A Mutation in the Gene Encoding the Saccharomyces cerevisiae Single-Stranded DNA-Binding Protein Rfa1 Stimulates a RAD52-Independent Pathway for Direct-Repeat Recombination

REFERENCES

• Aboussekhra, A., R. Chanet, Z. Zgaga, C. Cassier-Chauvat, M. Heude, and F. Fabre. 1989. RADH, a gene of Saccharomyces cerevisiae encoding a putative DNA helicase involved in DNA repair. Nucleic Acids Res. 17:7211–7219.
   PubMedGoogle Scholar
• Adachi, Y., and U. K. Laemmli. 1992. Identification of nuclear pre-replication centers poised for DNA synthesis in Xenopus egg extracts: immunolo-calization study of replication protein A. J. Cell Biol. 119:1–15.
   PubMedGoogle Scholar
• Aguilera, A., and H. L. Klein. 1988. Genetic control of intrachromosomal recombination in Saccharomyces cerevisiae. I. Isolation and genetic charac-terization of hyper-recombination mutations. Genetics 119:779–790.
   Google Scholar
• Alonso, J. C., G. Luder, and R. H. Tailor. 1991. Characterization of Bacillus subtilis recombinational pathways. J. Bacteriol. 173:3977–3980.
   PubMedGoogle Scholar
• Bailly, V., C. H. Sommers, P. Sung, L. Prakash, and S. Prakash. 1992. Specific complex formation between proteins encoded by the yeast DNA repair and recombination genes RAD1 and RAD10. Proc. Natl. Acad. Sci. USA 89:8273–8277.
   PubMedGoogle Scholar
• Balbinder, E. 1993. Multiple pathways of deletion formation in Escherichia coli. Mutat. Res. 299:193–209.
   PubMedGoogle Scholar
• Barbour, S. D., H. Nagaishi, A. Templin, and A. J. Clark. 1970. Biochemical and genetic studies of recombination proficiency in Escherichia coli. II. Rec1 revertants caused by indirect suppression of rec2 mutations. Proc. Natl. Acad. Sci. USA 67:128–135.
   Google Scholar
• Bardwell, L., A. J. Cooper, and E. C. Friedberg. 1992. Stable and specific association between the yeast recombination and DNA repair proteins Rad1 and Rad10 in vitro. Mol. Cell. Biol. 12:3041–3049.
   PubMedGoogle Scholar
• Brill, S. J., and B. Stillman. 1989. Yeast replication factor-A functions in the unwinding of the SV40 origin of DNA replication. Nature (London) 342: 92–95.
   PubMed Web of Science ®Google Scholar
• Brill, S. J., and B. Stillman. 1991. Replication factor-A from Saccharomyces cerevisiae is encoded by three essential genes coordinately expressed at S phase. Genes Dev. 5:1589–1600.
   PubMed Web of Science ®Google Scholar
• Brown, G. W., J. C. Hines, P. Fisher, and D. S. Ray. 1994. Isolation of the genes encoding the 51-kilodalton and 28-kilodalton subunits of Crithidia fasciculata replication protein A. Mol. Biochem. Parasitol. 59:135–142.
   Google Scholar
• Clark, A. J. 1971. Toward a metabolic interpretation of genetic recombination of Escherichia coli and its phages. Annu. Rev. Microbiol. 25:438–464.
   Google Scholar
• Clark, A. J., and A. Margulies. 1965. Isolation and characterization of recombination-deficient mutants in Escherichia coli K12. Proc. Natl. Acad. Sci. USA 53:451–459.
   PubMed Web of Science ®Google Scholar
• Coverley, D., M. K. Kenny, D. P. Lane, and R. D. Wood. 1992. A role for the human single-stranded DNA binding protein HSSB/RPA in an early stage of nucleotide excision repair. Nucleic Acids Res. 20:3873–3880.
   PubMedGoogle Scholar
• Coverley, D., M. K. Kenny, M. Munn, W. D. Rupp, D. P. Lane, and R. D. Wood. 1991. Requirement for the replication protein SSB in human DNA excision repair. Nature (London) 349:538–541.
   PubMed Web of Science ®Google Scholar
• Devereux, J., P. Haeberli, and O. Smithies. 1984. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 12:387–395.
