Skip to main content
NCBI home page
Genetics logoLink to Genetics
. 2001 Sep;159(1):77–89. doi: 10.1093/genetics/159.1.77

The Ras/PKA signaling pathway of Saccharomyces cerevisiae exhibits a functional interaction with the Sin4p complex of the RNA polymerase II holoenzyme.

S C Howard 1, Y W Chang 1, Y V Budovskaya 1, P K Herman 1
PMCID: PMC1461800  PMID: 11560888

Abstract

Saccharomyces cerevisiae cells enter into the G(0)-like resting state, stationary phase, in response to specific types of nutrient limitation. We have initiated a genetic analysis of this resting state and have identified a collection of rye mutants that exhibit a defective transcriptional response to nutrient deprivation. These transcriptional defects appear to disrupt the control of normal growth because the rye mutants are unable to enter into a normal stationary phase upon nutrient deprivation. In this study, we examined the mutants in the rye1 complementation group and found that rye1 mutants were also defective for stationary phase entry. Interestingly, the RYE1 gene was found to be identical to SIN4, a gene that encodes a component of the yeast Mediator complex within the RNA polymerase II holoenzyme. Moreover, mutations that affected proteins within the Sin4p module of the Mediator exhibited specific genetic interactions with the Ras protein signaling pathway. For example, mutations that elevated the levels of Ras signaling, like RAS2(val19), were synthetic lethal with sin4. In all, our data suggest that specific proteins within the RNA polymerase II holoenzyme might be targets of signal transduction pathways that are responsible for coordinating gene expression with cell growth.

Full Text

The Full Text of this article is available as a PDF (265.2 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Balciunas D., Gälman C., Ronne H., Björklund S. The Med1 subunit of the yeast mediator complex is involved in both transcriptional activation and repression. Proc Natl Acad Sci U S A. 1999 Jan 19;96(2):376–381. doi: 10.1073/pnas.96.2.376. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baudin A., Ozier-Kalogeropoulos O., Denouel A., Lacroute F., Cullin C. A simple and efficient method for direct gene deletion in Saccharomyces cerevisiae. Nucleic Acids Res. 1993 Jul 11;21(14):3329–3330. doi: 10.1093/nar/21.14.3329. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bon E. P., Carvajal E., Stanbrough M., Rowen D., Magasanik B. Asparaginase II of Saccharomyces cerevisiae. GLN3/URE2 regulation of a periplasmic enzyme. Appl Biochem Biotechnol. 1997 Spring;63-65:203–212. doi: 10.1007/978-1-4612-2312-2_19. [DOI] [PubMed] [Google Scholar]
  4. Cannon J. F., Tatchell K. Characterization of Saccharomyces cerevisiae genes encoding subunits of cyclic AMP-dependent protein kinase. Mol Cell Biol. 1987 Aug;7(8):2653–2663. doi: 10.1128/mcb.7.8.2653. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chang M., French-Cornay D., Fan H. Y., Klein H., Denis C. L., Jaehning J. A. A complex containing RNA polymerase II, Paf1p, Cdc73p, Hpr1p, and Ccr4p plays a role in protein kinase C signaling. Mol Cell Biol. 1999 Feb;19(2):1056–1067. doi: 10.1128/mcb.19.2.1056. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chang Y. W., Howard S. C., Budovskaya Y. V., Rine J., Herman P. K. The rye mutants identify a role for Ssn/Srb proteins of the RNA polymerase II holoenzyme during stationary phase entry in Saccharomyces cerevisiae. Genetics. 2001 Jan;157(1):17–26. doi: 10.1093/genetics/157.1.17. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chen S., West R. W., Jr, Johnson S. L., Gans H., Kruger B., Ma J. TSF3, a global regulatory protein that silences transcription of yeast GAL genes, also mediates repression by alpha 2 repressor and is identical to SIN4. Mol Cell Biol. 1993 Feb;13(2):831–840. doi: 10.1128/mcb.13.2.831. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cherest H., Kerjan P., Surdin-Kerjan Y. The Saccharomyces cerevisiae MET3 gene: nucleotide sequence and relationship of the 5' non-coding region to that of MET25. Mol Gen Genet. 1987 Dec;210(2):307–313. doi: 10.1007/BF00325699. [DOI] [PubMed] [Google Scholar]
  9. Choder M. A general topoisomerase I-dependent transcriptional repression in the stationary phase in yeast. Genes Dev. 1991 Dec;5(12A):2315–2326. doi: 10.1101/gad.5.12a.2315. [DOI] [PubMed] [Google Scholar]
  10. Christianson T. W., Sikorski R. S., Dante M., Shero J. H., Hieter P. Multifunctional yeast high-copy-number shuttle vectors. Gene. 1992 Jan 2;110(1):119–122. doi: 10.1016/0378-1119(92)90454-w. [DOI] [PubMed] [Google Scholar]
  11. Cooper K. F., Mallory M. J., Smith J. B., Strich R. Stress and developmental regulation of the yeast C-type cyclin Ume3p (Srb11p/Ssn8p). EMBO J. 1997 Aug 1;16(15):4665–4675. doi: 10.1093/emboj/16.15.4665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Covitz P. A., Song W., Mitchell A. P. Requirement for RGR1 and SIN4 in RME1-dependent repression in Saccharomyces cerevisiae. Genetics. 1994 Nov;138(3):577–586. doi: 10.1093/genetics/138.3.577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. DeRisi J. L., Iyer V. R., Brown P. O. Exploring the metabolic and genetic control of gene expression on a genomic scale. Science. 1997 Oct 24;278(5338):680–686. doi: 10.1126/science.278.5338.680. [DOI] [PubMed] [Google Scholar]
  14. Denis C. L., Kemp B. E., Zoller M. J. Substrate specificities for yeast and mammalian cAMP-dependent protein kinases are similar but not identical. J Biol Chem. 1991 Sep 25;266(27):17932–17935. [PubMed] [Google Scholar]
  15. Destruelle M., Holzer H., Klionsky D. J. Identification and characterization of a novel yeast gene: the YGP1 gene product is a highly glycosylated secreted protein that is synthesized in response to nutrient limitation. Mol Cell Biol. 1994 Apr;14(4):2740–2754. doi: 10.1128/mcb.14.4.2740. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Field J., Xu H. P., Michaeli T., Ballester R., Sass P., Wigler M., Colicelli J. Mutations of the adenylyl cyclase gene that block RAS function in Saccharomyces cerevisiae. Science. 1990 Jan 26;247(4941):464–467. doi: 10.1126/science.2405488. [DOI] [PubMed] [Google Scholar]
  17. Friesen H., Tanny J. C., Segall J. Spe3, which encodes spermidine synthase, is required for full repression through NRE(DIT) in Saccharomyces cerevisiae. Genetics. 1998 Sep;150(1):59–73. doi: 10.1093/genetics/150.1.59. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Gibbs J. B., Marshall M. S. The ras oncogene--an important regulatory element in lower eucaryotic organisms. Microbiol Rev. 1989 Jun;53(2):171–185. doi: 10.1128/mr.53.2.171-185.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Görner W., Durchschlag E., Martinez-Pastor M. T., Estruch F., Ammerer G., Hamilton B., Ruis H., Schüller C. Nuclear localization of the C2H2 zinc finger protein Msn2p is regulated by stress and protein kinase A activity. Genes Dev. 1998 Feb 15;12(4):586–597. doi: 10.1101/gad.12.4.586. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Han S. J., Lee Y. C., Gim B. S., Ryu G. H., Park S. J., Lane W. S., Kim Y. J. Activator-specific requirement of yeast mediator proteins for RNA polymerase II transcriptional activation. Mol Cell Biol. 1999 Feb;19(2):979–988. doi: 10.1128/mcb.19.2.979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Holstege F. C., Jennings E. G., Wyrick J. J., Lee T. I., Hengartner C. J., Green M. R., Golub T. R., Lander E. S., Young R. A. Dissecting the regulatory circuitry of a eukaryotic genome. Cell. 1998 Nov 25;95(5):717–728. doi: 10.1016/s0092-8674(00)81641-4. [DOI] [PubMed] [Google Scholar]
  22. Iida H., Yahara I. Specific early-G1 blocks accompanied with stringent response in Saccharomyces cerevisiae lead to growth arrest in resting state similar to the G0 of higher eucaryotes. J Cell Biol. 1984 Apr;98(4):1185–1193. doi: 10.1083/jcb.98.4.1185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Jiang Y. W., Dohrmann P. R., Stillman D. J. Genetic and physical interactions between yeast RGR1 and SIN4 in chromatin organization and transcriptional regulation. Genetics. 1995 May;140(1):47–54. doi: 10.1093/genetics/140.1.47. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Jiang Y. W., Stillman D. J. Involvement of the SIN4 global transcriptional regulator in the chromatin structure of Saccharomyces cerevisiae. Mol Cell Biol. 1992 Oct;12(10):4503–4514. doi: 10.1128/mcb.12.10.4503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Jiang Y. W., Stillman D. J. Regulation of HIS4 expression by the Saccharomyces cerevisiae SIN4 transcriptional regulator. Genetics. 1995 May;140(1):103–114. doi: 10.1093/genetics/140.1.103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Jiang Y. W., Veschambre P., Erdjument-Bromage H., Tempst P., Conaway J. W., Conaway R. C., Kornberg R. D. Mammalian mediator of transcriptional regulation and its possible role as an end-point of signal transduction pathways. Proc Natl Acad Sci U S A. 1998 Jul 21;95(15):8538–8543. doi: 10.1073/pnas.95.15.8538. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Johnson L. M., Bankaitis V. A., Emr S. D. Distinct sequence determinants direct intracellular sorting and modification of a yeast vacuolar protease. Cell. 1987 Mar 13;48(5):875–885. doi: 10.1016/0092-8674(87)90084-5. [DOI] [PubMed] [Google Scholar]
  28. Kataoka T., Powers S., McGill C., Fasano O., Strathern J., Broach J., Wigler M. Genetic analysis of yeast RAS1 and RAS2 genes. Cell. 1984 Jun;37(2):437–445. doi: 10.1016/0092-8674(84)90374-x. [DOI] [PubMed] [Google Scholar]
  29. Koleske A. J., Young R. A. The RNA polymerase II holoenzyme and its implications for gene regulation. Trends Biochem Sci. 1995 Mar;20(3):113–116. doi: 10.1016/s0968-0004(00)88977-x. [DOI] [PubMed] [Google Scholar]
  30. Kuchin S., Treich I., Carlson M. A regulatory shortcut between the Snf1 protein kinase and RNA polymerase II holoenzyme. Proc Natl Acad Sci U S A. 2000 Jul 5;97(14):7916–7920. doi: 10.1073/pnas.140109897. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Kuranda M. J., Robbins P. W. Chitinase is required for cell separation during growth of Saccharomyces cerevisiae. J Biol Chem. 1991 Oct 15;266(29):19758–19767. [PubMed] [Google Scholar]
  32. Lee M., Chatterjee S., Struhl K. Genetic analysis of the role of Pol II holoenzyme components in repression by the Cyc8-Tup1 corepressor in yeast. Genetics. 2000 Aug;155(4):1535–1542. doi: 10.1093/genetics/155.4.1535. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Lee T. I., Young R. A. Transcription of eukaryotic protein-coding genes. Annu Rev Genet. 2000;34:77–137. doi: 10.1146/annurev.genet.34.1.77. [DOI] [PubMed] [Google Scholar]
  34. Li Y., Bjorklund S., Jiang Y. W., Kim Y. J., Lane W. S., Stillman D. J., Kornberg R. D. Yeast global transcriptional regulators Sin4 and Rgr1 are components of mediator complex/RNA polymerase II holoenzyme. Proc Natl Acad Sci U S A. 1995 Nov 21;92(24):10864–10868. doi: 10.1073/pnas.92.24.10864. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Maliepaard M., Sitters K. A., de Mol N. J., Janssen L. H., Stratford I. J., Stephens M., Verboom W., Reinhoudt D. N. Potential antitumour mitosenes: relationship between in vitro DNA interstrand cross-link formation and DNA damage in Escherichia coli K-12 strains. Biochem Pharmacol. 1994 Oct 7;48(7):1371–1377. doi: 10.1016/0006-2952(94)90559-2. [DOI] [PubMed] [Google Scholar]
  36. Malik S., Roeder R. G. Transcriptional regulation through Mediator-like coactivators in yeast and metazoan cells. Trends Biochem Sci. 2000 Jun;25(6):277–283. doi: 10.1016/s0968-0004(00)01596-6. [DOI] [PubMed] [Google Scholar]
  37. Marchler G., Schüller C., Adam G., Ruis H. A Saccharomyces cerevisiae UAS element controlled by protein kinase A activates transcription in response to a variety of stress conditions. EMBO J. 1993 May;12(5):1997–2003. doi: 10.1002/j.1460-2075.1993.tb05849.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Matsumoto K., Uno I., Ishikawa T. Control of cell division in Saccharomyces cerevisiae mutants defective in adenylate cyclase and cAMP-dependent protein kinase. Exp Cell Res. 1983 Jun;146(1):151–161. doi: 10.1016/0014-4827(83)90333-6. [DOI] [PubMed] [Google Scholar]
