1932

Abstract

Most cells live in environments that are permissive for proliferation only a small fraction of the time. Entering quiescence enables cells to survive long periods of nondivision and reenter the cell cycle when signaled to do so. Here, we describe what is known about the molecular basis for quiescence in , with emphasis on the progress made in the last decade. Quiescence is triggered by depletion of an essential nutrient. It begins well before nutrient exhaustion, and there is extensive crosstalk between signaling pathways to ensure that all proliferation-specific activities are stopped when any one essential nutrient is limiting. Every aspect of gene expression is modified to redirect and conserve resources. Chromatin structure and composition change on a global scale, from histone modifications to three-dimensional chromatin structure. Thousands of proteins and RNAs aggregate, forming unique structures with unique fates, and the cytoplasm transitions to a glass-like state.

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2022-11-30
2024-05-09
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Literature Cited

  1. 1.
    Adachi A, Koizumi M, Ohsumi Y. 2017. Autophagy induction under carbon starvation conditions is negatively regulated by carbon catabolite repression. J. Biol. Chem. 292:19905–18
    [Google Scholar]
  2. 2.
    Alfatah M, Wong JH, Krishnan VG, Lee YC, Sin QF et al. 2021. TORC1 regulates the transcriptional response to glucose and developmental cycle via the Tap42-Sit4-Rrd1/2 pathway in Saccharomyces cerevisiae. BMC Biol 19:95
    [Google Scholar]
  3. 3.
    Allen C, Büttner S, Aragon AD, Thomas JA, Meirelles O et al. 2006. Isolation of quiescent and nonquiescent cells from yeast stationary-phase cultures. J. Cell Biol. 174:89–100
    [Google Scholar]
  4. 4.
    Alver B, Kelly MK, Kirkpatrick DT. 2013. Novel checkpoint pathway organization promotes genome stability in stationary-phase yeast cells. Mol. Cell. Biol. 33:457–72
    [Google Scholar]
  5. 5.
    Alvers AL, Fishwick LK, Wood MS, Hu D, Chung HS et al. 2009. Autophagy and amino acid homeostasis are required for chronological longevity in Saccharomyces cerevisiae. Aging Cell 8:353–69
    [Google Scholar]
  6. 6.
    Alvers AL, Wood MS, Hu D, Kaywell AC, Dunn WA Jr., Aris JP. 2009. Autophagy is required for extension of yeast chronological life span by rapamycin. Autophagy 5:847–49
    [Google Scholar]
  7. 7.
    Argüello-Miranda O, Liu Y, Wood NE, Kositangool P, Doncic A. 2018. Integration of multiple metabolic signals determines cell fate prior to commitment. Mol. Cell 71:733–44.e11
    [Google Scholar]
  8. 8.
    Argüello-Miranda O, Marchand AJ, Kennedy T, Russo MAX, Noh J. 2022. Cell cycle–independent integration of stress signals by Xbp1 promotes Non-G1/G0 quiescence entry. J. Cell Biol. 221:e202103171
    [Google Scholar]
  9. 9.
    Austin S, Mayer A. 2020. Phosphate homeostasis—a vital metabolic equilibrium maintained through the INPHORS signaling pathway. Front. Microbiol. 11:1367
    [Google Scholar]
  10. 10.
    Bajorek M, Finley D, Glickman MH. 2003. Proteasome disassembly and downregulation is correlated with viability during stationary phase. Curr. Biol. 13:1140–44
    [Google Scholar]
  11. 11.
    Bankapalli K, Saladi S, Awadia SS, Goswami AV, Samaddar M, D'Silva P 2015. Robust glyoxalase activity of Hsp31, a ThiJ/DJ-1/PfpI family member protein, is critical for oxidative stress resistance in Saccharomyces cerevisiae. J. Biol. Chem. 290:26491–507
    [Google Scholar]
  12. 12.
    Bankapalli K, Vishwanathan V, Susarla G, Sunayana N, Saladi SD et al. 2020. Redox-dependent regulation of mitochondrial dynamics by DJ-1 paralogs in Saccharomyces cerevisiae. Redox Biol. 32:101451
    [Google Scholar]
  13. 13.
    Beck T, Hall MN. 1999. The TOR signalling pathway controls nuclear localization of nutrient-regulated transcription factors. Nature 402:689–92
    [Google Scholar]
  14. 14.
    Berger SE, Nolte AM, Kamiya E, Hines JK. 2020. Three J-proteins impact Hsp104-mediated variant-specific prion elimination: a new critical role for a low-complexity domain. Curr. Genet. 66:51–58
    [Google Scholar]
  15. 15.
    Boer VM, Amini S, Botstein D. 2008. Influence of genotype and nutrition on survival and metabolism of starving yeast. PNAS 105:6930–35
    [Google Scholar]
  16. 16.
    Boer VM, de Winde JH, Pronk JT, Piper MDW. 2003. The genome-wide transcriptional responses of Saccharomyces cerevisiae grown on glucose in aerobic chemostat cultures limited for carbon, nitrogen, phosphorus, or sulfur. J. Biol. Chem. 278:3265–74
    [Google Scholar]
  17. 17.
    Bojsen R, Regenberg B, Folkesson A. 2017. Persistence and drug tolerance in pathogenic yeast. Curr. Genet. 63:19–22
    [Google Scholar]
  18. 18.
    Bonifati V, Rizzu P, van Baren MJ, Schaap O, Breedveld GJ et al. 2003. Mutations in the DJ-1 gene associated with autosomal recessive early-onset parkinsonism. Science 299:256–59
    [Google Scholar]
  19. 19.
    Bontron S, Jaquenoud M, Vaga S, Talarek N, Bodenmiller B et al. 2013. Yeast endosulfines control entry into quiescence and chronological life span by inhibiting protein phosphatase 2A. Cell Rep 3:16–22
    [Google Scholar]
  20. 20.
    Boucherie H. 1985. Protein synthesis during transition and stationary phases under glucose limitation in Saccharomyces cerevisiae. J. Bacteriol. 161:385–92
    [Google Scholar]
  21. 21.
    Boy-Marcotte E, Ikonomi P, Jacquet M. 1996. SDC25, a dispensable Ras guanine nucleotide exchange factor of Saccharomyces cerevisiae differs from CDC25 by its regulation. Mol. Biol. Cell 7:529–39
    [Google Scholar]
  22. 22.
