Magnitude and sign epistasis among deleterious mutations in a positive-sense plant RNA virus

Heredity

Volumn 109, Issue 2, 2012, Pages 71-77

  Lali, J ^a   Elena, S F ^a,b  

^a Ciudad Politécnica de la Innovación   (Spain)

^b SANTA FE INSTITUTE   (United States)

Author keywords

Epistasis; fitness landscapes; genome architecture; virus evolution

Indexed keywords

EPISTASIS; EVOLUTIONARY BIOLOGY; FITNESS; GENOME; GENOMICS; GENOTYPE; HYPOTHESIS TESTING; MUTATION; PROTEIN; VIRUS;

ARTICLE; GENETIC EPISTASIS; GENETICS; MOLECULAR EVOLUTION; PLANT DISEASE; PLANT VIRUS; POINT MUTATION; POTYVIRUS; TOBACCO; VIROLOGY;

EPISTASIS, GENETIC; EVOLUTION, MOLECULAR; PLANT DISEASES; PLANT VIRUSES; POINT MUTATION; POTYVIRUS; TOBACCO;

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

EID: 84864290431     PISSN: 0018067X     EISSN: 13652540     Source Type: Journal    
DOI: 10.1038/hdy.2012.15     Document Type: Article

References (60)

1. Bagheri HC, Wagner GP (2004). Evolution of dominance in metabolic pathways. Genetics 168: 1716-1735.
2. Bedoya LC, Daròs JA (2010). Stability of Tobacco etch virus infectious clones in plasmid vectors. Virus Res 149: 234-240.
3. Bershtein S, Segal M, Bekerman R, Tokuriki N, Tawfik DS (2006). Robustness- epistasis link shapes the fitness landscape of a randomly drifting protein. Nature 444: 929-932. (Pubitemid 46025005)
4. Betancourt AJ (2010). Lack of evidence for sign epistasis between beneficial mutations in an RNA bacteriophage. J Mol Evol 71: 437-443.
5. Bonhoeffer S, Chappey C, Parkin NT, Whitcomb JM, Petropoulos CJ (2004). Evidence for positive epistasis in HIV-1. Science306: 1547-1550. (Pubitemid 39564948)
6. Burch CL, Chao L (2004). Epistasis and its relationship to canalization in the RNA virus φ6. Genetics 167: 559-567. (Pubitemid 38931847)
7. Carrasco P, Daròs JA, Agudelo-Romero P, Elena SF (2007a). A real-time RT-PCR assay for quantifying the fitness of Tobacco etch virus in competition experiments. J Virol Meth 139: 181-188. (Pubitemid 46074179)
8. Carrasco P, de la Iglesia F, Elena SF (2007b). Distribution of fitness and virulence effects caused by single-nucleotide substitutions in Tobacco etch virus. J Virol 81: 12979-12984. (Pubitemid 350156936)
9. Cong M, Heneine W, García-Lerma JG (2007). The fitness cost of mutations associated with Human immunodeficiency virustype 1 drug resistance is modulated by mutational interactions. J Virol81: 3037-3041. (Pubitemid 46447070)
10. Coyne JA(1992).Geneticsandspeciation. Nature355: 511-515.
11. Crow JF, Kimura M (1970). An Introduction to Population Genetics Theory. Harper and Row: New York.
12. Da Silva J, Coetzer M, Nedellec R, Pastore C, Mosier DE (2010). Fitness epistasis and constraints on adaptation in a Human immunodeficiency virus type 1 protein region. Genetics 185: 293-303.
13. Desai MM, Weissman D, Feldman MW (2007). Evolution can favor antagonistic epistasis. Genetics 177: 1001-1010. (Pubitemid 350005650)
14. De la Iglesia F, Elena SF (2007). Fitness declines in Tobacco etch virus upon serial bottlenecktransfers. J Virol81: 4941-4947. (Pubitemid 46744405)
15. De Visser JAGM, Elena SF (2007). The evolution of sex: empirical insights into the roles of epistasisand drift. Nat Rev Genet 8: 139-149. (Pubitemid 46122842)
16. De Visser JAGM, Hermisson J, Wagner GP, Ancel-Meyers L, Bagheri-Chaichian H, Blanchard JL etal. (2003). Perspective: Evolution and detection of genetic robustness. Evolution57: 1959-1972. (Pubitemid 37207656)
