Skip to main content
PMC home page
Genetics logoLink to Genetics
. 1988 Aug;119(4):779–790. doi: 10.1093/genetics/119.4.779

Genetic Control of Intrachromosomal Recombination in Saccharomyces Cerevisiae. I. Isolation and Genetic Characterization of Hyper-Recombination Mutations

A Aguilera 1, H L Klein 1
PMCID: PMC1203464  PMID: 3044923

Abstract

Eight complementation groups have been defined for recessive mutations conferring an increased mitotic intrachromosomal recombination phenotype (hpr genes) in Saccharomyces cerevisiae. Some of the mutations preferentially increase intrachromosomal gene conversion (hpr4, hpr5 and hpr8) between repeated sequences, some increase loss of a marker between duplicated genes (hpr1 and hpr6), and some increase both types of events (hpr2, hpr3 and hpr7). New alleles of the CDC2 and CDC17 genes were recovered among these mutants. The mutants were also characterized for sensitivity to DNA damaging agents and for mutator activity. Among the more interesting mutants are hpr5, which shows a biased gene conversion in a leu2-112::URA3::leu2-k duplication; and hpr1, which has a much weaker effect on interchromosomal mitotic recombination than on intrachromosomal mitotic recombination. These analyses suggest that gene conversion and reciprocal exchange can be separated mutationally. Further studies are required to show whether different recombination pathways or different outcomes of the same recombination pathway are controlled by the genes identified in this study.

Full Text

The Full Text of this article is available as a PDF (2.2 MB).

Selected References

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

  1. Arthur H. M., Lloyd R. G. Hyper-recombination in uvrD mutants of Escherichia coli K-12. Mol Gen Genet. 1980;180(1):185–191. doi: 10.1007/BF00267368. [DOI] [PubMed] [Google Scholar]
  2. Baltimore D. Gene conversion: some implications for immunoglobulin genes. Cell. 1981 Jun;24(3):592–594. doi: 10.1016/0092-8674(81)90082-9. [DOI] [PubMed] [Google Scholar]
  3. Borts R. H., Haber J. E. Meiotic recombination in yeast: alteration by multiple heterozygosities. Science. 1987 Sep 18;237(4821):1459–1465. doi: 10.1126/science.2820060. [DOI] [PubMed] [Google Scholar]
  4. Borts R. H., Lichten M., Haber J. E. Analysis of meiosis-defective mutations in yeast by physical monitoring of recombination. Genetics. 1986 Jul;113(3):551–567. doi: 10.1093/genetics/113.3.551. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Carson M. J., Hartwell L. CDC17: an essential gene that prevents telomere elongation in yeast. Cell. 1985 Aug;42(1):249–257. doi: 10.1016/s0092-8674(85)80120-3. [DOI] [PubMed] [Google Scholar]
  6. Clewell D. B., Helinski D. R. Properties of a supercoiled deoxyribonucleic acid-protein relaxation complex and strand specificity of the relaxation event. Biochemistry. 1970 Oct 27;9(22):4428–4440. doi: 10.1021/bi00824a026. [DOI] [PubMed] [Google Scholar]
  7. Conrad M. N., Newlon C. S. Saccharomyces cerevisiae cdc2 mutants fail to replicate approximately one-third of their nuclear genome. Mol Cell Biol. 1983 Jun;3(6):1000–1012. doi: 10.1128/mcb.3.6.1000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Eckardt-Schupp F., Siede W., Game J. C. The RAD24 (= Rs1) gene product of Saccharomyces cerevisiae participates in two different pathways of DNA repair. Genetics. 1987 Jan;115(1):83–90. doi: 10.1093/genetics/115.1.83. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Egel R. Intergenic conversion and reiterated genes. Nature. 1981 Mar 19;290(5803):191–192. doi: 10.1038/290191a0. [DOI] [PubMed] [Google Scholar]
  10. Ernst J. F., Hampsey D. M., Sherman F. DNA sequences of frameshift and other mutations induced by ICR-170 in yeast. Genetics. 1985 Oct;111(2):233–241. doi: 10.1093/genetics/111.2.233. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ernst J. F., Stewart J. W., Sherman F. The cyc1-11 mutation in yeast reverts by recombination with a nonallelic gene: composite genes determining the iso-cytochromes c. Proc Natl Acad Sci U S A. 1981 Oct;78(10):6334–6338. doi: 10.1073/pnas.78.10.6334. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Esposito M. S., Hosoda J., Golin J., Moise H., Bjornstad K., Maleas D. Recombination in Saccharomyces cerevisiae: REC-gene mutants and DNA-binding proteins. Cold Spring Harb Symp Quant Biol. 1984;49:41–48. doi: 10.1101/sqb.1984.049.01.007. [DOI] [PubMed] [Google Scholar]
  13. Feinberg A. P., Vogelstein B. "A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity". Addendum. Anal Biochem. 1984 Feb;137(1):266–267. doi: 10.1016/0003-2697(84)90381-6. [DOI] [PubMed] [Google Scholar]
  14. Feinstein S. I., Low K. B. Hyper-recombining recipient strains in bacterial conjugation. Genetics. 1986 May;113(1):13–33. doi: 10.1093/genetics/113.1.13. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Game J. C., Johnston L. H., von Borstel R. C. Enhanced mitotic recombination in a ligase-defective mutant of the yeast Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4589–4592. doi: 10.1073/pnas.76.9.4589. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hamza H., Kalogeropoulos A., Nicolas A., Rossignol J. L. Two mechanisms for directional gene conversion. Proc Natl Acad Sci U S A. 1986 Oct;83(19):7386–7390. doi: 10.1073/pnas.83.19.7386. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hartwell L. H., Smith D. Altered fidelity of mitotic chromosome transmission in cell cycle mutants of S. cerevisiae. Genetics. 1985 Jul;110(3):381–395. doi: 10.1093/genetics/110.3.381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hurst D. D., Fogel S., Mortimer R. K. Conversion-associated recombination in yeast (hybrids-meiosis-tetrads-marker loci-models). Proc Natl Acad Sci U S A. 1972 Jan;69(1):101–105. doi: 10.1073/pnas.69.1.101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Jackson J. A., Fink G. R. Gene conversion between duplicated genetic elements in yeast. Nature. 1981 Jul 23;292(5821):306–311. doi: 10.1038/292306a0. [DOI] [PubMed] [Google Scholar]
  20. Jackson J. A., Fink G. R. Meiotic recombination between duplicated genetic elements in Saccharomyces cerevisiae. Genetics. 1985 Feb;109(2):303–332. doi: 10.1093/genetics/109.2.303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Jinks-Robertson S., Petes T. D. Chromosomal translocations generated by high-frequency meiotic recombination between repeated yeast genes. Genetics. 1986 Nov;114(3):731–752. doi: 10.1093/genetics/114.3.731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Jinks-Robertson S., Petes T. D. High-frequency meiotic gene conversion between repeated genes on nonhomologous chromosomes in yeast. Proc Natl Acad Sci U S A. 1985 May;82(10):3350–3354. doi: 10.1073/pnas.82.10.3350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Johnston L. H., Nasmyth K. A. Saccharomyces cerevisiae cell cycle mutant cdc9 is defective in DNA ligase. Nature. 1978 Aug 31;274(5674):891–893. doi: 10.1038/274891a0. [DOI] [PubMed] [Google Scholar]
  24. Kern R., Zimmermann F. K. The influence of defects in excision and error prone repair on spontaneous and induced mitotic recombination and mutation in Saccharomyces cerevisiae. Mol Gen Genet. 1978 Apr 25;161(1):81–88. doi: 10.1007/BF00266618. [DOI] [PubMed] [Google Scholar]
  25. Klein H. L. Lack of association between intrachromosomal gene conversion and reciprocal exchange. 1984 Aug 30-Sep 5Nature. 310(5980):748–753. doi: 10.1038/310748a0. [DOI] [PubMed] [Google Scholar]
  26. Klein H. L., Petes T. D. Intrachromosomal gene conversion in yeast. Nature. 1981 Jan 15;289(5794):144–148. doi: 10.1038/289144a0. [DOI] [PubMed] [Google Scholar]
  27. Konrad E. B. Method for the isolation of Escherichia coli mutants with enhanced recombination between chromosomal duplications. J Bacteriol. 1977 Apr;130(1):167–172. doi: 10.1128/jb.130.1.167-172.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Kowalski S., Laskowski W. The effect of three rad genes on survival, inter- and intragenic mitotic recombination in Saccharomyces. I. UV irradiation without photoreactivation or liquid-holding post-treatment. Mol Gen Genet. 1975;136(1):75–86. doi: 10.1007/BF00275450. [DOI] [PubMed] [Google Scholar]
  29. Kunz B. A., Haynes R. H. Phenomenology and genetic control of mitotic recombination in yeast. Annu Rev Genet. 1981;15:57–89. doi: 10.1146/annurev.ge.15.120181.000421. [DOI] [PubMed] [Google Scholar]
  30. Lichten M., Borts R. H., Haber J. E. Meiotic gene conversion and crossing over between dispersed homologous sequences occurs frequently in Saccharomyces cerevisiae. Genetics. 1987 Feb;115(2):233–246. doi: 10.1093/genetics/115.2.233. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. 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]
  32. Malone R. E., Esposito R. E. The RAD52 gene is required for homothallic interconversion of mating types and spontaneous mitotic recombination in yeast. Proc Natl Acad Sci U S A. 1980 Jan;77(1):503–507. doi: 10.1073/pnas.77.1.503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Maloney D. H., Fogel S. Mitotic recombination in yeast: isolation and characterization of mutants with enhanced spontaneous mitotic gene conversion rates. Genetics. 1980 Apr;94(4):825–839. doi: 10.1093/genetics/94.4.825. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Marinus M. G., Konrad E. B. Hyper-recombination in dam mutants of Escherichia coli K-12. Mol Gen Genet. 1976 Dec 22;149(3):273–277. doi: 10.1007/BF00268528. [DOI] [PubMed] [Google Scholar]
  35. Mathison L., Culbertson M. R. Suppressible and nonsuppressible +1 G-C base pair insertions induced by ICR-170 at the his4 locus in Saccharomyces cerevisiae. Mol Cell Biol. 1985 Sep;5(9):2247–2256. doi: 10.1128/mcb.5.9.2247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Meselson M. S., Radding C. M. A general model for genetic recombination. Proc Natl Acad Sci U S A. 1975 Jan;72(1):358–361. doi: 10.1073/pnas.72.1.358. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Mikus M. D., Petes T. D. Recombination between genes located on nonhomologous chromosomes in Saccharomyces cerevisiae. Genetics. 1982 Jul-Aug;101(3-4):369–404. doi: 10.1093/genetics/101.3-4.369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Montelone B. A., Hoekstra M. F., Malone R. E. Spontaneous mitotic recombination in yeast: the hyper-recombinational rem1 mutations are alleles of the RAD3 gene. Genetics. 1988 Jun;119(2):289–301. doi: 10.1093/genetics/119.2.289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Prakash L., Strauss B. Repair of alkylation damage: stability of methyl groups in Bacillus subtilis treated with methyl methanesulfonate. J Bacteriol. 1970 Jun;102(3):760–766. doi: 10.1128/jb.102.3.760-766.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. ROMAN H. Studies of gene mutation in Saccharomyces. Cold Spring Harb Symp Quant Biol. 1956;21:175–185. doi: 10.1101/sqb.1956.021.01.015. [DOI] [PubMed] [Google Scholar]
  41. Resnick M. A. Genetic control of radiation sensitivity in Saccharomyces cerevisiae. Genetics. 1969 Jul;62(3):519–531. doi: 10.1093/genetics/62.3.519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Roberts J. M., Buck L. B., Axel R. A structure for amplified DNA. Cell. 1983 May;33(1):53–63. doi: 10.1016/0092-8674(83)90334-3. [DOI] [PubMed] [Google Scholar]
  43. Scherer S., Davis R. W. Recombination of dispersed repeated DNA sequences in yeast. Science. 1980 Sep 19;209(4463):1380–1384. doi: 10.1126/science.6251545. [DOI] [PubMed] [Google Scholar]
  44. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  45. Szostak J. W., Orr-Weaver T. L., Rothstein R. J., Stahl F. W. The double-strand-break repair model for recombination. Cell. 1983 May;33(1):25–35. doi: 10.1016/0092-8674(83)90331-8. [DOI] [PubMed] [Google Scholar]
  46. Varmus H. E., Quintrell N., Ortiz S. Retroviruses as mutagens: insertion and excision of a nontransforming provirus alter expression of a resident transforming provirus. Cell. 1981 Jul;25(1):23–36. doi: 10.1016/0092-8674(81)90228-2. [DOI] [PubMed] [Google Scholar]
  47. Wagstaff J. E., Klapholz S., Waddell C. S., Jensen L., Esposito R. E. Meiotic exchange within and between chromosomes requires a common Rec function in Saccharomyces cerevisiae. Mol Cell Biol. 1985 Dec;5(12):3532–3544. doi: 10.1128/mcb.5.12.3532. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Willis K. K., Klein H. L. Intrachromosomal recombination in Saccharomyces cerevisiae: reciprocal exchange in an inverted repeat and associated gene conversion. Genetics. 1987 Dec;117(4):633–643. doi: 10.1093/genetics/117.4.633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Zieg J., Maples V. F., Kushner S. R. Recombinant levels of Escherichia coli K-12 mutants deficient in various replication, recombination, or repair genes. J Bacteriol. 1978 Jun;134(3):958–966. doi: 10.1128/jb.134.3.958-966.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES