Opposing Roles of the Holliday Junction Processing Systems of Escherichia coli in Recombination-Dependent Adaptive Mutation

INVESTIGATIONS

Opposing Roles of the Holliday Junction Processing Systems of Escherichia coli in Recombination-Dependent Adaptive Mutation

R. S. Harris, K. J. Ross and S. M. Rosenberg
Department of Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2H7, Canada

Aspects of the molecular mechanism of ``adaptive'' mutation are emerging from one experimental system: reversion of an Escherichia coli lac frameshift mutation carried on a conjugative plasmid. Homologous recombination is required and the mutations resemble polymerase errors. Reports implicating a role for conjugal transfer proteins suggested that the mutation mechanism is ordinary replication error occurring during transfer synthesis, followed by conjugation-like recombination, to capture the replicated fragment into an intact replicon. Whereas conjugational recombination uses either of two systems of Holliday junction resolution, we find that the adaptive lac reversions are inhibited by one resolution system and promoted by the other. Moreover, temporary absence of both resolution systems promotes mutation. These results imply that recombination intermediates themselves promote the mutations.

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				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]

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				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]

				S. M. Rosenberg and P. J. Hastings Rebuttal: Growth under Selection Stimulates Lac+ Reversion (Roth and Andersson) J. Bacteriol., August 1, 2004; 186(15): 4862 - 4863. [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]

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				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]

				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]

				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]

				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]

				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]

				S. Stambuk and M. Radman Mechanism and Control of Interspecies Recombination in Escherichia coli. I. Mismatch Repair, Methylation, Recombination and Replication Functions Genetics, October 1, 1998; 150(2): 533 - 542. [Abstract] [Full Text]

				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]