Impact of gene expression noise on organismal fitness and the efficacy of natural selection

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 16, 2011, Pages

  Wang, Zhi ^a,b   Zhang, Jianzhi ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b SAGE BIONETWORKS   (United States)

Author keywords

Flux balance analysis; Metabolic network

Indexed keywords

ARTICLE; BIOMASS PRODUCTION; CONTROLLED STUDY; DIPLOIDY; ENERGY COST; GENE EXPRESSION NOISE; GENE EXPRESSION SYSTEM; GENE OVEREXPRESSION; HAPLOIDY; NATURAL SELECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; YEAST; YEAST CELL;

BIOMASS; GENE EXPRESSION REGULATION, FUNGAL; MODELS, BIOLOGICAL; SACCHAROMYCES CEREVISIAE; SELECTION, GENETIC;

EID: 79955613183     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1100059108     Document Type: Article

References (68)

1. Raj A, van Oudenaarden A (2008) Nature, nurture, or chance: Stochastic gene expression and its consequences. Cell 135:216-226.
2. Kaern M, Elston TC, Blake WJ, Collins JJ (2005) Stochasticity in gene expression: From theories to phenotypes. Nat Rev Genet 6:451-464. (Pubitemid 40733890)
3. Maheshri N, O'Shea EK (2007) Living with noisy genes: How cells function reliably with inherent variability in gene expression. Annu Rev Biophys Biomol Struct 36:413-434. (Pubitemid 46998126)
4. Ozbudak EM, Thattai M, Kurtser I, Grossman AD, van Oudenaarden A (2002) Regulation of noise in the expression of a single gene. Nat Genet 31:69-73.
5. Newman JR, et al. (2006) Single-cell proteomic analysis of S. cerevisiae reveals the architecture of biological noise. Nature 441:840-846.
6. Elowitz MB, Levine AJ, Siggia ED, Swain PS (2002) Stochastic gene expression in a single cell. Science 297:1183-1186. (Pubitemid 36193353)
7. Ramsey S, et al. (2006) Transcriptional noise and cellular heterogeneity in mammalian macrophages. Philos Trans R Soc Lond B Biol Sci 361:495-506. (Pubitemid 44870106)
8. Raser JM, O'Shea EK (2004) Control of stochasticity in eukaryotic gene expression. Science 304:1811-1814. (Pubitemid 38787899)
9. Taniguchi Y, et al. (2010) Quantifying E. coli proteome and transcriptome with single-molecule sensitivity in single cells. Science 329:533-538.
10. Raser JM, O'Shea EK (2005) Noise in gene expression: Origins, consequences, and control. Science 309:2010-2013. (Pubitemid 41362308)
11. Volfson D, et al. (2006) Origins of extrinsic variability in eukaryotic gene expression. Nature 439:861-864. (Pubitemid 43255705)
12. Acar M, Mettetal JT, van Oudenaarden A (2008) Stochastic switching as a survival strategy in fluctuating environments. Nat Genet 40:471-475. (Pubitemid 351450880)
13. Zhang Z, Qian W, Zhang J (2009) Positive selection for elevated gene expression noise in yeast. Mol Syst Biol 5:299.
14. Bahar R, et al. (2006) Increased cell-to-cell variation in gene expression in ageing mouse heart. Nature 441:1011-1014. (Pubitemid 43980358)
15. Kemkemer R, Schrank S, Vogel W, Gruler H, Kaufmann D (2002) Increased noise as an effect of haploinsufficiency of the tumor-suppressor gene neurofibromatosis type 1 in vitro. Proc Natl Acad Sci USA 99:13783-13788. (Pubitemid 35215458)
16. Fraser HB, Hirsh AE, Giaever G, Kumm J, Eisen MB (2004) Noise minimization in eukaryotic gene expression. PLoS Biol 2:e137.
17. Batada NN, Hurst LD (2007) Evolution of chromosome organization driven by selection for reduced gene expression noise. Nat Genet 39:945-949. (Pubitemid 47185175)
18. Lehner B (2008) Selection to minimise noise in living systems and its implications for the evolution of gene expression. Mol Syst Biol 4:170.
19. Becskei A, Serrano L (2000) Engineering stability in gene networks by autoregulation. Nature 405:590-593.
20. Pedraza JM, van Oudenaarden A (2005) Noise propagation in gene networks. Science 307:1965-1969.
21. Ramsey SA, et al. (2006) Dual feedback loops in the GAL regulon suppress cellular heterogeneity in yeast. Nat Genet 38:1082-1087. (Pubitemid 44325937)
22. Kovács K, Hurst LD, Papp B (2009) Stochasticity in protein levels drives colinearity of gene order in metabolic operons of Escherichia coli. PLoS Biol 7:e1000115.
23. Wagner A (2005) Energy constraints on the evolution of gene expression. Mol Biol Evol 22:1365-1374.
24. Rosenfeld N, Young JW, Alon U, Swain PS, Elowitz MB (2005) Gene regulation at the single-cell level. Science 307:1962-1965. (Pubitemid 40404705)
25. Kacser H, Burns JA (1981) The molecular basis of dominance. Genetics 97:639-666. (Pubitemid 12224399)
26. Kacser H, Burns JA (1973) The control of flux. Symp Soc Exp Biol 27:65-104.
27. Berg JM, Tymoczko JL, Stryer L (2002) Biochemistry (Freeman, New York), 5th Ed.
28. He X, Qian W, Wang Z, Li Y, Zhang J (2010) Prevalent positive epistasis in Escherichia coli and Saccharomyces cerevisiae metabolic networks. Nat Genet 42:272-276.
29. Duarte NC, Herrgård MJ, Palsson BO (2004) Reconstruction and validation of Saccharomyces cerevisiae iND750, a fully compartmentalized genome-scale metabolic model. Genome Res 14:1298-1309. (Pubitemid 39036129)
30. Price ND, Reed JL, Palsson BO (2004) Genome-scale models of microbial cells: Evaluating the consequences of constraints. Nat Rev Microbiol 2:886-897. (Pubitemid 39567269)
31. Orth JD, Thiele I, Palsson BO (2010) What is flux balance analysis? Nat Biotechnol 28:245-248.
32. Wang Z, Zhang J (2009) Why is the correlation between gene importance and gene evolutionary rate so weak? PLoS Genet 5:e1000329.
33. Papp B, Pál C, Hurst LD (2004) Metabolic network analysis of the causes and evolution of enzyme dispensability in yeast. Nature 429:661-664. (Pubitemid 38812317)
34. Pál C, Papp B, Lercher MJ (2005) Adaptive evolution of bacterial metabolic networks by horizontal gene transfer. Nat Genet 37:1372-1375. (Pubitemid 41722195)
35. Wagner A (2007) From bit to it: How a complex metabolic network transforms information into living matter. BMC Syst Biol 1:33.
36. Matias Rodrigues JF, Wagner A (2009) Evolutionary plasticity and innovations in complex metabolic reaction networks. PLoS Comput Biol 5:e1000613.
37. Pál C, et al. (2006) Chance and necessity in the evolution of minimal metabolic networks. Nature 440:667-670.
38. Wang Z, Zhang J (2009) Abundant indispensable redundancies in cellular metabolic networks. Genome Biol Evol 1:23-33.
39. Snitkin ES, et al. (2008) Model-driven analysis of experimentally determined growth phenotypes for 465 yeast gene deletion mutants under 16 different conditions. Genome Biol 9:R140.
40. Papp B, Pál C, Hurst LD (2003) Dosage sensitivity and the evolution of gene families in yeast. Nature 424:194-197. (Pubitemid 36858686)
41. Edwards JS, Ibarra RU, Palsson BO (2001) In silico predictions of Escherichia coli metabolic capabilities are consistent with experimental data. Nat Biotechnol 19:125-130.
42. Ibarra RU, Edwards JS, Palsson BO (2002) Escherichia coli K-12 undergoes adaptive evolution to achieve in silico predicted optimal growth. Nature 420:186-189. (Pubitemid 35340123)
43. Fong SS, Palsson BO (2004) Metabolic gene-deletion strains of Escherichia coli evolve to computationally predicted growth phenotypes. Nat Genet 36:1056-1058. (Pubitemid 41184464)
44. Famili I, Forster J, Nielsen J, Palsson BO (2003) Saccharomyces cerevisiae phenotypes can be predicted by using constraint-based analysis of a genome-scale reconstructed metabolic network. Proc Natl Acad Sci USA 100:13134-13139. (Pubitemid 37444707)
