circulating virus load determines the size of bottlenecks in viral populations progressing within a host. PLoS Pathog. 8: e1003009
31. Heidel AJ, Clarke JD, Antonovics J, Dong X. (2004). Fitness costs of mutations affecting the systemic acquired resistance pathway in Arabidopsis thaliana. Genetics 168: 2197-2206
32. Heil M. (2001). The ecological concept of costs of induced systemic resistance (ISR). Eur J Plant Pathol. 107: 137-146
33. Hillung J, Cuevas JM, Valverde S, Elena SF. (2014). Experimental evolution of an emerging plant virus in host genotypes that differ in their susceptibility to infection. Evolution 68: 2467-2480
34. Holland J, Spindler K, Horodyski F, Grabau E, Nichol S, VandePol S. (1982). Rapid evolution of RNA genomes. Science 215: 1577-1585
35. Johnson JB, Omland KS. (2004). Model selection in ecology and evolution. Trends Ecol Evol. 19: 101-108
36. Kleczkowski A. (1950). Interpreting relationships between the concentrations of plant viruses and numbers of local lesions. J Gen Microbiol. 4: 53-69
37. Koboldt D, Zhang Q, Larson D, Shen D, McLellan M, Lin L, Miller C, Mardis E, Ding L, Wilson R. (2012). VarScan 2: somatic mutation and copy number alteration discovery in cancer by exome sequencing. Genome Res. 22: 568-576
38. Lalić J, Cuevas JM, Elena SF. (2011). Effect of host species on the distribution of mutational fitness effects for an RNA virus. PLoS Genet. 7: e1002378
39. Lalić J, Elena SF. (2012). Magnitude and sign epistasis among deleterious mutations in a positive-sense plant RNA virus. Heredity 109: 71-77
40. Langmead B, Salzberg S. (2012). Fast gapped-read alignment with Bowtie 2. Nat Methods. 9: 357-359
41. Lenski RE, May RM. (1994). The evolution of virulence in parasites and pathogens: reconciliation between two competing hypotheses. J Theor Biol. 169: 253-265
42. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R 1000 Genome Project Data Processing Subgroup. (2009). The sequence alignment/map (SAM) format and SAMtools. Bioinformatics 25: 2078-2079
43. Li H, Roossinck MJ. (2004). Genetic bottlenecks reduce population variation in an experimental RNA virus population. J Virol. 78: 10582-10587
44. Li WH. (1997). Molecular evolution. Sunderland (MA): Sinauer Associates Inc
45. Martínez F, Darós JA. (2014). Tobacco etch virus protein P1 traffics to the nucleolus and associates with the host 60S ribosomal subunits during infection. J Virol. 88: 10725-10737
46. Martínez F, Sardanyés J, Elena SF, Darós JA. (2011). Dynamics of a plant RNA virus intracellular accumulation: stamping machine vs. geometric replication. Genetics 188: 637-646
47. Miralles R, Gerrish PJ, Moya A, Elena SF. (1999). Clonal interference and the evolution of RNA viruses. Science 285: 1745-1747
48. Miralles R, Moya A, Elena SF. (1997). Is group selection a factor modulating the virulence of RNA viruses?. Genet Res. 69: 165-172
49. Miralles R, Moya A, Elena SF. (2000). Diminishing returns of population size in the rate of RNA virus adaptation. J Virol. 74: 3566-3571
50. Morel JB, Dangl JL. (1997). The hypersensitive response and the induction of cell death in plants. Cell Death Differ. 4: 671-683
51. Novella IS, Zárate S, Metzgar D, Ebendick-Corpus BE. (2004). Positive selection of synonymous mutations in Vesicular stomatitis virus. J Mol Biol. 342: 1415-1421
52. Pagán I, Alonso-Blanco C, García-Arenal F. (2008). Host responses in lifehistory traits and tolerance to virus infection in Arabidopsis thaliana. PLoS Pathog. 4: e1000124
53. Quinn GP, Keough MJ. (2002). Experimental design and data analysis for biologists, Vol. 133. Cambridge: Cambridge University Press
54. RCoreTeam. (2013). R: Alanguage and environment for statistical computing. Vienna (Austria): R Foundation for Statistical Computing
55. Remold SK, Rambaut A, Turner PE. (2008). Evolutionary genomics of host adaptation in Vesicular stomatitis virus. Mol Biol Evol. 25: 1138-1147
56. Rico P, Ivars P, Elena SF, Hernández C. (2006). Insights into the selective pressures restricting Pelargonium flower break virus genome variability: evidence for host adaptation. J Virol. 80: 8124-8132
57. Riechmann JL, Laín S, García JA. (1992). Highlights and prospects of potyvirus molecular biology. J Gen Virol. 73: 1-16
58. Sanjuán R, Cuevas JM, Furió V, Holmes EC, Moya A. (2007). Selection for robustness in mutagenized RNA viruses. PLoS Genet. 3: e93
59. Sanjuán R, Elena SF. (2006). Epistasis correlates to genomic complexity. Proc Natl Acad Sci USA. 103: 14402-14405
60. Sanjuán R, Moya A, Elena SF. 2004a. The contribution of epistasis to the architecture of fitness in an RNA virus. Proc Natl Acad Sci USA. 101: 15376-15379
61. Sanjuán R, Moya A, Elena SF. 2004b. The distribution of fitness effects caused by single-nucleotide substitutions in an RNA virus. Proc Natl Acad Sci USA. 101: 8396-8401
62. Schmieder R, Edwards R. (2011). Quality control and preprocessing of metagenomic datasets. Bioinformatics 27: 863-864
63. Schuster P, Swetina J. (1988). Stationary mutant distributions and evolutionary optimization. Bull Math Biol. 50: 635-660
64. Shukla DD, Ward CW, Brunt AA. (1994). The Potyviridae. Wallingford (United Kingdom): CABI
65. Strelkowa N, Lässig M. (2012). Clonal interference in the evolution of influenza. Genetics 192: 671-682
66. Su G, Morris JH, Demchak B, Bader GC. (2014). Biological network exploration with Cytoscape 3. Curr Protoc Bioinformatics. 47: 8; 13.1-8.13.24
67. Tromas N, Elena SF. (2010). The rate and spectrum of spontaneous mutations in a plant RNA virus. Genetics 185: 983-989
68. Tromas N, Zwart MP, Lafforgue G, Elena SF. (2014). Within-host spatiotemporal dynamics of plant virus infection at the cellular level. PLoS Genet. 10: e1004186
69. Tromas N, Zwart MP, Poulain M, Elena SF. (2014). Estimation of the in vivo recombination rate for a plant RNA virus. J Gen Virol. 95: 724-732
70. Urcuqui-Inchima S, Haenni AL, Bernardi F. (2001). Potyvirus proteins: a wealth of functions. Virus Res. 74: 157-175
71. Wichman HA, Badgett MR, Scott LA, Boulianne CM, Bull JJ. (1999). Different trajectories of parallel evolution during viral adaptation. Science 285: 422-424
72. Wilke CO, Adami C. (2001). Interaction between directional epistasis and average mutational effects. Proc R Soc Lond B Biol Sci. 268: 1469-1474
73. Zwart MP, Darós JA, Elena SF. (2011). One is enough: in vivo effective population size is dose-dependent for a plant RNA virus. PLoS Pathog. 7: e1002122
74. Zwart MP, Darós JA, Elena SF. (2012). Effects of Potyvirus effective population size in inoculated leaves on viral accumulation and the onset of symptoms. J Virol. 86: 9737-9747
75. Zwart MP, Willemsen A, Darós JA, Elena SF. (2014). Experimental evolution of pseudogenization and gene loss in a plant RNA virus. Mol Biol Evol. 31: 121-134