Multiple pathways of duplication formation with and without recombination (RecA) in Salmonella enterica

Genetics

Volumn 192, Issue 2, 2012, Pages 397-415

  Reams, Andrew B ^a   Kofoid, Eric ^a   Kugelberg, Elisabeth ^a   Roth, John R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; PLASMID DNA; RECA PROTEIN; SINGLE STRANDED DNA; TRANSPOSASE;

ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; GENE DUPLICATION; GENE SEQUENCE; LAC GENE; NONHUMAN; PRIORITY JOURNAL; SALMONELLA ENTERICA; SISTER CHROMATID;

CHROMOSOMES, BACTERIAL; CROSSING OVER, GENETIC; DNA TRANSPOSABLE ELEMENTS; GENE DUPLICATION; LAC OPERON; METABOLIC NETWORKS AND PATHWAYS; MUTATION RATE; PLASMIDS; REC A RECOMBINASES; RECOMBINATION, GENETIC; SALMONELLA ENTERICA; TRANSPOSASES;

BACTERIA (MICROORGANISMS); SALMONELLA ENTERICA;

EID: 84867183205     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.112.142570     Document Type: Article

References (91)

1. Anderson, R. P., and J. R. Roth, 1978 Tandem chromosomal duplications in Salmonella typhimurium: fusion of histidine genes to novel promoters. J. Mol. Biol. 119: 147-166.
2. Anderson, P., and J. Roth, 1981 Spontaneous tandem genetic duplications in Salmonella typhimurium arise by unequal recombination between rRNA (rrn) cistrons. Proc. Natl. Acad. Sci. USA 78: 3113-3117.
3. Andersson, D. I., E. S. Slechta, and J. R. Roth, 1998 Evidence that gene amplification underlies adaptive mutability of the bacterial lac operon. Science 282: 1133-1135.
4. Andersson, D. I., D. Hughes, and J. R. Roth (Editors), 2011 The Origin of Mutants Under Selection: Interactions of Mutation, Growth, and Selection. ASM Press, Washington, DC.
5. Araya, C. L., C. Payen, M. J. Dunham, and S. Fields, 2010 Whole-genome sequencing of a laboratory-evolved yeast strain. BMC Genomics 11: 88.
6. Bachellier, S., J. M. Clement, M. Hofnung, and E. Gilson, 1997 Bacterial interspersed mosaic elements (BIMEs) are a major source of sequence polymorphism in Escherichia coli intergenic regions including specific associations with a new insertion sequence. Genetics 145: 551-562.
7. Bachellier, S., J. M. Clement, and M. Hofnung, 1999 Short palindromic repetitive DNA elements in enterobacteria: a survey. Res. Microbiol. 150: 627-639.
8. Barre, F. X., and D. J. Sherratt, 2005 Chromosome dimer resolution, pp. 513-524 in The Bacterial Chromosome, edited by N. P. Higgins. ASM Press, Washington, DC.
9. Bergthorsson, U., D. I. Andersson, and J. R. Roth, 2007 Ohno's dilemma: evolution of new genes under continuous selection. Proc. Natl. Acad. Sci. USA 104: 17004-17009.
10. Biek, D. P., and S. N. Cohen, 1986 Identification and characterization of recD, a gene affecting plasmid maintenance and recombination in Escherichia coli. J. Bacteriol. 167: 594-603.
11. Botchan, M., W. Topp, and J. Sambrook, 1979 Studies on simian virus 40 excision from cellular chromosomes. Cold Spring Harb. Symp. Quant. Biol. 43(2): 709-719.
12. Brewer, B. J., C. Payen, M. K. Raghuraman, and M. J. Dunham, 2011 Origin-dependent inverted-repeat amplification: a replication-based model for generating palindromic amplicons. PLoS Genet. 7: e1002016.
13. Bridges, C. B., 1936 The bar "gene": a duplication. Science 83: 210-211.
14. Bzymek, M., and S. T. Lovett, 2001 Evidence for two mechanisms of palindrome-stimulated deletion in Escherichia coli: single- strand annealing and replication slipped mispairing. Genetics 158: 527-540.
15. Cairns, J., and P. L. Foster, 1991 Adaptive reversion of a frameshift mutation in Escherichia coli. Genetics 128: 695-701.
