Nonlinear fitness consequences of variation in expression level of a eukaryotic gene

Molecular Biology and Evolution

Volumn 30, Issue 2, 2013, Pages 448-456

  Rest, Joshua S ^a   Morales, Christopher M ^a   Waldron, John B ^a   Opulente, Dana A ^a   Fisher, Julius ^a   Moon, Seungjae ^a,d   Bullaughey, Kevin ^b   Carey, Lucas B ^c   Dedousis, Demitri ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^d Weill Cornell Graduate School of Biomedical Sciences   (United States)

Author keywords

Fitness function; Gene expression; Gene regulatory evolution; Saccharomyces cerevisiae; Sphingolipids

Indexed keywords

SPHINGOLIPID; CARRIER PROTEIN; LCB2 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; SERINE PALMITOYLTRANSFERASE;

ARTICLE; DOWN REGULATION; ESSENTIAL GENE; FUNGAL CELL; FUNGAL GENE; GENE CONTROL; GENE EXPRESSION; GENETIC VARIABILITY; GENOTYPE ENVIRONMENT INTERACTION; LCB2 GENE; LIPOGENESIS; NONHUMAN; OSMOTIC STRESS; PHENOTYPE; SACCHAROMYCES CEREVISIAE; UPREGULATION; ENVIRONMENT; EVOLUTION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PROTEIN BINDING; REPRODUCTIVE FITNESS;

BIOLOGICAL EVOLUTION; CARRIER PROTEINS; ENVIRONMENT; GENE EXPRESSION REGULATION, FUNGAL; GENETIC FITNESS; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SERINE C-PALMITOYLTRANSFERASE;

MLCS; MLOWN;

EID: 84879303337     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/mss248     Document Type: Article

References (69)

1. Bayer TS. 2010. Using synthetic biology to understand the evolution of gene expression. Curr Biol. 20:R772-R779.
2. Bielawski J, Szulc ZM, Hannun Y.A., Bielawska A. 2006. Simultaneous quantitative analysis of bioactive sphingolipids by high-performance liquid chromatography-tandem mass spectrometry. Methods 39: 82-91.
3. Birchler JA, Bhadra U, Bhadra M.P., Auger DL 2001. Dosage-dependent gene regulation in multicellular eukaryotes: implications for dosage compensation, aneuploid syndromes, and quantitative traits. Dev Biol. 234: 275-288.
4. Brachmann CB, Davies A, Cost C.J., Caputo E., Li J, Hieter P, Boeke JD. 1998. Designer deletion strains derived from Saccharomyces cerevi-siae S288C a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14: 115-132.
5. Brem RB, Yvert CI, Clinton R, Kruglyak L 2002. Genetic dissection of transcriptional regulation in budding yeast. Science 296: 752-755.
6. Breslow DK, Collins SR, Bodenmiller B, Aebersold R., Simons K, Shevchenko A, Ejsing C.S., Weissman JS. 2010. Orm family proteins mediate sphingolipid homeostasis. Nature 463: 1048-1053.
7. Cowart LA, Obeid LM. 2007. Yeast sphingolipids: recent developments in understanding biosynthesis, regulation, and function. Biochim Biophys Acta. 1771: 421-431.
8. Dekel E, Alon U. 2005. Optimality and evolutionary tuning of the expression level of a protein. Nature 436: 588-592.
9. Delneri D, Hoyle DC Ckargkas K, et al. (12 co-authors). 2008. Identification and characterization of high-flux-control genes of yeast through competition analyses in continuous cultures. Nat Genet 40: 113-117.
10. Deutschbauer AM, Davis RW. 2005. Quantitative trait loci mapped to single-nucleotide resolution in yeast. Nat Genet 37: 1333-1340.
11. Deutschbauer AM, Jaramillo DF, Proctor M, Kumm J., Hillenmeyer ME, Davis RW, Nislow C, Giaever C. 2005. Mechanisms of haploinsuffi-ciency revealed by genome-wide profiling in yeast. Genetics 169: 1915-1925.
12. Dickson RC 2010. Roles for sphingolipids in Saccharomyces cerevisiae. In: Chalfant C, Del Poeta M, editors. Sphingolipids as signaling and regulatory molecules. New York Springer, p. 217-231.
13. Dykhuizen DE, Dean AM, Hartl DL 1987. Metabolic flux and fitness. Genetics 115: 25-31.
14. Dykhuizen DE, Hartl DL 1983. Selection in chemostats. Microbiol Rev. 47: 150.
15. Eanes WF. 1999. Analysis of selection on enzyme polymorphisms. Annu Rev Ecol Syst 30: 301-326.
16. Eanes WF. 2011. Molecular population genetics and selection in the glycolytic pathway. J Exp Biol. 214: 165-171.
17. Elena SF, Lenski RE. 1997. Test of synergistic interactions among deleterious mutations in bacteria. Nature 390: 395-398.
18. Eng KH, Kvitek DJ, Keles, S, Gasch AP. 2010. Transient genotype-by-environment interactions following environmental shock provide a source of expression variation for essential genes. Genetics 184: 587-593.
19. Fisher RA. 1928. The possible modification of the response of the wild type to recurrent mutations. Am Nat 62: 115-126.
20. Cable K, Han C, Monaghan E., Bacikova D, Natarajan M, Williams R., Dunn TM. 2001 Mutations in the yeast LCB1 and LCB2 genes, including those corresponding to the hereditary sensory neuropathy type I mutations, dominantly inactivate serine palmitoyltransferase. J Biol Chem. 277: 10194-10200.
21. Gable K, Slife H, Bacikova D., Monaghan E, Dunn TM. 2000. Tsc3p is an 80-amino acid protein associated with serine palmitoyltransferase and required for optimal enzyme activity. J Biol Chem. 275: 7597-7603.
22. Gerke J, Lorenz K, Ramnarine S., Cohen B. 2010. Gene-environment interactions at nucleotide resolution. PLoS Genet 6: e1001144.
23. Gerke J.P., Chen CTL Cohen BA. 2006. Natural isolates of Saccharomyces cerevisiae display complex genetic variation in sporulation efficiency. Genetics 174: 985.
24. Giaever G, Chu AM, Ni L Connelly C, Riles L Veronneau S, Dow S, Lucau-Danila A, Anderson K, Andre B. 2001 Functional profiling of the Saccharomyces cerevisiae genome. Nature 418: 387-391.
25. Gresham D, Desai MM, Tucker C.M., Jenq HT, Pai DA, Ward A, DeSevo C.G., Botstein D., Dunham MJ. 2008. The repertoire and dynamics of evolutionary adaptations to controlled nutrient-limited environments in yeast. PLoS Genet 4:e1000303.
26. Gu Z, David L Petrov D, Jones T, Davis RW, Steinmetz LM. 2005. Elevated evolutionary rates in the laboratory strain of Saccharomyces cerevisiae. Proc Natl Acad Sci USA 102: 1092-1097.
27. Haldane JBS. 1930. A note on Fisher's theory of the origin of dominance, and on a correlation between dominance and linkage. Am Nat 64: 87-90.
28. Hannun YA Obeid LM. 2008. Principles of bioactive lipid signaling lessons from sphingolipids. Nat Rev Mol Cell Biol. 9: 139-150.
29. Hannun YA Obeid LM. 2011. Many ceramides. J Biol Chem. 286: 27855-27862.
30. Hartl DL Dykhuizen DE, Dean AM. 1985. Limits of adaptation: the evolution of selective neutrality. Genetics 111: 655-674.
31. Hillenmeyer ME, Fung E, Wildenhain J., et al. (14 co-authors). 2008. The chemical genomic portrait of yeasc uncovering a phenotype for all genes. Science 320: 362-365.
32. Huang X, Liu J, Dickson RC 2012. Down-regulating sphingolipid synthesis increases yeast lifespan. PLoS Genet 8:e1002493.
33. Hughes TR, Marton MJ, Jones A.R., Roberts CJ, Stoughton R, Armour CD, Bennett H.A., Coffey E., Dai H, He YD. 2000. Functional discovery via a compendium of expression profiles. Cell 102: 109-126.
34. Huh W-K, Falvo J.V., Cerke LC, Carroll AS, Howson RW, Weissman J.S., O'Shea EK. 2003. Global analysis of protein localization in budding yeast. Nature 425: 686-691.