45. Harrison R, Papp B, Pál C, Oliver SG, Delneri D (2007) Plasticity of genetic interactions in metabolic networks of yeast. Proc Natl Acad Sci USA 104:2307-2312. (Pubitemid 46391393)
46. Di Talia S, Skotheim JM, Bean JM, Siggia ED, Cross FR (2007) The effects of molecular noise and size control on variability in the budding yeast cell cycle. Nature 448:947-951. (Pubitemid 47312778)
47. Wagner A (2007) Energy costs constrain the evolution of gene expression. J Exp Zoolog B Mol Dev Evol 308:322-324.
48. Blake WJ, et al. (2006) Phenotypic consequences of promoter-mediated transcriptional noise. Mol Cell 24:853-865. (Pubitemid 44960090)
49. Ansel J, et al. (2008) Cell-to-cell stochastic variation in gene expression is a complex genetic trait. PLoS Genet 4:e1000049.
50. Steinmetz LM, et al. (2002) Systematic screen for human disease genes in yeast. Nat Genet 31:400-404. (Pubitemid 35154450)
51. Hartl DL, Clark AG (1997) Principles of Population Genetics (Sinauer, Sunderland, MA), 3rd Ed.
52. Lestas I, Vinnicombe G, Paulsson J (2010) Fundamental limits on the suppression of molecular fluctuations. Nature 467:174-178.
53. Tsai IJ, Bensasson D, Burt A, Koufopanou V (2008) Population genomics of the wild yeast Saccharomyces paradoxus: Quantifying the life cycle. Proc Natl Acad Sci USA 105:4957-4962. (Pubitemid 351753853)
54. Dublanche Y, Michalodimitrakis K, Kümmerer N, Foglierini M, Serrano L (2006) Noise in transcription negative feedback loops: Simulation and experimental analysis. Mol Syst Biol 2:41.
55. Paulsson J (2004) Summing up the noise in gene networks. Nature 427:415-418.
56. Vavouri T, Semple JI, Garcia-Verdugo R, Lehner B (2009) Intrinsic protein disorder and interaction promiscuity are widely associated with dosage sensitivity. Cell 138:198-208.
57. Drummond DA, Wilke CO (2008) Mistranslation-induced protein misfolding as a dominant constraint on coding-sequence evolution. Cell 134:341-352. (Pubitemid 352010328)
58. Yang JR, Zhuang SM, Zhang J (2010) Impact of translational error-induced and errorfree misfolding on the rate of protein evolution. Mol Syst Biol 6:421.
59. Crow JF, Morton NE (1955) Measurement of gene frequency drift in small populations. Evolution 9:202-214.
60. Zhang J (2010) Evolutionary genetics: Progress and challenges. Evolution Since Darwin: The First 150 Years, eds Bell MA, Futuyma DJ, Eanes WF, Levinton JS (Sinauer, Sunderland, MA), pp 87-118.
61. Lynch M (2007) The Origins of Genome Architecture (Sinauer, Sunderland, MA).
62. Kimura M (1983) The Neutral Theory of Molecular Evolution (Cambridge University Press, Cambridge, UK).
63. Becker SA, et al. (2007) Quantitative prediction of cellular metabolism with constraint-based models: The COBRA toolbox. Nat Protoc 2:727-738. (Pubitemid 47040034)
64. Edwards JS, Covert M, Palsson BO (2002) Metabolic modelling of microbes: The flux-balance approach. Environ Microbiol 4:133-140. (Pubitemid 34544038)
65. Förster J, Famili I, Palsson BO, Nielsen J (2003) Large-scale evaluation of in silico gene deletions in Saccharomyces cerevisiae. OMICS 7:193-202. (Pubitemid 36896124)
66. Burgard AP, Nikolaev EV, Schilling CH, Maranas CD (2004) Flux coupling analysis of genome-scale metabolic network reconstructions. Genome Res 14:301-312. (Pubitemid 38219844)
67. Gillespie JH (1975) Natural selection for within-generation variance in offspring number II. Discrite haploid models. Genetics 81:403-413.
68. Hill WG, Zhang XS (2004) Effects on phenotypic variability of directional selection arising through genetic differences in residual variability. Genet Res 83:121-132. (Pubitemid 38779822)