16. Clugston, C. K., and A. P. Jessop, 1991 A bacterial position effect: when the F factor in E. coli K12 is integrated in cis to a chromosomal gene that is flanked by IS1 repeats the elements are activated so that amplification and other regulatory changes that affect the gene can occur. Mutat. Res. 248: 1-15.
17. Conrad, D. F., D. Pinto, R. Redon, L. Feuk, O. Gokcumen et al., 2010 Origins and functional impact of copy number variation in the human genome. Nature 464: 704-712.
18. Cuff, L. E., K. T. Elliott, S. C. Seaton, M. K. Ishaq, N. S. Laniohan et al., 2012 Analysis of IS1236-mediated gene amplification events in Acinetobacter baylyi ADP1. J. Bacteriol. 194: 4395-4405.
19. Derbyshire, K. M., and N. D. Grindley, 1996 Cis preference of the IS903 transposase is mediated by a combination of transposase instability and inefficient translation. Mol. Microbiol. 21: 1261-1272.
20. Dianov, G. L., A. V. Kuzminov, A. V. Mazin, and R. I. Salganik, 1991 Molecular mechanisms of deletion formation in Escherichia coli plasmids. I. Deletion formation mediated by long direct repeats. Mol. Gen. Genet. 228: 153-159.
21. Farabaugh, P. J., U. Schmeissner, M. Hofer, and J. H. Miller, 1978 Genetic studies of the lac repressor. VII. On the molecular nature of spontaneous hotspots in the lacI gene of Escherichia coli. J. Mol. Biol. 126: 847-857.
22. Flores, M., P. Mavingui, X. Perret, W. J. Broughton, D. Romero et al., 2000 Prediction, identification, and artificial selection of DNA rearrangements in Rhizobium: toward a natural genomic design. Proc. Natl. Acad. Sci. USA 97: 9138-9143.
23. Frost, L. S., K. Ippen-Ihler, and R. A. Skurray, 1994 Analysis of the sequence and gene products of the transfer region of the F sex factor. Microbiol. Rev. 58: 162-210.
24. Galitski, T., and J. R. Roth, 1997 Pathways for homologous recombination between chromosomal direct repeats in Salmonella typhimurium. Genetics 146: 751-767.
25. Gilson, E., S. Bachellier, S. Perrin, D. Perrin, P. A. Grimont et al., 1990 Palindromic unit highly repetitive DNA sequences exhibit species specificity within Enterobacteriaceae. Res. Microbiol. 141: 1103-1116.
26. Goldberg, I., and J. J. Mekalanos, 1986 Effect of a recA mutation on cholera toxin gene amplification and deletion events. J. Bacteriol. 165: 723-731.
27. Goldfless, S. J., A. S. Morag, K. A. Belisle, V. A. Sutera Jr., and S. T. Lovett, 2006 DNA repeat rearrangements mediated by DnaK-dependent replication fork repair. Mol. Cell 21: 595-604.
28. Gordenin, D. A., K. S. Lobachev, N. P. Degtyareva, A. L. Malkova, E. Perkins et al., 1993 Inverted DNA repeats: a source of eukaryotic genomic instability. Mol. Cell. Biol. 13: 5315-5322.
29. Gore, J. M., F. A. Ran, and L. N. Ornston, 2006 Deletion mutations caused by DNA strand slippage in Acinetobacter baylyi. Appl. Environ. Microbiol. 72: 5239-5245.
30. Green, M. M., 1985 The role of mobile DNA elements in unequal and inftrachromosomal crossing-over in Drosophila melanogaster, pp. 353-362 in Aneuploidy, edited by V. Dellarco, P. Voytek, and A. Hollaender. Plenum Press, New York.
31. Haack, K. R., and J. R. Roth, 1995 Recombination between chromosomal IS200 elements supports frequent duplication formation in Salmonella typhimurium. Genetics 141: 1245-1252.
32. Hastings, P. J., and S. M. Rosenberg, 2002 In pursuit of a molecular mechanism for adaptive gene amplification. DNA Repair 1: 111-123.
33. Hastings, P. J., G. Ira, and J. R. Lupski, 2009 A microhomology-mediated break-induced replication model for the origin of human copy number variation. PLoS Genet. 5: e1000327.
34. Hopkins, J. D., M. B. Clements, T. Y. Liang, R. R. Isberg, and M. Syvanen, 1980 Recombination genes on the Escherichia coli sex factor specific for transposable elements. Proc. Natl. Acad. Sci. USA 77: 2814-2818.
35. Jain, C., and N. Kleckner, 1993 Preferential cis action of IS10 transposase depends upon its mode of synthesis. Mol. Microbiol. 9: 249-260.
36. Kofoid, E., U. Bergthorsson, E. S. Slechta, and J. R. Roth, 2003 Formation of an F' plasmid by recombination between imperfectly repeated chromosomal Rep sequences: a closer look at an old friend (F'(128) pro lac). J. Bacteriol. 185: 660-663.
37. Kugelberg, E., E. Kofoid, A. B. Reams, D. I. Andersson, and J. R. Roth, 2006 Multiple pathways of selected gene amplification during adaptive mutation. Proc. Natl. Acad. Sci. USA 103: 17319-17324.
38. Kugelberg, E., E. Kofoid, D. I. Andersson, Y. Lu, J. Mellor et al., 2010 The tandem inversion duplication in Salmonella enterica: selection drives unstable precursors to final mutation types. Genetics 185: 65-80.
39. Kuzminov, A., 1995 Collapse and repair of replication forks in Escherichia coli. Mol. Microbiol. 16: 373-384.
40. Lane, D., R. de Feyter, M. Kennedy, S. H. Phua, and D. Semon, 1986 D protein of miniF plasmid acts as a repressor of transcription and as a site-specific resolvase. Nucleic Acids Res. 14: 9713-9728.
41. Lawes, M., and S. Maloy, 1995 MudSacI, a transposon with strong selectable and counterselectable markers: use for rapid mapping of chromosomal mutations in Salmonella typhimurium. J. Bacteriol. 177: 1383-1387.
42. Leach, D. R., 1994 Long DNA palindromes, cruciform structures, genetic instability and secondary structure repair. BioEssays 16: 893-900.
43. Lin, D., I. B. Gibson, J. M. Moore, P. C. Thornton, S. M. Leal et al., 2011 Global chromosomal structural instability in a subpopulation of starving Escherichia coli cells. PLoS Genet. 7: e1002223.
44. Lin, R. J., M. Capage, and C. W. Hill, 1984 A repetitive DNA sequence, rhs, responsible for duplications within the Escherichia coli K-12 chromosome. J. Mol. Biol. 177: 1-18.
45. Liu, J., J. Sneeden, and W. D. Heyer, 2011 In vitro assays for DNA pairing and recombination-associated DNA synthesis. Methods Mol. Biol. 745: 363-383.
46. Lovett, S. T., 2004 Encoded errors: mutations and rearrangements mediated by misalignment at repetitive DNA sequences.Mol. Microbiol. 52: 1243-1253.
47. Lovett, S. T., P. T. Drapkin, V. A. Sutera Jr., and T. J. Gluckman-Peskind, 1993 A sister-strand exchange mechanism for recA-independent deletion of repeated DNA sequences in Escherichia coli. Genetics 135: 631-642.
48. Lu, X. Y., M. T. Phung, C. A. Shaw, K. Pham, S. E. Neil et al., 2008 Genomic imbalances in neonates with birth defects: high detection rates by using chromosomal microarray analysis. Pediatrics 122: 1310-1318.
49. Lupski, J. R., and G. M. Weinstock, 1992 Short, interspersed repetitive DNA sequences in prokaryotic genomes. J. Bacteriol. 174: 4525-4529.
50. Mazin, A. V., A. V. Kuzminov, G. L. Dianov, and R. I. Salganik, 1991 Mechanisms of deletion formation in Escherichia coli plasmids. II. Deletions mediated by short direct repeats. Mol. Gen. Genet. 228: 209-214.
51. Mehan, M. R., N. B. Freimer, and R. A. Ophoff, 2004 A genome-wide survey of segmental duplications that mediate common human genetic variation of chromosomal architecture. Hum. Genomics 1: 335-344.
52. Morag, A. S., C. J. Saveson, and S. T. Lovett, 1999 Expansion of DNA repeats in Escherichia coli: effects of recombination and replication functions. J. Mol. Biol. 289: 21-27.
53. Morgan, L. V., 1925 Polyploidy in Drosophila melanogaster with two attached X Chromosomes. Genetics 10: 148-178.
54. Morris, C. F., and R. Rownd, 1974 Transition of the R factor R12 in Proteus mirabilis. J. Bacteriol. 118: 867-879.
55. Mortensen, U. H., C. Bendixen, I. Sunjevaric, and R. Rothstein, 1996 DNA strand annealing is promoted by the yeast Rad52 protein. Proc. Natl. Acad. Sci. USA 93: 10729-10734.
56. Muller, H. J., 1936 Bar duplication. Science 83: 528-530.
57. Muro-Pastor, A. M., and S. Maloy, 1995 Direct cloning of mutant alleles from the bacterial chromosome into plasmid vectors in vivo. Biotechniques 18: 386-388, 390.
58. Narayanan, V., P. A. Mieczkowski, H. M. Kim, T. D. Petes, and K. S. Lobachev, 2006 The pattern of gene amplification is determined by the chromosomal location of hairpin-capped breaks. Cell 125: 1283-1296.
59. Nicoloff, H., V. Perreten, and S. B. Levy, 2007 Increased genome instability in Escherichia coli lon mutants: relation to emergence of multiple-antibiotic-resistant (Mar) mutants caused by insertion sequence elements and large tandem genomic amplifications. Antimicrob. Agents Chemother. 51: 1293-1303.
60. Ogawa, N., and K. Miyashita, 1995 Recombination of a 3-chlorobenzoate catabolic plasmid from Alcaligenes eutrophus NH9 mediated by direct repeat elements. Appl. Environ. Microbiol. 61: 3788-3795.
61. Ohno, S., 1970 Evolution by Gene Duplication. Springer-Verlag, New York.
62. Perals, K., F. Cornet, Y. Merlet, I. Delon, and J. M. Louarn, 2000 Functional polarization of the Escherichia coli chromosome terminus: the dif site acts in chromosome dimer resolution only when located between long stretches of opposite polarity. Mol. Microbiol. 36: 33-43.
63. Petes, T. D., and C. W. Hill, 1988 Recombination between repeated genes in microorganisms. Annu. Rev. Genet. 22: 147-168.
64. Petit, M. A., J. M. Mesas, P. Noirot, F. Morel-Deville, and S. D. Ehrlich, 1992 Induction of DNA amplification in the Bacillus subtilis chromosome. EMBO J. 11: 1317-1326.
65. Poteete, A. R., 2009 Expansion of a chromosomal repeat in Escherichia coli: roles of replication, repair, and recombination functions. BMC Mol. Biol. 10: 14.
66. Quiñones-Soto, S., and J. R. Roth, 2011 Effect of growth under selection on appearance of chromosomal mutations in Salmonella enterica. Genetics 189: 37-53
67. Rattray, A. J., B. K. Shafer, B. Neelam, and J. N. Strathern, 2005 A mechanism of palindromic gene amplification in Saccharomyces cerevisiae. Genes Dev. 19: 1390-1399.
68. Reams, A. B., and E. L. Neidle, 2003 Genome plasticity in Acinetobacter: new degradative capabilities acquired by the spontaneous amplification of large chromosomal segments. Mol. Microbiol. 47: 1291-1304.
69. Reams, A. B., and E. L. Neidle, 2004a Gene amplification involves site-specific short homology-independent illegitimate recombination in Acinetobacter sp. strain ADP1. J. Mol. Biol. 338: 643-656.
70. Reams, A. B., and E. L. Neidle, 2004b Selection for gene clustering by tandem duplication. Annu. Rev. Microbiol. 58: 119-142.
71. Reams, A. B., E. C. Kofoid, M. Savageau, and J. R. Roth, 2010 Duplication frequency in a population of Salmonella enterica rapidly approaches steady state with or without recombination. Genetics 184: 1077-1094.
72. Redon, R., S. Ishikawa, K. R. Fitch, L. Feuk, G. H. Perry et al., 2006 Global variation in copy number in the human genome. Nature 444: 444-454.
73. Roth, J. R., N. Benson, T. Galitski, K. Haack, J. G. Lawrence et al., 1996 Rearrangement of the bacterial chromosome: formation and applications, pp. 2256-2276 in Escherichia coli and Salmonella, edited by F. C. Neidhardt ASM Press, Washington, DC.
74. Seaton, S. C., K. T. Elliott, L. E. Cuff, N. S. Laniohan, P. R. Patel et al., 2012 Genome-wide selection for increased copy number in Acinetobacter baylyi ADP1: locus and context-dependent variation in gene amplification. Mol. Microbiol. 83: 520-535.
75. Seifert, H. S., and R. D. Porter, 1984 Enhanced recombination between lambda plac5 and F42lac: identification of cisand trans-acting factors. Proc. Natl. Acad. Sci. USA 81: 7500-7504.
76. Sekine, Y., K. Aihara, and E. Ohtsubo, 1999 Linearization and transposition of circular molecules of insertion sequence IS3. J. Mol. Biol. 294: 21-34.
77. Sinden, R. R., G. X. Zheng, R. G. Brankamp, and K. N. Allen, 1991 On the deletion of inverted repeated DNA in Escherichia coli: effects of length, thermal stability, and cruciform formation in vivo. Genetics 129: 991-1005.
78. Spielmann-Ryser, J., M. Moser, P. Kast, and H. Weber, 1991 Factors determining the frequency of plasmid cointegrate formation mediated by insertion sequence IS3 from Escherichia coli. Mol. Gen. Genet. 226: 441-448.
79. Spies, M. S. K., 2005 Homologous recombination by the RecBCD and RecF Pathways, pp. 389-404 in The Bacterial Chromosome, edited by N. Higgins. ASM Press, Washington, DC.
80. Spradling, A. C., 1981 The organization and amplification of two chromosomal domains containing Drosophila chorion genes. Cell 27: 193-201.
81. Stern, M. J., G. F. Ames, N. H. Smith, E. C. Robinson, and C. F. Higgins, 1984 Repetitive extragenic palindromic sequences: a major component of the bacterial genome. Cell 37: 1015-1026.
82. Streisinger, G., Y. Okada, J. Emrich, J. Newton, A. Tsugita et al., 1966 Frameshift mutations and the genetic code. Cold Spring Harb. Symp. Quant. Biol. 31: 77-84.
83. Syvanen, M., J. D. Hopkins, T. J. t. Griffin, T. Y. Liang, K. Ippen-Ihler et al., 1986 Stimulation of precise excision and recombination by conjugal proficient F'plasmids. Mol. Gen. Genet. 203: 1-7.
84. Tice, S. C., 1914 A new sex-linked character in Drosophila. Biol. Bull. 26: 221-230.
85. Traxler, B. A., and E. G. Minkley Jr., 1987 Revised genetic map of the distal end of the F transfer operon: implications for DNA helicase I, nicking at oriT, and conjugal DNA transport. J. Bacteriol. 169: 3251-3259.
86. Trinh, T. Q., and R. R. Sinden, 1991 Preferential DNA secondary structure mutagenesis in the lagging strand of replication in E. coli. Nature 352: 544-547.
87. Tsubota, S. I., D. Rosenberg, H. Szostak, D. Rubin, and P. Schedl, 1989 The cloning of the Bar region and the B breakpoint in Drosophila melanogaster: evidence for a transposon-induced rearrangement. Genetics 122: 881-890.
88. Weinreich, M. D., A. Gasch, and W. S. Reznikoff, 1994 Evidence that the cis preference of the Tn5 transposase is caused by non-productive multimerization. Genes Dev. 8: 2363-2374.
89. Williams, P. A., R. J. Ingebretsen, and R. J. Dawson, 2006 14.6 mT ELF magnetic field exposure yields no DNA breaks in model system Salmonella, but provides evidence of heat stress protection. Bioelectromagnetics 27: 445-450.
90. Yu, D., J. A. Sawitzke, H. Ellis, and D. L. Court, 2003 Recombineering with overlapping single-stranded DNA oligonucleotides: testing a recombination intermediate. Proc. Natl. Acad. Sci. USA 100: 7207-7212.
91. Zhang, F., C. M. Carvalho, and J. R. Lupski, 2009 Complex human chromosomal and genomic rearrangements. Trends Genet. 25: 298-307.