Robustness to noise in gene expression evolves despite epistatic constraints in a model of gene networks

Evolution

Volumn 69, Issue 9, 2015, Pages 2345-2358

  Draghi, Jeremy ^a   Whitlock, Michael ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Adaptation; Epistasis; Models simulations

Indexed keywords

EPISTASIS; FITNESS; GENE EXPRESSION; GRADUALISM; MUTATION; NOISE; NUMERICAL MODEL; PHENOTYPE;

ADAPTATION; BIOLOGICAL MODEL; EPISTASIS; EVOLUTION; GENE EXPRESSION; GENE REGULATORY NETWORK; GENETICS; MUTATION; REPRODUCTIVE FITNESS;

ADAPTATION, BIOLOGICAL; BIOLOGICAL EVOLUTION; EPISTASIS, GENETIC; GENE EXPRESSION; GENE REGULATORY NETWORKS; GENETIC FITNESS; MODELS, GENETIC; MUTATION;

EID: 84941599037     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/evo.12732     Document Type: Article

References (73)

1. Alon, U. 2006. An introduction to systems biology: design principles of biological circuits. CRC Press, Boca Raton, FL
2. Ancel, L. W., and W. Fontana. 2000. Plasticity, evolvability, and modularity in RNA. J. Exp. Zool. 288:242-283.
3. Azevedo, R. B., R. Lohaus, S. Srinivasan, K. K. Dang, and C. L. Burch. 2006. Sexual reproduction selects for robustness and negative epistasis in artificial gene networks. Nature 440:87-90.
4. Bar-Even, A., J. Paulsson, N. Maheshri, M. Carmi, E. O'Shea, Y. Pilpel, and N. Barkai. 2006. Noise in protein expression scales with natural protein abundance. Nat. Genet. 38:636-643.
5. Batada, N. N., and L. D. Hurst. 2007. Evolution of chromosome organization driven by selection for reduced gene expression noise. Nat. Genet. 39:945-949.
6. Bintu, L., N. E. Buchler, H. G. Garcia, U. Gerland, T. Hwa, J. Kondev, and R. Phillips. 2005. Transcriptional regulation by the numbers: models. Curr. Opin. Genet. Dev. 15 (April):116-124.
7. Bloom, J. D., S. T. Labthavikul, C. R. Otey, and F. H. Arnold. 2006. Protein stability promotes evolvability. Proc. Natl. Acad. Sci. U.S.A. 103:5869-5874.
8. Braunewell, S., and S. Bornholdt. 2008. Reliability of genetic networks is evolvable. Phys. Rev. E 77:060902.
9. Cai, L., N. Friedman, and X. S. Xie. 2006. Stochastic protein expression in individual cells at the single molecule level. Nature 440:358-362.
10. Chalancon, G., C. N. Ravarani, S. Balaji, A. Martinez-Arias, L. Aravind, R. Jothi, and M. M. Babu. 2012. Interplay between gene expression noise and regulatory network architecture. Trends Genet. 28:221-232.
11. Ciliberti, S., O. C. Martin, and A. Wagner. 2007. Robustness can evolve gradually in complex regulatory gene networks with varying topology. PLoS Comput Biol 3:e15.
12. Clarke, G. M., and J. A. McKenzie. 1987. Developmental stability of insecticide resistant phenotypes in blowfly; a result of canalizing natural selection. Nature 325:345-346.
13. Crombach, A., and P. Hogeweg. 2008. Evolution of evolvability in gene regulatory networks. PLoS Comput. Biol. 4:e1000112.
14. Cuevas, J. M., A. Moya, and R. Sanjuán. 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.
15. Dar, R. D., B. S. Razooky, A. Singh, T. V. Trimeloni, J. M. McCollum, C. D. Cox, and L. S. Weinberger. 2012. Transcriptional burst frequency and burst size are equally modulated across the human genome. Proc. Natl. Acad. Sci. 109:17454-17459.
16. de Visser, J. A. G. M., J. Hermisson, G. P. Wagner, L. A. Meyers, H. Bagheri-Chaichian, J. L. Blanchard, and M. C. Whitlock. 2003. Perspective: evolution and detection of genetic robustness. Evolution 57:1959-1972.
17. Draghi, J. A., and G. P. Wagner. 2009. The evolutionary dynamics of evolvability in a gene network model. J. Evol. Biol. 22: 599-611.
18. Draghi, J. A., and M. C. Whitlock. 2012. Phenotypic plasticity facilitates mutational variance, genetic variance, and evolvability along the major axis of environmental variation. Evolution 66:2891-2902.
19. Draghi, J. A., T. L. Parsons, G. P. Wagner, and J. B. Plotkin. 2010. Mutational robustness can facilitate adaptation. Nature 463(7279):353-355.
20. Elena, S. F., and R. Sanjuán. 2008. The effect of genetic robustness on evolvability in digital organisms. BMC Evol. Biol. 8:284. doi:10.1186/1471-2148-8-284.
21. Elowitz, M. B., A. J. Levine, E. D. Siggia, and P. S. Swain. 2002. Stochastic gene expression in a single cell. Science 297:1183-1186.
22. Espinosa-Soto, C., O. C. Martin, and A. Wagner. 2011. Phenotypic plasticity can facilitate adaptive evolution in gene regulatory circuits. BMC Evol. Biol. 11:5. doi:10.1186/1471-2148-11-5.
23. Fierst, J. L. 2011. A history of phenotypic plasticity accelerates adaptation to a new environment. J. Evol. Biol. 24:1992-2001.
24. Fraser, H. B., A. E. Hirsh, G. Giaever, J. Kumm, and M. B. Eisen. 2004. Noise minimization in eukaryotic gene expression. PLoS Biol. 2:e137.
25. Gavrilets, S., and A. Hastings. 1994. A quantitative-genetic model for selection on developmental noise. Evolution 48:1478-1486.
26. Gerland, U., J. D. Moroz, and T. Hwa. 2002. Physical constraints and functional characteristics of transcription factor-DNA interaction. Proc. Natl. Acad. Sci. U.S.A. 99 (September 17):12015-12020. doi:10.1073/pnas.192693599.
27. Gertz, J., E. D. Siggia, and B. A. Cohen. 2009. Analysis of combinatorial cis-regulation in synthetic and genomic promoters. Nature 457:215-218.
28. Gibson, G., and G. Wagner. 2000. Canalization in evolutionary genetics: a stabilizing theory? Bioessays 22:372-380.
29. Gillespie, D. T. 2007. Stochastic simulation of chemical kinetics. Annu. Rev. Phys. Chem. 58(January): 35-55.
30. Goldhill, D., A. Lee, E. S. Williams, and P. E. Turner. 2014. Evolvability and robustness in populations of RNA virus Φ6. Front. Microbiol. 5. doi:10.3389/fmicb.2014.00035
31. Jenkins, D. J., and D. J. Stekel. 2010. Stochasticity versus determinism: consequences for realistic gene regulatory network modelling and evolution. J. Mol. Evol. 70:215-231.
32. Kærn, M., T. C. Elston, W. J. Blake, and J. J. Collins. 2005. Stochasticity in gene expression: from theories to phenotypes. Nat. Rev. Genet. 6:451-464.
33. Kaneko, K. 2007. Evolution of robustness to noise and mutation in gene expression dynamics. PLoS One 2:e434.
34. Kratz, A., M. Tomita, and A. Krishnan. 2008. GeNESiS: gene network evolution simulation software. BMC Bioinform. 9:541.
35. Krishnan, A., A. Giuliani, M. Tomita. Evolution of gene regulatory networks: robustness as an emergent property of evolution. Phys. A 2008 387:2170-2186.
36. Kussell, E., and S. Leibler. 2005. Phenotypic diversity, population growth, and information in fluctuating environments. Science 309:2075-2078.
37. Lauring, A. S., A. Acevedo, S. B. Cooper, and R. Andino. 2012. Codon usage determines the mutational robustness, evolutionary capacity, and virulence of an RNA virus. Cell Host Microbe 12:623-632.
38. Latchman, D. S. 2010 Gene control. Garland Science, Taylor & Francis Group, New York, NY.
39. Leclerc, R. D. 2008. Survival of the sparsest: robust gene networks are parsimonious. Mol. Syst. Biol. 4. doi:10.1038/msb.2008.52
40. Lehner, B. 2008. Selection to minimise noise in living systems and its implications for the evolution of gene expression. Mol. Syst. Biol. 4. doi:10.1038/msb.2008.11
41. Lestas, I., G. Vinnicombe, and J. Paulsson. 2010. Fundamental limits on the suppression of molecular fluctuations. Nature 467:174-178.
42. Macía, J., R. V. Solé, and S. F. Elena. 2012. The causes of epistasis in genetic networks. Evolution 66:586-596.
43. Marquez-Lago, T. T., and J. Stelling. 2010. Counter-intuitive stochastic behavior of simple gene circuits with negative feedback. Biophys. J. 98:1742-1750.
44. Masel, J., and M. V. Trotter. 2010. Robustness and evolvability. Trends Genet. 26:406-414.
45. McBride, R. C., C. B. Ogbunugafor, and P. E. Turner. 2008. Robustness promotes evolvability of thermotolerance in an RNA virus. BMC Evol. Biol. 8:231.
46. Newman, J. R. S., S. Ghaemmaghami, J. Ihmels, D. K. Breslow, M. Noble, J. L. DeRisi, and J. S. Weissman. 2006. "Single-cell proteomic analysis of S. Cerevisiae reveals the architecture of biological noise. Nature 441 (June 15):840-846.
47. Ozbudak, E. M., M. Thattai, I. Kurtser, A. D. Grossman, and A. vanOudenaarden. 2002. Regulation of noise in the expression of a single gene. Nat. Genet. 31:69-73.
48. Pedraza, J. M., and J. Paulsson. 2008. Effects of molecular memory and bursting on fluctuations in gene expression. Science 319:339-343.
49. Pujato, M., T. MacCarthy, A. Fiser, and A. Bergman. 2013. The underlying molecular and network level mechanisms in the evolution of robustness in gene regulatory networks. PLoS Comput Biol. 9:e1002865.
50. Raj, A., and A. vanOudenaarden. 2008. Nature, nurture, or chance: stochastic gene expression and its consequences. Cell 135:216-226.
51. Raser, J. M., and E. K. O'Shea. 2005. Noise in gene expression: origins, consequences, and control. Science 309:2010-2013.
52. Rohlf, T., and C. R. Winkler. 2009. Emergent network structure, evolvable robustness, and nonlinear effects of point mutations in an artificial genome model. Adv. Complex Syst. 12:293-310.
53. Sevim, V., and P. A. Rikvold. 2008. Chaotic gene regulatory networks can be robust against mutations and noise. J. Theor. Biol. 253:323-332.
54. Sherman, M. S., and B. A. Cohen. 2012. Thermodynamic state ensemble models of cis-regulation. PLoS Comput. Biol. 8 (January):e1002407. doi:10.1371/journal.pcbi.1002407.
55. Siegal, M. L., and A. Bergman. 2002. Waddington's canalization revisited: developmental stability and evolution. Proc. Natl. Acad. Sci. 99:10528-10532.
56. Silva-Rocha, R., and V. deLorenzo. 2010. Noise and robustness in prokaryotic regulatory networks. Annu. Rev. Microbiol. 64:257-275.
57. Stekel, D. J., and D. J. Jenkins. 2008. Strong negative self-regulation of prokaryotic transcription factors increases the intrinsic noise of protein expression. BMC Syst. Biol. 2:6.
58. Stewart, A. J., T. L. Parsons, and J. B. Plotkin. 2012. Environmental robustness and the adaptability of populations. Evolution 66:1598-1612.
59. Stewart, A. J., R. M. Seymour, A. Pomiankowski, and M. Reuter. 2013. Under-dominance constrains the evolution of negative autoregulation in diploids. PLoS Comput. Biol. 9:e1002992.
60. Swain, P. S., M. B. Elowitz, and E. D. Siggia. 2002. Intrinsic and extrinsic contributions to stochasticity in gene expression. Proc. Natl. Acad. Sci. U.S.A. 99:12795-12800.
61. Tănase-Nicola, S., and P. R. ten Wolde. 2008. Regulatory control and the costs and benefits of biochemical noise. PLoS Comput. Biol. 4:e1000125. doi:10.1371/journal.pcbi.1000125
62. Thattai, M., and A. Van Oudenaarden. 2001. Intrinsic noise in gene regulatory networks. Proc. Natl. Acad. Sci. U.S.A. 98:8614-8619.
63. Van Dijk, A. D., S. vanMourik, and R. C. van Ham. 2012. Mutational robustness of gene regulatory networks. PloS One 7:e30591.
64. Veening, J. W., W. K. Smits, and O. P. Kuipers. 2008. Bistability, epigenetics, and bet-hedging in bacteria. Annu. Rev. Microbiol. 62:193-210.
65. Waddington, C. H. 1942. Canalization of development and the inheritance of acquired characters. Nature 150:563-565.
66. Wagner, A. 1996. Does evolutionary plasticity evolve? Evolution 50:1008-1023.
67. Wagner, A. 2005. Robustness and evolvability in living systems. Princeton Univ. Press, Princeton, NJ.
68. Wagner, A. 2011. The origins of evolutionary innovations: a theory of transformative change in living systems. Oxford Univ. Press, Oxford, UK.
69. Wagner, G. P., and L. Altenberg. 1996. Perspective: complex adaptations and the evolution of evolvability. Evolution 50:967-976.
70. Wagner, G. P., G. Booth, and H. Bagheri-Chaichian. 1997. A population genetic theory of canalization. Evolution 51:329-347.
71. Wang, Z., and J. Zhang. 2011. Impact of gene expression noise on organismal fitness and the efficacy of natural selection. Proc. Natl. Acad. Sci. U.S.A 108:E67-E76.
72. Yu, J., J. Xiao, X. Ren, K. Lao, and X. S. Xie. 2006. Probing gene expression in live cells, one protein molecule at a time. Science 311:1600-1603.
73. Zenklusen, D., D. R. Larson, and R. H. Singer. 2008. Single-RNA counting reveals alternative modes of gene expression in yeast. Nat. Struct. Mol. Biol. 15:1263-1271.