The Nutrient Stress Response in Yeast

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Stress Response Mechanisms in Fungi

Abstract

Nutrients such as glucose and glutamine provide yeast not only with substrates for energy production and mass accumulation but also with signals specifying the metabolic and transcriptional program appropriate for the condition in which the yeast cells find themselves. In nutrient replete conditions, nutrient signaling pathways activate growth programs promoting both continuous mass accumulation and the discontinuous process of the cell cycle. Under nutrient limiting conditions, these pathways activate a canonical stress response program and attenuate cell growth in proportion to the extent of nutrient limitation. In this review, we describe recent results elaborating the nature of these nutrient signaling pathways. In addition, we describe the short-term and long-term consequences of nutrient limitation on both the canonical stress response and the regulation of cell growth. We highlight the stochastic nature of the stress response, which permits genetically identical cells in a common environment to pursue distinct survival strategies, maximizing the potential for overall persistence of the clonal population regardless of subsequent environmental conditions. Finally, we examine the mechanistic connection between activation of the stress response and attenuation of cell growth. These recent results provide insight not only into the biology of yeast but also on homologous signaling pathways and stress responses of larger eukaryotes.

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References

  • Airoldi EM, Huttenhower C, Gresham D, Lu C, Caudy AA, Dunham MJ, Broach JR, Botstein D, Troyanskaya OG (2009) Predicting cellular growth from gene expression signatures. PLoS Comput Biol 5(1):e1000257

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ashe MP, De Long SK, Sachs AB (2000) Glucose depletion rapidly inhibits translation initiation in yeast. Mol Biol Cell 11:833–848

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Balaban NQ, Merrin J, Chait R, Kowalik L, Leibler S (2004) Bacterial persistence as a phenotypic switch. Science 305:1622–1625

    Article  CAS  PubMed  Google Scholar 

  • Balagopal V, Parker R (2009) Polysomes, P bodies and stress granules: states and fates of eukaryotic mRNAs. Curr Opin Cell Biol 21:403–408

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beck T, Hall MN (1999) The TOR signalling pathway controls nuclear localization of nutrient-regulated transcription factors. Nature 402:689–692

    Article  CAS  PubMed  Google Scholar 

  • Berry DB, Gasch AP (2008) Stress-activated genomic expression changes serve a preparative role for impending stress in yeast. Mol Biol Cell 19:4580–4587

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berset C, Trachsel H, Altmann M (1998) The TOR (target of rapamycin) signal transduction pathway regulates the stability of translation initiation factor eIF4G in the yeast Saccharomyces cerevisiae. Proc Natl Acad Sci USA 95:4264–4269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bertram PG, Choi JH, Carvalho J, Ai W, Zeng C, Chan TF, Zheng XF (2000) Tripartite regulation of Gln3p by TOR, Ure2p, and phosphatases. J Biol Chem 275:35727–35733

    Article  CAS  PubMed  Google Scholar 

  • Binda M, Peli-Gulli MP, Bonfils G, Panchaud N, Urban J, Sturgill TW, Loewith R, De Virgilio C (2009) The Vam6 GEF controls TORC1 by activating the EGO complex. Mol Cell 35:563–573

    Article  CAS  PubMed  Google Scholar 

  • Bonfils G, Jaquenoud M, Bontron S, Ostrowicz C, Ungermann C, De Virgilio C (2012) Leucyl-tRNA synthetase controls TORC1 via the EGO complex. Mol Cell 46:105–110

    Article  CAS  PubMed  Google Scholar 

  • Brauer MJ, Huttenhower C, Airoldi EM, Rosenstein R, Matese JC, Gresham D, Boer VM, Troyanskaya OG, Botstein D (2008) Coordination of growth rate, cell cycle, stress response, and metabolic activity in yeast. Mol Biol Cell 19:352–367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Breitkreutz A, Choi H, Sharom JR, Boucher L, Neduva V, Larsen B, Lin ZY, Breitkreutz BJ, Stark C, Liu G et al (2010) A global protein kinase and phosphatase interaction network in yeast. Science 328:1043–1046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Broach JR (2012) Nutritional control of growth and development in yeast. Genetics 192:73–105

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Brown CR, Boeger H (2014) Nucleosomal promoter variation generates gene expression noise. Proc Natl Acad Sci USA 111:17893–17898

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Budovskaya YV, Stephan JS, Deminoff SJ, Herman PK (2005) An evolutionary proteomics approach identifies substrates of the cAMP-dependent protein kinase. Proc Natl Acad Sci USA 102:13933–13938

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burnetti AJ, Aydin M, Buchler NE (2016) Cell cycle start is coupled to entry into the yeast metabolic cycle across diverse strains and growth rates. Mol Biol Cell 27:64–74

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bystricky K, Heun P, Gehlen L, Langowski J, Gasser SM (2004) Long-range compaction and flexibility of interphase chromatin in budding yeast analyzed by high-resolution imaging techniques. Proc Natl Acad Sci USA 101:16495–16500

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cameroni E, Hulo N, Roosen J, Winderickx J, De Virgilio C (2004) The novel yeast PAS kinase Rim 15 orchestrates G0-associated antioxidant defense mechanisms. Cell Cycle 3:462–468

    Article  CAS  PubMed  Google Scholar 

  • Cardenas ME, Cutler NS, Lorenz MC, Di Como CJ, Heitman J (1999) The TOR signaling cascade regulates gene expression in response to nutrients. Genes Dev 13:3271–3279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chandrashekarappa DG, McCartney RR, Schmidt MC (2011) Subunit and domain requirements for adenylate-mediated protection of Snf1 kinase activation loop from dephosphorylation. J Biol Chem 286:44532–44541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chang YL, Tseng SF, Huang YC, Shen ZJ, Hsu PH, Hsieh MH, Yang CW, Tognetti S, Canal B, Subirana L et al (2017) Yeast Cip1 is activated by environmental stress to inhibit Cdk1-G1 cyclins via Mcm1 and Msn2/4. Nat Commun 8:56

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Charng YY, Liu HC, Liu NY, Hsu FC, Ko SS (2006) Arabidopsis Hsa32, a novel heat shock protein, is essential for acquired thermotolerance during long recovery after acclimation. Plant Physiol 140:1297–1305

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Z, Odstrcil EA, Tu BP, McKnight SL (2007) Restriction of DNA replication to the reductive phase of the metabolic cycle protects genome integrity. Science 316:1916–1919

    Article  CAS  PubMed  Google Scholar 

  • Cherkasova VA, Hinnebusch AG (2003) Translational control by TOR and TAP42 through dephosphorylation of eIF2alpha kinase GCN2. Genes Dev 17:859–872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chinnusamy V, Schumaker K, Zhu JK (2004) Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. J Exp Bot 55:225–236

    Article  CAS  PubMed  Google Scholar 

  • Colombo S, Ma P, Cauwenberg L, Winderickx J, Crauwels M, Teunissen A, Nauwelaers D, de Winde JH, Gorwa MF, Colavizza D et al (1998) Involvement of distinct G-proteins, Gpa2 and Ras, in glucose- and intracellular acidification-induced cAMP signalling in the yeast Saccharomyces cerevisiae. Embo J 17:3326–3341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cooper TG (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

    Article  CAS  PubMed  Google Scholar 

  • Costanzo M, Nishikawa JL, Tang X, Millman JS, Schub O, Breitkreuz K, Dewar D, Rupes I, Andrews B, Tyers M (2004) CDK activity antagonizes Whi5, an inhibitor of G1/S transcription in yeast. Cell 117:899–913

    Article  CAS  PubMed  Google Scholar 

  • Dalal CK, Cai L, Lin Y, Rahbar K, Elowitz MB (2014) Pulsatile dynamics in the yeast proteome. Curr Biol 24:2189–2194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Virgilio C (2012) The essence of yeast quiescence. FEMS Microbiol Rev 36:306–339

    Article  PubMed  CAS  Google Scholar 

  • De Virgilio C, Loewith R (2006) The TOR signalling network from yeast to man. Int J Biochem Cell Biol 38:1476–1481

    Article  PubMed  CAS  Google Scholar 

  • De Wever V, Reiter W, Ballarini A, Ammerer G, Brocard C (2005) A dual role for PP1 in sha** the Msn2-dependent transcriptional response to glucose starvation. Embo J 24:4115–4123

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dechant R, Binda M, Lee SS, Pelet S, Winderickx J, Peter M (2010) Cytosolic pH is a second messenger for glucose and regulates the PKA pathway through V-ATPase. EMBO J 29:2515–2526

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dubouloz F, Deloche O, Wanke V, Cameroni E, De Virgilio C (2005) The TOR and EGO protein complexes orchestrate microautophagy in yeast. Mol Cell 19:15–26

    Article  CAS  PubMed  Google Scholar 

  • Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209

    Article  CAS  PubMed  Google Scholar 

  • Duvel K, Santhanam A, Garrett S, Schneper L, Broach JR (2003) Multiple roles of Tap42 in mediating rapamycin-induced transcriptional changes in yeast. Mol Cell 11:1467–1478

    Article  PubMed  Google Scholar 

  • Elfving N, Chereji RV, Bharatula V, Bjorklund S, Morozov AV, Broach JR (2014) A dynamic interplay of nucleosome and Msn2 binding regulates kinetics of gene activation and repression following stress. Nucleic Acids Res 42:5468–5482

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eltschinger S, Loewith R (2016) TOR complexes and the maintenance of cellular homeostasis. Trends Cell Biol 26:148–159

