Glucose, nitrogen, and phosphate repletion in saccharomyces cerevisiae: Common transcriptional responses to different nutrient signals

G3: Genes, Genomes, Genetics

Volumn 2, Issue 9, 2012, Pages 1003-1017

  Conway, Michael K ^a   Grunwald, Douglas ^a   Heideman, Warren ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

CAMP; Glucose; Mitogenesis; Nitrogen; Phosphate; Protein kinase A; RRPE; TOR; Transcription; Yeast

Indexed keywords

CYCLIC AMP; GLUCOSE; NITROGEN; PHOSPHATE; TARGET OF RAPAMYCIN KINASE; TRANSCRIPTION FACTOR; TRANSCRIPTOME;

ARTICLE; BINDING SITE; CLUSTER ANALYSIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PHYSIOLOGICAL STRESS; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION;

BINDING SITES; CLUSTER ANALYSIS; CYCLIC AMP; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; GLUCOSE; NITROGEN; PHOSPHATES; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; TOR SERINE-THREONINE KINASES; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSCRIPTOME;

EID: 84883150055     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.112.002808     Document Type: Article

References (84)

1. Boy-Marcotte, E., H. Garreau, and M. Jacquet, 1987 Cyclic AMP controls the switch between division cycle and resting state programs in response to ammonium availability in Saccharomyces cerevisiae. Yeast 3: 85-93.
2. Cain, N. E., and C. A. Kaiser, 2011 Transport activity-dependent intracellular sorting of the yeast general amino acid permease. Mol. Biol. Cell 22: 1919-1929.
3. Camonis, J. H., M. Kalekine, G. Bernard, H. Garreau, E. Boy-Marcotte et al., 1986 Characterization, cloning and sequence analysis of the CDC25 gene which controls the cAMP level of Saccharomyces cerevisiae. EMBO 5: 375-380.
4. Cardenas, M. E., N. S. Cutler, M. C. Lorenz, C. J. Di Como, and J. Heitman, 1999 The TOR signaling cascade regulates gene expression in response to nutrients. Genes Dev. 13: 3271-3279.
5. Carlson, M., 1999 Glucose repression in yeast. Curr. Opin. Microbiol. 2: 202-207.
6. Chua, G., Q. D. Morris, R. Sopko, M. D. Robinson, O. Ryan et al., 2006 Identifying transcription factor functions and targets by phenotypic activation. Proc. Natl. Acad. Sci. USA 103: 12045-12050.
7. Cooper, T. G., 2002 Transmitting the signal of excess nitrogen in Saccharomyces cerevisiae from the Tor proteins to the GATA factors: connecting the dots. FEMS Microbiol. Rev. 26: 223-238.
8. Crespo, J. L., T. Powers, B. Fowler, and M. N. Hall, 2002 The TOR-controlled transcription activators GLN3, RTG1, and RTG3 are regulated in response to intracellular levels of glutamine. Proc. Natl. Acad. Sci. USA 99: 6784-6789.
9. Dequard-Chablat, M., M. Riva, C. Carles, and A. Sentenac, 1991 RPC19, the gene for a subunit common to yeast RNA polymerases A (I) and C (III). J. Biol. Chem. 266: 15300-15307.
10. Donaton, M. C., I. Holsbeeks, O. Lagatie, G. Van Zeebroeck, M. Crauwels et al., 2003 The Gap1 general amino acid permease acts as an amino acid sensor for activation of protein kinase A targets in the yeast Saccharomyces cerevisiae. Mol. Microbiol. 50: 911-929.
11. Fingerman, I., V. Nagaraj, D. Norris, and A. K. Vershon, 2003 Sfp1 plays a key role in yeast ribosome biogenesis. Eukaryot. Cell 2: 1061-1068.
12. Forsberg, H., and P. O. Ljungdahl, 2001 Sensors of extracellular nutrients in Saccharomyces cerevisiae. Curr. Genet. 40: 91-109.
