Positive selection for elevated gene expression noise in yeast

Molecular Systems Biology

Volumn 5, Issue , 2009, Pages

  Zhang, Zhihua ^a   Qian, Wenfeng ^a   Zhang, Jianzhi ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Adaptive evolution; Expression noise; Plasma membrane transporters; Positive selection; Yeast

Indexed keywords

ARTICLE; CELL MEMBRANE; GENE EXPRESSION; GENE MUTATION; GENETIC VARIABILITY; MEMBRANE TRANSPORT; NATURAL SELECTION; NOISE; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; THEORETICAL MODEL; YEAST; BIOLOGICAL MODEL; COMPUTER SIMULATION; FUNGAL GENOME; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR EVOLUTION; MUTATION; NUCLEIC ACID HYBRIDIZATION; STATISTICAL MODEL;

FUNGAL PROTEIN;

CELL MEMBRANE; COMPUTER SIMULATION; EVOLUTION, MOLECULAR; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GENOME, FUNGAL; MODELS, BIOLOGICAL; MODELS, STATISTICAL; MODELS, THEORETICAL; MUTATION; NUCLEIC ACID HYBRIDIZATION; SACCHAROMYCES CEREVISIAE;

EID: 69249106061     PISSN: 17444292     EISSN: 17444292     Source Type: Journal    
DOI: 10.1038/msb.2009.58     Document Type: Article

References (56)

1. Acar M, Mettetal JT, van Oudenaarden A (2008) Stochastic switching as a survival strategy in fluctuating environments. Nat Genet 40: 471-475
2. Ansel J, Bottin H, Rodriguez-Beltran C, Damon C, Nagarajan M, Fehrmann S, Francois J, Yvert G (2008) Cell-to-cell stochastic variation in gene expression is a complex genetic trait. PLoS Genet 4: e1000049
3. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25: 25-29
4. Bahar R, Hartmann CH, Rodriguez KA, Denny AD, Busuttil RA, Dolle ME, Calder RB, Chisholm GB, Pollock BH, Klein CA, Vijg J (2006) Increased cell-to-cell variation in gene expression in ageing mouse heart. Nature 441: 1011-1014
5. Bar-Even A, Paulsson J, Maheshri N, Carmi M, O'Shea E, Pilpel Y, Barkai N (2006) Noise in protein expression scales with natural protein abundance. Nat Genet 38: 636-643
6. Basehoar AD, Zanton SJ, Pugh BF (2004) Identification and distinct regulation of yeast TATA box-containing genes. Cell 116: 699-709
7. Batada NN, Reguly T, Breitkreutz A, Boucher L, Breitkreutz BJ, Hurst LD, TyersM(2006) Stratus not altocumulus: a new viewof the yeast protein interaction network. PLoS Biol 4: e317
8. Batada NN, Hurst LD (2007) Evolution of chromosome organization driven by selection for reduced gene expression noise. Nat Genet 39: 945-949
9. Becskei A, Serrano L (2000) Engineering stability in gene networks by autoregulation. Nature 405: 590-593
10. Bedford T, Hartl DL (2009) Optimization of gene expression by natural selection. Proc Natl Acad Sci USA 106: 1133-1138
11. Blake WJ, Kaern M, Cantor CR, Collins JJ (2003) Noise in eukaryotic gene expression. Nature 422: 633-637
12. Blake WJ, Balazsi G, Kohanski MA, Isaacs FJ, Murphy KF, Kuang Y, Cantor CR,Walt DR, Collins JJ (2006) Phenotypic consequences of promoter-mediated transcriptional noise. Mol Cell 24: 853-865
13. Brem RB, Kruglyak L (2005) The landscape of genetic complexity across 5,700 gene expression traits in yeast. Proc Natl Acad Sci USA 102: 1572-1577
14. Colman-Lerner A, Gordon A, Serra E, Chin T, Resnekov O, Endy D, Pesce CG, Brent R (2005) Regulated cell-to-cell variation in a cellfate decision system. Nature 437: 699-706
15. Cook DL, Gerber AN, Tapscott SJ (1998) Modeling stochastic gene expression: implications for haploinsufficiency. Proc Natl Acad Sci USA 95: 15641-15646
16. Dekel E, Alon U (2005) Optimality and evolutionary tuning of the expression level of a protein. Nature 436: 588-592
17. Deutschbauer AM, Jaramillo DF, Proctor M, Kumm J, Hillenmeyer ME, Davis RW, Nislow C, Giaever G (2005) Mechanisms of haploinsufficiency revealed by genome-wide profiling in yeast. Genetics 169: 1915-1925
18. Elowitz MB, Levine AJ, Siggia ED, Swain PS (2002) Stochastic gene expression in a single cell. Science 297: 1183-1186
19. Fisher RA (1924) The distribution of the partial correlation coefficient. Metron 3: 329-332
20. Fraser HB, Hirsh AE, Giaever G, Kumm J, Eisen MB (2004) Noise minimization in eukaryotic gene expression. PLoS Biol 2: e137
21. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G et al. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80
22. Giaever G, Chu AM, Ni L, Connelly C, Riles L, Veronneau S, Dow S, Lucau-Danila A, Anderson K, Andre B, Arkin AP, Astromoff A, El-Bakkoury M, Bangham R, Benito R, Brachat S, Campanaro S, Curtiss M, Davis K, Deutschbauer A et al. (2002) Functionalprofiling of the Saccharomyces cerevisiae genome. Nature 418:87-391
23. Hartl DL, Dykhuizen DE, Dean AM (1985) Limits of adaptation: the evolution of selective neutrality. Genetics 111: 655-674
24. Kacser H, Burns JA (1981) The molecular basis of dominance. Genetics 97: 639-666
25. Kaern M, Elston TC, Blake WJ, Collins JJ (2005) Stochasticity in gene expression: from theories to phenotypes. Nat Rev Genet 6: 451-464
26. Kaneko K, Furusawa C (2008) Relevance of phenotypic noise to adaptation and evolution. IET Syst Biol 2: 234-246
27. Kemkemer R, Schrank S, Vogel W, Gruler H, Kaufmann D (2002) Increased noise as an effect of haploinsufficiency of the tumorsuppressor gene neurofibromatosis type 1 in vitro. Proc Natl Acad Sci USA 99: 13783-13788
28. Khaitovich P, Enard W, Lachmann M, Paabo S (2006) Evolution of primate gene expression. Nat Rev Genet 7: 693-702
29. Landry CR, Lemos B, Rifkin SA, Dickinson WJ, Hartl DL (2007) Genetic properties influencing the evolvability of gene expression. Science 317: 118-121
30. Lehner B (2008) Selection to minimise noise in living systems and its implications for the evolution of gene expression. Mol Syst Biol 4: 170
31. Lopez-Maury L, Marguerat S, Bahler J (2008) Tuning gene expression to changing environments: from rapid responses to evolutionary adaptation. Nat Rev Genet 9: 583-593
32. Losick R, Desplan C (2008) Stochasticity and cell fate. Science 320: 65-68
33. 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
34. Newman JR, Ghaemmaghami S, Ihmels J, Breslow DK, Noble M, DeRisi JL, Weissman JS (2006) Single-cell proteomic analysis of S. cerevisiae reveals the architecture of biological noise. Nature 441: 840-846
35. Orphanides G, Reinberg D (2002) A unified theory of gene expression. Cell 108: 439-451
36. 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
37. Pedraza JM, van Oudenaarden A (2005) Noise propagation in gene networks. Science 307: 1965-1969
38. Perez-Ortin JE, Alepuz PM, Moreno J (2007) Genomics and gene transcription kinetics in yeast. Trends Genet 23: 250-257
39. Raj A, van Oudenaarden A (2008) Nature, nurture, or chance: stochastic gene expression and its consequences. Cell 135: 216-226
40. Ramsey S, Ozinsky A, Clark A, Smith KD, de Atauri P, Thorsson V, Orrell D, Bolouri H (2006) Transcriptional noise and cellular heterogeneity in mammalian macrophages. Philos Trans R Soc Lond B Biol Sci 361: 495-506
41. Rao CV,Wolf DM, Arkin AP (2002) Control, exploitation and tolerance of intracellular noise. Nature 420: 231-237
42. Raser JM, O'Shea EK (2004) Control of stochasticity in eukaryotic gene expression. Science 304: 1811-1814
43. Raser JM, O'Shea EK (2005) Noise in gene expression: origins, consequences, and control. Science 309: 2010-2013
44. Rosenfeld N, Young JW, Alon U, Swain PS, Elowitz MB (2005) Gene regulation at the single-cell level. Science 307: 1962-1965
45. Schrodinger E (1944) What is Life? Cambridge, UK: Cambridge University Press
46. Sean D, Meltzer PS (2007) GEOquery: a bridge between the Gene Expression Omnibus (GEO) and BioConductor. Bioinformatics 23: 1846-1847
47. Sopko R, Huang D, Preston N, Chua G, Papp B, Kafadar K, Snyder M, Oliver SG, Cyert M, Hughes TR, Boone C, Andrews B (2006) Mapping pathways and phenotypes by systematic gene overexpression. Mol Cell 21: 319-330
48. Steinmetz LM, Scharfe C, Deutschbauer AM, Mokranjac D, Herman ZS, Jones T, Chu AM, Giaever G, Prokisch H, Oefner PJ, Davis RW (2002) Systematic screen for human disease genes in yeast. Nat Genet 31: 400-404
49. Stoebel DM, Dean AM, Dykhuizen DE (2008) The cost of expression of Escherichia coli lac operon proteins is in the process, not in the products. Genetics 178: 1653-1660
50. Storey JD, Tibshirani R (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci USA 100: 9440-9445
51. Thattai M, van Oudenaarden A (2004) Stochastic gene expression in fluctuating environments. Genetics 167: 523-530
52. Tirosh I, Weinberger A, Carmi M, Barkai N (2006) A genetic signature of interspecies variations in gene expression. Nat Genet 38: 830-834
53. Tirosh I, Barkai N (2008) Evolution of gene sequence and gene expression are not correlated in yeast. Trends Genet 24: 109-113
54. Volfson D, Marciniak J, Blake WJ, Ostroff N, Tsimring LS, Hasty J (2006) Origins of extrinsic variability in eukaryotic gene expression. Nature 439: 861-864
55. Wagner A (2005) Energy constraints on the evolution of gene expression. Mol Biol Evol 22: 1365-1374
56. Zeeberg BR, Feng W, Wang G, Wang MD, Fojo AT, Sunshine M, Narasimhan S, KaneDW, ReinholdWC, Lababidi S, Bussey KJ, Riss J, Barrett JC, Weinstein JN (2003) GoMiner: a resource for biological interpretation of genomic and proteomic data. Genome Biol 4: R28