    Article  CAS  PubMed  Google Scholar 

  • Ferrezuelo F, Colomina N, Palmisano A, Gari E, Gallego C, Csikasz-Nagy A, Aldea M (2012) The critical size is set at a single-cell level by growth rate to attain homeostasis and adaptation. Nat Commun 3:1012

    Article  PubMed  CAS  Google Scholar 

  • Freddolino PL, Yang J, Momen-Roknabadi A, Tavazoie S (2018) Stochastic tuning of gene expression enables cellular adaptation in the absence of pre-existing regulatory circuitry. eLife 7:e31867. https://doi.org/10.7554/eLife.31867

    Article  PubMed  PubMed Central  Google Scholar 

  • Gadura N, Robinson LC, Michels CA (2006) Glc7-Reg1 phosphatase signals to Yck1,2 casein kinase 1 to regulate transport activity and glucose-induced inactivation of Saccharomyces maltose permease. Genetics 172:1427–1439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garcia-Martinez J, Delgado-Ramos L, Ayala G, Pelechano V, Medina DA, Carrasco F, Gonzalez R, Andres-Leon E, Steinmetz L, Warringer J et al (2016) The cellular growth rate controls overall mRNA turnover, and modulates either transcription or degradation rates of particular gene regulons. Nucleic Acids Res 44:3643–3658

    Article  CAS  PubMed  Google Scholar 

  • Garmendia-Torres C, Goldbeter A, Jacquet M (2007) Nucleocytoplasmic oscillations of the yeast transcription factor Msn2: evidence for periodic PKA activation. Curr Biol 17:1044–1049

    Article  CAS  PubMed  Google Scholar 

  • Garrett S, Broach J (1989) Loss of Ras activity in Saccharomyces cerevisiae is suppressed by disruptions of a new kinase gene, YAKI, whose product may act downstream of the cAMP-dependent protein kinase. Genes Dev 3:1336–1348

    Article  CAS  PubMed  Google Scholar 

  • Gasch AP, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB, Storz G, Botstein D, Brown PO (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11:4241–4257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gasch AP, Yu FB, Hose J, Escalante LE, Place M, Bacher R, Kanbar J, Ciobanu D, Sandor L, Grigoriev IV et al (2017) Single-cell RNA sequencing reveals intrinsic and extrinsic regulatory heterogeneity in yeast responding to stress. PLoS Biol 15:e2004050

    Article  PubMed  PubMed Central  Google Scholar 

  • Gorner W, Durchschlag E, Martinez-Pastor MT, Estruch F, Ammerer G, Hamilton B, Ruis H, Schuller C (1998) Nuclear localization of the C2H2 zinc finger protein Msn2p is regulated by stress and protein kinase A activity. Genes Dev 12:586–597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gorner W, Durchschlag E, Wolf J, Brown EL, Ammerer G, Ruis H, Schuller C (2002) Acute glucose starvation activates the nuclear localization signal of a stress-specific yeast transcription factor. EMBO J 21:135–144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gray JV, Petsko GA, Johnston GC, Ringe D, Singer RA, Werner-Washburne M (2004) “Slee** beauty”: quiescence in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 68:187–206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gresham D, Boer VM, Caudy A, Ziv N, Brandt NJ, Storey JD, Botstein D (2011) System-level analysis of genes and functions affecting survival during nutrient starvation in Saccharomyces cerevisiae. Genetics 187:299–317

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guacci V, Hogan E, Koshland D (1997) Centromere position in budding yeast: evidence for anaphase A. Mol Biol Cell 8:957–972

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hansen AS, O’Shea EK (2013) Promoter decoding of transcription factor dynamics involves a trade-off between noise and control of gene expression. Mol Syst Biol 9:704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hao N, O’Shea EK (2012) Signal-dependent dynamics of transcription factor translocation controls gene expression. Nat Struct Mol Biol 19:31–39

    Article  CAS  Google Scholar 

  • Hao N, Budnik BA, Gunawardena J, O’Shea EK (2013) Tunable signal processing through modular control of transcription factor translocation. Science 339:460–464

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hartwell LH (1974) Saccharomyces cerevisiae cell cycle. Bacteriol Rev 38:164–198

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hartwell LH, Culotti J, Reid B (1970) Genetic control of the cell-division cycle in yeast. I. Detection of mutants. Proc Natl Acad Sci USA 66:352–359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hong SP, Leiper FC, Woods A, Carling D, Carlson M (2003) Activation of yeast Snf1 and mammalian AMP-activated protein kinase by upstream kinases. Proc Natl Acad Sci USA 100:8839–8843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huber A, Bodenmiller B, Uotila A, Stahl M, Wanka S, Gerrits B, Aebersold R, Loewith R (2009) Characterization of the rapamycin-sensitive phosphoproteome reveals that Sch9 is a central coordinator of protein synthesis. Genes Dev 23(16):1929–1943