13. François, J., P. Eraso, and C. Gancedo, 1987 Changes in the concentration of cAMP, fructose 2,6-biphosphate and related metabolites and enzymes in Saccharomyces cerevisiae during growth on glucose. Eur. J. Biochem. 164: 369-373.
14. Gasch, A. P., P. T. Spellman, C. M. Kao, O. Carmel-Harel, M. B. Eisen et al., 2000 Genomic expression programs in the response of yeast cells to environmental changes. Mol. Biol. Cell 11: 4241-4257.
15. Gentleman, R. C., V. J. Carey, D. M. Bates, B. Bolstad, M. Dettling et al., 2004 Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5: R80.
16. Giots, F., M. C. Donaton, and J. M. Thevelein, 2003 Inorganic phosphate is sensed by specific phosphate carriers and acts in concert with glucose as a nutrient signal for activation of the protein kinase A pathway in the yeast Saccharomyces cerevisiae. Mol. Microbiol. 47: 1163-1181.
17. Gray, J. V., G. A. Petsko, G. C. Johnston, D. Ringe, R. A. Singer et al., 2004 "Sleeping beauty": quiescence in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 68: 187-206.
18. Greenberg, M. L., and J. M. Lopes, 1996 Genetic regulation of phospholipid biosynthesis in Saccharomyces cerevisiae. Microbiol. Rev. 60: 1-20.
19. Grenson, M., C. Hou, and M. Crabeel, 1970 Multiplicity of the amino acid permeases in Saccharomyces cerevisiae. IV. Evidence for a general amino acid permease. J. Bacteriol. 103: 770-777.
20. Griffioen, G., R. J. Laan, W. H. Mager, and R. J. Planta, 1996 Ribosomal protein gene transcription in Saccharomyces cerevisiae shows a biphasic response to nutritional changes. Microbiology 142: 2279-2287.
21. Grigull, J., S. Mnaimneh, J. Pootoolal, M. D. Robinson, and T. R. Hughes, 2004 Genome-wide analysis of mRNA stability using transcription inhibitors and microarrays reveals posttranscriptional control of ribosome biogenesis factors. Mol. Cell. Biol. 24: 5534-5547.
22. Hahn, J. S., Z. Hu, D. J. Thiele, and V. R. Iyer, 2004 Genome-wide analysis of the biology of stress responses through heat shock transcription factor. Mol. Cell. Biol. 24: 5249-5256.
23. Harbison, C. T., D. B. Gordon, T. I. Lee, N. J. Rinaldi, K. D. Macisaac et al., 2004 Transcriptional regulatory code of a eukaryotic genome. Nature 431: 99-104.
24. Hardwick, J. S., F. G. Kuruvilla, J. K. Tong, A. F. Shamji, and S. L. Schreiber, 1999 Rapamycin-modulated transcription defines the subset of nutrient-sensitive signaling pathways directly controlled by the Tor proteins. Proc. Natl. Acad. Sci. USA 96: 14866-14870.
25. Hedbacker, K., and M. Carlson, 2008 SNF1/AMPK pathways in yeast. Front. Biosci. 13: 2408-2420.
26. Heideman, W., G. F. Casperson, and H. R. Bourne, 1990 Adenylyl cyclase in yeast: antibodies and mutations identify a regulatory domain. J. Cell. Biochem. 42: 229-242.
27. Hinnebusch, A. G., 2005 Translational regulation of GCN4 and the general amino acid control of yeast. Annu. Rev. Microbiol. 59: 407-450.
28. Hughes, J. D., P. W. Estep, S. Tavazoie, and G. M. Church, 2000 Computational identification of cis-regulatory elements associated with groups of functionally related genes in Saccharomyces cerevisiae. J. Mol. Biol. 296: 1205-1214.
29. Jauniaux, J. C., and M. Grenson, 1990 GAP1, the general amino acid permease gene of Saccharomyces cerevisiae. Nucleotide sequence, protein similarity with the other bakers yeast amino acid permeases, and nitrogen catabolite repression. Eur. J. Biochem. 190: 39-44.
30. Johnston, G. C., R. A. Singer, and S. McFarlane, 1977 Growth and cell division during nitrogen starvation of the yeast Saccharomyces cerevisiae. J. Bacteriol. 132: 723-730.
