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. 1993 Mar;133(3):489–498. doi: 10.1093/genetics/133.3.489

a/α-Control of DNA Repair in the Yeast Saccharomyces Cerevisiae: Genetic and Physiological Aspects

M Heude 1, F Fabre 1
PMCID: PMC1205337  PMID: 8454201

Abstract

It has long been known that diploid strains of yeast are more resistant to γ-rays than haploid cells, and that this is in part due to heterozygosity at the mating type (MAT) locus. It is shown here that the genetic control exerted by the MAT genes on DNA repair involves the a1 and α2 genes, in a RME1-independent way. In rad18 diploids, affected in the error-prone repair, the a/α effects are of a very large amplitude, after both UV and γ-rays, and also depends on a1 and α2. The coexpression of a and α in rad18 haploids suppresses the sensitivity of a subpopulation corresponding to the G(2) phase cells. Related to this, the coexpression of a and α in RAD(+) haploids depresses UV-induced mutagenesis in G(2) cells. For srs2 null diploids, also affected in the error-prone repair pathway, we show that their G(1) UV sensitivity, likely due to lethal recombination events, is partly suppressed by MAT homozygosity. Taken together, these results led to the proposal that a1-α2 promotes a channeling of some DNA structures from the mutagenic into the recombinational repair process.