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huber A, French SL, Tekotte H, Yerlikaya S, Stahl M, Perepelkina MP, Tyers M, Rougemont J, Beyer AL, Loewith R (2011) Sch9 regulates ribosome biogenesis via Stb3, Dot6 and Tod6 and the histone deacetylase complex RPD3L. EMBO J 30(15):3052–3064

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Humphrey EL, Shamji AF, Bernstein BE, Schreiber SL (2004) Rpd3p relocation mediates a transcriptional response to rapamycin in yeast. Chem Biol 11:295–299

    Article  CAS  PubMed  Google Scholar 

  • Isom DG, Page SC, Collins LB, Kapolka NJ, Taghon GJ, Dohlman HG (2017) Coordinated regulation of intracellular pH by two glucose sensing pathways in yeast. J Biol Chem 293(7):2318–2329

    Article  PubMed  PubMed Central  Google Scholar 

  • Jiang Y, Broach JR (1999) Tor proteins and protein phosphatase 2A reciprocally regulate Tap42 in controlling cell growth in yeast. EMBO J 18:2782–2792

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang Y, Davis C, Broach JR (1998) Efficient transition to growth on fermentable carbon sources in Saccharomyces cerevisiae requires signaling through the Ras pathway. EMBO J 17:6942–6951

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang Y, AkhavanAghdam Z, Tsimring LS, Hao N (2017) Coupled feedback loops control the stimulus-dependent dynamics of the yeast transcription factor Msn2. J Biol Chem 292:12366–12372

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson A, Skotheim JM (2013) Start and the restriction point. Curr Opin Cell Biol 25:717–723

    Article  CAS  PubMed  Google Scholar 

  • Johnston M, Carlson M (1992) Carbon regulation in Saccharomyces. In: Broach JR, Pringle JR, Jones EW (eds) Molecular and cellular biology of the yeast Saccharomyces. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY

    Google Scholar 

  • Johnston M, Kim JH (2005) Glucose as a hormone: receptor-mediated glucose sensing in the yeast Saccharomyces cerevisiae. Biochem Soc Trans 33:247–252

    Article  CAS  PubMed  Google Scholar 

  • Jorgensen P, Tyers M (2004) How cells coordinate growth and division. Curr Biol 14:R1014–R1027

    Article  CAS  PubMed  Google Scholar 

  • Jorgensen P, Rupes I, Sharom JR, Schneper L, Broach JR, Tyers M (2004) A dynamic transcriptional network communicates growth potential to ribosome synthesis and critical cell size. Genes Dev 18:2491–2505

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaniak A, Xue Z, Macool D, Kim JH, Johnston M (2004) Regulatory network connecting two glucose signal transduction pathways in Saccharomyces cerevisiae. Eukaryot Cell 3:221–231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karhumaa K, Wu B, Kielland-Brandt MC (2010) Conditions with high intracellular glucose inhibit sensing through glucose sensor Snf3 in Saccharomyces cerevisiae. J Cell Biochem 110:920–925

    Article  CAS  PubMed  Google Scholar 

  • Keren L, van Dijk D, Weingarten-Gabbay S, Davidi D, Jona G, Weinberger A, Milo R, Segal E (2015) Noise in gene expression is coupled to growth rate. Genome Res 25:1893–1902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klevecz RR, Bolen J, Forrest G, Murray DB (2004) A genomewide oscillation in transcription gates DNA replication and cell cycle. Proc Natl Acad Sci USA 101:1200–1205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klosinska MM, Crutchfield CA, Bradley PH, Rabinowitz JD, Broach JR (2011) Yeast cells can access distinct quiescent states. Genes Dev 25:336–349

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kresnowati MT, van Winden WA, Almering MJ, ten Pierick A, Ras C, Knijnenburg TA, Daran-Lapujade P, Pronk JT, Heijnen JJ, Daran JM (2006) When transcriptome meets metabolome: fast cellular responses of yeast to sudden relief of glucose limitation. Mol Syst Biol 2:49

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuchin S, Vyas VK, Kanter E, Hong SP, Carlson M (2003) Std1p (Msn3p) positively regulates the Snf1 kinase in Saccharomyces cerevisiae. Genetics 163:507–514

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kussell E, Kishony R, Balaban NQ, Leibler S (2005) Bacterial persistence: a model of survival in changing environments. Genetics 169:1807–1814

    Article  PubMed  PubMed Central  Google Scholar 

  • Lakshmanan J, Mosley AL, Ozcan S (2003) Repression of transcription by Rgt1 in the absence of glucose requires Std1 and Mth1. Curr Genet 44:19–25

    Article  CAS  PubMed  Google Scholar 

  • Laporte D, Courtout F, Salin B, Ceschin J, Sagot I (2013) An array of nuclear microtubules reorganizes the budding yeast nucleus during quiescence. J Cell Biol 203:585–594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laporte D, Courtout F, Tollis S, Sagot I (2016) Quiescent Saccharomyces cerevisiae forms telomere hyperclusters at the nuclear membrane vicinity through a multifaceted mechanism involving Esc1, the Sir complex, and chromatin condensation. Mol Biol Cell 27:1875–1884

    Article  PubMed  PubMed Central  Google Scholar 

  • Lascaris R, Bussemaker HJ, Boorsma A, Piper M, van der Spek H, Grivell L, Blom J (2003) Hap4p overexpression in glucose-grown Saccharomyces cerevisiae induces cells to enter a novel metabolic state. Genome Biol 4:R3

    Article  PubMed  Google Scholar 

  • Lavoie H, Whiteway M (2008) Increased respiration in the sch9Delta mutant is required for increasing chronological life span but not replicative life span. Eukaryot Cell 7:1127–1135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laxman S, Sutter BM, Tu BP (2014) Methionine is a signal of amino acid sufficiency that inhibits autophagy through the methylation of PP2A. Autophagy 10:386–387

    Article  CAS  PubMed  Google Scholar 

  • Lee CD, Tu BP (2015) Glucose-regulated phosphorylation of the PUF protein Puf3 regulates the translational fate of its bound mRNAs and association with RNA granules. Cell Rep 11:1638–1650

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee P, Cho BR, Joo HS, Hahn JS (2008) Yeast Yak1 kinase, a bridge between PKA and stress-responsive transcription factors, Hsf1 and Msn2/Msn4. Mol Microbiol 70:882–895

    CAS  PubMed  Google Scholar 

  • Lee P, Paik SM, Shin CS, Huh WK, Hahn JS (2011) Regulation of yeast Yak1 kinase by PKA and autophosphorylation-dependent 14-3-3 binding. Mol Microbiol 79:633–646

    Article  CAS  PubMed  Google Scholar 

  • Lemaire K, Van de Velde S, Van Dijck P, Thevelein JM (2004) Glucose and sucrose act as agonist and mannose as antagonist ligands of the G protein-coupled receptor Gpr1 in the yeast Saccharomyces cerevisiae. Mol Cell 16:293–299

    Article  CAS  PubMed  Google Scholar 

  • Lempiainen H, Uotila A, Urban J, Dohnal I, Ammerer G, Loewith R, Shore D (2009) Sfp1 interaction with TORC1 and Mrs6 reveals feedback regulation on TOR signaling. Mol Cell 33:704–716

    Article  CAS  PubMed  Google Scholar 

  • Levy S, Barkai N (2009) Coordination of gene expression with growth rate: a feedback or a feed-forward strategy? FEBS Lett 583:3974–3978

    Article  CAS  PubMed  Google Scholar 

  • Levy S, Ihmels J, Carmi M, Weinberger A, Friedlander G, Barkai N (2007) Strategy of transcription regulation in the budding yeast. PLoS One 2:e250

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Levy SF, Ziv N, Siegal ML (2012) Bet hedging in yeast by heterogeneous, age-correlated expression of a stress protectant. PLoS Biol 10:e1001325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li J, Yan G, Liu S, Jiang T, Zhong M, Yuan W, Chen S, Zheng Y, Jiang Y, Jiang Y (2017) Target of rapamycin complex 1 and Tap42-associated phosphatases are required for sensing changes in nitrogen conditions in the yeast Saccharomyces cerevisiae. Mol Microbiol 106:938–948

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liko D, Conway MK, Grunwald DS, Heideman W (2010) Stb3 plays a role in the glucose-induced transition from quiescence to growth in Saccharomyces cerevisiae. Genetics 185(3):797–810

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin Y, Sohn CH, Dalal CK, Cai L, Elowitz MB (2015) Combinatorial gene regulation by modulation of relative pulse timing. Nature 527:54–58

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lippman SI, Broach JR (2009) Protein kinase A and TORC1 activate genes for ribosomal biogenesis by inactivating repressors encoded by Dot6 and its homolog Tod6. Proc Natl Acad Sci USA 106:19928–19933

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Z, Butow RA (1999) A transcriptional switch in the expression of yeast tricarboxylic acid cycle genes in response to a reduction or loss of respiratory function. Mol Cell Biol 19:6720–6728

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Z, Butow RA (2006) Mitochondrial retrograde signaling. Annu Rev Genet 40:159–185

    Article  CAS  PubMed  Google Scholar 

  • Lu C, Brauer MJ, Botstein D (2009) Slow growth induces heat-shock resistance in normal and respiratory-deficient yeast. Mol Biol Cell 20:891–903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Magasanik B, Kaiser CA (2002) Nitrogen regulation in Saccharomyces cerevisiae. Gene 290:1–18

    Article  CAS  PubMed  Google Scholar 

  • Malcher M, Schladebeck S, Mosch HU (2011) The Yak1 protein kinase lies at the center of a regulatory cascade affecting adhesive growth and stress resistance in Saccharomyces cerevisiae. Genetics 187:717–730

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marion RM, Regev A, Segal E, Barash Y, Koller D, Friedman N, O’Shea EK (2004) Sfp1 is a stress- and nutrient-sensitive regulator of ribosomal protein gene expression. Proc Natl Acad Sci USA 101:14315–14322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matsumoto H, Hamada N, Takahashi A, Kobayashi Y, Ohnishi T (2007) Vanguards of paradigm shift in radiation biology: radiation-induced adaptive and bystander responses. J Radiat Res (Tokyo) 48:97–106

    Article  CAS  Google Scholar 

  • Mayer FV, Heath R, Underwood E, Sanders MJ, Carmena D, McCartney RR, Leiper FC, **ao B, **g C, Walker PA et al (2011) ADP regulates SNF1, the Saccharomyces cerevisiae homolog of AMP-activated protein kinase. Cell Metab 14:707–714

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moore N, Houghton J, Lyle S (2012) Slow-cycling therapy-resistant cancer cells. Stem Cells Dev 21:1822–1830

    Article  CAS  PubMed  Google Scholar 

  • Moreno-Torres M, Jaquenoud M, De Virgilio C (2015) TORC1 controls G1-S cell cycle transition in yeast via Mpk1 and the greatwall kinase pathway. Nat Commun 6:8256

    Article  PubMed  Google Scholar 

  • Moriya H, Shimizu-Yoshida Y, Omori A, Iwashita S, Katoh M, Sakai A (2001) Yak1p, a DYRK family kinase, translocates to the nucleus and phosphorylates yeast Pop2p in response to a glucose signal. Genes Dev 15:1217–1228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mosley AL, Lakshmanan J, Aryal BK, Ozcan S (2003) Glucose-mediated phosphorylation converts the transcription factor Rgt1 from a repressor to an activator. J Biol Chem 278:10322–10327

    Article  CAS  PubMed  Google Scholar 

  • Nath N, McCartney RR, Schmidt MC (2003) Yeast Pak1 kinase associates with and activates Snf1. Mol Cell Biol 23:3909–3917

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Neklesa TK, Davis RW (2009) A genome-wide screen for regulators of TORC1 in response to amino acid starvation reveals a conserved Npr2/3 complex. PLoS Genet 5:e1000515

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nicastro R, Sardu A, Panchaud N, De Virgilio C (2017) The architecture of the rag GTPase signaling network. Biomolecules 7(3):48

    Article  PubMed Central  CAS  Google Scholar 

  • Pedruzzi I, Burckert N, Egger P, De Virgilio C (2000) Saccharomyces cerevisiae Ras/cAMP pathway controls post-diauxic shift element-dependent transcription through the zinc finger protein Gis1. Embo J 19:2569–2579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pedruzzi I, Dubouloz F, Cameroni E, Wanke V, Roosen J, Winderickx J, De Virgilio C (2003) TOR and PKA signaling pathways converge on the protein kinase Rim15 to control entry into G0. Mol Cell 12:1607–1613

    Article  CAS  PubMed  Google Scholar 

  • Peeters T, Louwet W, Gelade R, Nauwelaers D, Thevelein JM, Versele M (2006) Kelch-repeat proteins interacting with the Galpha protein Gpa2 bypass adenylate cyclase for direct regulation of protein kinase A in yeast. Proc Natl Acad Sci USA 103:13034–13039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petrenko N, Chereji RV, McClean MN, Morozov AV, Broach JR (2013) Noise and interlocking signaling pathways promote distinct transcription factor dynamics in response to different stresses. Mol Biol Cell 24:2045–2057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ptacek J, Devgan G, Michaud G, Zhu H, Zhu X, Fasolo J, Guo H, Jona G, Breitkreutz A, Sopko R et al (2005) Global analysis of protein phosphorylation in yeast. Nature 438:679–684

    Article  CAS  PubMed  Google Scholar 

  • Radmaneshfar E, Kaloriti D, Gustin MC, Gow NA, Brown AJ, Grebogi C, Romano MC, Thiel M (2013) From START to FINISH: the influence of osmotic stress on the cell cycle. PLoS One 8:e68067

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramachandran V, Shah KH, Herman PK (2011) The cAMP-dependent protein kinase signaling pathway is a key regulator of P body foci formation. Mol Cell 43:973–981