17. De Visser JAGM, Cooper TF, Elena SF (2011). The causes of epistasis. Proc R Soc B 10: 3617-3624.
18. Edlund JA, Adami C (2004). Evolution of robustness in digital organisms. Artif Life 10: 167-179.
19. Elena SF (1999). Little evidence for synergism among deleterious mutations in a nonsegmented RNA virus. JMol Evol49: 703-707. (Pubitemid 32268727)
20. Elena SF, Solé RV, Sardanyés J (2010). Simple genomes, complex interactions: epistasis in RNA virus. Chaos 20: 026106.
21. Franke J, Klözer A, de Visser JAGM, Krug J (2011). Evolutionary accessibility of mutational pathways. PLo S Comp Biol7: e1002134.
22. Killcoyne S, Carter GW, Smith J, Boyle J (2009). Cytoscape: a community-based framework for network modeling. Meth Mol Biol563: 219-239.
23. Kondrashov AS (1994). Muller's ratchet under epistatic selection. Genetics 136: 1469-1473. (Pubitemid 24097873)
24. Kondrashov AS, Crow JF (1991). Haploidy or diploidy: which is better. Nature 351: 314-315.
25. Kondrashov FA, Kondrashov AS (2001). Multidimensional epistasis and the disadvantage of sex. Proc Natl Acad Sci USA 98: 12089-12092. (Pubitemid 32959831)
26. Kouyos RD, Silander OK, Bonhoeffer S (2007). Epistasis between deleterious mutations and the evolution of recombination. Trends Ecol Evol6: 308-315. (Pubitemid 46734517)
27. Kvitek DJ, Sherlock G (2011). Reciprocal sign epistasis between frequently experimentally evolved adaptive mutations causes a rugged fitness landscape. PLo S Genet 7: e1002056.
28. Macía J, Solé RV, Elena SF (2012). The causes of epistasis in genetic networks. Evolution 66: 586-596.
29. Maisnier-Patin S, Berg OG, Lijas L, Andersson DI (2002). Compensatory adaptation to the deleterious effect of antibiotic resistance in Salmonella typhimurium. Mol Microbiol 46: 355-366. (Pubitemid 35340949)
30. Martínez JP, Bocharov G, Ignatovich A, Reiter J, Dittmar MT, Wain-Hobson S etal. (2011). Fitness ranking of individual mutants drives patterns of epistatic interactions in HIV-1. PLo S ONE 6: e18375.
31. Martínez-Picado J, Martínez MA (2009). HIV-1 reverse transcriptase inhibitor resistance mutations and fitness: a view from the clinic and ex vivo. Virus Res 134: 104-123.
32. Molla A, Korneyeve M, Gao Q, Vasavanonda S, Schipper PJ, Mo HM etal. (1996). Ordered accumulation of mutations in HIV protease confers resistance to ritonavir. Nat Med 2: 760-766. (Pubitemid 26225091)
33. Parera M, Pérez-Álvarez N, Clotet B, Martínez MA (2009). Epistasis among deleterious mutations in the HIV-1 protease. J Mol Biol392: 243-250.
34. Pepin KM, Wichman HA (2007). Variable epistatic effects between mutations at host recognition sites in φX174. Evolution67: 1710-1724. (Pubitemid 47013476)
35. Pfaffl MV (2004). Quantification strategies in real-time PCR. In Bustin SA (ed A-Z of Quantitative PCR, International University Line. La Jolla: USA, pp 87-112.
36. Phillips PC (2008). Epistasis- the essential role of gene interactions in the structure and evolution of genetic systems. Nat Rev Genet 9: 855-867.
37. Poelwijk FJ, Kiviet DJ, Weinreich DM, Tans SJ (2007). Empirical fitness landscapes reveal accessible evolutionary paths. Nature 445: 383-386. (Pubitemid 46160901)
38. Poelwijk FJ, Tanase-Nicola S, Kiviet DJ, Tans SJ (2011). Reciprocal sign epistasis is a necessary condition for multi-peaked fitness landscapes. J Theor Biol 272: 141-144.
39. Poon AFY, Chao L (2006). Functional origins of fitness effect-sizes of compensatory mutations in the DNA bacteriophage φX174. Evolution 60: 2032-2043. (Pubitemid 44808214)
40. Proulx SR, Phillips PC (2005). The opportunity for canalization and the evolution of genetic networks. Am Nat 165: 147-162. (Pubitemid 40263657)
41. Remold SK, Lenski RE (2004). Pervasive joint influence of epistasis and plasticity on mutational effects in Escherichia coli. Nat Genet36: 423 426. (Pubitemid 38437268)
42. Rice WR (1989). Analyzing tables of statistical tests. Evolution 43: 223-225.
43. Rodrigo G, Carrera J, Ruiz-Ferrer V, Del Toro FJ, Llave C, Voinnet O et al. (2011). Characterization of the Arabidopsis thaliana interactome targeted by viruses. Santa Fe Institute Working Paper 11-10-049.
44. Rokyta DR, Joyce P, Caudle B, Miller C, Beisel CJ, Wichman HA (2011). Epistasis between beneficial mutations and the phenotype-to-fitness map for a ss DNA virus. PLo S Genet 7: e1002075.
45. Salverda MLM, Dellus E, Gorter FA, Debets AJM, Van der Oost J, Hoekstra RF et al. (2011). Initial mutations direct alternative pathways of protein evolution. PLo S Genet 7: e1001321.
46. Sanjuán R (2006). Quantifying antagonistic epistasis in a multifunctional RNA secondary structure of the Rous sarcoma virus. J Gen Virol 87: 1595-1602. (Pubitemid 43827213)
47. Sanjuán R, Elena SF (2006). Epistasis correlates to genomic complexity. Proc Natl Acad Sci USA 103: 14402-14405. (Pubitemid 44484762)
48. Sanjuán R, Forment J, Elena SF (2006). In silico predicted robustness of viroids RNA secondary structure. II. Interaction between mutation pairs. Mol Biol Evol 23: 2123-2130. (Pubitemid 44536820)
49. Sanjuán R, Moya A, Elena SF (2004). The contribution of epistasis to the architecture of fitness in an RNA virus. Proc Natl Acad Sci USA 101: 15376-15379. (Pubitemid 39441549)
50. Sanjuán R, Nebot MR (2008). A network model for the correlation between epistasis and genomic complexity. PLo S ONE3: e2663.
51. Schrag SJ, Perrot V, Levin BR (1997). Adaptation to the fitness cost of antibiotic resistance in E. coli. Proc R Soc B 264: 1287-1291. (Pubitemid 27445226)
52. Van Opijnen T, Boerlijst MC, Berkhout B (2006). Effects of random mutations in the Human immunodeficiency virus type 1 transcriptional promoter on viral fitness in different host cell environments. J Virol80: 6678-6685. (Pubitemid 43927470)
53. Weinreich DM (2005). The rank ordering of genotypic fitness values predicts genetic constraints on natural selection on landscapes lacking sign epistasis. Genetics 171: 1397-1405. (Pubitemid 43234870)
54. Weinreich DM, Delaney NF, De Pristo MA, Hartl DL (2006). Darwinian evolution can follow onlyveryfew mutational pathstofitterproteins. Science312: 111-114.
55. Weinreich DM, Watson RA, Chao L (2005). Perspective: sign epistasis and genetic constraintonevolutionarytrajectories. Evolution59: 1165-1174. (Pubitemid 40870413)
56. Welch JJ, Waxman D (2005). The nk model and population genetics. J Theor Biol 234: 329-340. (Pubitemid 40387458)
57. Wilke CO, Adami C (2001). Interaction between directional epistasis and average mutational effects. Proc R Soc B 298: 1469-1474. (Pubitemid 32675433)
58. Wilke CO, Lenski RE, Adami C (2003). Compensatory mutations cause excess of antagonistic epistasis in RNA secondary structure folding. BMC Evol Biol 3: 1-14.
59. Withlock MC, Phillips PC, Moore FBG, Tonsor SJ (1995). Multiple fitness peaks and epistasis. Annu Rev Ecol Evol Syst 26: 601-629.
60. You L, Yin J (2002). Dependence of epistasis on environment and mutation severity as revealed by in silico mutagenesis of phage T7. Genetics 160: 1273-1281. (Pubitemid 34454354)