  39. Matsumoto K., Uno I., Oshima Y., Ishikawa T. Isolation and characterization of yeast mutants deficient in adenylate cyclase and cAMP-dependent protein kinase. Proc Natl Acad Sci U S A. 1982 Apr;79(7):2355–2359. doi: 10.1073/pnas.79.7.2355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Miyao T., Woychik N. A. RNA polymerase subunit RPB5 plays a role in transcriptional activation. Proc Natl Acad Sci U S A. 1998 Dec 22;95(26):15281–15286. doi: 10.1073/pnas.95.26.15281. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Morishita T., Mitsuzawa H., Nakafuku M., Nakamura S., Hattori S., Anraku Y. Requirement of Saccharomyces cerevisiae Ras for completion of mitosis. Science. 1995 Nov 17;270(5239):1213–1215. doi: 10.1126/science.270.5239.1213. [DOI] [PubMed] [Google Scholar]
  42. Mountain H. A., Byström A. S., Larsen J. T., Korch C. Four major transcriptional responses in the methionine/threonine biosynthetic pathway of Saccharomyces cerevisiae. Yeast. 1991 Nov;7(8):781–803. doi: 10.1002/yea.320070804. [DOI] [PubMed] [Google Scholar]
  43. Myers L. C., Gustafsson C. M., Hayashibara K. C., Brown P. O., Kornberg R. D. Mediator protein mutations that selectively abolish activated transcription. Proc Natl Acad Sci U S A. 1999 Jan 5;96(1):67–72. doi: 10.1073/pnas.96.1.67. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Myers L. C., Kornberg R. D. Mediator of transcriptional regulation. Annu Rev Biochem. 2000;69:729–749. doi: 10.1146/annurev.biochem.69.1.729. [DOI] [PubMed] [Google Scholar]
  45. Mösch H. U., Roberts R. L., Fink G. R. Ras2 signals via the Cdc42/Ste20/mitogen-activated protein kinase module to induce filamentous growth in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1996 May 28;93(11):5352–5356. doi: 10.1073/pnas.93.11.5352. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Padilla P. A., Fuge E. K., Crawford M. E., Errett A., Werner-Washburne M. The highly conserved, coregulated SNO and SNZ gene families in Saccharomyces cerevisiae respond to nutrient limitation. J Bacteriol. 1998 Nov;180(21):5718–5726. doi: 10.1128/jb.180.21.5718-5726.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Piruat J. I., Chávez S., Aguilera A. The yeast HRS1 gene is involved in positive and negative regulation of transcription and shows genetic characteristics similar to SIN4 and GAL11. Genetics. 1997 Dec;147(4):1585–1594. doi: 10.1093/genetics/147.4.1585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Praekelt U. M., Meacock P. A. HSP12, a new small heat shock gene of Saccharomyces cerevisiae: analysis of structure, regulation and function. Mol Gen Genet. 1990 Aug;223(1):97–106. doi: 10.1007/BF00315801. [DOI] [PubMed] [Google Scholar]
  49. Ptashne M., Gann A. Transcriptional activation by recruitment. Nature. 1997 Apr 10;386(6625):569–577. doi: 10.1038/386569a0. [DOI] [PubMed] [Google Scholar]
  50. Reinders A., Bürckert N., Boller T., Wiemken A., De Virgilio C. Saccharomyces cerevisiae cAMP-dependent protein kinase controls entry into stationary phase through the Rim15p protein kinase. Genes Dev. 1998 Sep 15;12(18):2943–2955. doi: 10.1101/gad.12.18.2943. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Riou C., Nicaud J. M., Barre P., Gaillardin C. Stationary-phase gene expression in Saccharomyces cerevisiae during wine fermentation. Yeast. 1997 Aug;13(10):903–915. doi: 10.1002/(SICI)1097-0061(199708)13:10<903::AID-YEA145>3.0.CO;2-1. [DOI] [PubMed] [Google Scholar]
  52. Roberts S. M., Winston F. Essential functional interactions of SAGA, a Saccharomyces cerevisiae complex of Spt, Ada, and Gcn5 proteins, with the Snf/Swi and Srb/mediator complexes. Genetics. 1997 Oct;147(2):451–465. doi: 10.1093/genetics/147.2.451. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Robinson J. S., Klionsky D. J., Banta L. M., Emr S. D. Protein sorting in Saccharomyces cerevisiae: isolation of mutants defective in the delivery and processing of multiple vacuolar hydrolases. Mol Cell Biol. 1988 Nov;8(11):4936–4948. doi: 10.1128/mcb.8.11.4936. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Schmitt A. P., McEntee K. Msn2p, a zinc finger DNA-binding protein, is the transcriptional activator of the multistress response in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1996 Jun 11;93(12):5777–5782. doi: 10.1073/pnas.93.12.5777. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Shah H. C., Carlson G. P. Alteration by phenobarbital and 3-methyl-cholanthrene of functional and structural changes in rat liver due to carbon tetrachloride inhalation. J Pharmacol Exp Ther. 1975 Apr;193(1):281–292. [PubMed] [Google Scholar]
