Genetics, Vol 135, 631-642, Copyright © 1993

INVESTIGATIONS

A Sister-Strand Exchange Mechanism For recA-Independent Deletion of Repeated DNA Sequences in Escherichia coli

S. T. Lovett, P. T. Drapkin, V. A. Sutera-Jr. and T. J. Gluckman-Peskind
Department of Biology and Rosenstiel Basic Medical Sciences Center, Brandeis University, Waltham, Massachusetts 02254-9110

In the genomes of many organisms, deletions arise between tandemly repeated DNA sequences of lengths ranging from several kilobases to only a few nucleotides. Using a plasmid-based assay for deletion of a 787-bp tandem repeat, we have found that a recA-independent mechanism contributes substantially to the deletion process of even this large region of homology. No Escherichia coli recombination gene tested, including recA, had greater than a fivefold effect on deletion rates. The recA-independence of deletion formation is also observed with constructions present on the chromosome. RecA promotes synapsis and transfer of homologous DNA strands in vitro and is indispensable for intermolecular recombination events in vivo measured after conjugation. Because deletion formation in E. coli shows little or no dependence on recA, it has been assumed that homologous recombination contributes little to the deletion process. However, we have found recA-independent deletion products suggestive of reciprocal crossovers when branch migration in the cell is inhibited by a ruvA mutation. We propose a model for recA-independent crossovers between replicating sister strands, which can also explain deletion or amplification of repeated sequences. We suggest that this process may be initiated as post-replicational DNA repair; subsequent strand misalignment at repeated sequences leads to genetic rearrangements.

This article has been cited by other articles:

				T. Nolan, G. Cecere, C. Mancone, T. Alonzi, M. Tripodi, C. Catalanotto, and C. Cogoni The RNA-dependent RNA polymerase essential for post-transcriptional gene silencing in Neurospora crassa interacts with replication protein A Nucleic Acids Res., February 2, 2008; 36(2): 532 - 538. [Abstract] [Full Text] [PDF]

				B. E. Dutra, V. A. Sutera Jr., and S. T. Lovett RecA-independent recombination is efficient but limited by exonucleases PNAS, January 2, 2007; 104(1): 216 - 221. [Abstract] [Full Text] [PDF]

				J. Kang and M. J. Blaser UvrD Helicase Suppresses Recombination and DNA Damage-Induced Deletions. J. Bacteriol., August 1, 2006; 188(15): 5450 - 5459. [Abstract] [Full Text] [PDF]

				J. Zuniga-Castillo, D. Romero, and J. M. Martinez-Salazar The Recombination Genes addAB Are Not Restricted to Gram-Positive Bacteria: Genetic Analysis of the Recombination Initiation Enzymes RecF and AddAB in Rhizobium etli J. Bacteriol., December 1, 2004; 186(23): 7905 - 7913. [Abstract] [Full Text] [PDF]

				K. Ichiyanagi, A. Beauregard, and M. Belfort A bacterial group II intron favors retrotransposition into plasmid targets PNAS, December 23, 2003; 100(26): 15742 - 15747. [Abstract] [Full Text] [PDF]

				C. A. Hendricks, K. H. Almeida, M. S. Stitt, V. S. Jonnalagadda, R. E. Rugo, G. F. Kerrison, and B. P. Engelward Spontaneous mitotic homologous recombination at an enhanced yellow fluorescent protein (EYFP) cDNA direct repeat in transgenic mice PNAS, May 27, 2003; 100(11): 6325 - 6330. [Abstract] [Full Text] [PDF]

				A. Miranda and A. Kuzminov Chromosomal Lesion Suppression and Removal in Escherichia coli via Linear DNA Degradation Genetics, April 1, 2003; 163(4): 1255 - 1271. [Abstract] [Full Text] [PDF]

				V. V. Feschenko, L. A. Rajman, and S. T. Lovett Stabilization of perfect and imperfect tandem repeats by single-strand DNA exonucleases PNAS, February 4, 2003; 100(3): 1134 - 1139. [Abstract] [Full Text] [PDF]

				C. E. Beam, C. J. Saveson, and S. T. Lovett Role for radA/sms in Recombination Intermediate Processing in Escherichia coli J. Bacteriol., December 15, 2002; 184(24): 6836 - 6844. [Abstract] [Full Text] [PDF]

				M. Napierala, P. Parniewski, A. Pluciennik, and R. D. Wells Long CTG{middle dot}CAG Repeat Sequences Markedly Stimulate Intramolecular Recombination J. Biol. Chem., September 6, 2002; 277(37): 34087 - 34100. [Abstract] [Full Text] [PDF]

				K. M. Puopolo, S. K. Hollingshead, V. J. Carey, and L. C. Madoff Tandem Repeat Deletion in the Alpha C Protein of Group B Streptococcus Is recA Independent Infect. Immun., August 1, 2001; 69(8): 5037 - 5045. [Abstract] [Full Text] [PDF]

				M. Bzymek and S. T. Lovett Instability of repetitive DNA sequences: The role of replication in multiple mechanisms PNAS, July 17, 2001; 98(15): 8319 - 8325. [Abstract] [Full Text] [PDF]

				M. Bzymek and S. T. Lovett Evidence for Two Mechanisms of Palindrome-Stimulated Deletion in Escherichia coli: Single-Strand Annealing and Replication Slipped Mispairing Genetics, June 1, 2001; 158(2): 527 - 540. [Abstract] [Full Text] [PDF]

				P. J. M. Nuijten, A. J. G. van den Berg, I. Formentini, B. A. M. van der Zeijst, and A. A. C. Jacobs DNA Rearrangements in the Flagellin Locus of an flaA Mutant of Campylobacter jejuni during Colonization of Chicken Ceca Infect. Immun., December 1, 2000; 68(12): 7137 - 7140. [Abstract] [Full Text] [PDF]

				D. J. Tomso and K. N. Kreuzer Double-Strand Break Repair in Tandem Repeats During Bacteriophage T4 Infection Genetics, August 1, 2000; 155(4): 1493 - 1504. [Abstract] [Full Text]

				C. J. Saveson and S. T. Lovett Tandem Repeat Recombination Induced by Replication Fork Defects in Escherichia coli Requires a Novel Factor, RadC Genetics, May 1, 1999; 152(1): 5 - 13. [Abstract] [Full Text]

				M. Bzymek, C. J. Saveson, V. V. Feschenko, and S. T. Lovett Slipped Misalignment Mechanisms of Deletion Formation: In Vivo Susceptibility to Nucleases J. Bacteriol., January 15, 1999; 181(2): 477 - 482. [Abstract] [Full Text]

				W. W. Steiner and P. L. Kuempel Sister Chromatid Exchange Frequencies in Escherichia coli Analyzed by Recombination at the dif Resolvase Site J. Bacteriol., December 1, 1998; 180(23): 6269 - 6275. [Abstract] [Full Text]

				A. Galli and R. H. Schiestl Effects of DNA Double-Strand and Single-Strand Breaks on Intrachromosomal Recombination Events in Cell-Cycle-Arrested Yeast Cells Genetics, July 1, 1998; 149(3): 1235 - 1250. [Abstract] [Full Text] [PDF]

				D. M. DeMarini, M. L. Shelton, A. Abu-Shakra, A. Szakmary, and J. G. Levine Spectra of Spontaneous Frameshift Mutations at the hisD3052 Allele of Salmonella typhimurium in Four DNA Repair Backgrounds Genetics, May 1, 1998; 149(1): 17 - 36. [Abstract] [Full Text] [PDF]

				L. L. Stoike and B. B. Sears Plastome Mutator–Induced Alterations Arise in Oenothera Chloroplast DNA Through Template Slippage Genetics, May 1, 1998; 149(1): 347 - 353. [Abstract] [Full Text] [PDF]

				Evidence for Independent Mismatch Repair Processing on Opposite Sides of a Double-Strand Break in Saccharomyces cerevisiae Genetics, January 1, 1998; 148(1): 59 - 70.

				A. Pluciennik, R. R. Iyer, P. Parniewski, and R. D. Wells Tandem Duplication. A NOVEL TYPE OF TRIPLET REPEAT INSTABILITY J. Biol. Chem., September 8, 2000; 275(37): 28386 - 28397. [Abstract] [Full Text] [PDF]