Interaction Between Mismatch Repair and Genetic Recombination in Saccharomyces cerevisiae

INVESTIGATIONS

Interaction Between Mismatch Repair and Genetic Recombination in Saccharomyces cerevisiae

E. Alani, RAG. Reenan and R. D. Kolodner
Division of Cellular and Molecular Biology, The Dana Farber Cancer Institute, Boston, Massachusetts 02115, and Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, Massachusetts 02115

The yeast Saccharomyces cerevisiae encodes a set of genes that show strong amino acid sequence similarity to MutS and MutL, proteins required for mismatch repair in Escherichia coli. We examined the role of MSH2 and PMS1, yeast homologs of mutS and mutL, respectively, in the repair of base pair mismatches formed during meiotic recombination. By using specifically marked HIS4 and ARG4 alleles, we showed that msh2 mutants displayed a severe defect in the repair of all base pair mismatches as well as 1-, 2- and 4-bp insertion/deletion mispairs. The msh2 and pms1 phenotypes were indistinguishable, suggesting that the wild-type gene products act in the same repair pathway. A comparison of gene conversion events in wild-type and msh2 mutants indicated that mismatch repair plays an important role in genetic recombination. (1) Tetrad analysis at five different loci revealed that, in msh2 mutants, the majority of aberrant segregants displayed a sectored phenotype, consistent with a failure to repair mismatches created during heteroduplex formation. In wild type, base pair mismatches were almost exclusively repaired toward conversion rather than restoration. (2) In msh2 strains 10-19% of the aberrant tetrads were Ab4:4. (3) Polarity gradients at HIS4 and ARG4 were nearly abolished in msh2 mutants. The frequency of gene conversion at the 3' end of these genes was increased and was nearly the frequency observed at the 5' end. (4) Co-conversion studies were consistent with mismatch repair acting to regulate heteroduplex DNA tract length. We favor a model proposing that recombination events occur through the formation and resolution of heteroduplex intermediates and that mismatch repair proteins specifically interact with recombination enzymes to regulate the length of symmetric heteroduplex DNA.

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				E. R. Hoffmann, E. Eriksson, B. J. Herbert, and R. H. Borts MLH1 and MSH2 Promote the Symmetry of Double-Strand Break Repair Events at the HIS4 Hotspot in Saccharomyces cerevisiae Genetics, March 1, 2005; 169(3): 1291 - 1303. [Abstract] [Full Text] [PDF]

				R. M. Spell and S. Jinks-Robertson Examination of the Roles of Sgs1 and Srs2 Helicases in the Enforcement of Recombination Fidelity in Saccharomyces cerevisiae Genetics, December 1, 2004; 168(4): 1855 - 1865. [Abstract] [Full Text] [PDF]

				R. J. Pratt, D. W. Lee, and R. Aramayo DNA Methylation Affects Meiotic trans-sensing, Not Meiotic Silencing, in Neurospora Genetics, December 1, 2004; 168(4): 1925 - 1935. [Abstract] [Full Text] [PDF]

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				L. Maloisel, J. Bhargava, and G. S. Roeder A Role for DNA Polymerase {delta} in Gene Conversion and Crossing Over During Meiosis in Saccharomyces cerevisiae Genetics, July 1, 2004; 167(3): 1133 - 1142. [Abstract] [Full Text] [PDF]

				N. Sugawara, T. Goldfarb, B. Studamire, E. Alani, and J. E. Haber Heteroduplex rejection during single-strand annealing requires Sgs1 helicase and mismatch repair proteins Msh2 and Msh6 but not Pms1 PNAS, June 22, 2004; 101(25): 9315 - 9320. [Abstract] [Full Text] [PDF]

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				J. S. Bell and R. McCulloch Mismatch Repair Regulates Homologous Recombination, but Has Little Influence on Antigenic Variation, in Trypanosoma brucei J. Biol. Chem., November 14, 2003; 278(46): 45182 - 45188. [Abstract] [Full Text] [PDF]

				J. D. Merker, M. Dominska, and T. D. Petes Patterns of Heteroduplex Formation Associated With the Initiation of Meiotic Recombination in the Yeast Saccharomyces cerevisiae Genetics, September 1, 2003; 165(1): 47 - 63. [Abstract] [Full Text] [PDF]

				V. N. Dobrovolsky, P. B. McKinzie, J. G. Shaddock, R. A. Mittelstaedt, R. H. Heflich, and B. L. Parsons Pms2 deficiency results in increased mutation in the Hprt gene but not the Tk gene of Tk+/- transgenic mice Mutagenesis, July 1, 2003; 18(4): 365 - 370. [Abstract] [Full Text] [PDF]

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				A. Mohindra, L. E. Hays, E. N. Phillips, B. D. Preston, T. Helleday, and M. Meuth Defects in homologous recombination repair in mismatch-repair-deficient tumour cell lines Hum. Mol. Genet., September 1, 2002; 11(18): 2189 - 2200. [Abstract] [Full Text] [PDF]

				J. A. Birdsell Integrating Genomics, Bioinformatics, and Classical Genetics to Study the Effects of Recombination on Genome Evolution Mol. Biol. Evol., July 1, 2002; 19(7): 1181 - 1197. [Abstract] [Full Text] [PDF]

				J. L. Argueso, D. Smith, J. Yi, M. Waase, S. Sarin, and E. Alani Analysis of Conditional Mutations in the Saccharomyces cerevisiae MLH1 Gene in Mismatch Repair and in Meiotic Crossing Over Genetics, March 1, 2002; 160(3): 909 - 921. [Abstract] [Full Text] [PDF]

				C.-G. Gendrel and M. Dutreix (CA/TG) Microsatellite Sequences Escape the Inhibition of Recombination by Mismatch Repair in Saccharomyces cerevisiae Genetics, December 1, 2001; 159(4): 1539 - 1545. [Abstract] [Full Text] [PDF]