The fitness effects of random mutations in single-stranded DNA and RNA bacteriophages

PLoS Genetics

Volumn 5, Issue 11, 2009, Pages

  Domingo Calap, Pilar ^a   Cuevas, José M ^a   Sanjuán, Rafael ^a,b  

^a UNIVERSITY OF VALENCIA   (Spain)

^b UNIVERSITY OF VALENCIA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

SINGLE STRANDED DNA; SINGLE STRANDED RNA; VIRUS DNA; VIRUS RNA;

ARTICLE; BACTERIOPHAGE; GENE MUTATION; NONHUMAN; VIRUS GENOME; BIOLOGICAL MODEL; GENETIC SELECTION; GENETICS; MUTAGENESIS; MUTATION; POINT MUTATION; RNA PHAGE; SITE DIRECTED MUTAGENESIS;

ANIMALIA; BACTERIA (MICROORGANISMS); RNA VIRUSES;

DNA, SINGLE-STRANDED; MODELS, GENETIC; MUTAGENESIS; MUTAGENESIS, SITE-DIRECTED; MUTATION; POINT MUTATION; RNA PHAGES; SELECTION, GENETIC;

EID: 73649127602     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1000742     Document Type: Article

References (53)

1. de Visser JA, Hermisson J, Wagner GP, Ancel ML, Bagheri-Chaichian H, et al. (2003) Perspective: Evolution and detection of genetic robustness. Evolution 57: 1959-1972.
2. Ohta T (1992) The nearly neutral theory of molecular evolution. Annu Rev Ecol Syst 23: 263-286.
3. Peck JR, Barreau G, Heath SC (1997) Imperfect genes, Fisherian mutation and the evolution of sex. Genetics 145: 1171-1199.
4. Wagner A (2005) Robustness and evolvability in living systems. New Jersey: Princeton University Press.
5. Eyre-Walker A, Woolfit M, Phelps T (2006) The distribution of fitness effects of new deleterious amino acid mutations in humans. Genetics 173: 891-900.
6. Schultz ST, Lynch M (1997) Mutation and extinction: the role of variable mutational effects, synergistic epistasis, beneficial mutations, and degree of outcrossing. Evolution 51: 1363-1371.
7. Keightley PD (2004) Comparing analysis methods for mutation-accumulation data. Genetics 167: 551-553.
8. Mukai T (1964) The genetic structure of natural populations of Drosophila melanogaster. I. spontaneous mutation rate of polygenes controlling viability. Genetics 50: 1-19.
9. Eyre-Walker A, Keightley PD (2007) The distribution of fitness effects of new mutations. Nat Rev Genet 8: 610-618.
10. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, et al. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2: 2006.
11. Elena SF, Ekunwe L, Hajela N, Oden SA, Lenski RE (1998) Distribution of fitness effects caused by random insertion mutations in Escherichia coli. Genetica 102/103: 349-358.
12. Davies EK, Peters AD, Keightley PD (1999) High frequency of cryptic deleterious mutations in Caenorhabditis elegans. Science 285: 1748-1751.
13. Carrasco P, de la Iglesia F, Elena SF (2007) Distribution of fitness and virulence effects caused by single-nucleotide substitutions in Tobacco ech virus. J Virol 81: 12979-12984.
14. Sanjuán R, Moya A, Elena SF (2004) The distribution of fitness effects caused by single-nucleotide substitutions in an RNA virus. Proc Natl Acad Sci USA 101: 8396-8401.
15. Elena SF, Carrasco P, Daròs JA, Sanjuán R (2006) Mechanisms of genetic robustness in RNA viruses. EMBO Rep 7: 168-173.
16. Holmes EC (2008) Evolutionary history and phylogeography of human viruses. Annu Rev Microbiol 62: 307-328.
17. Duffy S, Shackelton LA, Holmes EC (2008) Rates of evolutionary change in viruses: patterns and determinants. Nat Rev Genet 9: 267-276.
18. Ahlquist P (2006) Parallels among positive-strand RNA viruses, reverse-transcribing viruses and double-stranded RNA viruses. Nat Rev Microbiol 4: 371-382.
19. Cuevas JM, Duffy S, Sanjuán R (2009) Point mutation rate of bacteriophage ΦX174. Genetics, in press.
20. Drake JW, Charlesworth B, Charlesworth D, Crow JF (1998) Rates of spontaneous mutation. Genetics 148: 1667-1686.
21. Sniegowski PD, Gerrish PJ, Johnson T, Shaver A (2000) The evolution of mutation rates: separating causes from consequences. BioEssays 22: 1057-1066.
22. Sanjuán R, Cuevas JM, Furió V, Holmes EC, Moya A (2007) Selection for robustness in mutagenized RNA viruses. PLoS Genet 3: e93. doi:10.1371/journal.pgen.0030093.
23. Schuster P, Swetina J (1988) Stationary mutant distributions and evolutionary optimization. Bull Math Biol 50: 635-660.
24. Wilke CO, Wang JL, Ofria C, Lenski RE, Adami C (2001) Evolution of digital organisms at high mutation rates leads to survival of the flattest. Nature 412: 331-333.
25. Belshaw R, Pybus OG, Rambaut A (2007) The evolution of genome compression and genomic novelty in RNA viruses. Genome Res 17: 1496-1504.
26. Eigen M, McCaskill J, Schuster P (1988) Molecular quasi-species. J Phys Chem 92: 6881-6891.
27. Holmes EC (2003) Error thresholds and the constraints to RNA virus evolution. Trends Microbiol 11: 543-546.
28. Chen M, Uchiyama A, Fane BA (2007) Eliminating the requirement of an essential gene product in an already very small virus: scaffolding protein B-free ΦX174, B-free. J Mol Biol 373: 308-314.
29. Bull JJ, Badgett MR, Springman R, Molineux IJ (2004) Genome properties and the limits of adaptation in bacteriophages. Evolution 58: 692-701.
30. Belshaw R, Gardner A, Rambaut A, Pybus OG (2008) Pacing a small cage: mutation and RNA viruses. Trends Ecol Evol 23: 188-193.
31. Calendar R (2006) The bacteriophages. Oxford University Press.
32. van der Ende A, Teertstra R, Weisbeek PJ (1982) Initiation and termination of the bacteriophage ΦX174 rolling circle DNA replication in vivo: packaging of plasmid single-stranded DNA into bacteriophage WX174 coats. Nucl Acids Res 10: 6849-6863.
33. Sanjuán R, Elena SF (2006) Epistasis correlates to genomic complexity. Proc Natl Acad Sci USA 103: 14402-14405.
34. Frank SA (2007) Maladaptation and the paradox of robustness in evolution. PLoS ONE 2: e1021. doi:10.1371/journal.pone.0001021.
35. Lenski RE, Barrick JE, Ofria C (2006) Balancing robustness and evolvability. PLoS Biol 4: e428. doi:10.1371/journal.pbio.0040428.
36. Wagner A (2008) Robustness and evolvability: a paradox resolved. Proc Biol Sci 275: 91-100.
37. Bull JJ, Badgett MR, Wichman HA (2000) Big-benefit mutations in a bacteriophage inhibited with heat. Mol Biol Evol 17: 942-950.
38. Rokyta DR, Joyce P, Caudle SB, Wichman HA (2005) An empirical test of the mutational landscape model of adaptation using a single-stranded DNA virus. Nat Genet 37: 441-444.
39. Rokyta DR, Beisel CJ, Joyce P, Ferris MT, Burch CL, Wichman HA (2008) Beneficial fitness effects are not exponential for two viruses. J Mol Evol 67: 368-376.
40. Cuevas JM, Moya A, Sanjuán R (2009) A genetic background with low mutational robustness is associated with increased adaptability to a novel host in an RNA virus. J Evol Biol 22: 2041-2048.
41. Orr HA (2000) The rate of adaptation in asexuals. Genetics 155: 961-968.
42. Bloom JD, Labthavikul ST, Otey CR, Arnold FH (2006) Protein stability promotes evolvability. Proc Natl Acad Sci USA 103: 5869-5874.
43. Ciliberti S, Martin OC, Wagner A (2007) Innovation and robustness in complex regulatory gene networks. Proc Natl Acad Sci USA 104: 13591-13596.
44. Kim Y (2007) Rate of adaptive peak shifts with partial genetic robustness. Evolution. 1847-1856.
45. McBride RC, Ogbunugafor CB, Turner PE (2008) Robustness promotes evolvability of thermotolerance in an RNA virus. BMC Evol Biol 8: 231.
46. Butcher D (1995) Muller's ratchet, epistasis and mutation effects. Genetics 141: 431-437.
47. Bull JJ, Sanjuán R, Wilke CO (2007) Theory of lethal mutagenesis for viruses. J Virol 81: 2930-2939.
48. Pybus OG, Rambaut A, Belshaw R, Freckleton RP, Drummond AJ, et al. (2007) Phylogenetic evidence for deleterious mutation load in RNA viruses and its contribution to viral evolution. Mol Biol Evol 24: 845-852.
49. Holland JJ, Spindler K, Horodyski F, Grabau E, Nichol S, et al. (1982) Rapid evolution of RNA genomes. Science 215: 1577-1585.
50. Shackelton LA, Parrish CR, Truyen U, Holmes EC (2005) High rate of viral evolution associated with the emergence of carnivore parvovirus. Proc Natl Acad Sci USA 102: 379-384.
51. Umemura T, Tanaka Y, Kiyosawa K, Alter HJ, Shih JW (2002) Observation of positive selection within hypervariable regions of a newly identified DNA virus (SEN virus - 1). FEBS Lett 510: 171-174.
52. Duffy S, Holmes EC (2008) Phylogenetic evidence for rapid rates of molecular evolution in the single-stranded DNA begomovirus Tomato yellow leaf curl virus. J Virol 82: 957-965.
53. Chao L (1990) Fitness of RNA virus decreased by Muller's ratchet. Nature 348: 454-455.