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. 1992 Sep;12(9):3706–3714. doi: 10.1128/mcb.12.9.3706

Meiotic induction of the yeast HOP1 gene is controlled by positive and negative regulatory sites.

A K Vershon 1, N M Hollingsworth 1, A D Johnson 1
PMCID: PMC360227  PMID: 1508177

Abstract

The process of meiosis and sporulation in the yeast Saccharomyces cerevisiae is a highly regulated developmental pathway dependent on genetic as well as nutritional signals. The HOP1 gene, which encodes a component of meiotic chromosomes, is not expressed in mitotically growing cells, but its transcription is induced shortly after yeast cells enter the meiotic pathway. Through a series of deletions and mutations in the HOP1 promoter, we located two regulatory sites that are essential for proper regulation of HOP1. One site, called URS1H, brings about repression of HOP1 in mitotic cells and functions as an activator sequence in cells undergoing meiosis. The second site, which we designated UASH, acts as an activator sequence in meiotic cells and has similarity to the binding site of the mammalian CCAAT/enhancer binding protein (C/EBP). Both sites are required for full meiotic induction of the HOP1 promoter. We conclude that in mitotic yeast cells, the URS1H site maintains the repressed state of the HOP1 promoter, masking the effect of the UASH site. Upon entry into meiosis, repression is lifted, allowing the URS1H and UASH sites to activate high-level transcription.

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Selected References

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  1. Atcheson C. L., DiDomenico B., Frackman S., Esposito R. E., Elder R. T. Isolation, DNA sequence, and regulation of a meiosis-specific eukaryotic recombination gene. Proc Natl Acad Sci U S A. 1987 Nov;84(22):8035–8039. doi: 10.1073/pnas.84.22.8035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bishop D. K., Park D., Xu L., Kleckner N. DMC1: a meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell. 1992 May 1;69(3):439–456. doi: 10.1016/0092-8674(92)90446-j. [DOI] [PubMed] [Google Scholar]
  3. Buckingham L. E., Wang H. T., Elder R. T., McCarroll R. M., Slater M. R., Esposito R. E. Nucleotide sequence and promoter analysis of SPO13, a meiosis-specific gene of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1990 Dec;87(23):9406–9410. doi: 10.1073/pnas.87.23.9406. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Dynan W. S., Tjian R. The promoter-specific transcription factor Sp1 binds to upstream sequences in the SV40 early promoter. Cell. 1983 Nov;35(1):79–87. doi: 10.1016/0092-8674(83)90210-6. [DOI] [PubMed] [Google Scholar]
  5. Engebrecht J., Roeder G. S. MER1, a yeast gene required for chromosome pairing and genetic recombination, is induced in meiosis. Mol Cell Biol. 1990 May;10(5):2379–2389. doi: 10.1128/mcb.10.5.2379. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Gidoni D., Dynan W. S., Tjian R. Multiple specific contacts between a mammalian transcription factor and its cognate promoters. 1984 Nov 29-Dec 5Nature. 312(5993):409–413. doi: 10.1038/312409a0. [DOI] [PubMed] [Google Scholar]
  7. Guarente L., Hoar E. Upstream activation sites of the CYC1 gene of Saccharomyces cerevisiae are active when inverted but not when placed downstream of the "TATA box". Proc Natl Acad Sci U S A. 1984 Dec;81(24):7860–7864. doi: 10.1073/pnas.81.24.7860. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gustafson T. A., Kedes L. Identification of multiple proteins that interact with functional regions of the human cardiac alpha-actin promoter. Mol Cell Biol. 1989 Aug;9(8):3269–3283. doi: 10.1128/mcb.9.8.3269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hollingsworth N. M., Byers B. HOP1: a yeast meiotic pairing gene. Genetics. 1989 Mar;121(3):445–462. doi: 10.1093/genetics/121.3.445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hollingsworth N. M., Goetsch L., Byers B. The HOP1 gene encodes a meiosis-specific component of yeast chromosomes. Cell. 1990 Apr 6;61(1):73–84. doi: 10.1016/0092-8674(90)90216-2. [DOI] [PubMed] [Google Scholar]
  11. Johnson P. F., Landschulz W. H., Graves B. J., McKnight S. L. Identification of a rat liver nuclear protein that binds to the enhancer core element of three animal viruses. Genes Dev. 1987 Apr;1(2):133–146. doi: 10.1101/gad.1.2.133. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. Keleher C. A., Goutte C., Johnson A. D. The yeast cell-type-specific repressor alpha 2 acts cooperatively with a non-cell-type-specific protein. Cell. 1988 Jun 17;53(6):927–936. doi: 10.1016/s0092-8674(88)90449-7. [DOI] [PubMed] [Google Scholar]
  14. Keleher C. A., Redd M. J., Schultz J., Carlson M., Johnson A. D. Ssn6-Tup1 is a general repressor of transcription in yeast. Cell. 1992 Feb 21;68(4):709–719. doi: 10.1016/0092-8674(92)90146-4. [DOI] [PubMed] [Google Scholar]
  15. Kihara K., Nakamura M., Akada R., Yamashita I. Positive and negative elements upstream of the meiosis-specific glucoamylase gene in Saccharomyces cerevisiae. Mol Gen Genet. 1991 May;226(3):383–392. doi: 10.1007/BF00260650. [DOI] [PubMed] [Google Scholar]
  16. Kovari L., Sumrada R., Kovari I., Cooper T. G. Multiple positive and negative cis-acting elements mediate induced arginase (CAR1) gene expression in Saccharomyces cerevisiae. Mol Cell Biol. 1990 Oct;10(10):5087–5097. doi: 10.1128/mcb.10.10.5087. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Luche R. M., Sumrada R., Cooper T. G. A cis-acting element present in multiple genes serves as a repressor protein binding site for the yeast CAR1 gene. Mol Cell Biol. 1990 Aug;10(8):3884–3895. doi: 10.1128/mcb.10.8.3884. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Malavasic M. J., Elder R. T. Complementary transcripts from two genes necessary for normal meiosis in the yeast Saccharomyces cerevisiae. Mol Cell Biol. 1990 Jun;10(6):2809–2819. doi: 10.1128/mcb.10.6.2809. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Malone R. E. Dual regulation of meiosis in yeast. Cell. 1990 May 4;61(3):375–378. doi: 10.1016/0092-8674(90)90517-i. [DOI] [PubMed] [Google Scholar]
  20. Menees T. M., Ross-MacDonald P. B., Roeder G. S. MEI4, a meiosis-specific yeast gene required for chromosome synapsis. Mol Cell Biol. 1992 Mar;12(3):1340–1351. doi: 10.1128/mcb.12.3.1340. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Mukai Y., Harashima S., Oshima Y. AAR1/TUP1 protein, with a structure similar to that of the beta subunit of G proteins, is required for a1-alpha 2 and alpha 2 repression in cell type control of Saccharomyces cerevisiae. Mol Cell Biol. 1991 Jul;11(7):3773–3779. doi: 10.1128/mcb.11.7.3773. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. SHERMAN F., ROMAN H. Evidence for two types of allelic recombination in yeast. Genetics. 1963 Feb;48:255–261. doi: 10.1093/genetics/48.2.255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Siliciano P. G., Tatchell K. Transcription and regulatory signals at the mating type locus in yeast. Cell. 1984 Jul;37(3):969–978. doi: 10.1016/0092-8674(84)90431-8. [DOI] [PubMed] [Google Scholar]
  26. Smith H. E., Mitchell A. P. A transcriptional cascade governs entry into meiosis in Saccharomyces cerevisiae. Mol Cell Biol. 1989 May;9(5):2142–2152. doi: 10.1128/mcb.9.5.2142. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Smith H. E., Su S. S., Neigeborn L., Driscoll S. E., Mitchell A. P. Role of IME1 expression in regulation of meiosis in Saccharomyces cerevisiae. Mol Cell Biol. 1990 Dec;10(12):6103–6113. doi: 10.1128/mcb.10.12.6103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Smith M. In vitro mutagenesis. Annu Rev Genet. 1985;19:423–462. doi: 10.1146/annurev.ge.19.120185.002231. [DOI] [PubMed] [Google Scholar]
  29. Strich R., Slater M. R., Esposito R. E. Identification of negative regulatory genes that govern the expression of early meiotic genes in yeast. Proc Natl Acad Sci U S A. 1989 Dec;86(24):10018–10022. doi: 10.1073/pnas.86.24.10018. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Sumrada R. A., Cooper T. G. Point mutation generates constitutive expression of an inducible eukaryotic gene. Proc Natl Acad Sci U S A. 1985 Feb;82(3):643–647. doi: 10.1073/pnas.82.3.643. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Sumrada R. A., Cooper T. G. Ubiquitous upstream repression sequences control activation of the inducible arginase gene in yeast. Proc Natl Acad Sci U S A. 1987 Jun;84(12):3997–4001. doi: 10.1073/pnas.84.12.3997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Thompson E. A., Roeder G. S. Expression and DNA sequence of RED1, a gene required for meiosis I chromosome segregation in yeast. Mol Gen Genet. 1989 Aug;218(2):293–301. doi: 10.1007/BF00331281. [DOI] [PubMed] [Google Scholar]
  33. Trumbly R. J. Isolation of Saccharomyces cerevisiae mutants constitutive for invertase synthesis. J Bacteriol. 1986 Jun;166(3):1123–1127. doi: 10.1128/jb.166.3.1123-1127.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Wang H. T., Frackman S., Kowalisyn J., Esposito R. E., Elder R. Developmental regulation of SPO13, a gene required for separation of homologous chromosomes at meiosis I. Mol Cell Biol. 1987 Apr;7(4):1425–1435. doi: 10.1128/mcb.7.4.1425. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. West R. W., Jr, Yocum R. R., Ptashne M. Saccharomyces cerevisiae GAL1-GAL10 divergent promoter region: location and function of the upstream activating sequence UASG. Mol Cell Biol. 1984 Nov;4(11):2467–2478. doi: 10.1128/mcb.4.11.2467. [DOI] [PMC free article] [PubMed] [Google Scholar]

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