31. Jorgensen, P., I. Rupes, J. R. Sharom, L. Schneper, J. R. Broach et al., 2004 A dynamic transcriptional network communicates growth potential to ribosome synthesis and critical cell size. Genes Dev. 18: 2491-2505.
32. Klosinska, M. M., C. A. Crutchfield, P. H. Bradley, J. D. Rabinowitz, and J. R. Broach, 2011 Yeast cells can access distinct quiescent states. Genes Dev. 25: 336-349.
33. Kriel, J., S. Haesendonckx, M. Rubio-Texeira, G. Van Zeebroeck, and J. M. Thevelein, 2011 From transporter to transceptor: signaling from transporters provokes re-evaluation of complex trafficking and regulatory controls: endocytic internalization and intracellular trafficking of nutrient transceptors may, at least in part, be governed by their signaling function. Bioessays 33: 870-879.
34. Lagerstedt, J. O., J. C. Voss, A.Wieslander, and B. L. Persson, 2004 Structural modeling of dual-affinity purified Pho84 phosphate transporter. FEBS Lett. 578: 262-268.
35. Lieb, J. D., X. Liu, D. Botstein, and P. O. Brown, 2001 Promoter-specific binding of Rap1 revealed by genome-wide maps of protein-DNA association. Nat. Genet. 28: 327-334.
36. Lillie, S. H., and J. R. Pringle, 1980 Reserve carbohydrate metabolism in Saccharomyces cerevisiae: responses to nutrient limitation. J. Bacteriol. 143: 1384-1394.
37. Lorenz, M. C., and J. Heitman, 1998 The MEP2 ammonium permease regulates pseudohyphal differentiation in Saccharomyces cerevisiae. EMBO J. 17: 1236-1247.
38. Lundh, F., J. M. Mouillon, D. Samyn, K. Stadler, Y. Popova et al., 2009 Molecular mechanisms controlling phosphate-induced downregulation of the yeast Pho84 phosphate transporter. Biochemistry 48: 4497-4505.
39. Macisaac, K. D., D. B. Gordon, L. Nekludova, D. T. Odom, J. Schreiber et al., 2006 A hypothesis-based approach for identifying the binding specificity of regulatory proteins from chromatin immunoprecipitation data. Bioinformatics 22: 423-429.
40. Magasanik, B., and C. A. Kaiser, 2002 Nitrogen regulation in Saccharomyces cerevisiae. Gene 290: 1-18.
41. Marion, R. M., A. Regev, E. Segal, Y. Barash, D. Koller et al., 2004 Sfp1 is a stress- and nutrient-sensitive regulator of ribosomal protein gene expression. Proc. Natl. Acad. Sci. USA 101: 14315-14322.
42. Martin, D. E., A. Soulard, and M. N. Hall, 2004 TOR regulates ribosomal protein gene expression via PKA and the Forkhead transcription factor FHL1. Cell 119: 969-979.
43. Martinez, M. J., S. Roy, A. B. Archuletta, P. D. Wentzell, S. S. Anna-Arriola et al., 2004 Genomic analysis of stationary-phase and exit in Saccharomyces cerevisiae: gene expression and identification of novel essential genes. Mol. Biol. Cell 15: 5295-5305.
44. Martinez-Pastor, M. T., G. Marchler, C. Schuller, A. Marchler-Bauer, H. Ruis et al., 1996 The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress response element (STRE). EMBO J. 15: 2227-2235.
45. Matsumoto, K., I. Uno, Y. Oshima, and T. Ishikawa, 1982 Isolation and characterization of yeast mutants defective in adenylate cyclase and cAMPdepenent protein kinase. Proc. Natl. Acad. Sci. USA 79: 2355-2359.
46. Matsumoto, K., I. Uno, and T. Ishikawa, 1985 Genetic analysis of the role of cAMP in yeast. Yeast 1: 15-24.
47. Mazon, M. J., 1978 Effect of glucose starvation on the nicotinamide adenine dinucleotide phosphate-dependent glutamate dehydrogenase of yeast. J. Bacteriol. 133: 780-785.
