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. 1990 Oct;9(10):3225–3232. doi: 10.1002/j.1460-2075.1990.tb07521.x

The adenylate cyclase/protein kinase cascade regulates entry into meiosis in Saccharomyces cerevisiae through the gene IME1.

A Matsuura 1, M Treinin 1, H Mitsuzawa 1, Y Kassir 1, I Uno 1, G Simchen 1
PMCID: PMC552053  PMID: 2209544

Abstract

Entry into meiosis in Saccharomyces cerevisiae cells is regulated by starvation through the adenylate cyclase/cAMP-dependent protein kinase (AC/PK) pathway. The gene IME1 is also involved in starvation control of meiosis. Multicopy IME1 plasmids overcome the meiotic deficiency of bcy1 and of RASval19 diploids. Double mutants ime1 cdc25 and ime1 ras2 are sporulation deficient. These results suggest that IME1 comes after the AC/PK cascade. Furthermore, the level of IME1 transcripts is affected by mutations in the AC/PK genes CDC25, CYR1 and BCY1. Moreover, the addition of cAMP to a cyr1-2 diploid suppresses IME1 transcription. The presence in a bcy1 diploid of IME1 multicopy plasmids does not cure the failure of bcy1 cells to arrest as unbudded cells following starvation and to enter the G0 state (thermotolerance, synthesis of unique G0 proteins). This indicates that the pathway downstream of the AC/PK cascade branches to control meiosis through IME1, and to control entry into G0 and cell cycle initiation, independently of IME1.

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Selected References

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

  1. Broek D., Toda T., Michaeli T., Levin L., Birchmeier C., Zoller M., Powers S., Wigler M. The S. cerevisiae CDC25 gene product regulates the RAS/adenylate cyclase pathway. Cell. 1987 Mar 13;48(5):789–799. doi: 10.1016/0092-8674(87)90076-6. [DOI] [PubMed] [Google Scholar]
  2. Cameron S., Levin L., Zoller M., Wigler M. cAMP-independent control of sporulation, glycogen metabolism, and heat shock resistance in S. cerevisiae. Cell. 1988 May 20;53(4):555–566. doi: 10.1016/0092-8674(88)90572-7. [DOI] [PubMed] [Google Scholar]
  3. Carlson M., Botstein D. Two differentially regulated mRNAs with different 5' ends encode secreted with intracellular forms of yeast invertase. Cell. 1982 Jan;28(1):145–154. doi: 10.1016/0092-8674(82)90384-1. [DOI] [PubMed] [Google Scholar]
  4. Daniel J., Simchen G. Clones from two different genomic regions complement the cdc25 start mutation of Saccharomyces cerevisiae. Curr Genet. 1986;10(9):643–646. doi: 10.1007/BF00410911. [DOI] [PubMed] [Google Scholar]
  5. Esposito R. E., Esposito M. S. Genetic recombination and commitment to meiosis in Saccharomyces. Proc Natl Acad Sci U S A. 1974 Aug;71(8):3172–3176. doi: 10.1073/pnas.71.8.3172. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Granot D., Margolskee J. P., Simchen G. A long region upstream of the IME1 gene regulates meiosis in yeast. Mol Gen Genet. 1989 Aug;218(2):308–314. doi: 10.1007/BF00331283. [DOI] [PubMed] [Google Scholar]
  7. Hartwell L. H. Periodic density fluctuation during the yeast cell cycle and the selection of synchronous cultures. J Bacteriol. 1970 Dec;104(3):1280–1285. doi: 10.1128/jb.104.3.1280-1285.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Ito H., Fukuda Y., Murata K., Kimura A. Transformation of intact yeast cells treated with alkali cations. J Bacteriol. 1983 Jan;153(1):163–168. doi: 10.1128/jb.153.1.163-168.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Kassir Y., Granot D., Simchen G. IME1, a positive regulator gene of meiosis in S. cerevisiae. Cell. 1988 Mar 25;52(6):853–862. doi: 10.1016/0092-8674(88)90427-8. [DOI] [PubMed] [Google Scholar]
  10. Kassir Y., Simchen G. Regulation of mating and meiosis in yeast by the mating-type region. Genetics. 1976 Feb;82(2):187–206. doi: 10.1093/genetics/82.2.187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. Matsumoto K., Uno I., Ishikawa T. Genetic analysis of the role of cAMP in yeast. Yeast. 1985 Sep;1(1):15–24. doi: 10.1002/yea.320010103. [DOI] [PubMed] [Google Scholar]
  13. Matsumoto K., Uno I., Ishikawa T. Initiation of meiosis in yeast mutants defective in adenylate cyclase and cyclic AMP-dependent protein kinase. Cell. 1983 Feb;32(2):417–423. doi: 10.1016/0092-8674(83)90461-0. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. Mitchell A. P., Herskowitz I. Activation of meiosis and sporulation by repression of the RME1 product in yeast. 1986 Feb 27-Mar 5Nature. 319(6056):738–742. doi: 10.1038/319738a0. [DOI] [PubMed] [Google Scholar]
  16. Mitsuzawa H., Uno I., Oshima T., Ishikawa T. Isolation and characterization of temperature-sensitive mutations in the RAS2 and CYR1 genes of Saccharomyces cerevisiae. Genetics. 1989 Dec;123(4):739–748. doi: 10.1093/genetics/123.4.739. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. O'Farrell P. H. High resolution two-dimensional electrophoresis of proteins. J Biol Chem. 1975 May 25;250(10):4007–4021. [PMC free article] [PubMed] [Google Scholar]
  18. O'Farrell P. Z., Goodman H. M., O'Farrell P. H. High resolution two-dimensional electrophoresis of basic as well as acidic proteins. Cell. 1977 Dec;12(4):1133–1141. doi: 10.1016/0092-8674(77)90176-3. [DOI] [PubMed] [Google Scholar]
  19. Shilo V., Simchen G., Shilo B. Initiation of meiosis in cell cycle initiation mutants of Saccharomyces cerevisiae. Exp Cell Res. 1978 Mar 15;112(2):241–248. doi: 10.1016/0014-4827(78)90206-9. [DOI] [PubMed] [Google Scholar]
  20. Shin D. Y., Matsumoto K., Iida H., Uno I., Ishikawa T. Heat shock response of Saccharomyces cerevisiae mutants altered in cyclic AMP-dependent protein phosphorylation. Mol Cell Biol. 1987 Jan;7(1):244–250. doi: 10.1128/mcb.7.1.244. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Shin D. Y., Uno I., Ishikawa T. Control of the G1-G0 transition and G0 protein synthesis by cyclic AMP in Saccharomyces cerevisiae. Curr Genet. 1987;12(8):577–582. doi: 10.1007/BF00368059. [DOI] [PubMed] [Google Scholar]
  22. Suzuki T., Nishibayashi S., Kuroiwa T., Kanbe T., Tanaka K. Variance of ploidy in Candida albicans. J Bacteriol. 1982 Nov;152(2):893–896. doi: 10.1128/jb.152.2.893-896.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Tatchell K., Chaleff D. T., DeFeo-Jones D., Scolnick E. M. Requirement of either of a pair of ras-related genes of Saccharomyces cerevisiae for spore viability. Nature. 1984 Jun 7;309(5968):523–527. doi: 10.1038/309523a0. [DOI] [PubMed] [Google Scholar]
  24. Tatchell K., Robinson L. C., Breitenbach M. RAS2 of Saccharomyces cerevisiae is required for gluconeogenic growth and proper response to nutrient limitation. Proc Natl Acad Sci U S A. 1985 Jun;82(11):3785–3789. doi: 10.1073/pnas.82.11.3785. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. 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]
  26. 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]
  27. Uno I., Matsumoto K., Adachi K., Ishikawa T. Genetic and biochemical evidence that trehalase is a substrate of cAMP-dependent protein kinase in yeast. J Biol Chem. 1983 Sep 25;258(18):10867–10872. [PubMed] [Google Scholar]
  28. Uno I., Mitsuzawa H., Tanaka K., Oshima T., Ishikawa T. Identification of the domain of Saccharomyces cerevisiae adenylate cyclase associated with the regulatory function of RAS products. Mol Gen Genet. 1987 Dec;210(2):187–194. doi: 10.1007/BF00325683. [DOI] [PubMed] [Google Scholar]
  29. Yamano S., Tanaka K., Matsumoto K., Toh-e A. Mutant regulatory subunit of 3',5'-cAMP-dependent protein kinase of yeast Saccharomyces cerevisiae. Mol Gen Genet. 1987 Dec;210(3):413–418. doi: 10.1007/BF00327191. [DOI] [PubMed] [Google Scholar]

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