Skip to main content
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1990 Dec;10(12):6356–6361. doi: 10.1128/mcb.10.12.6356

Induction of yeast histone genes by stimulation of stationary-phase cells.

M A Drebot 1, L M Veinot-Drebot 1, R A Singer 1, G C Johnston 1
PMCID: PMC362911  PMID: 2247060

Abstract

In the cell cycle of the budding yeast Saccharomyces cerevisiae, expression of the histone genes H2A and H2B of the TRT1 and TRT2 loci is regulated by the performance of "start," the step that also regulates the cell cycle. Here we show that histone production is also subject to an additional form of regulation that is unrelated to the mitotic cell cycle. Expression of histone genes, as assessed by Northern (RNA) analysis, was shown to increase promptly after the stimulation, brought about by fresh medium, that activates stationary-phase cells to reenter the mitotic cell cycle. The use of a yeast mutant that is conditionally blocked in the resumption of proliferation at a step that is not part of the mitotic cell cycle (M.A. Drebot, G.C. Johnston, and R.A. Singer, Proc. Natl. Acad. Sci. 84:7948, 1987) showed that this increased gene expression that occurs upon stimulation of stationary-phase cells took place in the absence of DNA synthesis and without the performance of start. This stimulation-specific gene expression was blocked by the mating pheromone alpha-factor, indicating that alpha-factor directly inhibits expression of these histone genes, independently of start.

Full text

PDF
6356

Images in this article

Selected References

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

  1. Blumer K. J., Reneke J. E., Thorner J. The STE2 gene product is the ligand-binding component of the alpha-factor receptor of Saccharomyces cerevisiae. J Biol Chem. 1988 Aug 5;263(22):10836–10842. [PubMed] [Google Scholar]
  2. Bücking-Throm E., Duntze W., Hartwell L. H., Manney T. R. Reversible arrest of haploid yeast cells in the initiation of DNA synthesis by a diffusible sex factor. Exp Cell Res. 1973 Jan;76(1):99–110. doi: 10.1016/0014-4827(73)90424-2. [DOI] [PubMed] [Google Scholar]
  3. Drebot M. A., Barnes C. A., Singer R. A., Johnston G. C. Genetic assessment of stationary phase for cells of the yeast Saccharomyces cerevisiae. J Bacteriol. 1990 Jul;172(7):3584–3589. doi: 10.1128/jb.172.7.3584-3589.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Drebot M. A., Johnston G. C., Singer R. A. A yeast mutant conditionally defective only for reentry into the mitotic cell cycle from stationary phase. Proc Natl Acad Sci U S A. 1987 Nov;84(22):7948–7952. doi: 10.1073/pnas.84.22.7948. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Hagen D. C., Sprague G. F., Jr Induction of the yeast alpha-specific STE3 gene by the peptide pheromone a-factor. J Mol Biol. 1984 Oct 5;178(4):835–852. doi: 10.1016/0022-2836(84)90314-0. [DOI] [PubMed] [Google Scholar]
  6. Hartig A., Holly J., Saari G., MacKay V. L. Multiple regulation of STE2, a mating-type-specific gene of Saccharomyces cerevisiae. Mol Cell Biol. 1986 Jun;6(6):2106–2114. doi: 10.1128/mcb.6.6.2106. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Hartwell L. H. Macromolecule synthesis in temperature-sensitive mutants of yeast. J Bacteriol. 1967 May;93(5):1662–1670. doi: 10.1128/jb.93.5.1662-1670.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. Hartwell L. H. Saccharomyces cerevisiae cell cycle. Bacteriol Rev. 1974 Jun;38(2):164–198. doi: 10.1128/br.38.2.164-198.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hereford L. M., Hartwell L. H. Sequential gene function in the initiation of Saccharomyces cerevisiae DNA synthesis. J Mol Biol. 1974 Apr 15;84(3):445–461. doi: 10.1016/0022-2836(74)90451-3. [DOI] [PubMed] [Google Scholar]
  11. Hereford L. M., Osley M. A., Ludwig T. R., 2nd, McLaughlin C. S. Cell-cycle regulation of yeast histone mRNA. Cell. 1981 May;24(2):367–375. doi: 10.1016/0092-8674(81)90326-3. [DOI] [PubMed] [Google Scholar]
  12. Hereford L., Bromley S., Osley M. A. Periodic transcription of yeast histone genes. Cell. 1982 Aug;30(1):305–310. doi: 10.1016/0092-8674(82)90036-8. [DOI] [PubMed] [Google Scholar]
  13. Hereford L., Fahrner K., Woolford J., Jr, Rosbash M., Kaback D. B. Isolation of yeast histone genes H2A and H2B. Cell. 1979 Dec;18(4):1261–1271. doi: 10.1016/0092-8674(79)90237-x. [DOI] [PubMed] [Google Scholar]
  14. Iida H., Yahara I. Durable synthesis of high molecular weight heat shock proteins in G0 cells of the yeast and other eucaryotes. J Cell Biol. 1984 Jul;99(1 Pt 1):199–207. doi: 10.1083/jcb.99.1.199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. Jahng K. Y., Ferguson J., Reed S. I. Mutations in a gene encoding the alpha subunit of a Saccharomyces cerevisiae G protein indicate a role in mating pheromone signaling. Mol Cell Biol. 1988 Jun;8(6):2484–2493. doi: 10.1128/mcb.8.6.2484. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Johnston G. C., Singer R. A., McFarlane S. Growth and cell division during nitrogen starvation of the yeast Saccharomyces cerevisiae. J Bacteriol. 1977 Nov;132(2):723–730. doi: 10.1128/jb.132.2.723-730.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Johnston S. A., Hopper J. E. Isolation of the yeast regulatory gene GAL4 and analysis of its dosage effects on the galactose/melibiose regulon. Proc Natl Acad Sci U S A. 1982 Nov;79(22):6971–6975. doi: 10.1073/pnas.79.22.6971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Konrad M. Analysis and in vivo disruption of the gene coding for adenylate kinase (ADK1) in the yeast Saccharomyces cerevisiae. J Biol Chem. 1988 Dec 25;263(36):19468–19474. [PubMed] [Google Scholar]
  20. Kronstad J. W., Holly J. A., MacKay V. L. A yeast operator overlaps an upstream activation site. Cell. 1987 Jul 31;50(3):369–377. doi: 10.1016/0092-8674(87)90491-0. [DOI] [PubMed] [Google Scholar]
  21. Lycan D. E., Osley M. A., Hereford L. M. Role of transcriptional and posttranscriptional regulation in expression of histone genes in Saccharomyces cerevisiae. Mol Cell Biol. 1987 Feb;7(2):614–621. doi: 10.1128/mcb.7.2.614. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. McCaffrey G., Clay F. J., Kelsay K., Sprague G. F., Jr Identification and regulation of a gene required for cell fusion during mating of the yeast Saccharomyces cerevisiae. Mol Cell Biol. 1987 Aug;7(8):2680–2690. doi: 10.1128/mcb.7.8.2680. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Messing J. New M13 vectors for cloning. Methods Enzymol. 1983;101:20–78. doi: 10.1016/0076-6879(83)01005-8. [DOI] [PubMed] [Google Scholar]
  24. Nakayama N., Kaziro Y., Arai K., Matsumoto K. Role of STE genes in the mating factor signaling pathway mediated by GPA1 in Saccharomyces cerevisiae. Mol Cell Biol. 1988 Sep;8(9):3777–3783. doi: 10.1128/mcb.8.9.3777. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Nakayama N., Miyajima A., Arai K. Nucleotide sequences of STE2 and STE3, cell type-specific sterile genes from Saccharomyces cerevisiae. EMBO J. 1985 Oct;4(10):2643–2648. doi: 10.1002/j.1460-2075.1985.tb03982.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Norris D., Osley M. A. The two gene pairs encoding H2A and H2B play different roles in the Saccharomyces cerevisiae life cycle. Mol Cell Biol. 1987 Oct;7(10):3473–3481. doi: 10.1128/mcb.7.10.3473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Oechsner U., Magdolen V., Zoglowek C., Häcker U., Bandlow W. Yeast adenylate kinase is transcribed constitutively from a promoter in the short intergenic region to the histone H2A-1 gene. FEBS Lett. 1988 Dec 19;242(1):187–193. doi: 10.1016/0014-5793(88)81013-5. [DOI] [PubMed] [Google Scholar]
  28. Orlean P. Two chitin synthases in Saccharomyces cerevisiae. J Biol Chem. 1987 Apr 25;262(12):5732–5739. [PubMed] [Google Scholar]
  29. Osley M. A., Gould J., Kim S., Kane M. Y., Hereford L. Identification of sequences in a yeast histone promoter involved in periodic transcription. Cell. 1986 May 23;45(4):537–544. doi: 10.1016/0092-8674(86)90285-0. [DOI] [PubMed] [Google Scholar]
  30. Osley M. A., Hereford L. M. Yeast histone genes show dosage compensation. Cell. 1981 May;24(2):377–384. doi: 10.1016/0092-8674(81)90327-5. [DOI] [PubMed] [Google Scholar]
  31. Osley M. A., Lycan D. Trans-acting regulatory mutations that alter transcription of Saccharomyces cerevisiae histone genes. Mol Cell Biol. 1987 Dec;7(12):4204–4210. doi: 10.1128/mcb.7.12.4204. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Penn M. D., Thireos G., Greer H. Temporal analysis of general control of amino acid biosynthesis in Saccharomyces cerevisiae: role of positive regulatory genes in initiation and maintenance of mRNA derepression. Mol Cell Biol. 1984 Mar;4(3):520–528. doi: 10.1128/mcb.4.3.520. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Singer R. A., Bedard D. P., Johnston G. C. Bud formation by the yeast Saccharomyces cerevisiae is directly dependent on "start". J Cell Biol. 1984 Feb;98(2):678–684. doi: 10.1083/jcb.98.2.678. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Stetler G. L., Thorner J. Molecular cloning of hormone-responsive genes from the yeast Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1984 Feb;81(4):1144–1148. doi: 10.1073/pnas.81.4.1144. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Storms R. K., Ord R. W., Greenwood M. T., Mirdamadi B., Chu F. K., Belfort M. Cell cycle-dependent expression of thymidylate synthase in Saccharomyces cerevisiae. Mol Cell Biol. 1984 Dec;4(12):2858–2864. doi: 10.1128/mcb.4.12.2858. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Teague M. A., Chaleff D. T., Errede B. Nucleotide sequence of the yeast regulatory gene STE7 predicts a protein homologous to protein kinases. Proc Natl Acad Sci U S A. 1986 Oct;83(19):7371–7375. doi: 10.1073/pnas.83.19.7371. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Throm E., Duntze W. Mating-Type-Dependent Inhibition of Deoxyribonucleic Acid Synthesis in Saccharomyces cerevisiae. J Bacteriol. 1970 Dec;104(3):1388–1390. doi: 10.1128/jb.104.3.1388-1390.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Trueheart J., Boeke J. D., Fink G. R. Two genes required for cell fusion during yeast conjugation: evidence for a pheromone-induced surface protein. Mol Cell Biol. 1987 Jul;7(7):2316–2328. doi: 10.1128/mcb.7.7.2316. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Van Arsdell S. W., Stetler G. L., Thorner J. The yeast repeated element sigma contains a hormone-inducible promoter. Mol Cell Biol. 1987 Feb;7(2):749–759. doi: 10.1128/mcb.7.2.749. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. White J. H., Green S. R., Barker D. G., Dumas L. B., Johnston L. H. The CDC8 transcript is cell cycle regulated in yeast and is expressed coordinately with CDC9 and CDC21 at a point preceding histone transcription. Exp Cell Res. 1987 Jul;171(1):223–231. doi: 10.1016/0014-4827(87)90265-5. [DOI] [PubMed] [Google Scholar]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES