Network hubs buffer environmental variation in Saccharomyces cerevisiae

PLoS Biology

Volumn 6, Issue 11, 2008, Pages 2588-2604

  Levy, Sasha F ^a   Siegal, Mark L ^a  

^a NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; DNA; GENE PRODUCT; PHENOTYPIC CAPACITOR; RNA; UNCLASSIFIED DRUG; SACCHAROMYCES CEREVISIAE PROTEIN;

ARABIDOPSIS; ARTICLE; CELL CYCLE; CHROMOSOME STRUCTURE; DNA POLYMORPHISM; DROSOPHILA; GENE DELETION; GENE MUTATION; GENETIC VARIABILITY; NONHUMAN; PARALOGY; PHENOTYPIC VARIATION; PLEIOTROPY; PROTEIN INTERACTION; PROTEIN MODIFICATION; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; STRESS; YEAST CELL; CHROMOSOMAL INSTABILITY; DUPLICATE GENE; EVOLUTION; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; GENOTYPE; PHENOTYPE;

ARABIDOPSIS; SACCHAROMYCES CEREVISIAE;

BIOLOGICAL EVOLUTION; CHROMOSOMAL INSTABILITY; GENE EXPRESSION REGULATION, FUNGAL; GENE REGULATORY NETWORKS; GENES, DUPLICATE; GENOTYPE; PHENOTYPE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 56849091295     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.0060264     Document Type: Article

References (88)

1. Wagner A (2005) Robustness and evolvability in living systems. Princeton (New Jersey): Princeton University Press.
2. Waddington CH (1942) Canalization of development and the inheritance of acquired characteristics. Nature 150: 563-565.
3. Siegal ML, Bergman A (2006) Canalization. Fox CW, Wolf JB, editors. Evolutionary genetics: concepts and case studies. New York: Oxford University Press. pp. 235-251.
4. Hansen TF (2006) The evolution of genetic architecture. Annu Rev Ecol Evol Syst 37: 123-157.
5. Wagner A (2005) Robustness, evolvability, and neutrality. FEBS Lett 579: 1772-1778.
6. Queitsch C, Sangster TA, Lindquist S (2002) Hsp90 as a capacitor of phenotypic variation. Nature 417: 618-624.
7. Rutherford SL, Lindquist S (1998) Hsp90 as a capacitor for morphological evolution. Nature 396: 336-342.
8. Milton CC, Ulane CM, Rutherford S (2006) Control of canalization and evolvability by Hsp90. PLoS ONE 1: e75. doi:10.1371/journal.pone.0000075
9. Wagner GP, Chiu CH, Hansen TF (1999) Is Hsp90 a regulator of evolvability? J Exp Zool 285: 116-118.
10. Carey CC, Gorman KF, Rutherford S (2006) Modularity and intrinsic evolvability of Hsp90-buffered change. PLoS ONE 1: e76. doi:10.1371/journal. pone.0000076
11. Earl DJ, Deem MW (2004) Evolvability is a selectable trait. Proc Natl Acad Sci U S A 101: 11531-11536.
12. Masel J (2005) Evolutionary capacitance may be favored by natural selection. Genetics 170: 1359-1371.
13. King OD, Masel J (2007) The evolution of bet-hedging adaptations to rare scenarios. Theor Popul Biol 72: 560-575.
14. Meiklejohn CD, Hartl DL (2002) A single mode of canalization. Trends Ecol Evol 17: 468.
15. Siegal ML, Bergman A (2002) Waddington's canalization revisited: developmental stability and evolution. Proc Natl Acad Sci U S A 99: 10528-10532.
16. Bergman A, Siegal ML (2003) Evolutionary capacitance as a general feature of complex gene networks. Nature 424: 549-552.
17. Ohya Y, Sese J, Yukawa M, Sano F, Nakatani Y, et al. (2005) High-dimensional and large-scale phenotyping of yeast mutants. Proc Natl Acad Sci U S A 102: 19015-19020.
18. Dworkin I (2005) Canalization, cryptic variation, and developmental buffering: a critical examination and analytical perspective. Hallgrimssonm B, Hall BK, editors. Variation. San Diego: Elsevier Academic Press. pp. 132-144.
19. Pan X, Yuan DS, Xiang D, Wang X, Sookhai-Mahadeo S, et al. (2004) A robust toolkit for functional profiling of the yeast genome. Mol Cell 16: 487-496.
20. Kolodner RD, Marsischky GT (1999) Eukaryotic DNA mismatch repair. Curr Opin Genet Dev 9: 89-96.
21. Manukyan A, Zhang J, Thippeswamy U, Yang J, Zavala N, et al. (2008) Ccr4 Alters Cell Size in Yeast by Modulating the Timing of CLN1 and CLN2 Expression. Genetics 179: 345-357.
22. Minarikova L, Kuthan M, Ricicova M, Forstova J, Palkova Z (2001) Differentiated gene expression in cells within yeast colonies. Exp Cell Res 271: 296-304.
23. Raser JM, O'Shea EK (2004) Control of stochasticity in eukaryotic gene expression. Science 304: 1811-1814.
24. Colman-Lerner A, Gordon A, Serra E, Chin T, Resnekov O, et al. (2005) Regulated cell-to-cell variation in a cell-fate decision system. Nature 437: 699-706.
25. Pan X, Ye P, Yuan DS, Wang X, Bader JS, et al. (2006) A DNA integrity network in the yeast Saccharomyces cerevisiae. Cell 124: 1069-1081.
26. Jeong H, Mason SP, Barabasi AL, Oltvai ZN (2001) Lethality and centrality in protein networks. Nature 411: 41-42.
27. Tong AH, Evangelista M, Parsons AB, Xu H, Bader GD, et al. (2001) Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294: 2364-2368.
28. Siegal ML, Promislow DE, Bergman A (2007) Functional and evolutionary inference in gene networks: does topology matter? Genetica 129: 83-103.
29. Hartman JL 4th, Garvik B, Hartwell L (2001) Principles for the buffering of genetic variation. Science 291: 1001-1004.
30. Lehner B, Crombie C, Tischler J, Fortunato A, Fraser AG (2006) Systematic mapping of genetic interactions in Caenorhabditis elegans identifies common modifiers of diverse signaling pathways. Nat Genet 38: 896-903.
31. Sangster TA, Lindquist S, Queitsch C (2004) Under cover: causes, effects and implications of Hsp90-mediated genetic capacitance. Bioessays 26: 348-362.
32. Stark C, Breitkreutz BJ, Reguly T, Boucher L, Breitkreutz A, et al. (2006) BioGRID: a general repository for interaction datasets. Nucleic Acids Res 34: D535-D539.
33. Gavin AC, Aloy P, Grandi P, Krause R, Boesche M, et al. (2006) Proteome survey reveals modularity of the yeast cell machinery. Nature 440: 631-636.
34. Krogan NJ, Cagney G, Yu H, Zhong G, Guo X, et al. (2006) Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 440: 637-643.
35. Cowen LE, Lindquist S (2005) Hsp90 potentiates the rapid evolution of new traits: drug resistance in diverse fungi. Science 309: 2185-2189.
36. Bobula J, Tomala K, Jez E, Wloch DM, Borts RH, et al. (2006) Why molecular chaperones buffer mutational damage: a case study with a yeast Hsp40/70 system. Genetics 174: 937-944.
37. Warringer J, Ericson E, Fernandez L, Nerman O, Blomberg A (2003) High-resolution yeast phenomics resolves different physiological features in the saline response. Proc Natl Acad Sci U S A 100: 15724-15729.
38. Deutschbauer AM, Jaramillo DF, Proctor M, Kumm J, Hillenmeyer ME, et al. (2005) Mechanisms of haploinsufficiency revealed by genome-wide profiling in yeast. Genetics 169: 1915-1925.
39. Kafri R, Dahan O, Levy J, Pilpel Y (2008) Preferential protection of protein interaction network hubs in yeast: evolved functionality of genetic redundancy. Proc Natl Acad Sci U S A 105: 1243-1248.
40. Gu Z, Cavalcanti A, Chen FC, Bouman P, Li WH (2002) Extent of gene duplication in the genomes of Drosophila, nematode, and yeast. Mol Biol Evol 19: 256-262.
41. Gu Z, Steinmetz LM, Gu X, Scharfe C, Davis RW, et al. (2003) Role of duplicate genes in genetic robustness against null mutations. Nature 421: 63-66.
42. Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290: 1151-1155.
43. Drummond DA, Raval A, Wilke CO (2006) A single determinant dominates the rate of yeast protein evolution. Mol Biol Evol 23: 327-337.
44. Pal C, Papp B, Hurst LD (2001) Highly expressed genes in yeast evolve slowly. Genetics 158: 927-931.
45. Byrne KP, Wolfe KH (2005) The Yeast Gene Order Browser: combining curated homology and syntenic context reveals gene fate in polyploid species. Genome Res 15: 1456-1461.
46. Newman JR, Ghaemmaghami S, Ihmels J, Breslow DK, Noble M, et al. (2006) Single-cell proteomic analysis of S. cerevisiae reveals the architecture of biological noise. Nature 441: 840-846.
47. McGary KL, Lee I, Marcotte EM (2007) Broad network-based predictability of Saccharomyces cerevisiae gene loss-of-function phenotypes. Genome Biol 8: R258.
48. Myung K, Chen C, Kolodner RD (2001) Multiple pathways cooperate in the suppression of genome instability in Saccharomyces cerevisiae. Nature 411: 1073-1076.
49. Scholes DT, Banerjee M, Bowen B, Curcio MJ (2001) Multiple regulators of Ty1 transposition in Saccharomyces cerevisiae have conserved roles in genome maintenance. Genetics 159: 1449-1465.
50. Nyswaner KM, Checkley MA, Yi M, Stephens RM, Garfinkel DJ (2008) Chromatin-associated genes protect the yeast genome from Ty1 insertional mutagenesis. Genetics 178: 197-214.
51. Kolodner RD, Putnam CD, Myung K (2002) Maintenance of genome stability in Saccharomyces cerevisiae. Science 297: 552-557.
52. Richard GF, Paques F (2000) Mini- and microsatellite expansions: the recombination connection. EMBO Rep 1: 122-126.
53. Verstrepen KJ, Jansen A, Lewitter F, Fink GR (2005) Intragenic tandem repeats generate functional variability. Nat Genet 37: 986-990.
54. Fondon JW 3rd, Garner HR (2004) Molecular origins of rapid and continuous morphological evolution. Proc Natl Acad Sci U S A 101: 18058-18063.
55. Askree SH, Yehuda T, Smolikov S, Gurevich R, Hawk J, et al. (2004) A genome-wide screen for Saccharomyces cerevisiae deletion mutants that affect telomere length. Proc Natl Acad Sci U S A 101: 8658-8663.
56. Snyder M (2006) Telomere length as a quantitative trait: genome-wide survey and genetic mapping of telomere length-control genes in yeast. PLoS Genet 2: e35. doi:10.1371/journal.pgen.0020035
57. Weinert T (1998) DNA damage and checkpoint pathways: molecular anatomy and interactions with repair. Cell 94: 555-558.
58. Bender CF, Sikes ML, Sullivan R, Huye LE, Le Beau MM, et al. (2002) Cancer predisposition and hematopoietic failure in Rad50(S/S) mice. Genes Dev 16: 2237-2251.
59. Hiramoto T, Nakanishi T, Sumiyoshi T, Fukuda T, Matsuura S, et al. (1999) Mutations of a novel human RAD54 homologue, RAD54B, in primary cancer. Oncogene 18: 3422-3426.