35. Khaitovich P, Pääbo S, Weiss G. 2005. Toward a neutral evolutionary model of gene expression. Genetics 170: 529-939.
36. Koybasi S, Senkal CE, Sundararaj K, et al. (12 co-authors). 2004. Defects in cell growth regulation by C18: 0-ceramide and longevity assurance gene 1 in human head and neck squamous cell carcinomas. J Biol Chem. 279: 44311-44319.
37. Kvitek DJ, Will JL, Gasch AP. 2008. Variations in stress sensitivity and genomic expression in diverse S. cerevisiae isolates. PLoS Genet 4: e1000223.
38. Lebman DA, Spiegel S. 2008. Thematic review series: sphingolipids. Cross-talk at the crossroads of sphingosine-1-phosphate, growth factors, and cytokine signaling. J Lipid Res. 49: 1388-1394.
39. Liu H, Styles CA, Fink GR. 1996. Saccharomyces cerevisiae S288C has a mutation in FL08, a gene required for filamentous growth. Genetics 144: 567-978.
40. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402-408.
41. Manolio TA, Collins FS, Cox N.J., et al. (27 co-authors). 2009. Finding the missing heritability of complex diseases. Nature 461: 747-753.
42. McCusker JH, demons KV, Stevens D.A., Davis RW. 1994. Genetic characterization of pathogenic Saccharomyces cerevisiae isolates. Genetics 136: 1261-1269.
43. Mnaimneh S, Davierwala AP, Haynes J, et al. (24 co-authors). 2004. Exploration of essential gene functions via titratable promoter alleles. Cell 118: 31-44.
44. Monaghan E, Gable K, Dunn T. 2002. Mutations in the Lcb2p subunit of serine palmitoyltransferase eliminate the requirement for the TSC3 gene in Saccharomyces cerevisiae. Yeast 19: 659-670.
45. Murphy HA, Kuehne HA, Francis C.A., Sniegowski PD. 2006. Mate choice assays and mating propensity differences in natural yeast populations. Biol Lett 2: 553-556.
46. Nagiec MM, Baltisberger JA, Wells G.B., Lester RL, Dickson RC 1994. The LCB2 gene of Saccharomyces and the related LCB1 gene encode subunits of serine palmitoyltransferase, the initial enzyme in sphingolipid synthesis. Proc Natl Acad Sci USA 91: 7899-7902.
47. Newman JRS, 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.
48. Nijhout HF, Berg AM, Gibson WT. 2003. A mechanistic study of evol-vability using the mitogen-activated protein kinase cascade. Evol Dev. 5: 281-294.
49. Orr HA. 1991. A test of Fisher's theory of dominance. Proc Natl Acad Sci USA. 88: 11413-11415.
50. Papp B, Pal C Hurst LD. 2003. Dosage sensitivity and the evolution of gene families in yeast. Nature 424: 194-197.
51. Patton JL, Srinivasan B, Dickson R.C., Lester RL 1992. Phenotypes of sphingolipid-dependent strains of Saccharomyces cerevisiae. J Bacterial. 174: 7180-7184.
52. Patwardhan RP, Lee C, Litvin O., Young DL, Pe'er D, Shendure J. 2009. High-resolution analysis of DNA regulatory elements by synthetic saturation mutagenesis. Nat Biotechnol. 27: 1173-1175.
53. Peng W-T, Robinson M.D., Mnaimneh S., Krogan NJ, Cagney G, Morris Q, Davierwala A.P., Grigull J., Yang X, Zhang W. 2003. A panoramic view of yeast noncoding RNA processing. Cell 113: 519-933.
54. Perfeito L, Ghozzi S, Berg J., Schnetz K, Lässig M. 2011. Nonlinear fitness landscape of a molecular pathway. PLoS Genet 7:e1002160.
55. Rossouw D, Olivares-Hernandes R, Nielsen J., Bauer FF. 2009. Comparative transcriptomic approach to investigate differences in wine yeast physiology and metabolism during fermentation. Appl Environ Microbiol. 75: 6600-6612.
56. Sopko R, Huang D, Preston N., et al. (12 co-authors). 2006. Mapping pathways and phenotypes by systematic gene overexpression. Mol Cell. 21: 319-330.
57. Spellman PT, Sherlock G, Zhang M.Q., Iyer VR, Anders K, Eisen MB, Brown P.O., Botstein D., Futcher B. 1998. Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization. Mol Biol Cell. 9: 3273.
58. Teste M-A, Duquenne M., Francois J, Parrou J-L 2009. Validation of reference genes for quantitative expression analysis by real-time RT-PCR in Saccharomyces cerevisiae. BMC Mol Biol. 10: 99.
59. Tu BP, Kudlicki A, Rowicka M., McKnight SL 2005. Logic of the yeast metabolic cycle temporal compartmentalization of cellular processes. Science 310: 1152-1158.
60. Veitia RA 2002. Exploring the etiology of haploinsufficiency. BioEssays 24: 175-184.
61. Wagner A. 2005. Energy constraints on the evolution of gene expression. Mol Biol Evol. 22: 1365-1374.
62. Wagner A. 2007. Energy costs constrain the evolution of gene expression. J Exp Zool B Mol Dev Evol. 308B: 322-324.
63. Warringer J, Zörgö E, Cubillos FA, et al. (13 co-authors). 2011. Trait variation in yeast is defined by population history. PLoS Genet 7: e1002111.
64. Wright KM, Rausher MD. 2010. The evolution of control and distribution of adaptive mutations in a metabolic pathway. Genetics 184: 483-502.
65. Wright S. 1929. Fisher's theory of dominance. Am Nat 63: 274-279.
66. Wright S. 1931 The roles of mutation, inbreeding crossbreeding, and selection in evolution. Proceedings of the 6th International Congress of Genetics, Menasha, WI. Vol. 1. p. 356-366.
67. Wright S. 1934. Physiological and evolutionary theories of dominance. Am Nat 68: 24-53.
68. Yanai I, Hunter CP. 2009. Comparison of diverse developmental transcriptomes reveals that coexpression of gene neighbors is not evo-lutionarily conserved. Genome Res. 19: 2214-2220.
69. Yasuda S, Nishijima M, Hanada K. 2003. Localization, topology, and function of the LCB1 subunit of serine palmitoyltransferase in mammalian cells. J Biol Chem. 278: 4176-4183.