    Bresson S, Tuck A, Staneva D, Tollervey D. 2017. Nuclear RNA decay pathways aid rapid remodeling of gene expression in yeast. Mol. Cell 65:787–800.e5
    [Google Scholar]
  23. 23.
    Broach JR. 2012. Nutritional control of growth and development in yeast. Genetics 192:73–105
    [Google Scholar]
  24. 24.
    Buchan JR, Muhlrad D, Parker R. 2008. P bodies promote stress granule assembly in Saccharomyces cerevisiae. J. Cell Biol. 183:441–55
    [Google Scholar]
  25. 25.
    Buchan JR, Yoon JH, Parker R. 2011. Stress-specific composition, assembly and kinetics of stress granules in Saccharomyces cerevisiae. J. Cell Sci. 124:228–39
    [Google Scholar]
  26. 26.
    Budovskaya YV, Stephan JS, Reggiori F, Klionsky DJ, Herman PK. 2004. The Ras/cAMP-dependent protein kinase signaling pathway regulates an early step of the autophagy process in Saccharomyces cerevisiae. J. Biol. Chem. 279:20663–71
    [Google Scholar]
  27. 27.
    Canadell D, Gonzalez A, Casado C, Arino J. 2015. Functional interactions between potassium and phosphate homeostasis in Saccharomyces cerevisiae. Mol. Microbiol. 95:555–72
    [Google Scholar]
  28. 28.
    Casey JR, Grinstein S, Orlowski J. 2010. Sensors and regulators of intracellular pH. Nat. Rev. Mol. Cell Biol. 11:50–61
    [Google Scholar]
  29. 29.
    Chakrabortee S, Byers JS, Jones S, Garcia DM, Bhullar B et al. 2016. Intrinsically disordered proteins drive emergence and inheritance of biological traits. Cell 167:369–81.e12
    [Google Scholar]
  30. 30.
    Chakravarty AK, Jarosz DF. 2018. More than just a phase: prions at the crossroads of epigenetic inheritance and evolutionary change. J. Mol. Biol. 430:4607–18
    [Google Scholar]
  31. 31.
    Chang Y-W, Howard SC, Budovskaya YV, Rine J, Herman PK. 2001. The rye mutants identify a role for Ssn/Srb proteins of the RNA polymerase II holoenzyme during stationary phase entry in Saccharomyces cerevisiae. Genetics 157:17–26
    [Google Scholar]
  32. 32.
    Chen X, Wang G, Zhang Y, Dayhoff-Brannigan M, Diny NL et al. 2018. Whi2 is a conserved negative regulator of TORC1 in response to low amino acids. PLOS Genet 14:e1007592
    [Google Scholar]
  33. 33.
    Chernoff YO, Lindquist SL, Ono B-I, Inge-Vechtomov SG, Liebman SW. 1995. Role of the chaperone protein Hsp104 in propagation of the yeast prion-like factor [psi+]. Science 268:880–84
    [Google Scholar]
  34. 34.
    Cheung TH, Rando TA. 2013. Molecular regulation of stem cell quiescence. Nat. Rev. Mol. Cell Biol. 14:329–40
    [Google Scholar]
  35. 35.
    Coccetti P, Nicastro R, Tripodi F. 2018. Conventional and emerging roles of the energy sensor Snf1/AMPK in Saccharomyces cerevisiae. Microb. Cell 5:482–94
    [Google Scholar]
  36. 36.
    Coyle S, Kroll E. 2008. Starvation induces genomic rearrangements and starvation-resilient phenotypes in yeast. Mol. Biol. Evol. 25:310–18
    [Google Scholar]
  37. 37.
    Cucinotta CE, Dell RH, Braceros KCA, Tsukiyama T. 2021. RSC primes the quiescent genome for hypertranscription upon cell-cycle re-entry. eLife 10:e67033
    [Google Scholar]
  38. 38.
    Davidson GS, Joe RM, Roy S, Meirelles O, Allen CP et al. 2011. The proteomics of quiescent and nonquiescent cell differentiation in yeast stationary-phase cultures. Mol. Biol. Cell 22:988–98
    [Google Scholar]
  39. 39.
    De Virgilio C. 2011. The essence of yeast quiescence. FEMS Microbiol. Rev. 36:306–39
    [Google Scholar]
  40. 40.
    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 29:2515–26
    [Google Scholar]
  41. 41.
    Deprez M-A, Eskes E, Winderickx J, Wilms T. 2018. The TORC1-Sch9 pathway as a crucial mediator of chronological lifespan in the yeast Saccharomyces cerevisiae. FEMS Yeast Res 18:foy048
    [Google Scholar]
  42. 42.
    DeRisi JL, Iyer VR, Brown PO. 1997. Exploring the metabolic and genetic control of gene expression on a genomic scale. Science 278:680–86
    [Google Scholar]
  43. 43.
    Dong L, Xu CW. 2004. Carbohydrates induce mono-ubiquitination of H2B in yeast. J. Biol. Chem. 279:1577–80
    [Google Scholar]
  44. 44.
    Ebrahimi M, Habernig L, Broeskamp F, Aufschnaiter A, Diessl J et al. 2021. Phosphate restriction promotes longevity via activation of autophagy and the multivesicular body pathway. Cells 10:3161
    [Google Scholar]
  45. 45.
    Enriquez-Hesles E, Smith DL Jr., Maqani N, Wierman MB, Sutcliffe MD et al. 2021. A cell-nonautonomous mechanism of yeast chronological aging regulated by caloric restriction and one-carbon metabolism. J. Biol. Chem. 296:100125
    [Google Scholar]
  46. 46.
    Erjavec N, Larsson L, Grantham J, Nystrom T. 2007. Accelerated aging and failure to segregate damaged proteins in Sir2 mutants can be suppressed by overproducing the protein aggregation-remodeling factor Hsp104p. Genes Dev 21:2410–21
    [Google Scholar]
  47. 47.
    Evertts AG, Manning AL, Wang X, Dyson NJ, Garcia BA, Coller HA. 2013. H4K20 methylation regulates quiescence and chromatin compaction. Mol. Biol. Cell 24:3025–37
    [Google Scholar]
  48. 48.
    Finley D, Bartel B, Varshavsky A 1989. The tails of ubiquitin precursors are ribosomal proteins whose fusion to ubiquitin facilitates ribosome biogenesis. Nature 338:394–401
    [Google Scholar]
  49. 49.
    Finley D, Ozkaynak E, Varshavsky A. 1987. The yeast polyubiquitin gene is essential for resistance to high temperatures, starvation, and other stresses. Cell 48:1035–46
    [Google Scholar]
  50. 50.
    Foat BC, Houshmandi SS, Olivas WM, Bussemaker HJ. 2005. Profiling condition-specific, genome-wide regulation of mRNA stability in yeast. PNAS 102:17675–80
    [Google Scholar]
  51. 51.
    Friedson B, Cooper KF. 2021. Cdk8 kinase module: a mediator of life and death decisions in times of stress. Microorganisms 9:2152
    [Google Scholar]
  52. 52.
    Friis RM, Wu BP, Reinke SN, Hockman DJ, Sykes BD, Schultz MC. 2009. A glycolytic burst drives glucose induction of global histone acetylation by picNuA4 and SAGA. Nucleic Acids Res 37:3969–80
    [Google Scholar]
  53. 53.
    Fuge EK, Braun EL, Werner-Washburne M. 1994. Protein synthesis in long-term stationary-phase cultures of Saccharomyces cerevisiae. J. Bacteriol. 176:5802–13
    [Google Scholar]
  54. 54.
    Furuta S, Hidaka E, Ogata A, Yokota S, Kamata T. 2004. Ras is involved in the negative control of autophagy through the class I PI3-kinase. Oncogene 23:3898–904
    [Google Scholar]
  55. 55.
    Galello F, Pautasso C, Reca S, Cañonero L, Portela P et al. 2017. Transcriptional regulation of the protein kinase a subunits in Saccharomyces cerevisiae during fermentative growth. Yeast 34:495–508
    [Google Scholar]
  56. 56.
    Gasch AP, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB et al. 2000. Genomic expression programs in the response of yeast cells to environmental changes. Mol. Biol. Cell 11:4241–57
    [Google Scholar]
  57. 57.
    Gilbert WV, Zhou K, Butler TK, Doudna JA. 2007. Cap-independent translation is required for starvation-induced differentiation in yeast. Science 317:1224–27
    [Google Scholar]
  58. 58.
    Glover JR, Lindquist S. 1998. Hsp104, Hsp70, and Hsp40: a novel chaperone system that rescues previously aggregated proteins. Cell 94:73–82
    [Google Scholar]
  59. 59.
    Gu ZC, Wu E, Sailer C, Jando J, Styles E et al. 2017. Ubiquitin orchestrates proteasome dynamics between proliferation and quiescence in yeast. Mol. Biol. Cell 28:2479–91
    [Google Scholar]
  60. 60.
    Guidi M, Ruault M, Marbouty M, Loïodice I, Cournac A et al. 2015. Spatial reorganization of telomeres in long-lived quiescent cells. Genome Biol 16:206
    [Google Scholar]
  61. 61.
    Gurvich Y, Leshkowitz D, Barkai N. 2017. Dual role of starvation signaling in promoting growth and recovery. PLOS Biol 15:e2002039
    [Google Scholar]
  62. 62.
    Gutin J, Joseph-Strauss D, Sadeh A, Shalom E, Friedman N 2019. Genetic screen of the yeast environmental stress response dynamics uncovers distinct regulatory phases. Mol. Syst. Biol. 15:e8939
    [Google Scholar]
  63. 63.
    Halfmann R, Lindquist S. 2010. Epigenetics in the extreme: prions and the inheritance of environmentally acquired traits. Science 330:629–32
    [Google Scholar]
  64. 64.
    Harris N, MacLean M, Hatzianthis K, Panaretou B, Piper PW. 2001. Increasing Saccharomyces cerevisiae stress resistance, through the overactivation of the heat shock response resulting from defects in the Hsp90 chaperone, does not extend replicative life span but can be associated with slower chronological ageing of nondividing cells. Mol. Genet. Genom. 265:258–63
    [Google Scholar]
  65. 65.
    Haslbeck M, Braun N, Stromer T, Richter B, Model N et al. 2004. Hsp42 is the general small heat shock protein in the cytosol of Saccharomyces cerevisiae. EMBO J 23:638–49
    [Google Scholar]
  66. 66.
    Hassan AH, Prochasson P, Neely KE, Galasinski SC, Chandy M et al. 2002. Function and selectivity of bromodomains in anchoring chromatin-modifying complexes to promoter nucleosomes. Cell 111:369–79
    [Google Scholar]
  67. 67.
    Henry SA. 1973. Death resulting from fatty acid starvation in yeast. J. Bacteriol. 116:1293–303
    [Google Scholar]
  68. 68.
    Hinnebusch AG. 2005. Translational regulation of GCN4 and the general amino acid control of yeast. Annu. Rev. Microbiol. 59:407–50
    [Google Scholar]
  69. 69.
    Holmes DL, Lancaster AK, Lindquist S, Halfmann R. 2013. Heritable remodeling of yeast multicellularity by an environmentally responsive prion. Cell 153:153–65
    [Google Scholar]
  70. 70.
    Horvathova I, Voigt F, Kotrys AV, Zhan Y, Artus-Revel CG et al. 2017. The dynamics of mRNA turnover revealed by single-molecule imaging in single cells. Mol. Cell 68:615–25.e9
    [Google Scholar]
  71. 71.
    Huang H, Kawamata T, Horie T, Tsugawa H, Nakayama Y et al. 2015. Bulk RNA degradation by nitrogen starvation-induced autophagy in yeast. EMBO J 34:154–68
    [Google Scholar]
  72. 72.
    Hubstenberger A, Courel M, Bénard M, Souquere S, Ernoult-Lange M et al. 2017. P-body purification reveals the condensation of repressed mRNA regulons. Mol. Cell 68:144–57.e5
    [Google Scholar]
  73. 73.
    Hughes Hallett JE, Luo X, Capaldi AP 2014. State transitions in the TORC1 signaling pathway and information processing in Saccharomyces cerevisiae. Genetics 198:773–86
    [Google Scholar]
  74. 74.
    Itakura AK, Chakravarty AK, Jakobson CM, Jarosz DF. 2020. Widespread prion-based control of growth and differentiation strategies in Saccharomyces cerevisiae. Mol. Cell 77:266–78.e6
    [Google Scholar]
  75. 75.
    Iwama R, Ohsumi Y. 2019. Analysis of autophagy activated during changes in carbon source availability in yeast cells. J. Biol. Chem. 294:5590–603
    [Google Scholar]
  76. 76.