60. Matsuda M, Miyagawa K, Takahashi M, Fukuda T, Kataoka T, et al. (1999) Mutations in the RAD54 recombination gene in primary cancers. Oncogene 18: 3427-3430.
61. Strissel PL, Strick R, Tomek RJ, Roe BA, Rowley JD, et al. (2000) DNA structural properties of AF9 are similar to MLL and could act as recombination hot spots resulting in MLL/AF9 translocations and leukemogenesis. Hum Mol Genet 9: 1671-1679.
62. Vogelstein B, Lane D, Levine AJ (2000) Surfing the p53 network. Nature 408: 307-310.
63. Bao Z, Murray JI, Boyle T, Ooi SL, Sandel MJ, et al. (2006) Automated cell lineage tracing in Caenorhabditis elegans. Proc Natl Acad Sci U S A 103: 2707-2712.
64. Malone RE (1990) Dual regulation of meiosis in yeast. Cell 61: 375-378.
65. Waddington CH (1961) Genetic assimilation. Adv Genet 10: 257-293.
66. Kussell E, Leibler S (2005) Phenotypic diversity, population growth, and information in fluctuating environments. Science 309: 2075-2078.
67. Landry CR, Townsend JP, Hartl DL, Cavalieri D (2006) Ecological and evolutionary genomics of Saccharomyces cerevisiae. Mol Ecol 15: 575-591.
68. Mortimer RK (2000) Evolution and variation of the yeast (Saccharomyces) genome. Genome Res 10: 403-409.
69. Debat V, Milton CC, Rutherford S, Klingenberg CP, Hoffmann AA (2006) Hsp90 and the quantitative variation of wing shape in Drosophila melanogaster. Evolution Int J Org Evolution 60: 2529-2538.
70. Milton CC, Huynh B, Batterham P, Rutherford SL, Hoffmann AA (2003) Quantitative trait symmetry independent of Hsp90 buffering: distinct modes of genetic canalization and developmental stability. Proc Natl Acad Sci U S A 100: 13396-13401.
71. Samakovli D, Thanou A, Valmas C, Hatzopoulos P (2007) Hsp90 canalizes developmental perturbation. J Exp Bot 58: 3513-3524.
72. Palecek SP, Parikh AS, Kron SJ (2000) Genetic analysis reveals that FLO11 upregulation and cell polarization independently regulate invasive growth in Saccharomyces cerevisiae. Genetics 156: 1005-1023.
73. Bishop AL, Rab FA, Sumner ER, Avery SV (2007) Phenotypic heterogeneity can enhance rare-cell survival in 'stress-sensitive' yeast populations. Mol Microbiol 63: 507-520.
74. Sawyer SL, Malik HS (2006) Positive selection of yeast nonhomologous endjoining genes and a retrotransposon conflict hypothesis. Proc Natl Acad Sci U S A 103: 17614-17619.
75. Nogami S, Ohya Y, Yvert G (2007) Genetic complexity and quantitative trait loci mapping of yeast morphological traits. PLoS Genet 3: e31. doi:10. 1371/journal.pgen.0030031
76. Breslow DK, Cameron DM, Collins SR, Schuldiner M, Stewart-Ornstein J, et al. (2008) A comprehensive strategy enabling high-resolution functional analysis of the yeast genome. Nat Methods 5: 711-718.
77. Kaufman L, Rousseeuw PJ (1990) Partitioning Around Medoids (Program PAM). Finding groups in data: an introduction to cluster analysis. New York: Wiley.
78. van der Laan MJ, Pollard KS, Bryan J (2003) A new partitioning around medoids algorithm. Journal of Statistical Computation and Simulation 73: 575-584.
79. Freeman LC (1977) A set of measures of centrality based on betweenness. Sociometry 40: 35-41.
80. Watts DJ, Strogatz SH (1998) Collective dynamics of 'small-world' networks. Nature 393: 440-442.
81. Giaever G, Chu AM, Ni L, Connelly C, Riles L, et al. (2002) Functional profiling of the Saccharomyces cerevisiae genome. Nature 418: 387-391.
82. Tong AH, Lesage G, Bader GD, Ding H, Xu H, et al. (2004) Global mapping of the yeast genetic interaction network. Science 303: 808-813.
83. Holstege FC, Jennings EG, Wyrick JJ, Lee TI, Hengartner CJ, et al. (1998) Dissecting the regulatory circuitry of a eukaryotic genome. Cell 95: 717-728.
84. Ghaemmaghami S, Huh WK, Bower K, Howson RW, Belle A, et al. (2003) Global analysis of protein expression in yeast. Nature 425: 737-741.
85. Wall DP, Hirsh AE, Fraser HB, Kumm J, Giaever G, et al. (2005) Functional genomic analysis of the rates of protein evolution. Proc Natl Acad Sci U S A 102: 5483-5488.
86. Kellis M, Birren BW, Lander ES (2004) Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature 428: 617-624.
87. Yang Z (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13: 555-556.
88. Yang Z, Nielsen R (2000) Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol Biol Evol 17: 32-43.