  56. Sikorski R. S., Boeke J. D. In vitro mutagenesis and plasmid shuffling: from cloned gene to mutant yeast. Methods Enzymol. 1991;194:302–318. doi: 10.1016/0076-6879(91)94023-6. [DOI] [PubMed] [Google Scholar]
  57. Sikorski R. S., Hieter P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics. 1989 May;122(1):19–27. doi: 10.1093/genetics/122.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Smith A., Ward M. P., Garrett S. Yeast PKA represses Msn2p/Msn4p-dependent gene expression to regulate growth, stress response and glycogen accumulation. EMBO J. 1998 Jul 1;17(13):3556–3564. doi: 10.1093/emboj/17.13.3556. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Song W., Treich I., Qian N., Kuchin S., Carlson M. SSN genes that affect transcriptional repression in Saccharomyces cerevisiae encode SIN4, ROX3, and SRB proteins associated with RNA polymerase II. Mol Cell Biol. 1996 Jan;16(1):115–120. doi: 10.1128/mcb.16.1.115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Spencer F., Gerring S. L., Connelly C., Hieter P. Mitotic chromosome transmission fidelity mutants in Saccharomyces cerevisiae. Genetics. 1990 Feb;124(2):237–249. doi: 10.1093/genetics/124.2.237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Suzuki N., Choe H. R., Nishida Y., Yamawaki-Kataoka Y., Ohnishi S., Tamaoki T., Kataoka T. Leucine-rich repeats and carboxyl terminus are required for interaction of yeast adenylate cyclase with RAS proteins. Proc Natl Acad Sci U S A. 1990 Nov;87(22):8711–8715. doi: 10.1073/pnas.87.22.8711. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Thevelein J. M., de Winde J. H. Novel sensing mechanisms and targets for the cAMP-protein kinase A pathway in the yeast Saccharomyces cerevisiae. Mol Microbiol. 1999 Sep;33(5):904–918. doi: 10.1046/j.1365-2958.1999.01538.x. [DOI] [PubMed] [Google Scholar]
  63. Toda T., Cameron S., Sass P., Zoller M., Scott J. D., McMullen B., Hurwitz M., Krebs E. G., Wigler M. Cloning and characterization of BCY1, a locus encoding a regulatory subunit of the cyclic AMP-dependent protein kinase in Saccharomyces cerevisiae. Mol Cell Biol. 1987 Apr;7(4):1371–1377. doi: 10.1128/mcb.7.4.1371. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Toda T., Cameron S., Sass P., Zoller M., Wigler M. Three different genes in S. cerevisiae encode the catalytic subunits of the cAMP-dependent protein kinase. Cell. 1987 Jul 17;50(2):277–287. doi: 10.1016/0092-8674(87)90223-6. [DOI] [PubMed] [Google Scholar]
  65. Toda T., Uno I., Ishikawa T., Powers S., Kataoka T., Broek D., Cameron S., Broach J., Matsumoto K., Wigler M. In yeast, RAS proteins are controlling elements of adenylate cyclase. Cell. 1985 Jan;40(1):27–36. doi: 10.1016/0092-8674(85)90305-8. [DOI] [PubMed] [Google Scholar]
  66. Valay J. G., Simon M., Dubois M. F., Bensaude O., Facca C., Faye G. The KIN28 gene is required both for RNA polymerase II mediated transcription and phosphorylation of the Rpb1p CTD. J Mol Biol. 1995 Jun 9;249(3):535–544. doi: 10.1006/jmbi.1995.0316. [DOI] [PubMed] [Google Scholar]
  67. Werner-Washburne M., Braun E. L., Crawford M. E., Peck V. M. Stationary phase in Saccharomyces cerevisiae. Mol Microbiol. 1996 Mar;19(6):1159–1166. doi: 10.1111/j.1365-2958.1996.tb02461.x. [DOI] [PubMed] [Google Scholar]
  68. Werner-Washburne M., Braun E., Johnston G. C., Singer R. A. Stationary phase in the yeast Saccharomyces cerevisiae. Microbiol Rev. 1993 Jun;57(2):383–401. doi: 10.1128/mr.57.2.383-401.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES