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PMID: 1996088 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

A unique pathway of double-strand break repair operates in tandemly repeated genes.

Molecular and cellular biology ·Vol. 11 ·No. 3 ·1991-03-00 ·Pages 1222-31

Ozenberger BA, Roeder GS

Abstract

The RAD52 gene product of the yeast Saccharomyces cerevisiae is required for most spontaneous recombination and almost all double-strand break (DSB) repair. In contrast to recombination elsewhere in the genome, recombination in the ribosomal DNA (rDNA) array is RAD52 independent. To determine the fate of a DSB in the rDNA gene array, a cut site for the HO endonuclease was inserted into the rDNA in a strain containing an inducible HO gene. DSBs were efficiently repaired at this site, even in the absence of the RAD52 gene product. Efficient RAD52-independent DSB repair was also observed at another tandem gene array, CUP1, consisting of 18 repeat units. However, in a smaller CUP1 array, consisting of only three units, most DSBs (ca. 80%) were not repaired and resulted in cell death. All RAD52-independent DSB repair events examined resulted in the loss of one or more repeat units. We propose a model for DSB repair in repeated sequences involving the generation of single-stranded tails followed by reannealing.

Related Genes
CUP12 RAD52 RDN
MeSH Terms
Blotting, Southern Cloning, Molecular DNA Repair DNA, Ribosomal/genetics Gene Conversion Genes, Fungal Recombination, Genetic Repetitive Sequences, Nucleic Acid Saccharomyces cerevisiae/genetics
Chemicals
DNA, Ribosomal
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Ozenberger B A
Department of Biology, Yale University, New Haven, CT 06511-8112.
Roeder G S
References (52)
52 references, click to expand
  1. Deletions and single base pair changes in the yeast mating type locus that prevent homothallic mating type conversions.
    Proc Natl Acad Sci U S A. 1983 Jun;80(11):3401-5 PMID: 6304708
  2. Gene conversion between duplicated genetic elements in yeast.
    Nature. 1981 Jul 23;292(5821):306-11 PMID: 6265790
  3. Different types of recombination events are controlled by the RAD1 and RAD52 genes of Saccharomyces cerevisiae.
    Genetics. 1988 Oct;120(2):367-77 PMID: 3058548
  4. Homothallic mating type switching generates lethal chromosome breaks in rad52 strains of Saccharomyces cerevisiae.
    Mol Cell Biol. 1981 Jun;1(6):522-34 PMID: 6765605
  5. The repair of double-strand breaks in DNA; a model involving recombination.
    J Theor Biol. 1976 Jun;59(1):97-106 PMID: 940351
  6. Ribosomal RNA genes of Saccharomyces cerevisiae. I. Physical map of the repeating unit and location of the regions coding for 5 S, 5.8 S, 18 S, and 25 S ribosomal RNAs.
    J Biol Chem. 1977 Nov 25;252(22):8118-25 PMID: 334774
  7. 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):1020-34 PMID: 6330525
  8. High-frequency transformation of yeast: autonomous replication of hybrid DNA molecules.
    Proc Natl Acad Sci U S A. 1979 Mar;76(3):1035-9 PMID: 375221
  9. Rad52-independent mitotic gene conversion in Saccharomyces cerevisiae frequently results in chromosomal loss.
    Genetics. 1985 Sep;111(1):7-22 PMID: 3896928
  10. Tandem gene amplification mediates copper resistance in yeast.
    Proc Natl Acad Sci U S A. 1982 Sep;79(17):5342-6 PMID: 6291039
  11. Electron microscopic observations on the meiotic karyotype of diploid and tetraploid Saccharomyces cerevisiae.
    Proc Natl Acad Sci U S A. 1975 Dec;72(12):5056-60 PMID: 1108011
  12. Mitotic recombination in the rDNA of S. cerevisiae is suppressed by the combined action of DNA topoisomerases I and II.
    Cell. 1988 Nov 4;55(3):413-25 PMID: 2902925
  13. Efficient repair of HO-induced chromosomal breaks in Saccharomyces cerevisiae by recombination between flanking homologous sequences.
    Mol Cell Biol. 1988 Sep;8(9):3918-28 PMID: 3065627
  14. Analysis of wild-type and rad50 mutants of yeast suggests an intimate relationship between meiotic chromosome synapsis and recombination.
    Cell. 1990 May 4;61(3):419-36 PMID: 2185891
  15. A new role for a yeast transcriptional silencer gene, SIR2, in regulation of recombination in ribosomal DNA.
    Cell. 1989 Mar 10;56(5):771-6 PMID: 2647300
  16. The repair of double-strand breaks in chromosomal DNA of yeast.
    Basic Life Sci. 1975;5B:549-56 PMID: 1103871
  17. Genetic control of radiation sensitivity in Saccharomyces cerevisiae.
    Genetics. 1969 Jul;62(3):519-31 PMID: 5384484
  18. Gene conversion adjacent to regions of double-strand break repair.
    Mol Cell Biol. 1988 Dec;8(12):5292-8 PMID: 3072478
  19. Regulation of yeast mating-type interconversion: feedback control of HO gene expression by the mating-type locus.
    Proc Natl Acad Sci U S A. 1983 May;80(10):3035-9 PMID: 6344075
  20. RED1: a yeast gene required for the segregation of chromosomes during the reductional division of meiosis.
    Proc Natl Acad Sci U S A. 1988 Aug;85(16):6057-61 PMID: 3413075
  21. A pathway for generation and processing of double-strand breaks during meiotic recombination in S. cerevisiae.
    Cell. 1990 Jun 15;61(6):1089-101 PMID: 2190690
  22. Homothallic switching of yeast mating type cassettes is initiated by a double-stranded cut in the MAT locus.
    Cell. 1982 Nov;31(1):183-92 PMID: 6297747
  23. Separation of large DNA molecules by contour-clamped homogeneous electric fields.
    Science. 1986 Dec 19;234(4783):1582-5 PMID: 3538420
  24. The redundancy of ribosomal and transfer RNA genes in Saccharomyces cerevisiae.
    J Mol Biol. 1969 Mar 14;40(2):261-77 PMID: 5365012
  25. A DNA double chain break stimulates triparental recombination in Saccharomyces cerevisiae.
    Proc Natl Acad Sci U S A. 1989 Aug;86(16):6225-9 PMID: 2668958
  26. Cis-acting, recombination-stimulating activity in a fragment of the ribosomal DNA of S. cerevisiae.
    Cell. 1984 Dec;39(2 Pt 1):377-86 PMID: 6094015
  27. Recombination of homologous DNA fragments transfected into mammalian cells occurs predominantly by terminal pairing.
    Mol Cell Biol. 1986 Sep;6(9):3246-52 PMID: 3023971
  28. Intra-chromosomal gene conversion induced by a DNA double-strand break in Saccharomyces cerevisiae.
    J Mol Biol. 1988 May 20;201(2):247-60 PMID: 3047399
  29. Characterization of a transcription factor involved in mother cell specific transcription of the yeast HO gene.
    EMBO J. 1988 Feb;7(2):485-94 PMID: 3284746
  30. One-step gene disruption in yeast.
    Methods Enzymol. 1983;101:202-11 PMID: 6310324
  31. Simple Mendelian inheritance of the reiterated ribosomal DNA of yeast.
    Proc Natl Acad Sci U S A. 1977 Nov;74(11):5091-5 PMID: 337310
  32. 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):503-7 PMID: 6987653
  33. Effects of the RAD52 Gene on Recombination in SACCHAROMYCES CEREVISIAE.
    Genetics. 1980 Jan;94(1):31-50 PMID: 17248995
  34. Yeast mer1 mutants display reduced levels of meiotic recombination.
    Genetics. 1989 Feb;121(2):237-47 PMID: 2659434
  35. Meiotic mapping of yeast ribosomal deoxyribonucleic acid on chromosome XII.
    J Bacteriol. 1979 Apr;138(1):185-92 PMID: 374364
  36. Evidence for two pathways of meiotic intrachromosomal recombination in yeast.
    Proc Natl Acad Sci U S A. 1989 Sep;86(18):7072-6 PMID: 2674944
  37. Degradation of linear DNA by a strand-specific exonuclease activity in Xenopus laevis oocytes.
    Mol Cell Biol. 1989 Nov;9(11):4862-71 PMID: 2601699
  38. The double-strand-break repair model for recombination.
    Cell. 1983 May;33(1):25-35 PMID: 6380756
  39. Intermediates of recombination during mating type switching in Saccharomyces cerevisiae.
    EMBO J. 1990 Mar;9(3):663-73 PMID: 2178924
  40. Genetic and physical analysis of double-strand break repair and recombination in Saccharomyces cerevisiae.
    Genetics. 1989 Jul;122(3):519-34 PMID: 2668114
  41. DNA double-chain breaks in recombination of phage lambda and of yeast.
    Annu Rev Genet. 1988;22:169-97 PMID: 2977087
  42. Repair of double-stranded DNA breaks by homologous DNA fragments during transfer of DNA into mouse L cells.
    Mol Cell Biol. 1990 Jan;10(1):113-9 PMID: 2294397
  43. Meiotic chromosome behavior in spread preparations of yeast.
    J Cell Biol. 1988 Mar;106(3):567-73 PMID: 2450094
  44. The Role of Radiation (rad) Genes in Meiotic Recombination in Yeast.
    Genetics. 1980 Jan;94(1):51-68 PMID: 17248996
  45. Intramolecular recombination between transfected repeated sequences in mammalian cells is nonconservative.
    Mol Cell Biol. 1986 Jul;6(7):2520-6 PMID: 3023937
  46. Primary structure and transcription of an amplified genetic locus: the CUP1 locus of yeast.
    Proc Natl Acad Sci U S A. 1984 Jan;81(2):337-41 PMID: 6364141
  47. A positive selection for mutants lacking orotidine-5'-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance.
    Mol Gen Genet. 1984;197(2):345-6 PMID: 6394957
  48. RecBC enzyme nicking at Chi sites during DNA unwinding: location and orientation-dependence of the cutting.
    Cell. 1985 May;41(1):153-63 PMID: 3888405
  49. Yeast transformation: a model system for the study of recombination.
    Proc Natl Acad Sci U S A. 1981 Oct;78(10):6354-8 PMID: 6273866
  50. Double-strand breaks at an initiation site for meiotic gene conversion.
    Nature. 1989 Mar 2;338(6210):87-90 PMID: 2645528
  51. Double-strand breaks stimulate alternative mechanisms of recombination repair.
    J Mol Biol. 1989 Jun 5;207(3):527-41 PMID: 2668534
  52. The repair of double-strand breaks in the nuclear DNA of Saccharomyces cerevisiae and its genetic control.
    Mol Gen Genet. 1976 Jan 16;143(2):119-29 PMID: 765749
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
DOI
10.1128/mcb.11.3.1222-1231.1991
Published
1991-03-00
Pages
1222-31
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC369393
Subset
IM
Grants
NIGMS NIH HHS · GM12952 · United States
NIGMS NIH HHS · GM28904 · United States
External Links
PubMed source DOI: 10.1128/mcb.11.3.1222-1231.1991 PMC Full Text View journal details
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