    Jackrel ME, DeSantis ME, Martinez BA, Castellano LM, Stewart RM et al. 2014. Potentiated Hsp104 variants antagonize diverse proteotoxic misfolding events. Cell 156:170–82
    [Google Scholar]
  77. 77.
    Jacquel B, Aspert T, Laporte D, Sagot I, Charvin G. 2021. Monitoring single-cell dynamics of entry into quiescence during an unperturbed life cycle. eLife 10:e73186
    [Google Scholar]
  78. 78.
    Jang YK, Wang L, Sancar GB. 1999. RPH1 and GIS1 are damage-responsive repressors of PHR1. Mol. Cell. Biol. 19:7630–38
    [Google Scholar]
  79. 79.
    Jansen JM, Wanless AG, Seidel CW, Weiss EL. 2009. Cbk1 regulation of the RNA-binding protein Ssd1 integrates cell fate with translational control. Curr. Biol. 19:2114–20
    [Google Scholar]
  80. 80.
    Jarosz DF, Lancaster AK, Brown JCS, Lindquist S. 2014. An evolutionarily conserved prion-like element converts wild fungi from metabolic specialists to generalists. Cell 158:1072–82
    [Google Scholar]
  81. 81.
    Johnston GC, Pringle JR, Hartwell LH. 1977. Coordination of growth with cell division in the yeast Saccharomyces cerevisiae. Exp. Cell Res. 105:79–98
    [Google Scholar]
  82. 82.
    Johnston M. 1999. Feasting, fasting and fermenting: glucose sensing in yeast and other cells. Trends Genet 15:29–33
    [Google Scholar]
  83. 83.
    Kaida D, Yashiroda H, Toh-e A, Kikuchi Y 2002. Yeast Whi2 and Psr1-phosphatase form a complex and regulate STRE-mediated gene expression. Genes Cells 7:543–52
    [Google Scholar]
  84. 84.
    Kamada Y, Sekito T, Ohsumi Y. 2004. Autophagy in yeast: a TOR-mediated response to nutrient starvation. Curr. Top. Microbiol. Immunol. 279:73–84
    [Google Scholar]
  85. 85.
    Kawamata T, Horie T, Matsunami M, Sasaki M, Ohsumi Y. 2017. Zinc starvation induces autophagy in yeast. J. Biol. Chem. 292:8520–30
    [Google Scholar]
  86. 86.
    Kira S, Kumano Y, Ukai H, Takeda E, Matsuura A, Noda T. 2016. Dynamic relocation of the TORC1-Gtr1/2-Ego1/2/3 complex is regulated by Gtr1 and Gtr2. Mol. Biol. Cell 27:382–96
    [Google Scholar]
  87. 87.
    Klosinska MM, Crutchfield CA, Bradley PH, Rabinowitz JD, Broach JR. 2011. Yeast cells can access distinct quiescent states. Genes Dev 25:336–49
    [Google Scholar]
  88. 88.
    Kumar S, Mashkoor M, Grove A. 2022. Yeast Crf1p: An activator in need is an activator indeed. Comput. Struct. Biotechnol. J. 20:107–16
    [Google Scholar]
  89. 89.
    Kurischko C, Kuravi VK, Herbert CJ, Luca FC. 2011. Nucleocytoplasmic shuttling of Ssd1 defines the destiny of its bound mRNAs. Mol. Microbiol. 81:831–49
    [Google Scholar]
  90. 90.
    Lang MJ, Martinez-Marquez JY, Prosser DC, Ganser LR, Buelto D et al. 2014. Glucose starvation inhibits autophagy via vacuolar hydrolysis and induces plasma membrane internalization by down-regulating recycling. J. Biol. Chem. 289:16736–47
    [Google Scholar]
  91. 91.
    Laporte D, Jimenez L, Gouleme L, Sagot I. 2017. Yeast quiescence exit swiftness is influenced by cell volume and chronological age. Microb. Cell 5:104–11
    [Google Scholar]
  92. 92.
    Laporte D, Lebaudy A, Sahin A, Pinson B, Ceschin J et al. 2011. Metabolic status rather than cell cycle signals control quiescence entry and exit. J. Cell Biol. 192:949–57
    [Google Scholar]
  93. 93.
    Laporte D, Salin B, Daignan-Fornier B, Sagot I. 2008. Reversible cytoplasmic localization of the proteasome in quiescent yeast cells. J. Cell Biol. 181:737–45
    [Google Scholar]
  94. 94.
    Lee HY, Cheng KY, Chao JC, Leu JY. 2016. Differentiated cytoplasmic granule formation in quiescent and non-quiescent cells upon chronological aging. Microb. Cell 3:109–19
    [Google Scholar]
  95. 95.
    Lee PH, Osley MA. 2021. Chromatin structure restricts origin utilization when quiescent cells re-enter the cell cycle. Nucleic Acids Res 49:864–78
    [Google Scholar]
  96. 96.
    Levy S, Kafri M, Carmi M, Barkai N. 2011. The competitive advantage of a dual-transporter system. Science 334:1408–12
    [Google Scholar]
  97. 97.
    Li J, Yan G, Liu S, Jiang T, Zhong M et al. 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. 106:938–48
    [Google Scholar]
  98. 98.
    Li L, Miles S, Breeden LL. 2015. A genetic screen for Saccharomyces cerevisiae mutants that fail to enter quiescence. G3 5:1783–95
    [Google Scholar]
  99. 99.
    Li L, Miles S, Melville Z, Prasad A, Bradley G, Breeden LL. 2013. Key events during the transition from rapid growth to quiescence in budding yeast require posttranscriptional regulators. Mol. Biol. Cell 24:3697–709
    [Google Scholar]
  100. 100.
    Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T et al. 2009. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326:289–93
    [Google Scholar]
  101. 101.
    Lillie SH, Pringle JR. 1980. Reserve carbohydrate metabolism in Saccharomyces cerevisiae: responses to nutrient limitation. J. Bacteriol. 143:1384–94
    [Google Scholar]
  102. 102.
    Liu I-C, Chiu S-W, Lee H-Y, Leu J-Y. 2012. The histone deacetylase Hos2 forms an Hsp42-dependent cytoplasmic granule in quiescent yeast cells. Mol. Biol. Cell 23:1231–42
    [Google Scholar]
  103. 103.
    Lohr D, Ide G. 1979. Comparison of the structure and transcriptional capability of growing phase and stationary yeast chromatin: a model for reversible gene activation. Nucleic Acids Res 6:1909–27
    [Google Scholar]
  104. 104.
    Long LJ, Lee P-H, Small EM, Hillyer C, Guo Y, Osley MA. 2020. Regulation of UV damage repair in quiescent yeast cells. DNA Repair 90:102861
    [Google Scholar]
  105. 105.
    Lorenz MC, Fink GR. 2001. The glyoxylate cycle is required for fungal virulence. Nature 412:83–86
    [Google Scholar]
  106. 106.
    Luo X, Talarek N, De Virgilio C. 2011. Initiation of the yeast G0 program requires Igo1 and Igo2, which antagonize activation of decapping of specific nutrient-regulated mRNAs. RNA Biol 8:14–17
    [Google Scholar]
  107. 107.
    Mai B, Breeden L. 1997. Xbp1, a stress-induced transcriptional repressor of the Saccharomyces cerevisiae Swi4/Mbp1 family. Mol. Cell Biol. 17:6491–501
    [Google Scholar]
  108. 108.
    Marshall RS, McLoughlin F, Vierstra RD. 2016. Autophagic turnover of inactive 26S proteasomes in yeast is directed by the ubiquitin receptor Cue5 and the Hsp42 chaperone. Cell Rep 16:1717–32
    [Google Scholar]
  109. 109.
    Marshall RS, Vierstra RD. 2018. Proteasome storage granules protect proteasomes from autophagic degradation upon carbon starvation. eLife 7:e34532
    [Google Scholar]
  110. 110.
    Martinez MJ, Roy S, Archuletta AB, Wentzell PD, Anna-Arriola SS et al. 2004. Genomic analysis of stationary-phase and exit in Saccharomyces cerevisiae: gene expression and identification of novel essential genes. Mol. Biol. Cell 15:5295–305
    [Google Scholar]
  111. 111.
    Martinez-Pastor MT, Marchler G, Schuller C, Marchler-Bauer A, Ruis H, Estruch F. 1996. The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress response element (STRE). EMBO J 15:2227–35
    [Google Scholar]
  112. 112.
    May AI, Prescott M, Ohsumi Y. 2020. Autophagy facilitates adaptation of budding yeast to respiratory growth by recycling serine for one-carbon metabolism. Nat. Commun. 11:5052
    [Google Scholar]
  113. 113.
    McKnight JN, Boerma JW, Breeden LL, Tsukiyama T. 2015. Global promoter targeting of a conserved lysine deacetylase for transcriptional shutoff during quiescence entry. Mol. Cell 59:732–43
    [Google Scholar]
  114. 114.
    Medina EM, Turner JJ, Gordân R, Skotheim JM, Buchler NE. 2016. Punctuated evolution and transitional hybrid network in an ancestral cell cycle of fungi. eLife 5:e09492
    [Google Scholar]
  115. 115.
    Medina EM, Walsh E, Buchler NE 2019. Evolutionary innovation, fungal cell biology, and the lateral gene transfer of a viral KilA-N domain. Curr. Opin. Genet. Dev. 58–59:103–10
    [Google Scholar]
  116. 116.
    Mews P, Zee BM, Liu S, Donahue G, Garcia BA, Berger SL. 2014. Histone methylation has dynamics distinct from those of histone acetylation in cell cycle reentry from quiescence. Mol. Cell. Biol. 34:3968–80
    [Google Scholar]
  117. 117.
    Milanesi R, Coccetti P, Tripodi F. 2020. The regulatory role of key metabolites in the control of cell signaling. Biomolecules 10:862
    [Google Scholar]
  118. 118.
    Miles S, Croxford MW, Abeysinghe AP, Breeden LL. 2016. Msa1 and Msa2 modulate G1-specific transcription to promote G1 arrest and the transition to quiescence in budding yeast. PLOS Genet 12:e1006088
    [Google Scholar]
  119. 119.
    Miles S, Li L, Davison J, Breeden LL. 2013. Xbp1 directs global repression of budding yeast transcription during the transition to quiescence and is important for the longevity and reversibility of the quiescent state. PLOS Genet 9:e1003854
    [Google Scholar]
  120. 120.
    Miles S, Li LH, Melville Z, Breeden LL. 2019. Ssd1 and the cell wall integrity pathway promote entry, maintenance, and recovery from quiescence in budding yeast. Mol. Biol. Cell 30:2205–17
    [Google Scholar]
  121. 121.
    Miller SB, Mogk A, Bukau B. 2015. Spatially organized aggregation of misfolded proteins as cellular stress defense strategy. J. Mol. Biol. 427:1564–74
    [Google Scholar]
  122. 122.
    Miller-Fleming L, Antas P, Pais TF, Smalley JL, Giorgini F, Outeiro TF. 2014. Yeast DJ-1 superfamily members are required for diauxic-shift reprogramming and cell survival in stationary phase. PNAS 111:7012–17
    [Google Scholar]
  123. 123.
    Monteiro PT, Oliveira J, Pais P, Antunes M, Palma M et al. 2020. YEASTRACT+: a portal for cross-species comparative genomics of transcription regulation in yeasts. Nucleic Acids Res 48:D642–49
    [Google Scholar]
  124. 124.
    Montella-Manuel S, Pujol-Carrion N, de la Torre-Ruiz MA. 2021. The cell wall integrity receptor Mtl1 contributes to articulate autophagic responses when glucose availability is compromised. J. Fungi 7:903
    [Google Scholar]
  125. 125.
    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
    [Google Scholar]
  126. 126.
    Morgan JT, Fink GR, Bartel DP. 2019. Excised linear introns regulate growth in yeast. Nature 565:606–11
    [Google Scholar]
  127. 127.
    Mülleder M, Capuano F, Pir P, Christen S, Sauer U et al. 2012. A prototrophic deletion mutant collection for yeast metabolomics and systems biology. Nat. Biotechnol. 30:1176–78
    [Google Scholar]
  128. 128.
    Munder MC, Midtvedt D, Franzmann T, Nuske E, Otto O et al. 2016. A pH-driven transition of the cytoplasm from a fluid- to a solid-like state promotes entry into dormancy. eLife 5:e09347
    [Google Scholar]
  129. 129.
    Munding EM, Shiue L, Katzman S, Donohue JP, Ares M Jr. 2013. Competition between pre-mRNAs for the splicing machinery drives global regulation of splicing. Mol. Cell 51:338–48
    [Google Scholar]
  130. 130.
    Murphy JP, Stepanova E, Everley RA, Paulo JA, Gygi SP. 2015. Comprehensive temporal protein dynamics during the diauxic shift in Saccharomyces cerevisiae. Mol. Cell. Proteom. 14:2454–65
    [Google Scholar]
  131. 131.
    Narayanaswamy R, Levy M, Tsechansky M, Stovall GM, O'Connell JD et al. 2009. Widespread reorganization of metabolic enzymes into reversible assemblies upon nutrient starvation. PNAS 106:10147–52
    [Google Scholar]
  132. 132.
    Ngubo M, Kemp G, Patterton HG. 2011. Nano-electrospray tandem mass spectrometric analysis of the acetylation state of histones H3 and H4 in stationary phase in Saccharomyces cerevisiae. BMC Biochem 12:34
    [Google Scholar]
  133. 133.
    Nicastro R, Tripodi F, Gaggini M, Castoldi A, Reghellin V et al. 2015. Snf1 phosphorylates adenylate cyclase and negatively regulates protein kinase A-dependent transcription in Saccharomyces cerevisiae. J. Biol. Chem. 290:24715–26
    [Google Scholar]
  134. 134.
    Noda T, Ohsumi Y. 1998. Tor, a phosphatidylinositol kinase homologue, controls autophagy in yeast. J. Biol. Chem. 273:3963–66
    [Google Scholar]
  135. 135.
    Orzechowski Westholm J, Tronnersjö S, Nordberg N, Olsson I, Komorowski J, Ronne H 2012. Gis1 and Rph1 regulate glycerol and acetate metabolism in glucose depleted yeast cells. PLOS ONE 7:e31577
    [Google Scholar]
  136. 136.
    Padilla CA, Bárcena JA, López-Grueso MJ, Requejo-Aguilar R. 2019. The regulation of TORC1 pathway by the yeast chaperones Hsp31 is mediated by SFP1 and affects proteasomal activity. Biochim. Biophys. Acta Gen. Subj. 1863:534–46
    [Google Scholar]
  137. 137.
    Parenteau J, Maignon L, Berthoumieux M, Catala M, Gagnon V, Abou Elela S. 2019. Introns are mediators of cell response to starvation. Nature 565:612–17
    [Google Scholar]
  138. 138.
    Paz I, Abramovitz L, Choder M. 1999. Starved Saccharomyces cerevisiae cells have the capacity to support internal initiation of translation. J. Biol. Chem. 274:21741–45
    [Google Scholar]
  139. 139.
    Paz I, Meunier JR, Choder M. 1999. Monitoring dynamics of gene expression in yeast during stationary phase. Gene 236:33–42
    [Google Scholar]
  140. 140.
    Pedruzzi I, Dubouloz F, Cameroni E, Wanke V, Roosen J et al. 2003. TOR and PKA signaling pathways converge on the protein kinase Rim15 to control entry into G0. Mol. Cell 12:1607–13
    [Google Scholar]
  141. 141.
    Peterson PP, Liu Z. 2021. Identification and characterization of rapidly accumulating sch9Δ suppressor mutations in Saccharomyces cerevisiae. G3 11:jkab134
    [Google Scholar]
  142. 142.
    Petrovska I, Nüske E, Munder MC, Kulasegaran G, Malinovska L et al. 2014. Filament formation by metabolic enzymes is a specific adaptation to an advanced state of cellular starvation. eLife 3:e02409
    [Google Scholar]
  143. 143.
    Pfanzagl V, Görner W, Radolf M, Parich A, Schuhmacher R et al. 2018. A constitutive active allele of the transcription factor Msn2 mimicking low PKA activity dictates metabolic remodeling in yeast. Mol. Biol. Cell 29:2848–62
    [Google Scholar]
  144. 144.
    Pfeiffer T, Morley A. 2014. An evolutionary perspective on the Crabtree effect. Front. Mol. Biosci. 1:17
    [Google Scholar]
  145. 145.
    Piñon R. 1978. Folded chromosomes in non-cycling yeast cells: evidence for a characteristic g0 form. Chromosoma 67:263–74
    [Google Scholar]
  146. 146.
    Plank M, Perepelkina M, Muller M, Vaga S, Zou X et al. 2020. Chemical genetics of AGC-kinases reveals shared targets of Ypk1, protein kinase A and Sch9. Mol. Cell. Proteom. 19:655–71
    [Google Scholar]
  147. 147.
    Prouteau M, Desfosses A, Sieben C, Bourgoint C, Mozaffari NL et al. 2017. TORC1 organized in inhibited domains (TOROIDs) regulate TORC1 activity. Nature 550:265–69
    [Google Scholar]
  148. 148.
    Radonjic M, Andrau JC, Lijnzaad P, Kemmeren P, Kockelkorn TT 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 18:171–83
    [Google Scholar]
  149. 149.
    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 43:973–81
    [Google Scholar]
  150. 150.
    Rashida Z, Srinivasan R, Cyanam M, Laxman S. 2021. Kog1/Raptor mediates metabolic rewiring during nutrient limitation by controlling SNF1/AMPK activity. Sci. Adv. 7:eabe5544
    [Google Scholar]
  151. 151.
    Rawlings JS, Gatzka M, Thomas PG, Ihle JN. 2011. Chromatin condensation via the condensin II complex is required for peripheral T-cell quiescence. EMBO J 30:263–76
    [Google Scholar]
  152. 152.
    Reinke H, Gregory PD, Horz W. 2001. A transient histone hyperacetylation signal marks nucleosomes for remodeling at the PHO8 promoter in vivo. Mol. Cell 7:529–38
    [Google Scholar]
  153. 153.
    Rolland F, De Winde JH, Lemaire K, Boles E, Thevelein JM, Winderickx J. 2000. Glucose-induced cAMP signalling in yeast requires both a G-protein coupled receptor system for extracellular glucose detection and a separable hexose kinase-dependent sensing process. Mol. Microbiol. 38:348–58
    [Google Scholar]
  154. 154.
    Romero AM, Martínez-Pastor MT, Puig S 2021. Iron in translation: from the beginning to the end. Microorganisms 9:1058
    [Google Scholar]
  155. 155.
    Rutledge MT, Russo M, Belton JM, Dekker J, Broach JR. 2015. The yeast genome undergoes significant topological reorganization in quiescence. Nucleic Acids Res 43:8299–313
    [Google Scholar]
  156. 156.
    Sagot I, Laporte D. 2019. The cell biology of quiescent yeast—a diversity of individual scenarios. J. Cell Sci. 132:jcs213025
    [Google Scholar]
  157. 157.
    Saldanha AJ, Brauer MJ, Botstein D. 2004. Nutritional homeostasis in batch and steady-state culture of yeast. Mol. Biol. Cell 15:4089–104
    [Google Scholar]
  158. 158.
    Sanchez Y, Taulien J, Borkovich KA, Lindquist S. 1992. Hsp104 is required for tolerance to many forms of stress. EMBO J 11:2357–64
    [Google Scholar]
  159. 159.
    Sandmeier JJ, French S, Osheim Y, Cheung WL, Gallo CM et al. 2002. RPD3 is required for the inactivation of yeast ribosomal DNA genes in stationary phase. EMBO J 21:4959–68
    [Google Scholar]
  160. 160.
    Santos SM, Laflin S, Broadway A, Burnet C, Hartheimer J et al. 2021. High-resolution yeast quiescence profiling in human-like media reveals complex influences of auxotrophy and nutrient availability. Geroscience 43:941–64
    [Google Scholar]
  161. 161.
    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. PNAS 105:14838–43
    [Google Scholar]
  162. 162.
    Schmelzle T, Beck T, Martin DE, Hall MN. 2004. Activation of the RAS/cyclic AMP pathway suppresses a TOR deficiency in yeast. Mol. Cell. Biol. 24:338–51
    [Google Scholar]
  163. 163.
    Schmiady H, Sperling K. 1981. Length of human prematurely condensed chromosomes during G0 and G1 phase. Exp. Cell Res. 134:461–65
    [Google Scholar]
  164. 164.
    Shah KH, Nostramo R, Zhang B, Varia SN, Klett BM, Herman PK. 2014. Protein kinases are associated with multiple, distinct cytoplasmic granules in quiescent yeast cells. Genetics 198:1495–512
    [Google Scholar]
  165. 165.
    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 193:109–23
    [Google Scholar]
  166. 166.
    Shorter J, Southworth DR. 2019. Spiraling in control: structures and mechanisms of the Hsp104 disaggregase. Cold Spring Harb. Perspect. Biol. 11:a034033
    [Google Scholar]
  167. 167.
    Silva GM, Finley D, Vogel C. 2015. K63 polyubiquitination is a new modulator of the oxidative stress response. Nat. Struct. Mol. Biol. 22:116–23
    [Google Scholar]
  168. 168.
    Smets B, De Snijder P, Engelen K, Joossens E, Ghillebert R et al. 2008. Genome-wide expression analysis reveals TORC1-dependent and -independent functions of Sch9. FEMS Yeast Res. 8:1276–88
    [Google Scholar]
  169. 169.
    Spain MM, Braceros CA, Tsukiyama T. 2018. SWI/SNF coordinates transcriptional activation through Rpd3-mediated histone hypoacetylation during quiescence entry. bioRxiv 426288. https://doi.org/10.1101/426288
    [Crossref]
  170. 170.
    Sun S, Baryshnikova A, Brandt N, Gresham D. 2020. Genetic interaction profiles of regulatory kinases differ between environmental conditions and cellular states. Mol. Syst. Biol. 16:e9167
    [Google Scholar]
  171. 171.
    Suzuki SW, Onodera J, Ohsumi Y. 2011. Starvation induced cell death in autophagy-defective yeast mutants is caused by mitochondria dysfunction. PLOS ONE 6:e17412
    [Google Scholar]
  172. 172.
    Swanson MJ, Qiu H, Sumibcay L, Krueger A, Kim S-J et al. 2003. A multiplicity of coactivators is required by Gcn4p at individual promoters in vivo. Mol. Cell. Biol. 23:2800–20
    [Google Scholar]
  173. 173.
    Swygert SG, Kim S, Wu X, Fu T, Hsieh TH et al. 2019. Condensin-dependent chromatin compaction represses transcription globally during quiescence. Mol. Cell 73:533–46.e4
    [Google Scholar]
  174. 174.
    Swygert SG, Lin D, Portillo-Ledesma S, Lin PY, Hunt DR et al. 2021. Local chromatin fiber folding represses transcription and loop extrusion in quiescent cells. eLife 10:e72062
    [Google Scholar]
  175. 175.
    Teixeira D, Sheth U, Valencia-Sanchez MA, Brengues M, Parker R. 2005. Processing bodies require RNA for assembly and contain nontranslating mRNAs. RNA 11:371–82
    [Google Scholar]
  176. 176.
    Tessarz P, Schwarz M, Mogk A, Bukau B. 2009. The yeast AAA+ chaperone Hsp104 is part of a network that links the actin cytoskeleton with the inheritance of damaged proteins. Mol. Cell. Biol. 29:3738–45
    [Google Scholar]
  177. 177.
    Thevelein JM, de Winde JH. 1999. Novel sensing mechanisms and targets for the cAMP-protein kinase A pathway in the yeast Saccharomyces cerevisiae. Mol. Microbiol. 33:904–18
    [Google Scholar]
  178. 178.
    Thongsroy J, Matangkasombut O, Thongnak A, Rattanatanyong P, Jirawatnotai S, Mutirangura A. 2013. Replication-independent endogenous DNA double-strand breaks in Saccharomyces cerevisiae model. PLOS ONE 8:e72706
    [Google Scholar]
  179. 179.
    Thumm M, Egner R, Koch B, Schlumpberger M, Straub M et al. 1994. Isolation of autophagocytosis mutants of Saccharomyces cerevisiae. FEBS Lett. 349:275–80
    [Google Scholar]
  180. 180.
    Toda T, Uno I, Ishikawa T, Powers S, Kataoka T et al. 1985. In yeast, RAS proteins are controlling elements of the cyclic AMP pathway. Cell 40:27–36
    [Google Scholar]
  181. 181.
    Torres J, Di Como CJ, Herrero E, De La, Torre-Ruiz MA. 2002. Regulation of the cell integrity pathway by rapamycin-sensitive TOR function in budding yeast. J. Biol. Chem. 277:43495–504
    [Google Scholar]
  182. 182.
    Treger JM, Heichman KA, McEntee K. 1988. Expression of the yeast UB14 gene increases in response to DNA-damaging agents and in meiosis. Mol. Cell. Biol. 8:1132–36
    [Google Scholar]
  183. 183.
    Tsukada M, Ohsumi Y. 1993. Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett. 333:169–74
    [Google Scholar]
  184. 184.