48. Merhi, A., N. Gerard, E. Lauwers, M. Prevost, and B. Andre, 2011 Systematic mutational analysis of the intracellular regions of yeast Gap1 permease. PLoS ONE 6: e18457.
49. Mitts, M. R., D. B. Grant, and W. Heideman, 1990 Adenylate cyclase in Saccharomyces cerevisisae is a peripheral membrane protein. Mol. Cell. Biol. 10: 3873-3883.
50. Newcomb, L. L., J. A. Diderich, M. G. Slattery, and W. Heideman, 2003 Glucose regulation of Saccharomyces cerevisiae cell cycle genes. Eukaryot. Cell 2: 143-149.
51. Paris, S., and J. R. Pringle, 1983 Saccharomyces cerevisiae: heat and gluculase sensitivities of starved cells. Ann. Microbiol. (Paris) 134B: 379-385.
52. Pina, B., J. Fernandez-Larrea, N. Garcia-Reyero, and F. Z. Idrissi, 2003 The different (sur)faces of Rap1p. Mol. Genet. Genomics 268: 791-798.
53. Popova, Y., P. Thayumanavan, E. Lonati, M. Agrochao, and J. M. Thevelein, 2010 Transport and signaling through the phosphate-binding site of the yeast Pho84 phosphate transceptor. Proc. Natl. Acad. Sci. USA 107: 2890-2895.
54. Radonjic, M., J. C. Andrau, P. Lijnzaad, P. Kemmeren, T. T. Kockelkorn et al., 2005 Genome-wide analyses reveal RNA polymerase II located upstream of genes poised for rapid response upon S. cerevisiae stationary phase exit. Mol. Cell 18: 171-183.
55. Robert, F., D. K. Pokholok, N. M. Hannett, N. J. Rinaldi, M. Chandy et al., 2004 Global position and recruitment of HATs and HDACs in the yeast genome. Mol. Cell 16: 199-209.
56. Robinson, M. D., J. Grigull, N. Mohammad, and T. R. Hughes, 2002 FunSpec: a web-based cluster interpreter for yeast. BMC Bioinformatics 3: 35.
57. Roosen, J., K. Engelen, K. Marchal, J. Mathys, G. Griffioen et al., 2005 PKA and Sch9 control a molecular switch important for the proper adaptation to nutrient availability. Mol. Microbiol. 55: 862-880.
58. Rowley, A., G. Johnston, B. Butler, M. Werner-Washburne, and R. Singer, 1993 Heat shock-mediated cell cycle blockage and G1 cyclin expression in the yeast Saccharomyces cerevisiae. Mol. Cell. Biol. 13: 1034-1041.
59. Russell, M., J. Bradshaw-Rouse, D. Markwardt, and W. Heideman, 1993 Changes in gene expression in the Ras/adenylate cyclase system of Saccharomyces cerevisiae: correlation with cAMP levels and growth arrest. Mol. Biol. Cell 4: 757-765.
60. Rutherford, J. C., G. Chua, T. Hughes, M. E. Cardenas, and J. Heitman, 2008 A Mep2-dependent transcriptional profile links permease function to gene expression during pseudohyphal growth in Saccharomyces cerevisiae. Mol. Biol. Cell 19: 3028-3039.
61. Saeed, A. I., V. Sharov, J. White, J. Li, W. Liang et al., 2003 TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34: 374-378.
62. Saeed, A. I., N. K. Bhagabati, J. C. Braisted, W. Liang, V. Sharov et al., 2006 TM4 microarray software suite. Methods Enzymol. 411: 134-193.
63. Santangelo, G. M., 2006 Glucose signaling in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 70: 253-282.
64. Schawalder, S. B., M. Kabani, I. Howald, U. Choudhury, M. Werner et al., 2004 Growth-regulated recruitment of the essential yeast ribosomal protein gene activator Ifh1. Nature 432: 1058-1061.
65. Scherens, B., A. Feller, F. Vierendeels, F. Messenguy, and E. Dubois, 2006 Identification of direct and indirect targets of the Gln3 and Gat1 activators by transcriptional profiling in response to nitrogen availability in the short and long term. FEMS Yeast Res. 6: 777-791.
66. Schneper, L., K. Duvel, and J. R. Broach, 2004 Sense and sensibility: nutritional response and signal integration in yeast. Curr. Opin. Microbiol. 7: 624-630.
67. Slattery, M. G., and W. Heideman, 2007 Coordinated regulation of growth genes in Saccharomyces cerevisiae. Cell Cycle 6: 1210-1219.
68. Slattery, M. G., D. Liko, and W. Heideman, 2008 Protein kinase A, TOR, and glucose transport control the response to nutrient repletion in Saccharomyces cerevisiae. Eukaryot. Cell 7: 358-367.
69. Thevelein, J. M., and M. Beullens, 1985 Cyclic AMP and the stimulation of trehalase activity in the yeast Saccharomyces cerevisiae by carbon sources, nitrogen sources and inhibitors of protein synthesis. J. Gen. Microbiol. 131: 3199-3209.
70. Thevelein, J. M., R. Gelade, I. Holsbeeks, O. Lagatie, Y. Popova et al., 2005 Nutrient sensing systems for rapid activation of the protein kinase A pathway in yeast. Biochem. Soc. Trans. 33: 253-256.
71. Thomas-Chollier, M., O. Sand, J. V. Turatsinze, R. Janky, M. Defrance et al., 2008 RSAT: regulatory sequence analysis tools. Nucleic Acids Res. 36: W119-W127.
72. Unger, M. W., and L. H. Hartwell, 1976 Control of cell division in Saccharomyces cerevisiae by methionyl-tRNA. Proc. Natl. Acad. Sci. USA 73: 1664-1668. van Helden, J., 2003 Regulatory sequence analysis tools. Nucleic Acids Res. 31: 3593-3596.
73. van Helden, J., 2003 Regulatory sequence analysis tools. Nucleic Acids Res. 31: 3593-3596.
74. Van Nuland, A., P. Vandormael, M. Donaton, M. Alenquer, A. Lourenco et al., 2006 Ammonium permease-based sensing mechanism for rapid ammonium activation of the protein kinase A pathway in yeast. Mol. Microbiol. 59: 1485-1505.
75. Van Zeebroeck, G., B. M. Bonini, M. Versele, and J. M. Thevelein, 2009 Transport and signaling via the amino acid binding site of the yeast Gap1 amino acid transceptor. Nat. Chem. Biol. 5: 45-52.
76. Wade, C., K. A. Shea, R. V. Jensen, and M. A. McAlear, 2001 EBP2 is a member of the yeast RRB regulon, a transcriptionally coregulated set of genes that are required for ribosome and rRNA biosynthesis. Mol. Cell. Biol. 21: 8638-8650.
77. Wang, Y., M. Pierce, L. Schneper, C. G. Guldal, X. Zhang et al., 2004 Ras and Gpa2 mediate one branch of a redundant glucose signaling pathway in yeast. PLoS Biol. 2: E128.
78. Wu, J., N. Zhang, A. Hayes, K. Panoutsopoulou, and S. G. Oliver, 2004 Global analysis of nutrient control of gene expression in Saccharomyces cerevisiae during growth and starvation. Proc. Natl. Acad. Sci. USA 101: 3148-3153.
79. Wullschleger, S., R. Loewith, and M. N. Hall, 2006 TOR signaling in growth and metabolism. Cell 124: 471-484.
80. Wykoff, D. D., and E. K. O'Shea, 2001 Phosphate transport and sensing in Saccharomyces cerevisiae. Genetics 159: 1491-1499.
81. Zaman, S., S. I. Lippman, X. Zhao, and J. R. Broach, 2008 How Saccharomyces responds to nutrients. Annu. Rev. Genet. 42: 27-81.
82. Zaman, S., S. I. Lippman, L. Schneper, N. Slonim, and J. R. Broach, 2009 Glucose regulates transcription in yeast through a network of signaling pathways. Mol. Syst. Biol. 5: 245.
83. Zhu, C., K. J. Byers, R. P. McCord, Z. Shi, M. F. Berger et al., 2009 Highresolution DNA-binding specificity analysis of yeast transcription factors. Genome Res. 19: 556-566.
84. Zurita-Martinez, S. A., and M. E. Cardenas, 2005 Tor and cyclic AMPprotein kinase A: two parallel pathways regulating expression of genes required for cell growth. Eukaryot. Cell 4: 63-71.