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reinders A, Burckert N, Boller T, Wiemken A, De Virgilio C (1998) Saccharomyces cerevisiae cAMP-dependent protein kinase controls entry into stationary phase through the Rim15p protein kinase. Genes Dev 12:2943–2955

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roosen J, Engelen K, Marchal K, Mathys J, Griffioen G, Cameroni E, Thevelein JM, De Virgilio C, De Moor B, Winderickx J (2005) PKA and Sch9 control a molecular switch important for the proper adaptation to nutrient availability. Mol Microbiol 55:862–880

    Article  CAS  PubMed  Google Scholar 

  • Ruiz A, Xu X, Carlson M (2011) Roles of two protein phosphatases, Reg1-Glc7 and Sit4, and glycogen synthesis in regulation of SNF1 protein kinase. Proc Natl Acad Sci USA 108:6349–6354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rutledge MT, Russo M, Belton JM, Dekker J, Broach JR (2015) The yeast genome undergoes significant topological reorganization in quiescence. Nucleic Acids Res 43:8299–8313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schafer G, McEvoy CR, Patterton HG (2008) The Saccharomyces cerevisiae linker histone Hho1p is essential for chromatin compaction in stationary phase and is displaced by transcription. Proc Natl Acad Sci USA 105:14838–14843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmoller KM, Skotheim JM (2015) The biosynthetic basis of cell size control. Trends Cell Biol 25:793–802

    Article  PubMed  PubMed Central  Google Scholar 

  • Schmoller KM, Turner JJ, Koivomagi M, Skotheim JM (2015) Dilution of the cell cycle inhibitor Whi5 controls budding-yeast cell size. Nature 526:268–272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shah KH, Zhang B, Ramachandran V, Herman PK (2013) Processing body and stress granule assembly occur by independent and differentially regulated pathways in Saccharomyces cerevisiae. Genetics 193:109–123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Silverman SJ, Petti AA, Slavov N, Parsons L, Briehof R, Thiberge SY, Zenklusen D, Gandhi SJ, Larson DR, Singer RH et al (2010) Metabolic cycling in single yeast cells from unsynchronized steady-state populations limited on glucose or phosphate. Proc Natl Acad Sci USA 107:6946–6951

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simpson-Lavy K, Xu T, Johnston M, Kupiec M (2017) The Std1 activator of the Snf1/AMPK kinase controls glucose response in yeast by a regulated protein aggregation. Mol Cell 68(6):1120–1133

    Article  CAS  PubMed  Google Scholar 

  • Singh J, Tyers M (2009) A Rab escort protein integrates the secretion system with TOR signaling and ribosome biogenesis. Genes Dev 23:1944–1958

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Slavov N, Botstein D (2011) Coupling among growth rate response, metabolic cycle, and cell division cycle in yeast. Mol Biol Cell 22:1997–2009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smets B, Ghillebert R, De Snijder P, Binda M, Swinnen E, De Virgilio C, Winderickx J (2010) Life in the midst of scarcity: adaptations to nutrient availability in Saccharomyces cerevisiae. Curr Genet 56:1–32

    Article  CAS  PubMed  Google Scholar 

  • Smith A, Ward MP, Garrett S (1998) Yeast PKA represses Msn2p/Msn4p-dependent gene expression to regulate growth, stress response and glycogen accumulation. EMBO J 17:3556–3564

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Snowdon C, Johnston M (2016) A novel role for yeast casein kinases in glucose sensing and signaling. Mol Biol Cell 27:3369–3375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suel GM, Garcia-Ojalvo J, Liberman LM, Elowitz MB (2006) An excitable gene regulatory circuit induces transient cellular differentiation. Nature 440:545–550

    Article  PubMed  CAS  Google Scholar 

  • Suel GM, Kulkarni RP, Dworkin J, Garcia-Ojalvo J, Elowitz MB (2007) Tunability and noise dependence in differentiation dynamics. Science 315:1716–1719

    Article  PubMed  CAS  Google Scholar 

  • Sutherland CM, Hawley SA, McCartney RR, Leech A, Stark MJ, Schmidt MC, Hardie DG (2003) Elm1p is one of three upstream kinases for the Saccharomyces cerevisiae SNF1 complex. Curr Biol 13:1299–1305

    Article  CAS  PubMed  Google Scholar 

  • Sutter BM, Wu X, Laxman S, Tu BP (2013) Methionine inhibits autophagy and promotes growth by inducing the SAM-responsive methylation of PP2A. Cell 154:403–415

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tate JJ, Cooper TG (2003) Tor1/2 regulation of retrograde gene expression in Saccharomyces cerevisiae derives indirectly as a consequence of alterations in ammonia metabolism. J Biol Chem 278:36924–36933

    Article  CAS  PubMed  Google Scholar 

  • Tate JJ, Georis I, Feller A, Dubois E, Cooper TG (2009) Rapamycin-induced Gln3 dephosphorylation is insufficient for nuclear localization: Sit4 and PP2A phosphatases are regulated and function differently. J Biol Chem 284:2522–2534

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tate JJ, Buford D, Rai R, Cooper TG (2017) General amino acid control and 14-3-3 proteins Bmh1/2 are required for nitrogen catabolite repression-sensitive regulation of Gln3 and Gat1 localization. Genetics 205:633–655

    Article  CAS  PubMed  Google Scholar 

  • Thomson JM, Gaucher EA, Burgan MF, De Kee DW, Li T, Aris JP, Benner SA (2005) Resurrecting ancestral alcohol dehydrogenases from yeast. Nat Genet 37:630–635

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Toda T, Cameron S, Sass P, Zoller M, Wigler M (1987) Three different genes in S. cerevisiae encode the catalytic subunits of the cAMP-dependent protein kinase. Cell 50:277–287

    Article  CAS  PubMed  Google Scholar 

  • Toda T, Cameron S, Sass P, Wigler M (1988) SCH9, a gene of Saccharomyces cerevisiae that encodes a protein distinct from, but functionally and structurally related to, cAMP-dependent protein kinase catalytic subunits. Genes Dev 2:517–527

    Article  CAS  PubMed  Google Scholar 

  • Tu J, Carlson M (1995) REG1 binds to protein phosphatase type 1 and regulates glucose repression in Saccharomyces cerevisiae. EMBO J 14:5939–5946

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tu BP, Kudlicki A, Rowicka M, McKnight SL (2005) Logic of the yeast metabolic cycle: temporal compartmentalization of cellular processes. Science 310:1152–1158

    Article  CAS  PubMed  Google Scholar 

  • Turner JJ, Ewald JC, Skotheim JM (2012) Cell size control in yeast. Curr Biol 22:R350–R359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Urban J, Soulard A, Huber A, Lippman S, Mukhopadhyay D, Deloche O, Wanke V, Anrather D, Ammerer G, Riezman H et al (2007) Sch9 is a major target of TORC1 in Saccharomyces cerevisiae. Mol Cell 26:663–674

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Pierce M, Schneper L, Guldal CG, Zhang X, Tavazoie S, Broach JR (2004) Ras and Gpa2 mediate one branch of a redundant glucose signaling pathway in yeast. PLoS Biol 2:E128

    Article  PubMed  PubMed Central  Google Scholar 

  • Wanke V, Pedruzzi I, Cameroni E, Dubouloz F, De Virgilio C (2005) Regulation of G0 entry by the Pho80-Pho85 cyclin-CDK complex. EMBO J 24:4271–4278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Werner-Washburne M, Braun E, Johnston GC, Singer RA (1993) Stationary phase in the yeast Saccharomyces cerevisiae. Microbiol Rev 57:383–401

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu B, Ottow K, Poulsen P, Gaber RF, Albers E, Kielland-Brandt MC (2006) Competitive intra- and extracellular nutrient sensing by the transporter homologue Ssy1p. J Cell Biol 173:327–331

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xue Y, Batlle M, Hirsch JP (1998) GPR1 encodes a putative G protein-coupled receptor that associates with the Gpa2p Galpha subunit and functions in a Ras-independent pathway. EMBO J 17:1996–2007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan G, Lai Y, Jiang Y (2012) The TOR complex 1 is a direct target of Rho1 GTPase. Mol Cell 45:743–753

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Z, Klionsky DJ (2009) An overview of the molecular mechanism of autophagy. Curr Top Microbiol Immunol 335:1–32

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yorimitsu T, Zaman S, Broach JR, Klionsky DJ (2007) Protein kinase A and Sch9 cooperatively regulate induction of autophagy in Saccharomyces cerevisiae. Mol Biol Cell 18:4180–4189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zaman S, Lippman SI, Schneper L, Slonim N, Broach JR (2009) Glucose regulates transcription in yeast through a network of signaling pathways. Mol Syst Biol 5:245

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhao H, Wang JQ, Shimohata T, Sun G, Yenari MA, Sapolsky RM, Steinberg GK (2007) Conditions of protection by hypothermia and effects on apoptotic pathways in a rat model of permanent middle cerebral artery occlusion. J Neurosurg 107:636–641

    Article  CAS  PubMed  Google Scholar 

  • Zheng Y, Jiang Y (2005) The yeast phosphotyrosyl phosphatase activator is part of the Tap42-phosphatase complexes. Mol Biol Cell 16:2119–2127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Bharatula, V., Broach, J.R. (2018). The Nutrient Stress Response in Yeast. In: Skoneczny, M. (eds) Stress Response Mechanisms in Fungi. Springer, Cham. https://doi.org/10.1007/978-3-030-00683-9_4

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