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Selected References

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  1. Aboussekhra A., Chanet R., Adjiri A., Fabre F. Semidominant suppressors of Srs2 helicase mutations of Saccharomyces cerevisiae map in the RAD51 gene, whose sequence predicts a protein with similarities to procaryotic RecA proteins. Mol Cell Biol. 1992 Jul;12(7):3224–3234. doi: 10.1128/mcb.12.7.3224. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Aboussekhra A., Chanet R., Zgaga Z., Cassier-Chauvat C., Heude M., Fabre F. RADH, a gene of Saccharomyces cerevisiae encoding a putative DNA helicase involved in DNA repair. Characteristics of radH mutants and sequence of the gene. Nucleic Acids Res. 1989 Sep 25;17(18):7211–7219. doi: 10.1093/nar/17.18.7211. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Astell C. R., Ahlstrom-Jonasson L., Smith M., Tatchell K., Nasmyth K. A., Hall B. D. The sequence of the DNAs coding for the mating-type loci of Saccharomyces cerevisiae. Cell. 1981 Nov;27(1 Pt 2):15–23. doi: 10.1016/0092-8674(81)90356-1. [DOI] [PubMed] [Google Scholar]
  4. Cassier-Chauvat C., Fabre F. A similar defect in UV-induced mutagenesis conferred by the rad6 and rad18 mutations of Saccharomyces cerevisiae. Mutat Res. 1991 May;254(3):247–253. doi: 10.1016/0921-8777(91)90063-u. [DOI] [PubMed] [Google Scholar]
  5. Cassier-Chauvat C., Moustacchi E. Allelism between pso1-1 and rev3-1 mutants and between pso2-1 and snm1 mutants in Saccharomyces cerevisiae. Curr Genet. 1988;13(1):37–40. doi: 10.1007/BF00365754. [DOI] [PubMed] [Google Scholar]
  6. Chanet R., Magana-Schwencke N., Fabre F. Potential DNA-binding domains in the RAD18 gene product of Saccharomyces cerevisiae. Gene. 1988 Dec 30;74(2):543–547. doi: 10.1016/0378-1119(88)90187-4. [DOI] [PubMed] [Google Scholar]
  7. Cole G. M., Mortimer R. K. Failure to induce a DNA repair gene, RAD54, in Saccharomyces cerevisiae does not affect DNA repair or recombination phenotypes. Mol Cell Biol. 1989 Aug;9(8):3314–3322. doi: 10.1128/mcb.9.8.3314. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cole G. M., Schild D., Lovett S. T., Mortimer R. K. Regulation of RAD54- and RAD52-lacZ gene fusions in Saccharomyces cerevisiae in response to DNA damage. Mol Cell Biol. 1987 Mar;7(3):1078–1084. doi: 10.1128/mcb.7.3.1078. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Covitz P. A., Herskowitz I., Mitchell A. P. The yeast RME1 gene encodes a putative zinc finger protein that is directly repressed by a1-alpha 2. Genes Dev. 1991 Nov;5(11):1982–1989. doi: 10.1101/gad.5.11.1982. [DOI] [PubMed] [Google Scholar]
  10. Fabre F., Boulet A., Roman H. Gene conversion at different points in the mitotic cycle of Saccharomyces cerevisiae. Mol Gen Genet. 1984;195(1-2):139–143. doi: 10.1007/BF00332736. [DOI] [PubMed] [Google Scholar]
  11. Friedberg E. C. Deoxyribonucleic acid repair in the yeast Saccharomyces cerevisiae. Microbiol Rev. 1988 Mar;52(1):70–102. doi: 10.1128/mr.52.1.70-102.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Friis J., Roman H. The effect of the mating-type alleles on intragenic recombination in yeast. Genetics. 1968 May;59(1):33–36. doi: 10.1093/genetics/59.1.33. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Herskowitz I. Life cycle of the budding yeast Saccharomyces cerevisiae. Microbiol Rev. 1988 Dec;52(4):536–553. doi: 10.1128/mr.52.4.536-553.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hopper A. K., Kirsch J., Hall B. D. Mating type and sporulation in yeast. II. Meiosis, recombination, and radiation sensitivity in an alpha-alpha diploid with altered sporulation control. Genetics. 1975 May;80(1):61–76. doi: 10.1093/genetics/80.1.61. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. Ivy J. M., Klar A. J., Hicks J. B. Cloning and characterization of four SIR genes of Saccharomyces cerevisiae. Mol Cell Biol. 1986 Feb;6(2):688–702. doi: 10.1128/mcb.6.2.688. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Jentsch S., McGrath J. P., Varshavsky A. The yeast DNA repair gene RAD6 encodes a ubiquitin-conjugating enzyme. Nature. 1987 Sep 10;329(6135):131–134. doi: 10.1038/329131a0. [DOI] [PubMed] [Google Scholar]
  18. Kans J. A., Mortimer R. K. Nucleotide sequence of the RAD57 gene of Saccharomyces cerevisiae. Gene. 1991 Aug 30;105(1):139–140. doi: 10.1016/0378-1119(91)90527-i. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. Klar A. J., Strathern J. N., Broach J. R., Hicks J. B. Regulation of transcription in expressed and unexpressed mating type cassettes of yeast. Nature. 1981 Jan 22;289(5795):239–244. doi: 10.1038/289239a0. [DOI] [PubMed] [Google Scholar]
  21. Lawrence C. W., Christensen R. UV mutagenesis in radiation-sensitive strains of yeast. Genetics. 1976 Feb;82(2):207–232. doi: 10.1093/genetics/82.2.207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lawrence C. W. Mutagenesis in Saccharomyces cerevisiae. Adv Genet. 1982;21:173–254. doi: 10.1016/s0065-2660(08)60299-0. [DOI] [PubMed] [Google Scholar]
  23. Lemontt J. F. Pathways of ultraviolet mutability in Saccharomyces cerevisiae. II. The effect of rev genes on recombination. Mutat Res. 1971 Dec;13(4):319–326. doi: 10.1016/0027-5107(71)90042-x. [DOI] [PubMed] [Google Scholar]
  24. Lovett S. T., Mortimer R. K. Characterization of null mutants of the RAD55 gene of Saccharomyces cerevisiae: effects of temperature, osmotic strength and mating type. Genetics. 1987 Aug;116(4):547–553. doi: 10.1093/genetics/116.4.547. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. MORTIMER R. K. Radiobiological and genetic studies on a polyploid series (haploid to hexaploid) of Saccharomyces cerevisiae. Radiat Res. 1958 Sep;9(3):312–326. [PubMed] [Google Scholar]
  26. 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]
  27. Martin P., Prakash L., Prakash S. a/alpha-specific effect on the mms3 mutation on ultraviolet mutagenesis in Saccharomyces cerevisiae. J Bacteriol. 1981 May;146(2):684–691. doi: 10.1128/jb.146.2.684-691.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Matsuura A., Treinin M., Mitsuzawa H., Kassir Y., Uno I., Simchen G. The adenylate cyclase/protein kinase cascade regulates entry into meiosis in Saccharomyces cerevisiae through the gene IME1. EMBO J. 1990 Oct;9(10):3225–3232. doi: 10.1002/j.1460-2075.1990.tb07521.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. McKee R. H., Lawrence C. W. Genetic analysis of gamma-ray mutagenesis in yeast. I. Reversion in radiation-sensitive strains. Genetics. 1979 Oct;93(2):361–373. doi: 10.1093/genetics/93.2.361. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. McKee R. H., Lawrence C. W. Genetic analysis of gamma-ray mutagenesis in yeast. II. Allele-specific control of mutagenesis. Genetics. 1979 Oct;93(2):375–381. doi: 10.1093/genetics/93.2.375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. McKee R. H., Lawrence C. W. Genetic analysis of gamma-ray mutagenesis in yeast. III. Double-mutant strains. Mutat Res. 1980 Mar;70(1):37–48. doi: 10.1016/0027-5107(80)90056-1. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. Morrison A., Christensen R. B., Alley J., Beck A. K., Bernstine E. G., Lemontt J. F., Lawrence C. W. REV3, a Saccharomyces cerevisiae gene whose function is required for induced mutagenesis, is predicted to encode a nonessential DNA polymerase. J Bacteriol. 1989 Oct;171(10):5659–5667. doi: 10.1128/jb.171.10.5659-5667.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Mowat M. R., Jachymczyk W. J., Hastings P. J., von Borstel R. C. Repair of gamma-ray induced DNA strand breaks in the radiation-sensitive mutant rad18-2 of Saccharomyces cerevisiae. Mol Gen Genet. 1983;189(2):256–262. doi: 10.1007/BF00337814. [DOI] [PubMed] [Google Scholar]
  35. Nasmyth K. A. Molecular genetics of yeast mating type. Annu Rev Genet. 1982;16:439–500. doi: 10.1146/annurev.ge.16.120182.002255. [DOI] [PubMed] [Google Scholar]
  36. Nasmyth K. A., Tatchell K., Hall B. D., Astell C., Smith M. A position effect in the control of transcription at yeast mating type loci. Nature. 1981 Jan 22;289(5795):244–250. doi: 10.1038/289244a0. [DOI] [PubMed] [Google Scholar]
  37. Nasmyth K., Shore D. Transcriptional regulation in the yeast life cycle. Science. 1987 Sep 4;237(4819):1162–1170. doi: 10.1126/science.3306917. [DOI] [PubMed] [Google Scholar]
  38. Reynolds R. J., Friedberg E. C. Molecular mechanisms of pyrimidine dimer excision in Saccharomyces cerevisiae: incision of ultraviolet-irradiated deoxyribonucleic acid in vivo. J Bacteriol. 1981 May;146(2):692–704. doi: 10.1128/jb.146.2.692-704.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Rong L., Palladino F., Aguilera A., Klein H. L. The hyper-gene conversion hpr5-1 mutation of Saccharomyces cerevisiae is an allele of the SRS2/RADH gene. Genetics. 1991 Jan;127(1):75–85. doi: 10.1093/genetics/127.1.75. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Saeki T., Machida I., Nakai S. Genetic control of diploid recovery after gamma-irradiation in the yeast Saccharomyces cerevisiae. Mutat Res. 1980 Dec;73(2):251–265. doi: 10.1016/0027-5107(80)90192-x. [DOI] [PubMed] [Google Scholar]
  41. Sauer R. T., Smith D. L., Johnson A. D. Flexibility of the yeast alpha 2 repressor enables it to occupy the ends of its operator, leaving the center free. Genes Dev. 1988 Jul;2(7):807–816. doi: 10.1101/gad.2.7.807. [DOI] [PubMed] [Google Scholar]
  42. Schiestl R. H., Prakash S., Prakash L. The SRS2 suppressor of rad6 mutations of Saccharomyces cerevisiae acts by channeling DNA lesions into the RAD52 DNA repair pathway. Genetics. 1990 Apr;124(4):817–831. doi: 10.1093/genetics/124.4.817. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Shah J. C., Clancy M. J. IME4, a gene that mediates MAT and nutritional control of meiosis in Saccharomyces cerevisiae. Mol Cell Biol. 1992 Mar;12(3):1078–1086. doi: 10.1128/mcb.12.3.1078. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. 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]
  45. Story R. M., Steitz T. A. Structure of the recA protein-ADP complex. Nature. 1992 Jan 23;355(6358):374–376. doi: 10.1038/355374a0. [DOI] [PubMed] [Google Scholar]
  46. Yamashita I., Takano Y., Fukui S. Control of STA1 gene expression by the mating-type locus in yeasts. J Bacteriol. 1985 Nov;164(2):769–773. doi: 10.1128/jb.164.2.769-773.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. di Caprio L., Cox B. S. DNA synthesis in UV-irradiated yeast. Mutat Res. 1981 Jun;82(1):69–85. doi: 10.1016/0027-5107(81)90139-1. [DOI] [PubMed] [Google Scholar]

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