Skip to main content
PMC home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1994 Dec 20;91(26):12711–12715. doi: 10.1073/pnas.91.26.12711

Transcriptional induction of Ty recombination in yeast.

Y Nevo-Caspi 1, M Kupiec 1
PMCID: PMC45509  PMID: 7809107

Abstract

Families of repeated sequences are present in the genomes of all eukaryotes. Little is known about the mechanism(s) that prevents recombination between repeated sequences. In the yeast Saccharomyces cerevisiae, recombination between homologous sequences placed at nonhomologous locations in the genome (ectopic recombination) has been shown to occur at high frequencies for artificially created repeats, but at relatively low frequencies for a natural family of repeated sequences, the Ty family. We have previously shown that a high level of Ty cDNA in the cell causes an increase in the rate of nonreciprocal recombination (gene conversion) of a marked Ty element. In the present study, we show that it is also possible to elevate the rate of recombination of a marked Ty by increasing its transcription. This induction is different from, and acts synergistically to, the one seen upon increased levels of donor Ty cDNA. We show that the induction by transcription does not require the products of the RAD50, RAD51, and RAD57 genes. In contrast, cDNA-mediated recombination is dependent on the product of the RAD51 gene but not on products of the genes RAD50 or RAD57.

Full text

PDF

Selected References

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

  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. Basile G., Aker M., Mortimer R. K. Nucleotide sequence and transcriptional regulation of the yeast recombinational repair gene RAD51. Mol Cell Biol. 1992 Jul;12(7):3235–3246. doi: 10.1128/mcb.12.7.3235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bell S. P., Kobayashi R., Stillman B. Yeast origin recognition complex functions in transcription silencing and DNA replication. Science. 1993 Dec 17;262(5141):1844–1849. doi: 10.1126/science.8266072. [DOI] [PubMed] [Google Scholar]
  4. Blackwell T. K., Moore M. W., Yancopoulos G. D., Suh H., Lutzker S., Selsing E., Alt F. W. Recombination between immunoglobulin variable region gene segments is enhanced by transcription. Nature. 1986 Dec 11;324(6097):585–589. doi: 10.1038/324585a0. [DOI] [PubMed] [Google Scholar]
  5. Boeke J. D., Garfinkel D. J., Styles C. A., Fink G. R. Ty elements transpose through an RNA intermediate. Cell. 1985 Mar;40(3):491–500. doi: 10.1016/0092-8674(85)90197-7. [DOI] [PubMed] [Google Scholar]
  6. Boeke J. D., LaCroute F., Fink G. R. A positive selection for mutants lacking orotidine-5'-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance. Mol Gen Genet. 1984;197(2):345–346. doi: 10.1007/BF00330984. [DOI] [PubMed] [Google Scholar]
  7. Bohr V. A., Smith C. A., Okumoto D. S., Hanawalt P. C. DNA repair in an active gene: removal of pyrimidine dimers from the DHFR gene of CHO cells is much more efficient than in the genome overall. Cell. 1985 Feb;40(2):359–369. doi: 10.1016/0092-8674(85)90150-3. [DOI] [PubMed] [Google Scholar]
  8. Curcio M. J., Garfinkel D. J. Posttranslational control of Ty1 retrotransposition occurs at the level of protein processing. Mol Cell Biol. 1992 Jun;12(6):2813–2825. doi: 10.1128/mcb.12.6.2813. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Engebrecht J., Roeder G. S. Yeast mer1 mutants display reduced levels of meiotic recombination. Genetics. 1989 Feb;121(2):237–247. doi: 10.1093/genetics/121.2.237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Feaver W. J., Svejstrup J. Q., Bardwell L., Bardwell A. J., Buratowski S., Gulyas K. D., Donahue T. F., Friedberg E. C., Kornberg R. D. Dual roles of a multiprotein complex from S. cerevisiae in transcription and DNA repair. Cell. 1993 Dec 31;75(7):1379–1387. doi: 10.1016/0092-8674(93)90624-y. [DOI] [PubMed] [Google Scholar]
  11. Fleig U. N., Pridmore R. D., Philippsen P. Construction of LYS2 cartridges for use in genetic manipulations of Saccharomyces cerevisiae. Gene. 1986;46(2-3):237–245. doi: 10.1016/0378-1119(86)90408-7. [DOI] [PubMed] [Google Scholar]
  12. Foss M., McNally F. J., Laurenson P., Rine J. Origin recognition complex (ORC) in transcriptional silencing and DNA replication in S. cerevisiae. Science. 1993 Dec 17;262(5141):1838–1844. doi: 10.1126/science.8266071. [DOI] [PubMed] [Google Scholar]
  13. Grimm C., Schaer P., Munz P., Kohli J. The strong ADH1 promoter stimulates mitotic and meiotic recombination at the ADE6 gene of Schizosaccharomyces pombe. Mol Cell Biol. 1991 Jan;11(1):289–298. doi: 10.1128/mcb.11.1.289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Jenuwein T., Forrester W. C., Qiu R. G., Grosschedl R. The immunoglobulin mu enhancer core establishes local factor access in nuclear chromatin independent of transcriptional stimulation. Genes Dev. 1993 Oct;7(10):2016–2032. doi: 10.1101/gad.7.10.2016. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Kupiec M., Petes T. D. Meiotic recombination between repeated transposable elements in Saccharomyces cerevisiae. Mol Cell Biol. 1988 Jul;8(7):2942–2954. doi: 10.1128/mcb.8.7.2942. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lauster R., Reynaud C. A., Mårtensson I. L., Peter A., Bucchini D., Jami J., Weill J. C. Promoter, enhancer and silencer elements regulate rearrangement of an immunoglobulin transgene. EMBO J. 1993 Dec;12(12):4615–4623. doi: 10.1002/j.1460-2075.1993.tb06150.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Leadon S. A., Lawrence D. A. Strand-selective repair of DNA damage in the yeast GAL7 gene requires RNA polymerase II. J Biol Chem. 1992 Nov 15;267(32):23175–23182. [PubMed] [Google Scholar]
  19. Lin F. L., Sperle K., Sternberg N. Model for homologous recombination during transfer of DNA into mouse L cells: role for DNA ends in the recombination process. Mol Cell Biol. 1984 Jun;4(6):1020–1034. doi: 10.1128/mcb.4.6.1020. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Malone R. E., Ward T., Lin S., Waring J. The RAD50 gene, a member of the double strand break repair epistasis group, is not required for spontaneous mitotic recombination in yeast. Curr Genet. 1990 Aug;18(2):111–116. doi: 10.1007/BF00312598. [DOI] [PubMed] [Google Scholar]
  21. McDonald J. P., Rothstein R. Unrepaired heteroduplex DNA in Saccharomyces cerevisiae is decreased in RAD1 RAD52-independent recombination. Genetics. 1994 Jun;137(2):393–405. doi: 10.1093/genetics/137.2.393. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Melamed C., Nevo Y., Kupiec M. Involvement of cDNA in homologous recombination between Ty elements in Saccharomyces cerevisiae. Mol Cell Biol. 1992 Apr;12(4):1613–1620. doi: 10.1128/mcb.12.4.1613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Micklem G., Rowley A., Harwood J., Nasmyth K., Diffley J. F. Yeast origin recognition complex is involved in DNA replication and transcriptional silencing. Nature. 1993 Nov 4;366(6450):87–89. doi: 10.1038/366087a0. [DOI] [PubMed] [Google Scholar]
  24. Nickoloff J. A. Transcription enhances intrachromosomal homologous recombination in mammalian cells. Mol Cell Biol. 1992 Dec;12(12):5311–5318. doi: 10.1128/mcb.12.12.5311. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Oltz E. M., Alt F. W., Lin W. C., Chen J., Taccioli G., Desiderio S., Rathbun G. A V(D)J recombinase-inducible B-cell line: role of transcriptional enhancer elements in directing V(D)J recombination. Mol Cell Biol. 1993 Oct;13(10):6223–6230. doi: 10.1128/mcb.13.10.6223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Parket A., Kupiec M. Ectopic recombination between Ty elements in Saccharomyces cerevisiae is not induced by DNA damage. Mol Cell Biol. 1992 Oct;12(10):4441–4448. doi: 10.1128/mcb.12.10.4441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Qiu H., Park E., Prakash L., Prakash S. The Saccharomyces cerevisiae DNA repair gene RAD25 is required for transcription by RNA polymerase II. Genes Dev. 1993 Nov;7(11):2161–2171. doi: 10.1101/gad.7.11.2161. [DOI] [PubMed] [Google Scholar]
  28. Rothstein R. J. One-step gene disruption in yeast. Methods Enzymol. 1983;101:202–211. doi: 10.1016/0076-6879(83)01015-0. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. Schaeffer L., Roy R., Humbert S., Moncollin V., Vermeulen W., Hoeijmakers J. H., Chambon P., Egly J. M. DNA repair helicase: a component of BTF2 (TFIIH) basic transcription factor. Science. 1993 Apr 2;260(5104):58–63. doi: 10.1126/science.8465201. [DOI] [PubMed] [Google Scholar]
  31. Selby C. P., Sancar A. Molecular mechanism of transcription-repair coupling. Science. 1993 Apr 2;260(5104):53–58. doi: 10.1126/science.8465200. [DOI] [PubMed] [Google Scholar]
  32. Shinohara A., Ogawa H., Ogawa T. Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell. 1992 May 1;69(3):457–470. doi: 10.1016/0092-8674(92)90447-k. [DOI] [PubMed] [Google Scholar]
  33. Steele D. F., Morris M. E., Jinks-Robertson S. Allelic and ectopic interactions in recombination-defective yeast strains. Genetics. 1991 Jan;127(1):53–60. doi: 10.1093/genetics/127.1.53. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Sweder K. S., Hanawalt P. C. Preferential repair of cyclobutane pyrimidine dimers in the transcribed strand of a gene in yeast chromosomes and plasmids is dependent on transcription. Proc Natl Acad Sci U S A. 1992 Nov 15;89(22):10696–10700. doi: 10.1073/pnas.89.22.10696. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Sweder K. S., Hanawalt P. C. Transcription-coupled DNA repair. Science. 1993 Oct 15;262(5132):439–440. doi: 10.1126/science.8211165. [DOI] [PubMed] [Google Scholar]
  36. Thomas B. J., Rothstein R. Elevated recombination rates in transcriptionally active DNA. Cell. 1989 Feb 24;56(4):619–630. doi: 10.1016/0092-8674(89)90584-9. [DOI] [PubMed] [Google Scholar]
  37. Voelkel-Meiman K., Roeder G. S. A chromosome containing HOT1 preferentially receives information during mitotic interchromosomal gene conversion. Genetics. 1990 Mar;124(3):561–572. doi: 10.1093/genetics/124.3.561. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. White M. A., Wierdl M., Detloff P., Petes T. D. DNA-binding protein RAP1 stimulates meiotic recombination at the HIS4 locus in yeast. Proc Natl Acad Sci U S A. 1991 Nov 1;88(21):9755–9759. doi: 10.1073/pnas.88.21.9755. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES