Abstract
Whether or not homologous interaction of two DNA molecules results in crossing-over of the flanking sequences is an important decision in view of genome organization. Several homologous recombination models, including the double-strand break repair models, explain this decision as choice between two alternative modes of resolution of Holliday-type intermediates. We have demonstrated that a double-strand gap can be repaired through gene conversion copying a homologous duplex, as predicted by the double-strand break repair models, in the RecE pathway of Escherichia coli. This gap repair is often accompanied by crossing-over of the flanking sequences. Mutations in ruvC and recG, whose products interact with Holliday structures in vitro, do not block double-strand gap repair or its association with flanking crossing-over. However, two mutations in the recJ gene, which encodes a single-strand 5'-->3' exonuclease, severely decrease association of flanking crossing-over. Two mutations in the recQ gene, which encodes a helicase, moderately decrease association of flanking crossing-over by themselves and suppress the severe effect of a recJ mutation. Similar relationships of recJ and recQ mutations are observed in cell survival after ultraviolet light irradiation, gamma-ray irradiation, and H2O2 treatment. We discuss how cooperation of the recQ gene product and the recJ gene product brings about double-strand break repair accompanied by flanking crossing-over. We also discuss how this reaction is related to repair of chromosome damages.
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- Aboussekhra A., Chanet R., Zgaga Z., Cassier-Chauvat C., Heude M., Fabre F. RADH, a gene of Saccharomyces cerevisiae encoding a putative DNA helicase involved in DNA repair. Characteristics of radH mutants and sequence of the gene. Nucleic Acids Res. 1989 Sep 25;17(18):7211–7219. doi: 10.1093/nar/17.18.7211. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Aguilera A., Klein H. L. 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):683–694. doi: 10.1093/genetics/123.4.683. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bernstein H., Hopf F. A., Michod R. E. The molecular basis of the evolution of sex. Adv Genet. 1987;24:323–370. doi: 10.1016/s0065-2660(08)60012-7. [DOI] [PubMed] [Google Scholar]
- Connolly B., Parsons C. A., Benson F. E., Dunderdale H. J., Sharples G. J., Lloyd R. G., West S. C. Resolution of Holliday junctions in vitro requires the Escherichia coli ruvC gene product. Proc Natl Acad Sci U S A. 1991 Jul 15;88(14):6063–6067. doi: 10.1073/pnas.88.14.6063. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Duckett D. R., Murchie A. I., Diekmann S., von Kitzing E., Kemper B., Lilley D. M. The structure of the Holliday junction, and its resolution. Cell. 1988 Oct 7;55(1):79–89. doi: 10.1016/0092-8674(88)90011-6. [DOI] [PubMed] [Google Scholar]
- Fishel R. A., James A. A., Kolodner R. recA-independent general genetic recombination of plasmids. Nature. 1981 Nov 12;294(5837):184–186. doi: 10.1038/294184a0. [DOI] [PubMed] [Google Scholar]
- Gillen J. R., Willis D. K., Clark A. J. Genetic analysis of the RecE pathway of genetic recombination in Escherichia coli K-12. J Bacteriol. 1981 Jan;145(1):521–532. doi: 10.1128/jb.145.1.521-532.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hall S. D., Kane M. F., Kolodner R. D. Identification and characterization of the Escherichia coli RecT protein, a protein encoded by the recE region that promotes renaturation of homologous single-stranded DNA. J Bacteriol. 1993 Jan;175(1):277–287. doi: 10.1128/jb.175.1.277-287.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Huisman O., Fox M. S. A genetic analysis of primary products of bacteriophage lambda recombination. Genetics. 1986 Mar;112(3):409–420. doi: 10.1093/genetics/112.3.409. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Iwasaki H., Takahagi M., Shiba T., Nakata A., Shinagawa H. Escherichia coli RuvC protein is an endonuclease that resolves the Holliday structure. EMBO J. 1991 Dec;10(13):4381–4389. doi: 10.1002/j.1460-2075.1991.tb05016.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Joseph J. W., Kolodner R. Exonuclease VIII of Escherichia coli. II. Mechanism of action. J Biol Chem. 1983 Sep 10;258(17):10418–10424. [PubMed] [Google Scholar]
- Kleckner N., Chan R. K., Tye B. K., Botstein D. Mutagenesis by insertion of a drug-resistance element carrying an inverted repetition. J Mol Biol. 1975 Oct 5;97(4):561–575. doi: 10.1016/s0022-2836(75)80059-3. [DOI] [PubMed] [Google Scholar]
- Kobayashi I., Ikeda H. Double Holliday structure: a possible in vivo intermediate form of general recombination in Escherichia coli. Mol Gen Genet. 1983;191(2):213–220. doi: 10.1007/BF00334816. [DOI] [PubMed] [Google Scholar]
- Kobayashi I. Mechanisms for gene conversion and homologous recombination: the double-strand break repair model and the successive half crossing-over model. Adv Biophys. 1992;28:81–133. doi: 10.1016/0065-227x(92)90023-k. [DOI] [PubMed] [Google Scholar]
- Kobayashi I., Takahashi N. Double-stranded gap repair of DNA by gene conversion in Escherichia coli. Genetics. 1988 Aug;119(4):751–757. doi: 10.1093/genetics/119.4.751. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Krasin F., Hutchinson F. Repair of DNA double-strand breaks in Escherichia coli, which requires recA function and the presence of a duplicate genome. J Mol Biol. 1977 Oct 15;116(1):81–98. doi: 10.1016/0022-2836(77)90120-6. [DOI] [PubMed] [Google Scholar]
- Kusano K., Nakayama K., Nakayama H. Plasmid-mediated lethality and plasmid multimer formation in an Escherichia coli recBC sbcBC mutant. Involvement of RecF recombination pathway genes. J Mol Biol. 1989 Oct 20;209(4):623–634. doi: 10.1016/0022-2836(89)90000-4. [DOI] [PubMed] [Google Scholar]
- Lichten M., Fox M. S. 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):7180–7184. doi: 10.1073/pnas.81.22.7180. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Little J. W. An exonuclease induced by bacteriophage lambda. II. Nature of the enzymatic reaction. J Biol Chem. 1967 Feb 25;242(4):679–686. [PubMed] [Google Scholar]
- Lloyd R. G., Buckman C., Benson F. E. Genetic analysis of conjugational recombination in Escherichia coli K12 strains deficient in RecBCD enzyme. J Gen Microbiol. 1987 Sep;133(9):2531–2538. doi: 10.1099/00221287-133-9-2531. [DOI] [PubMed] [Google Scholar]
- Lloyd R. G., Buckman C. Genetic analysis of the recG locus of Escherichia coli K-12 and of its role in recombination and DNA repair. J Bacteriol. 1991 Feb;173(3):1004–1011. doi: 10.1128/jb.173.3.1004-1011.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lloyd R. G., Sharples G. J. Dissociation of synthetic Holliday junctions by E. coli RecG protein. EMBO J. 1993 Jan;12(1):17–22. doi: 10.1002/j.1460-2075.1993.tb05627.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lovett S. T., Clark A. J. Genetic analysis of the recJ gene of Escherichia coli K-12. J Bacteriol. 1984 Jan;157(1):190–196. doi: 10.1128/jb.157.1.190-196.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lovett S. T., Kolodner R. D. Identification and purification of a single-stranded-DNA-specific exonuclease encoded by the recJ gene of Escherichia coli. Proc Natl Acad Sci U S A. 1989 Apr;86(8):2627–2631. doi: 10.1073/pnas.86.8.2627. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Luisi-DeLuca C., Lovett S. T., Kolodner R. D. Genetic and physical analysis of plasmid recombination in recB recC sbcB and recB recC sbcA Escherichia coli K-12 mutants. Genetics. 1989 Jun;122(2):269–278. doi: 10.1093/genetics/122.2.269. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mandal T. N., Mahdi A. A., Sharples G. J., Lloyd R. G. Resolution of Holliday intermediates in recombination and DNA repair: indirect suppression of ruvA, ruvB, and ruvC mutations. J Bacteriol. 1993 Jul;175(14):4325–4334. doi: 10.1128/jb.175.14.4325-4334.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mendonca V. M., Kaiser-Rogers K., Matson S. W. Double helicase II (uvrD)-helicase IV (helD) deletion mutants are defective in the recombination pathways of Escherichia coli. J Bacteriol. 1993 Aug;175(15):4641–4651. doi: 10.1128/jb.175.15.4641-4651.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Muniyappa K., Radding C. M. The homologous recombination system of phage lambda. Pairing activities of beta protein. J Biol Chem. 1986 Jun 5;261(16):7472–7478. [PubMed] [Google Scholar]
- Nakayama K., Irino N., Nakayama H. The recQ gene of Escherichia coli K12: molecular cloning and isolation of insertion mutants. Mol Gen Genet. 1985;200(2):266–271. doi: 10.1007/BF00425434. [DOI] [PubMed] [Google Scholar]
- Rong L., Palladino F., Aguilera A., Klein H. L. The hyper-gene conversion hpr5-1 mutation of Saccharomyces cerevisiae is an allele of the SRS2/RADH gene. Genetics. 1991 Jan;127(1):75–85. doi: 10.1093/genetics/127.1.75. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stahl F. W., Kobayashi I., Stahl M. M. In phage lambda, cos is a recombinator in the red pathway. J Mol Biol. 1985 Jan 20;181(2):199–209. doi: 10.1016/0022-2836(85)90085-3. [DOI] [PubMed] [Google Scholar]
- 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]
- Takahashi N. K., Kusano K., Yokochi T., Kitamura Y., Yoshikura H., Kobayashi I. Genetic analysis of double-strand break repair in Escherichia coli. J Bacteriol. 1993 Aug;175(16):5176–5185. doi: 10.1128/jb.175.16.5176-5185.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Takahashi N. K., Yamamoto K., Kitamura Y., Luo S. Q., Yoshikura H., Kobayashi I. Nonconservative recombination in Escherichia coli. Proc Natl Acad Sci U S A. 1992 Jul 1;89(13):5912–5916. doi: 10.1073/pnas.89.13.5912. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Takahashi N., Kobayashi I. Evidence for the double-strand break repair model of bacteriophage lambda recombination. Proc Natl Acad Sci U S A. 1990 Apr;87(7):2790–2794. doi: 10.1073/pnas.87.7.2790. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Thaler D. S., Stahl F. W. DNA double-chain breaks in recombination of phage lambda and of yeast. Annu Rev Genet. 1988;22:169–197. doi: 10.1146/annurev.ge.22.120188.001125. [DOI] [PubMed] [Google Scholar]
- Umezu K., Nakayama K., Nakayama H. Escherichia coli RecQ protein is a DNA helicase. Proc Natl Acad Sci U S A. 1990 Jul;87(14):5363–5367. doi: 10.1073/pnas.87.14.5363. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yamamoto K., Kusano K., Takahashi N. K., Yoshikura H., Kobayashi I. Gene conversion in the Escherichia coli RecF pathway: a successive half crossing-over model. Mol Gen Genet. 1992 Jul;234(1):1–13. doi: 10.1007/BF00272339. [DOI] [PubMed] [Google Scholar]
- Yamamoto K., Yoshikura H., Takahashi N., Kobayashi I. Apparent gene conversion in an Escherichia coli rec+ strain is explained by multiple rounds of reciprocal crossing-over. Mol Gen Genet. 1988 Jun;212(3):393–404. doi: 10.1007/BF00330842. [DOI] [PubMed] [Google Scholar]