   PubMed Web of Science ®Google Scholar
• Erdile, L. F., W. D. Heyer, R. Kolodner, and T. J. Kelly. 1991. Characterization of a cDNA encoding the 70-kDa single-stranded DNA-binding subunit of human replication protein A and the role of the protein in DNA replication. J. Biol. Chem. 266:12090–12098.
   PubMedGoogle Scholar
• Erdile, L. F., M. S. Wold, and T. J. Kelly. 1990. The primary structure of the 32-kDa subunit of human replication protein A. J. Biol. Chem. 265:3177–3182.
   PubMedGoogle Scholar
• Fairman, M. P., and B. Stillman. 1988. Cellular factors required for multiple stages of SV40 DNA replication in vitro. EMBO J. 7:1211–1218.
   PubMedGoogle Scholar
• Firmenich, A. A., M. Elias-Arnanz, and P. Berg. 1995. A novel allele of Saccharomyces cerevisiae RFA1 that is deficient in recombination and repair and suppressible by RAD52. Mol. Cell. Biol. 15:1620–1631.
   PubMedGoogle Scholar
• Fishman-Lobell, J., and J. E. Haber. 1992. Removal of nonhomologous DNA ends in double-strand break recombination: the role of the yeast ultraviolet repair gene RAD1. Science 258:480–484.
   PubMedGoogle Scholar
• Fishman-Lobell, J., N. Rudin, and J. E. Haber. 1992. Two alternative pathways of double-strand break repair that are kinetically separable and independently modulated. Mol. Cell. Biol. 12:1292–1303.
   PubMed Web of Science ®Google Scholar
• Game, J. C., and B. S. Cox. 1971. Allelism tests of mutants affecting sensitivity to radiation in yeast and a proposed nomenclature. Mutat. Res. 6:37–55.
   Google Scholar
• Gietz, D., A. St Jean, R. A. Woods, and R. H. Schiestl. 1992. Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res. 20:1425.
   PubMed Web of Science ®Google Scholar
• Gillen, J. R., D. K. Willis, and A. J. Clark. 1981. Genetic analysis of the RecE pathway of genetic recombination in Escherichia coli K-12. J. Bacteriol. 145:521–532.
   PubMedGoogle Scholar
• Haber, J. E. 1992. Exploring the pathways of homologous recombination. Curr. Opin. Cell Biol. 4:401–412.
   PubMedGoogle Scholar
• Harlow, E., and D. Lane. 1988. Antibodies: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
   Google Scholar
• Hartwell, L., and D. Smith. 1985. Altered fidelity of mitotic chromosome transmission in cell cycle mutants of S. cerevisiae. Genetics 110:381–395.
   PubMed Web of Science ®Google Scholar
• Heyer, W. D., and R. D. Kolodner. 1989. Purification and characterization of a protein from Saccharomyces cerevisiae that binds tightly to single-stranded DNA and stimulates a cognate strand exchange protein. Biochemistry 28: 2856–2862.
   PubMedGoogle Scholar
• Heyer, W. D., M. R. Rao, L. F. Erdile, T. J. Kelly, and R. D. Kolodner. 1990. An essential Saccharomyces cerevisiae single-stranded DNA binding protein is homologous to the large subunit of human RP-A. EMBO J. 9:2321–2329.
   PubMedGoogle Scholar
• Hill, J. E., A. M. Myers, T. J. Koerner, and A. Tzagoloff. 1986. Yeast/E. coli shuttle vectors with multiple unique restriction sites. Yeast 2:163–167.
   PubMed Web of Science ®Google Scholar
• Hoekstra, M. F., T. Naughton, and R. E. Malone. 1986. Properties of spontaneous mitotic recombination occurring in the presence of the rad52-1 mutation of Saccharomyces cerevisiae. Genet. Res. 48:9–17.
   PubMedGoogle Scholar
• Hoffman, C. S., and F. Winston. 1987. A ten-minute DNA preparation efficiently releases autonomous plasmids for transformation of Escherichia coli. Gene 57:267–272.
   PubMed Web of Science ®Google Scholar
• Horii, Z. I., and A. J. Clark. 1973. Genetic analysis of the Rec F pathway to genetic recombination in Escherichia coli K12: isolation and characterization of mutants. J. Mol. Biol. 80:327–344.
   PubMedGoogle Scholar
• Jackson, J. A., and G. R. Fink. 1981. Gene conversion between duplicated genetic elements in yeast. Nature (London) 292:306–311.
   PubMedGoogle Scholar
• Kaback, D. B. Personal communication.
