Genetics, Vol 142, 25-37, Copyright © 1996

INVESTIGATIONS

Two Enzymes, Both of Which Process Recombination Intermediates, Have Opposite Effects on Adaptive Mutation in Escherichia coli

P. L. Foster, J. M. Trimarchi and R. A. Maurer
Department of Environmental Health, Boston University School of Public Health, Boston University School of Medicine, Boston, Massachusetts 02118-2394

Reversion of a lac(-) frameshift allele carried on an F' episome in Escherichia coli occurs at a high rate when the cells are placed under lactose selection. Unlike Lac(+) mutations that arise during nonselective growth, the production of these adaptive mutations requires the RecA-RecBCD pathway for recombination. In this report, we show that enzymes that process recombination intermediates are involved in the mutagenic process. RuvAB and RecG, E. coli's two enzymes for translocating Holliday junctions, have opposite effects: RuvAB is required for RecA-dependent adaptive mutations, whereas RecG inhibits them.

This article has been cited by other articles:

				J. F. Petrosino, R. S. Galhardo, L. D. Morales, and S. M. Rosenberg Stress-Induced {beta}-Lactam Antibiotic Resistance Mutation and Sequences of Stationary-Phase Mutations in the Escherichia coli Chromosome J. Bacteriol., October 1, 2009; 191(19): 5881 - 5889. [Abstract] [Full Text] [PDF]

				M. Castellanos and D. Romero The Extent of Migration of the Holliday Junction Is a Crucial Factor for Gene Conversion in Rhizobium etli J. Bacteriol., August 1, 2009; 191(15): 4987 - 4995. [Abstract] [Full Text] [PDF]

				R. S. Galhardo, R. Do, M. Yamada, E. C. Friedberg, P. J. Hastings, T. Nohmi, and S. M. Rosenberg DinB Upregulation Is the Sole Role of the SOS Response in Stress-Induced Mutagenesis in Escherichia coli Genetics, May 1, 2009; 182(1): 55 - 68. [Abstract] [Full Text] [PDF]

				D. Gawel, M. D. Hamilton, and R. M. Schaaper A Novel Mutator of Escherichia coli Carrying a Defect in the dgt Gene, Encoding a dGTP Triphosphohydrolase J. Bacteriol., November 1, 2008; 190(21): 6931 - 6939. [Abstract] [Full Text] [PDF]

				A. B. Williams and P. L. Foster The Escherichia coli Histone-like Protein HU Has a Role in Stationary Phase Adaptive Mutation Genetics, October 1, 2007; 177(2): 723 - 735. [Abstract] [Full Text] [PDF]

				J. D. Stumpf, A. R. Poteete, and P. L. Foster Amplification of lac Cannot Account for Adaptive Mutation to Lac+ in Escherichia coli J. Bacteriol., March 15, 2007; 189(6): 2291 - 2299. [Abstract] [Full Text] [PDF]

				J. C. Layton and P. L. Foster Error-Prone DNA Polymerase IV Is Regulated by the Heat Shock Chaperone GroE in Escherichia coli J. Bacteriol., January 15, 2005; 187(2): 449 - 457. [Abstract] [Full Text] [PDF]

				S. M. Rosenberg and P. J. Hastings Adaptive Point Mutation and Adaptive Amplification Pathways in the Escherichia coli Lac System: Stress Responses Producing Genetic Change J. Bacteriol., August 1, 2004; 186(15): 4838 - 4843. [Full Text] [PDF]

				P. L. Foster Adaptive Mutation in Escherichia coli J. Bacteriol., August 1, 2004; 186(15): 4846 - 4852. [Full Text] [PDF]

				R. Tegova, A. Tover, K. Tarassova, M. Tark, and M. Kivisaar Involvement of Error-Prone DNA Polymerase IV in Stationary-Phase Mutagenesis in Pseudomonas putida J. Bacteriol., May 1, 2004; 186(9): 2735 - 2744. [Abstract] [Full Text] [PDF]

				M. E. Robu, R. B. Inman, and M. M. Cox Situational Repair of Replication Forks: ROLES OF RecG AND RecA PROTEINS J. Biol. Chem., March 19, 2004; 279(12): 10973 - 10981. [Abstract] [Full Text] [PDF]

				M.-J. Lombardo, I. Aponyi, and S. M. Rosenberg General Stress Response Regulator RpoS in Adaptive Mutation and Amplification in Escherichia coli Genetics, February 1, 2004; 166(2): 669 - 680. [Abstract] [Full Text] [PDF]

				H.-M. Sung, G. Yeamans, C. A. Ross, and R. E. Yasbin Roles of YqjH and YqjW, Homologs of the Escherichiacoli UmuC/DinB or Y Superfamily of DNA Polymerases, in Stationary-Phase Mutagenesis and UV-Induced Mutagenesis of Bacillussubtilis J. Bacteriol., April 1, 2003; 185(7): 2153 - 2160. [Abstract] [Full Text] [PDF]

				C. Rodriguez, J. Tompkin, J. Hazel, and P. L. Foster Induction of a DNA Nickase in the Presence of Its Target Site Stimulates Adaptive Mutation in Escherichia coli J. Bacteriol., October 15, 2002; 184(20): 5599 - 5608. [Abstract] [Full Text] [PDF]

				H.-M. Sung and R. E. Yasbin Adaptive, or Stationary-Phase, Mutagenesis, a Component of Bacterial Differentiation in Bacillus subtilis J. Bacteriol., October 15, 2002; 184(20): 5641 - 5653. [Abstract] [Full Text] [PDF]

				A. R. Poteete, H. R. Wang, and P. L. Foster Phage {lambda} Red-Mediated Adaptive Mutation J. Bacteriol., July 1, 2002; 184(13): 3753 - 3755. [Abstract] [Full Text] [PDF]

				E. S. Slechta, J. Liu, D. I. Andersson, and J. R. Roth Evidence That Selected Amplification of a Bacterial lac Frameshift Allele Stimulates Lac+ Reversion (Adaptive Mutation) With or Without General Hypermutability Genetics, July 1, 2002; 161(3): 945 - 956. [Abstract] [Full Text] [PDF]

				J. F. Petrosino, A. R. Pendleton, J. H. Weiner, and S. M. Rosenberg Chromosomal System for Studying AmpC-Mediated {beta}-Lactam Resistance Mutation in Escherichia coli Antimicrob. Agents Chemother., May 1, 2002; 46(5): 1535 - 1539. [Abstract] [Full Text] [PDF]

				A. Kuzminov Single-strand interruptions in replicating chromosomes cause double-strand breaks PNAS, July 17, 2001; 98(15): 8241 - 8246. [Abstract] [Full Text] [PDF]

				H. J. Bull, M.-J. Lombardo, and S. M. Rosenberg Stationary-phase mutation in the bacterial chromosome: Recombination protein and DNA polymerase IV dependence PNAS, July 17, 2001; 98(15): 8334 - 8341. [Abstract] [Full Text] [PDF]

				M.-J. Lombardo and S. M. Rosenberg radC102 of Escherichia coli Is an Allele of recG J. Bacteriol., November 15, 2000; 182(22): 6287 - 6291. [Abstract] [Full Text] [PDF]

				H. J. Bull, G. J. McKenzie, P. J. Hastings, and S. M. Rosenberg Evidence That Stationary-Phase Hypermutation in the Escherichia coli Chromosome Is Promoted by Recombination Genetics, April 1, 2000; 154(4): 1427 - 1437. [Abstract] [Full Text]

				P.L. FOSTER Adaptive Mutation in Escherichia coli Cold Spring Harb Symp Quant Biol, January 1, 2000; 65(0): 21 - 30. [Abstract] [PDF]

				V. G. Godoy, F. S. Gizatullin, and M. S. Fox Some Features of the Mutability of Bacteria During Nonlethal Selection Genetics, January 1, 2000; 154(1): 49 - 59. [Abstract] [Full Text]

				A. Kuzminov Recombinational Repair of DNA Damage in Escherichia coli and Bacteriophage lambda Microbiol. Mol. Biol. Rev., December 1, 1999; 63(4): 751 - 813. [Abstract] [Full Text] [PDF]

				M. R. Motamedi, S. K. Szigety, and S. M. Rosenberg Double-strand-break repair recombination in Escherichia coli: physical evidence for a DNA replication mechanism in vivo Genes & Dev., November 1, 1999; 13(21): 2889 - 2903. [Abstract] [Full Text]

				D. Zahradka Chromosome Segregation and Cell Division Defects in recBC sbcBC ruvC Mutants of Escherichia coli J. Bacteriol., October 1, 1999; 181(19): 6179 - 6183. [Abstract] [Full Text] [PDF]

				A. R. Poteete, A. C. Fenton, and K. C. Murphy Roles of RuvC and RecG in Phage lambda Red-Mediated Recombination J. Bacteriol., September 1, 1999; 181(17): 5402 - 5408. [Abstract] [Full Text] [PDF]

				W. A. Rosche and P. L. Foster The role of transient hypermutators in adaptive mutation in Escherichia coli PNAS, June 8, 1999; 96(12): 6862 - 6867. [Abstract] [Full Text] [PDF]

				P. L. Foster and W. A. Rosche Increased Episomal Replication Accounts for the High Rate of Adaptive Mutation in recD Mutants of Escherichia coli Genetics, May 1, 1999; 152(1): 15 - 30. [Abstract] [Full Text]

				D. I. Andersson, E. S. Slechta, and J. R. Roth Evidence That Gene Amplification Underlies Adaptive Mutability of the Bacterial lac Operon Science, November 6, 1998; 282(5391): 1133 - 1135. [Abstract] [Full Text]

				M. K. B. Berlyn Linkage Map of Escherichia coli K-12, Edition 10: The Traditional Map Microbiol. Mol. Biol. Rev., September 1, 1998; 62(3): 814 - 984. [Abstract] [Full Text] [PDF]

				P. L. Foster and W. A. Rosche Levels of the Vsr Endonuclease Do Not Regulate Stationary-Phase Reversion of a Lac- Frameshift Allele in Escherichia coli J. Bacteriol., April 1, 1998; 180(7): 1944 - 1946. [Abstract] [Full Text] [PDF]

				P. L. Foster Adaptive Mutation: Has the Unicorn Landed? Genetics, April 1, 1998; 148(4): 1453 - 1459. [Abstract] [Full Text] [PDF]

				T. P. Gary, N. E. Colowick, and G. Mosig A Species Barrier Between Bacteriophages T2 and T4: Exclusion, Join-Copy and Join-Cut-Copy Recombination and Mutagenesis in the dCTPase Genes Genetics, April 1, 1998; 148(4): 1461 - 1473. [Abstract] [Full Text] [PDF]

				S. M. Rosenberg, C. Thulin, and R. S. Harris Transient and Heritable Mutators in Adaptive Evolution in the Lab and in Nature Genetics, April 1, 1998; 148(4): 1559 - 1566. [Abstract] [Full Text] [PDF]

				R. S. Harris, G. Feng, K. J. Ross, R. Sidhu, C. Thulin, S. Longerich, S. K. Szigety, M. E. Winkler, and S. M. Rosenberg Mismatch repair protein MutL becomes limiting during stationary-phase mutation Genes & Dev., September 15, 1997; 11(18): 2426 - 2437. [Abstract] [Full Text] [PDF]

				T. C. Zahrt and S. Maloy Barriers to recombination between closely related bacteria: MutS and RecBCD inhibit recombination between Salmonella typhimurium and Salmonella typhi PNAS, September 2, 1997; 94(18): 9786 - 9791. [Abstract] [Full Text] [PDF]

				G. J. McKenzie, R. S. Harris, P. L. Lee, and S. M. Rosenberg The SOS response regulates adaptive mutation PNAS, June 6, 2000; 97(12): 6646 - 6651. [Abstract] [Full Text] [PDF]