    Urban J, Soulard A, Huber A, Lippman S, Mukhopadhyay D et al. 2007. Sch9 is a major target of TORC1 in Saccharomyces cerevisiae. Mol. Cell 26:663–74
    [Google Scholar]
  185. 185.
    Van Zeebroeck G, Demuyser L, Zhang Z, Cottignie I, Thevelein JM. 2020. Nutrient sensing and cAMP signaling in yeast: G-protein coupled receptor versus transceptor activation of PKA. Microb. Cell 8:17–27
    [Google Scholar]
  186. 186.
    Waite KA, De-La Mota-Peynado A, Vontz G, Roelofs J 2016. Starvation induces proteasome autophagy with different pathways for core and regulatory particles. J. Biol. Chem. 291:3239–53
    [Google Scholar]
  187. 187.
    Walter D, Matter A, Fahrenkrog B. 2010. Bre1p-mediated histone H2B ubiquitylation regulates apoptosis in Saccharomyces cerevisiae. J. Cell Sci. 123:1931–39
    [Google Scholar]
  188. 188.
    Wang BD, Eyre D, Basrai M, Lichten M, Strunnikov A. 2005. Condensin binding at distinct and specific chromosomal sites in the Saccharomyces cerevisiae genome. Mol. Cell. Biol. 25:7216–25
    [Google Scholar]
  189. 189.
    Wang K, Melki R, Kabani M. 2017. A prolonged chronological lifespan is an unexpected benefit of the [PSI+] prion in yeast. PLOS ONE 12:e0184905
    [Google Scholar]
  190. 190.
    Wanke V, Cameroni E, Uotila A, Piccolis M, Urban J et al. 2008. Caffeine extends yeast lifespan by targeting TORC1. Mol. Microbiol. 69:277–85
    [Google Scholar]
  191. 191.
    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. 24:4271–78
    [Google Scholar]
  192. 192.
    Warner JR. 1999. The economics of ribosome biosynthesis in yeast. Trends Biochem. Sci. 24:437–40
    [Google Scholar]
  193. 193.
    Warner JR, Vilardell J, Sohn JH. 2001. Economics of ribosome biosynthesis. Cold Spring Harb. Symp. Quant. Biol. 66:567–74
    [Google Scholar]
  194. 194.
    Webb KJ, Xu T, Park SK, Yates JR 3rd 2013. Modified MuDPIT separation identified 4488 proteins in a system-wide analysis of quiescence in yeast. J. Proteome Res. 12:2177–84
    [Google Scholar]
  195. 195.
    Werner-Washburne M, Becker J, Kosic-Smithers J, Craig EA 1989. Yeast Hsp70 RNA levels vary in response to the physiological status of the cell. J. Bacteriol. 171:2680–88
    [Google Scholar]
  196. 196.
    Werner-Washburne M, Craig EA 1989. Expression of members of the Saccharomyces cerevisiae hsp70 multigene family. Genome 31:684–89
    [Google Scholar]
  197. 197.
    Westholm JO, Nordberg N, Murén E, Ameur A, Komorowski J, Ronne H 2008. Combinatorial control of gene expression by the three yeast repressors Mig1, Mig2 and Mig3. BMC Genom. 9:601
    [Google Scholar]
  198. 198.
    Wijsman M, Świat MA, Marques WL, Hettinga JK, van den Broek M et al. 2019. A toolkit for rapid CRISPR-SpCas9 assisted construction of hexose-transport-deficient Saccharomyces cerevisiae strains. FEMS Yeast Res 19:foy107
    [Google Scholar]
  199. 199.
    Winkler J, Tyedmers J, Bukau B, Mogk A. 2012. Hsp70 targets Hsp100 chaperones to substrates for protein disaggregation and prion fragmentation. J. Cell Biol. 198:387–404
    [Google Scholar]
  200. 200.
    Yasuda K, Clatterbuck-Soper SF, Jackrel ME, Shorter J, Mili S. 2017. FUS inclusions disrupt RNA localization by sequestering kinesin-1 and inhibiting microtubule detyrosination. J. Cell Biol. 216:1015–34
    [Google Scholar]
  201. 201.
    Yen HC, Xu Q, Chou DM, Zhao Z, Elledge SJ. 2008. Global protein stability profiling in mammalian cells. Science 322:918–23
    [Google Scholar]
  202. 202.
    Yokota H, Gomi K, Shintani T. 2017. Induction of autophagy by phosphate starvation in an Atg11-dependent manner in Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 483:522–27
    [Google Scholar]
  203. 203.
    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 18:4180–89
    [Google Scholar]
  204. 204.
    Yoshikawa K, Tanaka T, Furusawa C, Nagahisa K, Hirasawa T, Shimizu H. 2009. Comprehensive phenotypic analysis for identification of genes affecting growth under ethanol stress in Saccharomyces cerevisiae. FEMS Yeast Res 9:32–44
    [Google Scholar]
  205. 205.
    Youk H, van Oudenaarden A. 2009. Growth landscape formed by perception and import of glucose in yeast. Nature 462:875–79
    [Google Scholar]
  206. 206.
    Young CP, Hillyer C, Hokamp K, Fitzpatrick DJ, Konstantinov NK et al. 2017. Distinct histone methylation and transcription profiles are established during the development of cellular quiescence in yeast. BMC Genom 18:107
    [Google Scholar]
  207. 207.
    Yu F, Imamura Y, Ueno M, Suzuki SW, Ohsumi Y et al. 2015. The yeast chromatin remodeler Rsc1-RSC complex is required for transcriptional activation of autophagy-related genes and inhibition of the TORC1 pathway in response to nitrogen starvation. Biochem. Biophys. Res. Commun. 464:1248–53
    [Google Scholar]
  208. 208.
    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
    [Google Scholar]
  209. 209.
    Zampar GG, Kummel A, Ewald J, Jol S, Niebel B et al. 2013. Temporal system-level organization of the switch from glycolytic to gluconeogenic operation in yeast. Mol. Syst. Biol. 9:651
    [Google Scholar]
  210. 210.
    Zhang Z, Cottignie I, Van Zeebroeck G, Thevelein JM. 2021. Nutrient transceptors physically interact with the yeast S6/protein kinase B homolog, Sch9, a TOR kinase target. Biochem. J. 478:357–75
    [Google Scholar]
  211. 211.
    Zhou Y, Kastritis PL, Dougherty SE, Bouvette J, Hsu AL et al. 2020. Structural impact of K63 ubiquitin on yeast translocating ribosomes under oxidative stress. PNAS 117:22157–66
    [Google Scholar]
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