   Google Scholar
• Kenny, M. K., S. H. Lee, and J. Hurwitz. 1989. Multiple functions of human single-stranded-DNA binding protein in simian virus 40 DNA replication: single-strand stabilization and stimulation of DNA polymerases alpha and delta. Proc. Natl. Acad. Sci. USA 86:9757–9761.
   PubMedGoogle Scholar
• Klein, H. L. 1988. Different types of recombination events are controlled by the RAD1 and RAD52 genes of Saccharomyces cerevisiae. Genetics 120:367–377.
   PubMedGoogle Scholar
• Kunz, B. A., L. Kohalmi, X. Kang, and K. A. Magnusson. 1990. Specificity of the mutator effect caused by disruption of the RAD1 excision repair gene of Saccharomyces cerevisiae. J. Bacteriol. 172:3009–3014.
   PubMedGoogle Scholar
• Kunz, B. A., M. G. Peters, S. E. Kohalmi, D. Armstrong, M. Glattke, and K. Badiani. 1989. Disruption of the RAD52 gene alters the spectrum of spontaneous SUP4-o mutations in Saccharomyces cerevisiae. Genetics 122:535–542.
   PubMedGoogle Scholar
• Kushner, S. R., H. Nagaishi, A. Templin, and A. J. Clark. 1971. Genetic recombination in Escherichia coli: the role of exonuclease I. Proc. Natl. Acad. Sci. USA 68:824–827.
   PubMedGoogle Scholar
• Lavery, P. E., and S. C. Kowalczykowski. 1992. A postsynaptic role for single-stranded DNA-binding protein in recA protein-promoted DNA strand exchange. J. Biol. Chem. 267:9315–9320.
   PubMedGoogle Scholar
• Lea, D. E., and C. A. Coulson. 1949. The distribution in the numbers of mutants in bacterial populations. J. Genet. 49:264–285.
   PubMed Web of Science ®Google Scholar
• Lindgren, B. W. 1976. Statistical theory, 3rd ed. Macmillan, New York.
   Google Scholar
• Low, B. 1968. Formation of meriploids in matings with a class of rec2 recipient strains of Escherichia coli K12. Proc. Natl. Acad. Sci. USA 60:160–167.
   PubMedGoogle Scholar
• Low, R. L., J. Shlomai, and A. Kornberg. 1982. Protein n, a primosomal DNA replication protein of Escherichia coli. Purification and characterization. J. Biol. Chem. 257:6242–6250.
   PubMed Web of Science ®Google Scholar
• Lucchini, G., M. Muzi Falconi, A. Pizzagalli, A. Aguilera, H. L. Klein, and P. Plevani. 1990. Nucleotide sequence and characterization of temperature-sensitive polI mutants of Saccharomyces cerevisiae. Gene 90:99–104.
   PubMedGoogle Scholar
• Malone, R., and R. E. Esposito. 1980. The rad52 gene is required for ho-mothallic interconversion of mating types and spontaneous mitotic recombination in yeast. Proc. Natl. Acad. Sci. USA 77:503–507.
   PubMed Web of Science ®Google Scholar
• Malone, R. E., B. A. Montelone, C. Edwards, K. Carney, and M. F. Hoekstra. 1988. A reexamination of the role of the RAD52 gene in spontaneous mitotic recombination. Curr. Genet. 14:211–223.
   PubMedGoogle Scholar
• McDonald, J. P., and R. Rothstein. 1994. Unrepaired heteroduplex DNA in Saccharomyces cerevisiae is decreased in RAD1 RAD52-independent recombination. Genetics 137:393–405.
   PubMedGoogle Scholar
• Memet, S., W. Saurin, and A. Sentenac. 1988. RNA polymerases B and C are more closely related to each other than to RNA polymerase A. J. Biol. Chem. 263:10048–10051.
   PubMedGoogle Scholar
• Meyer, R. R., and P. S. Laine. 1990. The single-stranded DNA-binding protein of Escherichia coli. Microbiol. Rev. 54:342–380.
   PubMedGoogle Scholar
• Mitsis, P. G., S. C. Kowalczykowski, and I. R. Lehman. 1993. A single-stranded DNA binding protein from Drosophila melanogaster: characterization of the heterotrimeric protein and its interaction with single-stranded DNA. Biochemistry 32:5257–5266.
   PubMed Web of Science ®Google Scholar
• Montelone, B., S. Prakash, and L. Prakash. 1981. Spontaneous mitotic recombination in mms8-1, an allele of the CDC9 gene of Saccharomyces cerevisiae. J. Bacteriol. 147:517–525.
   PubMed Web of Science ®Google Scholar
• Mortimer, R. K., and C. R. Contopoulou. 1991. Glossary of gene symbols, p. 97. In Yeast Genetic Stock Center catalogue. Division of Genetics, University of California at Berkeley, Berkeley.
   Google Scholar
• Orr-Weaver, T., J. W. Szostak, and R. J. Rothstein. 1981. Yeast transformation: a model system for the study of recombination. Proc. Natl. Acad. Sci. USA 78:6354–6358.
   PubMed Web of Science ®Google Scholar
• Orr-Weaver, T. L., J. W. Szostak, and R. J. Rothstein. 1983. Genetic applications of yeast transformation with linear and gapped plasmids. Methods Enzymol. 101:228–245.
   PubMed Web of Science ®Google Scholar
• Ozenberger, B. A., and G. S. Roeder. 1991. A unique pathway of double-strand break repair operates in tandemly repeated genes. Mol. Cell. Biol. 11:1222–1231.
   PubMed Web of Science ®Google Scholar
• Petes, T. D., R. E. Malone, and L. S. Symington. 1991. Recombination in yeast, p. 407–521. In J. R. Broach, J. R. Pringle, and E. W. Jones (ed.), The molecular and cellular biology of the yeast Saccharomyces: genome dynamics, protein synthesis and energetics, vol. 1. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
   Google Scholar
• Prakash, S., L. Prakash, W. Burke, and B. Monteleone. 1980. Effects of the rad52 gene on recombination in Saccharomyces cerevisiae. Genetics 94:31–50.
   PubMed Web of Science ®Google Scholar
• Resnick, M. A. 1969. Genetic control of radiation sensitivity in Saccharomy-ces cerevisiae. Genetics 62:519–531.
   PubMedGoogle Scholar
• Resnick, M. A., and P. Martin. 1976. The repair of double-strand breaks in the nuclear DNA of Saccharomyces cerevisiae and its genetic control. Mol. Gen. Genet. 143:119–129.
   PubMedGoogle Scholar
• Reynolds, R. J., J. D. Love, and E. C. Friedberg. 1981. Molecular mechanisms of pyrimidine dimer excision in Saccharomyces cerevisiae: excision of dimers in cell extracts. J. Bacteriol. 147:705–708.
   PubMedGoogle Scholar
• Ronne, H., and R. Rothstein. 1988. Mitotic sectored colonies: evidence of heteroduplex DNA formation during direct repeat recombination. Proc. Natl. Acad. Sci. USA 85:2696–2700.
   PubMed Web of Science ®Google Scholar
• Ronne, H., and R. Rothstein. Unpublished data.
   Google Scholar
• Rose, M. D., P. Novick, J. H. Thomas, D. Botstein, and G. R. Fink. 1987. A Saccharomyces cerevisiae genomic plasmid bank based on a centromere-containing shuttle vector. Gene 60:237–243.
   PubMed Web of Science ®Google Scholar
• Rothstein, R., C. Helms, and N. Rosenberg. 1987. Concerted deletions and inversions are caused by mitotic recombination between delta sequences in Saccharomyces cerevisiae. Mol. Cell. Biol. 7:1198–1207.
   PubMedGoogle Scholar
• Saeki, T., I. Machida, and S. Nakai. 1980. Genetic control of diploid recovery after gamma-irradiation in the yeast Saccharomyces cerevisiae. Mutat. Res. 73:251–265.
   PubMedGoogle Scholar
• Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
   Google Scholar
• Sandigursky, M., and W. A. Franklin. 1994. Escherichia coli single-stranded DNA binding protein stimulates the DNA deoxyribophosphodiesterase activity of exonuclease I. Nucleic Acids Res. 22:247–250.
   PubMedGoogle Scholar
• Schiestl, R. H., and S. Prakash. 1988. RAD1, an excision repair gene of Saccharomyces cerevisiae, is also involved in recombination. Mol. Cell. Biol. 8:3619–3626.
   PubMed Web of Science ®Google Scholar
• Sherman, F. 1991. Getting started with yeast, p. 3–21. In C. Guthrie, and G. R. Fink (ed.), Guide to yeast genetics and molecular biology, vol. 194. Academic Press, Inc., San Diego, Calif.
