Mutational robustness accelerates the origin of novel RNA phenotypes through phenotypic plasticity

Biophysical Journal

Volumn 106, Issue 4, 2014, Pages 955-965

  Wagner, Andreas ^a,b,c  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

^c SANTA FE INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RNA;

ARTICLE; BIOLOGICAL MODEL; CHEMISTRY; GENETICS; GENOTYPE; MOLECULAR EVOLUTION; MUTATION; PHENOTYPE;

EVOLUTION, MOLECULAR; GENOTYPE; MODELS, GENETIC; MUTATION; PHENOTYPE; RNA;

EID: 84894468153     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2014.01.003     Document Type: Article

References (64)

1. M.J. West-Eberhard Developmental Plasticity and Evolution 2003 Oxford University Press Oxford, UK
2. M. Mandal, and R.R. Breaker Gene regulation by riboswitches Nat. Rev. Mol. Cell Biol. 5 2004 451 463
3. A.G. Vitreschak, and D.A. Rodionov M.S. Gelfand Riboswitches: the oldest mechanism for the regulation of gene expression? Trends Genet. 20 2004 44 50
4. N. Tokuriki, and D.S. Tawfik Protein dynamism and evolvability Science 324 2009 203 207
5. B.K. Muralidhara, and L. Sun J.R. Halpert Thermodynamic fidelity of the mammalian cytochrome P450 2B4 active site in binding substrates and inhibitors J. Mol. Biol. 377 2008 232 245
6. P.J. O'Brien, and D. Herschlag Catalytic promiscuity and the evolution of new enzymatic activities Chem. Biol. 6 1999 R91 R105
7. S. Gould, and E. Vrba Exaptation - a missing term in the science of form Paleobiology 8 1982 4 15
8. H.A. McKenzie, and F.H. White Jr. Lysozyme and alpha-lactalbumin: structure, function, and interrelationships Adv. Protein Chem. 41 1991 173 315
9. J. Gerhart, and M. Kirschner Cells, Embryos, and Evolution 1998 Blackwell Boston
10. L.W. Ancel, and W. Fontana Plasticity, evolvability, and modularity in RNA J. Exper. Zoo./Molec. Dev. Evol. 288 2000 242 283
11. A. Wagner Robustness and evolvability: a paradox resolved Proc. Biol. Sci. 275 2008 91 100
12. J.D. Bloom, and P.A. Romero F.H. Arnold Neutral genetic drift can alter promiscuous protein functions, potentially aiding functional evolution Biol. Direct 2 2007 17
13. J.D. Bloom, L.I. Gong, and D. Baltimore Permissive secondary mutations enable the evolution of influenza oseltamivir resistance Science 328 2010 1272 1275
14. J.D. Bloom, and S.T. Labthavikul F.H. Arnold Protein stability promotes evolvability Proc. Natl. Acad. Sci. USA 103 2006 5869 5874
15. S. Bershtein, K. Goldin, and D.S. Tawfik Intense neutral drifts yield robust and evolvable consensus proteins J. Mol. Biol. 379 2008 1029 1044
16. E. Ferrada, and A. Wagner Protein robustness promotes evolutionary innovations on large evolutionary time-scales Proc. Biol. Sci. 275 2008 1595 1602
17. A. Wagner The molecular origins of evolutionary innovations Trends Genet. 27 2011 397 410
18. P. Schuster, and W. Fontana I.L. Hofacker From sequences to shapes and back: a case study in RNA secondary structures Proc. Biol. Sci. 255 1994 279 284
19. C. Reidys, P.F. Stadler, and P. Schuster Generic properties of combinatory maps: neutral networks of RNA secondary structures Bull. Math. Biol. 59 1997 339 397
20. A. Wagner The role of robustness in phenotypic adaptation and innovation Proc. Biol. Sci. 279 2012 1249 1258
21. C. Espinosa-Soto, O.C. Martin, and A. Wagner Phenotypic plasticity can facilitate adaptive evolution in gene regulatory circuits BMC Evol. Biol. 11 2011 5
22. C.P. Ponting, P.L. Oliver, and W. Reik Evolution and functions of long noncoding RNAs Cell 136 2009 629 641
23. G. Storz, S. Altuvia, and K.M. Wassarman An abundance of RNA regulators Annu. Rev. Biochem. 74 2005 199 217
24. L.S. Waters, and G. Storz Regulatory RNAs in bacteria Cell 136 2009 615 628
25. D.P. Bartel MicroRNAs: target recognition and regulatory functions Cell 136 2009 215 233
26. B. Alberts, and A. Johnson P. Walter Molecular Biology of the Cell 2008 Garland Science New York
27. E.T. Dayton, and D.A. Konings A.I. Dayton Extensive sequence-specific information throughout the CAR/RRE, the target sequence of the human immunodeficiency virus type 1 Rev protein J. Virol. 66 1992 1139 1151
28. F. Baudin, and R. Marquet C. Ehresmann Functional sites in the 5′ region of human immunodeficiency virus type 1 RNA form defined structural domains J. Mol. Biol. 229 1993 382 397
29. D.M. Powell, and M.J. Zhang A.I. Dayton Sequence specificity in the higher-order interaction of the Rev protein of HIV-1 with its target sequence, the RRE J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 10 1995 317 323
30. R.J. Jackson, and A. Kaminski Internal initiation of translation in eukaryotes: the picornavirus paradigm and beyond RNA 1 1995 985 1000
31. C.W. Mandl, and H. Holzmann F.X. Heinz Spontaneous and engineered deletions in the 3′ noncoding region of tick-borne encephalitis virus: construction of highly attenuated mutants of a flavivirus J. Virol. 72 1998 2132 2140
32. J.M. Manzella, and W. Rychlik P.J. Blackshear Insulin induction of ornithine decarboxylase. Importance of messenger RNA secondary structure and phosphorylation of eukaryotic initiation factor eIF-4B and factor eIF-4E J. Biol. Chem. 266 1991 2383 2389
33. M. Van de Guchte, and T. Van der Lende G. Venema A possible contribution of messenger-RNA secondary structure to translation initiation efficiency in Lactococcus lactis FEMS Microbiol. Lett. 81 1991 201 208
34. K. Okamura-Ikeda, K. Fujiwara, and Y. Motokawa Molecular cloning of a cDNA encoding chicken T-protein of the glycine cleavage system and expression of the functional protein in Escherichia coli. Effect of mRNA secondary structure in the translational initiation region on expression J. Biol. Chem. 267 1992 18284 18290
35. S. Pati, D. DiSilvestre, and W.S. Brusilow Regulation of the Escherichia coli uncH gene by mRNA secondary structure and translational coupling Mol. Microbiol. 6 1992 3559 3566
36. I.L. Hofacker, and W. Fontana P. Schuster Fast folding and comparison of RNA secondary structures Monatsh. Chem. 125 1994 167 188
37. S. Wuchty, and W. Fontana P. Schuster Complete suboptimal folding of RNA and the stability of secondary structures Biopolymers 49 1999 145 165
38. Reference deleted in proof.
39. O.C.M. Sumedha, O.C. Martin, and A. Wagner New structural variation in evolutionary searches of RNA neutral networks Biosystems 90 2007 475 485
40. J.S. McCaskill The equilibrium partition function and base pair binding probabilities for RNA secondary structure Biopolymers 29 1990 1105 1119
41. T. Kin, and K. Yamada K. Asai fRNAdb: a platform for mining/annotating functional RNA candidates from non-coding RNA sequences Nucleic Acids Res. 35 Database issue 2007 D145 D148
42. T. Jörg, O.C. Martin, and A. Wagner Neutral network sizes of biological RNA molecules can be computed and are not atypically small BMC Bioinformatics 9 2008 464
43. W. Gruner, and R. Giegerich P. Schuster Analysis of RNA sequence structure maps by exhaustive enumeration. I. Neutral networks Monatsh. Chem. 127 1996 355 374
44. S.M. Freier, and R. Kierzek D.H. Turner Improved free-energy parameters for predictions of RNA duplex stability Proc. Natl. Acad. Sci. USA 83 1986 9373 9377
45. S. Freeman, and J.C. Herron Evolution 4th ed. 2007 Pearson San Francisco, CA
46. M. Kimura The Neutral Theory of Molecular Evolution 1983 Cambridge University Press Cambridge, UK
47. M.A. Huynen, P.F. Stadler, and W. Fontana Smoothness within ruggedness: the role of neutrality in adaptation Proc. Natl. Acad. Sci. USA 93 1996 397 401
48. M.A. Huynen Exploring phenotype space through neutral evolution J. Mol. Evol. 43 1996 165 169
49. C. Espinosa-Soto, O.C. Martin, and A. Wagner Phenotypic robustness can increase phenotypic variability after nongenetic perturbations in gene regulatory circuits J. Evol. Biol. 24 2011 1284 1297
50. Khersonsky, O., and D. S. Tawfik. 2010.Enzyme promiscuity: A mechanistic and evolutionary perspective. In Annual Review of Biochemistry, Vol. 79. R. D. Kornberg, C. R. H. Raetz, J. E. Rothman, and J. W. Thorner, editors. 471-505.
51. T. Sikosek, H.-S. Chan, and E. Bornberg-Bauer Escape from Adaptive Conflict follows from weak functional trade-offs and mutational robustness Proc. Natl. Acad. Sci. USA 109 2012 14888 14893
52. G. Amitai, R. Gupta, and D. Tawfik Latent evolutionary potentials under the neutral mutational drift of an enzyme HFSP Journal 1 2007 67 78
53. A. Aharoni, and L. Gaidukov D.S. Tawfik The 'evolvability' of promiscuous protein functions Nat. Genet. 37 2005 73 76
54. A. Barve, and A. Wagner A latent capacity for evolutionary innovation through exaptation in metabolic systems Nature 500 2013 203 206
55. S. Schaper, I.G. Johnston, and A.A. Louis Epistasis can lead to fragmented neutral spaces and contingency in evolution Proc. Biol. Sci. 279 2012 1777 1783
56. J. Parsch, J.M. Braverman, and W. Stephan Comparative sequence analysis and patterns of covariation in RNA secondary structures Genetics 154 2000 909 921
57. A.S. Kondrashov, S. Sunyaev, and F.A. Kondrashov Dobzhansky-Muller incompatibilities in protein evolution Proc. Natl. Acad. Sci. USA 99 2002 14878 14883
58. A.D. Kern, and F.A. Kondrashov Mechanisms and convergence of compensatory evolution in mammalian mitochondrial tRNAs Nat. Genet. 36 2004 1207 1212
59. M.V. Meer, and A.S. Kondrashov F.A. Kondrashov Compensatory evolution in mitochondrial tRNAs navigates valleys of low fitness Nature 464 2010 279 282
60. M. Tacker, and P. Stadler P. Schuster Algorithm independent properties of RNA secondary structure predictions Eur. Biophys. J. 25 1996 115 130
61. Manrubia, S. C., and J. A. Cuesta. 2013. Evolution on genotype networks leads to phenotypic entrapment. (http://arxiv.org/abs/1307.0968) (submitted).
62. L.W. Ancel Undermining the Baldwin expediting effect: does phenotypic plasticity accelerate evolution? Theor. Popul. Biol. 58 2000 307 319
63. G.R. Riley, R.A. Corell, and K. Stuart Multiple guide RNAs for identical editing of Trypanosoma brucei apocytochrome b mRNA have an unusual minicircle location and are developmentally regulated J. Biol. Chem. 269 1994 6101 6108
64. D.A. Benson, and M. Cavanaugh E.W. Sayers GenBank Nucleic Acids Res. 41 Database issue 2013 D36 D42