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PMID: 9475721 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Evidence for independent mismatch repair processing on opposite sides of a double-strand break in Saccharomyces cerevisiae.

Genetics ·Vol. 148 ·No. 1 ·1998-01-00 ·Pages 59-70

Weng YS, Nickoloff JA

Abstract

Double-strand break (DSB) induced gene conversion in Saccharomyces cerevisiae during meiosis and MAT switching is mediated primarily by mismatch repair of heteroduplex DNA (hDNA). We used nontandem ura3 duplications containing palindromic frameshift insertion mutations near an HO nuclease recognition site to test whether mismatch repair also mediates DSB-induced mitotic gene conversion at a non-MAT locus. Palindromic insertions included in hDNA are expected to produce a stem-loop mismatch, escape repair, and segregate to produce a sectored (Ura+/-) colony. If conversion occurs by gap repair, the insertion should be removed on both strands, and converted colonies will not be sectored. For both a 14-bp palindrome, and a 37-bp near-palindrome, approximately 75% of recombinant colonies were sectored, indicating that most DSB-induced mitotic gene conversion involves mismatch repair of hDNA. We also investigated mismatch repair of well-repaired markers flanking an unrepaired palindrome. As seen in previous studies, these additional markers increased loop repair (likely reflecting corepair). Among sectored products, few had additional segregating markers, indicating that the lack of repair at one marker is not associated with inefficient repair at nearby markers. Clear evidence was obtained for low levels of short tract mismatch repair. As seen with full gene conversions, donor alleles in sectored products were not altered. Markers on the same side of the DSB as the palindrome were involved in hDNA less often among sectored products than nonsectored products, but markers on the opposite side of the DSB showed similar hDNA involvement among both product classes. These results can be explained in terms of corepair, and they suggest that mismatch repair on opposite sides of a DSB involves distinct repair tracts.

MeSH Terms
Alleles DNA Damage/genetics DNA Repair/genetics DNA, Fungal/genetics Frameshift Mutation Fungal Proteins/genetics Genetic Markers/genetics Nucleic Acid Heteroduplexes/genetics Saccharomyces cerevisiae/genetics
Chemicals
DNA, Fungal Fungal Proteins Genetic Markers Nucleic Acid Heteroduplexes
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Weng Y S
Department of Cancer Biology, Harvard University School of Public Health, Boston, Massachusetts 02115, USA.
Nickoloff J A
References (61)
61 references, click to expand
  1. The double-strand-break repair model for recombination.
    Cell. 1983 May;33(1):25-35 PMID: 6380756
  2. Double-strand break-induced mitotic gene conversion: examination of tract polarity and products of multiple recombinational repair events.
    Curr Genet. 1996 Mar;29(4):335-43 PMID: 8598054
  3. A 24-base-pair DNA sequence from the MAT locus stimulates intergenic recombination in yeast.
    Proc Natl Acad Sci U S A. 1986 Oct;83(20):7831-5 PMID: 3020559
  4. Mitotic gene conversion lengths, coconversion patterns, and the incidence of reciprocal recombination in a Saccharomyces cerevisiae plasmid system.
    Mol Cell Biol. 1986 Nov;6(11):3685-93 PMID: 3540599
  5. Meiotic recombination in yeast: alteration by multiple heterozygosities.
    Science. 1987 Sep 18;237(4821):1459-65 PMID: 2820060
  6. Intrachromosomal recombination in Saccharomyces cerevisiae: reciprocal exchange in an inverted repeat and associated gene conversion.
    Genetics. 1987 Dec;117(4):633-43 PMID: 2828154
  7. Expansions and contractions of the genetic map relative to the physical map of yeast chromosome III.
    Mol Cell Biol. 1988 Feb;8(2):595-604 PMID: 2832729
  8. Mitotic sectored colonies: evidence of heteroduplex DNA formation during direct repeat recombination.
    Proc Natl Acad Sci U S A. 1988 Apr;85(8):2696-700 PMID: 3282237
  9. Physical lengths of meiotic and mitotic gene conversion tracts in Saccharomyces cerevisiae.
    Genetics. 1988 Mar;118(3):401-10 PMID: 2835285
  10. Differential mismatch repair can explain the disproportionalities between physical distances and recombination frequencies of cyc1 mutations in yeast.
    Genetics. 1988 May;119(1):21-34 PMID: 3294098
  11. 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
  12. Double-strand breaks at an initiation site for meiotic gene conversion.
    Nature. 1989 Mar 2;338(6210):87-90 PMID: 2645528
  13. Coconversion of flanking sequences with homothallic switching.
    Cell. 1989 May 5;57(3):459-67 PMID: 2541914
  14. Palindromic sequences in heteroduplex DNA inhibit mismatch repair in yeast.
    Nature. 1989 Jul 27;340(6231):318-20 PMID: 2546083
  15. Double-strand breaks stimulate alternative mechanisms of recombination repair.
    J Mol Biol. 1989 Jun 5;207(3):527-41 PMID: 2668534
  16. Length and distribution of meiotic gene conversion tracts and crossovers in Saccharomyces cerevisiae.
    Genetics. 1989 Sep;123(1):69-80 PMID: 2680758
  17. Yeast intrachromosomal recombination: long gene conversion tracts are preferentially associated with reciprocal exchange and require the RAD1 and RAD3 gene products.
    Genetics. 1989 Dec;123(4):683-94 PMID: 2558957
  18. In vivo analysis of the Saccharomyces cerevisiae HO nuclease recognition site by site-directed mutagenesis.
    Mol Cell Biol. 1990 Mar;10(3):1174-9 PMID: 2406563
  19. Intermediates of recombination during mating type switching in Saccharomyces cerevisiae.
    EMBO J. 1990 Mar;9(3):663-73 PMID: 2178924
  20. 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
  21. Meiotic recombination between dispersed repeated genes is associated with heteroduplex formation.
    Mol Cell Biol. 1990 Aug;10(8):4420-3 PMID: 2196454
  22. Detection of heteroduplex DNA molecules among the products of Saccharomyces cerevisiae meiosis.
    Proc Natl Acad Sci U S A. 1990 Oct;87(19):7653-7 PMID: 2217196
  23. Extensive 3'-overhanging, single-stranded DNA associated with the meiosis-specific double-strand breaks at the ARG4 recombination initiation site.
    Cell. 1991 Mar 22;64(6):1155-61 PMID: 2004421
  24. Spontaneous mutation at a 5-methylcytosine hotspot is prevented by very short patch (VSP) mismatch repair.
    Genetics. 1991 May;128(1):23-7 PMID: 1829427
  25. Subcloning with new ampicillin- and kanamycin-resistant analogs of pUC19.
    Biotechniques. 1991 Apr;10(4):469-70, 472 PMID: 1867854
  26. Heteroduplex formation and mismatch repair of the "stuck" mutation during mating-type switching in Saccharomyces cerevisiae.
    Mol Cell Biol. 1991 Oct;11(10):5372-80 PMID: 1922052
  27. Seven-base-pair inverted repeats in DNA form stable hairpins in vivo in Saccharomyces cerevisiae.
    Genetics. 1991 Nov;129(3):669-73 PMID: 1752412
  28. Measurements of excision repair tracts formed during meiotic recombination in Saccharomyces cerevisiae.
    Mol Cell Biol. 1992 Apr;12(4):1805-14 PMID: 1549127
  29. Mechanisms and biological effects of mismatch repair.
    Annu Rev Genet. 1991;25:229-53 PMID: 1812808
  30. Effects of terminal nonhomology and homeology on double-strand-break-induced gene conversion tract directionality.
    Mol Cell Biol. 1996 Jun;16(6):2951-7 PMID: 8649406
  31. The Saccharomyces cerevisiae Msh2 and Msh6 proteins form a complex that specifically binds to duplex oligonucleotides containing mismatched DNA base pairs.
    Mol Cell Biol. 1996 Oct;16(10):5604-15 PMID: 8816473
  32. Poorly repaired mismatches in heteroduplex DNA are hyper-recombinagenic in Saccharomyces cerevisiae.
    Genetics. 1996 Feb;142(2):407-16 PMID: 8852840
  33. A test of the double-strand break repair model for meiotic recombination in Saccharomyces cerevisiae.
    Genetics. 1996 Sep;144(1):27-41 PMID: 8878671
  34. Influence of DNA sequence identity on efficiency of targeted gene replacement.
    Mol Cell Biol. 1997 Jan;17(1):278-86 PMID: 8972208
  35. Repair of DNA loops involves DNA-mismatch and nucleotide-excision repair proteins.
    Nature. 1997 Jun 26;387(6636):929-31 PMID: 9202128
  36. Nonselective URA3 colony-color assay in yeast ade1 or ade2 mutants.
    Biotechniques. 1997 Aug;23(2):237-41 PMID: 9266076
  37. A general model for genetic recombination.
    Proc Natl Acad Sci U S A. 1975 Jan;72(1):358-61 PMID: 1054510
  38. Evidence that spontaneous mitotic recombination occurs at the two-strand stage.
    Proc Natl Acad Sci U S A. 1978 Sep;75(9):4436-40 PMID: 360220
  39. 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
  40. Insertions, deletions and mismatches in heteroduplex DNA made by recA protein.
    Cell. 1983 Dec;35(2 Pt 1):511-20 PMID: 6317195
  41. Analysis of a gene conversion gradient at the HIS4 locus in Saccharomyces cerevisiae.
    Genetics. 1992 Sep;132(1):113-23 PMID: 1398048
  42. Removal of nonhomologous DNA ends in double-strand break recombination: the role of the yeast ultraviolet repair gene RAD1.
    Science. 1992 Oct 16;258(5081):480-4 PMID: 1411547
  43. Sister chromatids are preferred over homologs as substrates for recombinational repair in Saccharomyces cerevisiae.
    Genetics. 1992 Oct;132(2):387-402 PMID: 1427035
  44. Chi enhances heteroduplex DNA levels during recombination.
    Genetics. 1992 Dec;132(4):879-91 PMID: 1459441
  45. Physical detection of heteroduplexes during meiotic recombination in the yeast Saccharomyces cerevisiae.
    Mol Cell Biol. 1993 Apr;13(4):2324-31 PMID: 8455614
  46. Marker effects of G to C transversions on intragenic recombination and mismatch repair in Schizosaccharomyces pombe.
    Genetics. 1993 Apr;133(4):825-35 PMID: 8462844
  47. Rapid kinetics of mismatch repair of heteroduplex DNA that is formed during recombination in yeast.
    Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3363-7 PMID: 8475081
  48. Meiosis-induced double-strand break sites determined by yeast chromatin structure.
    Science. 1994 Jan 28;263(5146):515-8 PMID: 8290959
  49. A sister-strand exchange mechanism for recA-independent deletion of repeated DNA sequences in Escherichia coli.
    Genetics. 1993 Nov;135(3):631-42 PMID: 8293969
  50. Efficient copying of nonhomologous sequences from ectopic sites via P-element-induced gap repair.
    Mol Cell Biol. 1994 Mar;14(3):1613-25 PMID: 8114699
  51. Efficient removal of uracil from G.U mispairs by the mismatch-specific thymine DNA glycosylase from HeLa cells.
    Proc Natl Acad Sci U S A. 1994 Mar 1;91(5):1642-6 PMID: 8127859
  52. Mismatch repair proteins MutS and MutL inhibit RecA-catalyzed strand transfer between diverged DNAs.
    Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):3238-41 PMID: 8159731
  53. One-sided invasion events in homologous recombination at double-strand breaks.
    Mutat Res. 1994 May;314(3):199-208 PMID: 7513053
  54. Fine-resolution mapping of spontaneous and double-strand break-induced gene conversion tracts in Saccharomyces cerevisiae reveals reversible mitotic conversion polarity.
    Mol Cell Biol. 1994 Jun;14(6):3863-75 PMID: 8196629
  55. Induction of recombination between homologous and diverged DNAs by double-strand gaps and breaks and role of mismatch repair.
    Mol Cell Biol. 1994 Jul;14(7):4802-14 PMID: 8007979
  56. Recombinators, recombinases and recombination genes of yeasts.
    Curr Genet. 1994 Jan;25(1):1-11 PMID: 8082158
  57. The Saccharomyces cerevisiae Msh2 protein specifically binds to duplex oligonucleotides containing mismatched DNA base pairs and insertions.
    Genes Dev. 1995 Jan 15;9(2):234-47 PMID: 7851796
  58. Efficient marker rescue and domain replacement without fragment subcloning.
    Anal Biochem. 1995 Jan 1;224(1):440-3 PMID: 7710108
  59. The nucleotide mapping of DNA double-strand breaks at the CYS3 initiation site of meiotic recombination in Saccharomyces cerevisiae.
    EMBO J. 1995 Sep 15;14(18):4589-98 PMID: 7556102
  60. Transfer of episomal and integrated plasmids from Saccharomyces cerevisiae to Escherichia coli by electroporation.
    Methods Mol Biol. 1995;47:55-66 PMID: 7550754
  61. Evidence for inclusion of regions of nonhomology in heteroduplex products of bacteriophage lambda recombination.
    Proc Natl Acad Sci U S A. 1984 Nov;81(22):7180-4 PMID: 6239288
Article Info
Journal
Genetics
Abbr.
Genetics
ISSN
0016-6731
Published
1998-01-00
Pages
59-70
Language
English
Region
United States
NLM ID
0374636
PMCID
PMC1459773
Subset
IM
Grants
NCI NIH HHS · CA55302 · United States
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