   Google Scholar
• Sherman, F., G. R. Fink, and J. B. Hicks. 1986. Methods in yeast genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
   Google Scholar
• Shinohara, A., H. Ogawa, and T. Ogawa. 1992. Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell 69:457–470.
   PubMed Web of Science ®Google Scholar
• Shivji, K. K., M. K. Kenny, and R. D. Wood. 1992. Proliferating cell nuclear antigen is required for DNA excision repair. Cell 69:367–374.
   PubMed Web of Science ®Google Scholar
• Sikorski, R. S., and P. Hieter. 1989. A system of shuttle vectors in yeast host strains designed for efficient manipulation in Saccharomyces cerevisiae. Genetics 122:19–27.
   PubMed Web of Science ®Google Scholar
• Smith, G. R. 1988. Homologous recombination in procaryotes. Microbiol. Rev. 52:1–28.
   PubMedGoogle Scholar
• Smith, G. R. 1989. Homologous recombination in E. coli: multiple pathways for multiple reasons. Cell 58:807–809.
   Google Scholar
• Steensma, H. Y., J. C. Crowley, and D. B. Kaback. 1987. Molecular cloning of chromosome I DNA from Saccharomyces cerevisiae: isolation and analysis of the CEN1-ADE1-CDC15 region. Mol. Cell. Biol. 7:410–419.
   PubMed Web of Science ®Google Scholar
• Struhl, K., D. T. Stinchcomb, S. Scherer, and R. W. Davis. 1979. High-frequency transformation of yeast: autonomous replication of hybrid DNA molecules. Proc. Natl. Acad. Sci. USA 76:1035–1039.
   PubMed Web of Science ®Google Scholar
• Thomas, B. J., and R. Rothstein. 1989. Elevated recombination rates in transcriptionally active DNA. Cell 56:619–630.
   PubMed Web of Science ®Google Scholar
• Thomas, B. J., and R. Rothstein. 1989. The genetic control of direct-repeat recombination in Saccharomyces: the effect of rad52 and rad1 on mitotic recombination at GAL10, a transcriptionally regulated gene. Genetics 123: 725–738.
   PubMed Web of Science ®Google Scholar
• Thuriaux, P., and A. Sentenac. 1992. Gene expression, p. 1–48. In E. Jones, J. Pringle, and J. R. Broach (ed.), The molecular biology and cellular biology of the yeast Saccharomyces, vol. 2. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
   Google Scholar
• Tomkinson, A. E., A. J. Bardwell, L. Bardwell, N. J. Tappe, and E. C. Friedberg. 1993. Yeast DNA repair and recombination proteins Rad1 and Rad10 constitute a single-stranded-DNA endonuclease. Nature (London) 362:860–862.
   PubMedGoogle Scholar
• Tsurimoto, T., and B. Stillman. 1989. Multiple replication factors augment DNA synthesis by the two eukaryotic DNA polymerases α and d. EMBO J. 8:3883–3889.
   PubMed Web of Science ®Google Scholar
• Umbricht, C. B., L. F. Erdile, E. W. Jabs, and T. J. Kelly. 1993. Cloning, overexpression, and genomic mapping of the 14-kDa subunit of human replication protein A. J. Biol. Chem. 268:6131–6138.
   PubMedGoogle Scholar
• Waldman, B. C., and A. S. Waldman. 1990. Illegitimate and homologous recombination in mammalian cells: differential sensitivity to an inhibitor of poly(ADP-ribosylation). Nucleic Acids Res. 18:5981–5988.
   PubMedGoogle Scholar
• Willetts, N. S., A. J. Clark, and B. Low. 1969. Genetic location of certain mutations conferring recombination deficiency in Escherichia coli. J. Bacte-riol. 97:244–249.
   PubMedGoogle Scholar
• Willetts, N. S., and D. W. Mount. 1969. Genetic analysis of recombination-deficient mutants of Escherichia coli K-12 carrying rec mutations cotransducible with thyA. J. Bacteriol. 100:923–934.
   PubMedGoogle Scholar
• Wold, M. S., and T. Kelly. 1988. Purification and characterization of replication protein A, a cellular protein required for in vitro replication of simian virus 40 DNA. Proc. Natl. Acad. Sci. USA 85:2523–2527.
   PubMed Web of Science ®Google Scholar