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PMID: 10747042 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Evidence that stationary-phase hypermutation in the Escherichia coli chromosome is promoted by recombination.

Genetics ·Vol. 154 ·No. 4 ·2000-04-00 ·Pages 1427-37

Bull HJ, McKenzie GJ, Hastings PJ, Rosenberg SM

Abstract

Adaptive (or stationary-phase) mutation is a group of phenomena in which mutations appear to occur more often when selected than when not. They may represent cellular responses to the environment in which the genome is altered to allow survival. The best-characterized assay system and mechanism is reversion of a lac allele on an F' sex plasmid in Escherichia coli, in which the stationary-phase mutability requires homologous recombination functions. A key issue has concerned whether the recombination-dependent mutation mechanism is F' specific or is general. Hypermutation of chromosomal genes occurs in association with adaptive Lac(+) mutation. Here we present evidence that the chromosomal hypermutation is promoted by recombination. Hyperrecombinagenic recD cells show elevated chromosomal hypermutation. Further, recG mutation, which promotes accumulation of recombination intermediates proposed to prime replication and mutation, also stimulates chromosomal hypermutation. The coincident mutations at lac (on the F') and chromosomal genes behave as independent events, whereas coincident mutations at lac and other F-linked sites do not. This implies that transient covalent linkage of F' and chromosomal DNA (Hfr formation) does not underlie chromosomal mutation. The data suggest that recombinational stationary-phase mutation occurs in the bacterial chromosome and thus can be a general strategy for programmed genetic change.

MeSH Terms
Bacterial Proteins/genetics Biological Evolution Chromosomes, Bacterial Escherichia coli/genetics Escherichia coli Proteins Exodeoxyribonuclease V Exodeoxyribonucleases/genetics Mutation Recombination, Genetic
Chemicals
Bacterial Proteins Escherichia coli Proteins RecG protein, E coli Exodeoxyribonucleases Exodeoxyribonuclease V exodeoxyribonuclease V, E coli
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Bull H J
Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, Texas 77030-3498, USA.
McKenzie G J
Hastings P J
Rosenberg S M
References (68)
68 references, click to expand
  1. Adaptive reversion of a frameshift mutation in Escherichia coli by simple base deletions in homopolymeric runs.
    Science. 1994 Jul 15;265(5170):407-9 PMID: 8023164
  2. Reverse branch migration of Holliday junctions by RecG protein: a new mechanism for resolution of intermediates in recombination and DNA repair.
    Cell. 1993 Oct 22;75(2):341-50 PMID: 8402917
  3. Mechanisms of genome-wide hypermutation in stationary phase.
    Ann N Y Acad Sci. 1999 May 18;870:275-89 PMID: 10415490
  4. DNA synthesis errors associated with double-strand-break repair.
    Genetics. 1995 Jul;140(3):965-72 PMID: 7672595
  5. Chi and the RecBC D enzyme of Escherichia coli.
    Annu Rev Genet. 1994;28:49-70 PMID: 7893137
  6. The origin of mutants.
    Nature. 1988 Sep 8;335(6186):142-5 PMID: 3045565
  7. Programmed cell death in bacterial populations.
    Science. 1995 Feb 10;267(5199):836-7 PMID: 7846528
  8. Biochemistry and genetics of eukaryotic mismatch repair.
    Genes Dev. 1996 Jun 15;10(12):1433-42 PMID: 8666228
  9. Adaptive reversion of an episomal frameshift mutation in Escherichia coli requires conjugal functions but not actual conjugation.
    Proc Natl Acad Sci U S A. 1995 Jun 6;92(12):5487-90 PMID: 7777535
  10. The role of transient hypermutators in adaptive mutation in Escherichia coli.
    Proc Natl Acad Sci U S A. 1999 Jun 8;96(12):6862-7 PMID: 10359804
  11. Analysis of the sequence and gene products of the transfer region of the F sex factor.
    Microbiol Rev. 1994 Jun;58(2):162-210 PMID: 7915817
  12. RuvAB acts at arrested replication forks.
    Cell. 1998 Oct 30;95(3):419-30 PMID: 9814711
  13. Evolutionary biology. A boost for "adaptive" mutation.
    Science. 1994 Jul 15;265(5170):318-9 PMID: 8023153
  14. Opposing roles of the holliday junction processing systems of Escherichia coli in recombination-dependent adaptive mutation.
    Genetics. 1996 Mar;142(3):681-91 PMID: 8849879
  15. Adaptive mutation: a general phenomenon or special case?
    Bioessays. 1997 Jan;19(1):9-11 PMID: 9008412
  16. Transient mutators: a semiquantitative analysis of the influence of translation and transcription errors on mutation rates.
    Genetics. 1991 Nov;129(3):957-62 PMID: 1752431
  17. recD: the gene for an essential third subunit of exonuclease V.
    Proc Natl Acad Sci U S A. 1986 Aug;83(15):5558-62 PMID: 3526335
  18. Hypermutation in derepressed operons of Escherichia coli K12.
    Proc Natl Acad Sci U S A. 1999 Apr 27;96(9):5089-94 PMID: 10220423
  19. Redundant homosexual F transfer facilitates selection-induced reversion of plasmid mutations.
    J Bacteriol. 1996 Jun;178(11):3037-43 PMID: 8655477
  20. Modulation of recombination and DNA repair by the RecG and PriA helicases of Escherichia coli K-12.
    J Bacteriol. 1996 Dec;178(23):6782-9 PMID: 8955297
  21. Some features of the mutability of bacteria during nonlethal selection.
    Genetics. 2000 Jan;154(1):49-59 PMID: 10628968
  22. Increased episomal replication accounts for the high rate of adaptive mutation in recD mutants of Escherichia coli.
    Genetics. 1999 May;152(1):15-30 PMID: 10224241
  23. Adaptive mutation: the uses of adversity.
    Annu Rev Microbiol. 1993;47:467-504 PMID: 8257106
  24. Proofreading-defective DNA polymerase II increases adaptive mutation in Escherichia coli.
    Proc Natl Acad Sci U S A. 1995 Aug 15;92(17):7951-5 PMID: 7644519
  25. Nonadaptive mutations occur on the F' episome during adaptive mutation conditions in Escherichia coli.
    J Bacteriol. 1997 Mar;179(5):1550-4 PMID: 9045812
  26. A new class of Escherichia coli recBC mutants: implications for the role of RecBC enzyme in homologous recombination.
    Proc Natl Acad Sci U S A. 1984 Dec;81(24):7850-4 PMID: 6393130
  27. The evolution of genetic intelligence.
    Science. 1994 Apr 8;264(5156):224-5 PMID: 8146652
  28. Mutation for survival.
    Curr Opin Genet Dev. 1997 Dec;7(6):829-34 PMID: 9468794
  29. Identification and characterization of recD, a gene affecting plasmid maintenance and recombination in Escherichia coli.
    J Bacteriol. 1986 Aug;167(2):594-603 PMID: 3015881
  30. Two enzymes, both of which process recombination intermediates, have opposite effects on adaptive mutation in Escherichia coli.
    Genetics. 1996 Jan;142(1):25-37 PMID: 8770582
  31. SELFER MUTANTS OF SALMONELLA TYPHIMURIUM.
    Genetics. 1963 Nov;48:1519-31 PMID: 14083047
  32. Somatic hypermutation: how many mechanisms diversify V region sequences?
    Cell. 1995 Oct 6;83(1):9-12 PMID: 7553877
  33. Editing DNA replication and recombination by mismatch repair: from bacterial genetics to mechanisms of predisposition to cancer in humans.
    Philos Trans R Soc Lond B Biol Sci. 1995 Jan 30;347(1319):97-103 PMID: 7746861
  34. A search for a general phenomenon of adaptive mutability.
    Genetics. 1996 Jun;143(2):645-59 PMID: 8725216
  35. How the genome readies itself for evolution.
    Science. 1998 Aug 21;281(5380):1131,1133-4 PMID: 9735027
  36. Biochemical and physical characterization of exonuclease V from Escherichia coli. Comparison of the catalytic activities of the RecBC and RecBCD enzymes.
    J Biol Chem. 1990 Feb 25;265(6):3447-54 PMID: 2154479
  37. Double-strand-break repair recombination in Escherichia coli: physical evidence for a DNA replication mechanism in vivo.
    Genes Dev. 1999 Nov 1;13(21):2889-903 PMID: 10557215
  38. A role for REV3 in mutagenesis during double-strand break repair in Saccharomyces cerevisiae.
    Genetics. 1997 Nov;147(3):1017-24 PMID: 9383049
  39. Recombination of bacteriophage lambda in recD mutants of Escherichia coli.
    Genome. 1989;31(1):53-67 PMID: 2556327
  40. Adaptive mutation in Escherichia coli: a role for conjugation.
    Science. 1995 Apr 21;268(5209):418-20 PMID: 7716545
  41. The split-end model for homologous recombination at double-strand breaks and at Chi.
    Biochimie. 1991 Apr;73(4):385-97 PMID: 1911939
  42. Spontaneous point mutations that occur more often when advantageous than when neutral.
    Genetics. 1990 Sep;126(1):5-16 PMID: 2227388
  43. Transient and heritable mutators in adaptive evolution in the lab and in nature.
    Genetics. 1998 Apr;148(4):1559-66 PMID: 9560375
  44. Spontaneous mutation.
    Annu Rev Genet. 1991;25:125-46 PMID: 1812804
  45. Mutations of Bacteria from Virus Sensitivity to Virus Resistance.
    Genetics. 1943 Nov;28(6):491-511 PMID: 17247100
  46. A direct role for DNA polymerase III in adaptive reversion of a frameshift mutation in Escherichia coli.
    Mutat Res. 1997 Apr 14;375(1):19-24 PMID: 9129676
  47. PsiB, and anti-SOS protein, is transiently expressed by the F sex factor during its transmission to an Escherichia coli K-12 recipient.
    Mol Microbiol. 1992 Apr;6(7):885-93 PMID: 1318487
  48. Genetics of selection-induced mutations: I. uvrA, uvrB, uvrC, and uvrD are selection-induced specific mutator loci.
    J Mol Evol. 1995 Jan;40(1):86-93 PMID: 7714915
  49. The recombination hot spot chi is a regulatory element that switches the polarity of DNA degradation by the RecBCD enzyme.
    Genes Dev. 1997 Mar 1;11(5):571-81 PMID: 9119222
  50. 'SELFERS' AND HIGH MUTATION RATE DURING MEIOSIS IN ASCOBOLUS IMMERSUS.
    Nature. 1964 Nov 21;204:809 PMID: 14235698
  51. Somatic hypermutation and the three R's: repair, replication and recombination.
    Mutat Res. 1999 Mar;436(2):157-78 PMID: 10095138
  52. "SELFERS"-ATTRIBUTED TO UNEQUAL CROSSOVERS IN SALMONELLA.
    Proc Natl Acad Sci U S A. 1962 Oct;48(10):1696-704 PMID: 16591003
  53. Adaptive mutation sequences reproduced by mismatch repair deficiency.
    Proc Natl Acad Sci U S A. 1995 Dec 19;92(26):12017-20 PMID: 8618835
  54. The roles of starvation and selective substrates in the emergence of araB-lacZ fusion clones.
    EMBO J. 1994 Nov 1;13(21):5229-39 PMID: 7957088
  55. Genome-wide hypermutation in a subpopulation of stationary-phase cells underlies recombination-dependent adaptive mutation.
    EMBO J. 1997 Jun 2;16(11):3303-11 PMID: 9214645
  56. Francis Ryan and the origins of directed mutagenesis.
    Mutat Res. 1993 Jan;285(1):9-12 PMID: 7678137
  57. Diploid yeast cells yield homozygous spontaneous mutations.
    Curr Genet. 1993 May-Jun;23(5-6):430-4 PMID: 8319299
  58. Adaptive reversion of a frameshift mutation in Escherichia coli.
    Genetics. 1991 Aug;128(4):695-701 PMID: 1916241
  59. recF and recR are required for the resumption of replication at DNA replication forks in Escherichia coli.
    Proc Natl Acad Sci U S A. 1997 Apr 15;94(8):3714-9 PMID: 9108043
  60. Replication fork assembly at recombination intermediates is required for bacterial growth.
    Proc Natl Acad Sci U S A. 1999 Mar 30;96(7):3552-5 PMID: 10097074
  61. Different Rates of Spontaneous Mutation during Mitosis and Meiosis in Yeast.
    Genetics. 1962 Aug;47(8):1097-108 PMID: 17248123
  62. DNA double-strand breaks caused by replication arrest.
    EMBO J. 1997 Jan 15;16(2):430-8 PMID: 9029161
  63. Mismatch repair protein MutL becomes limiting during stationary-phase mutation.
    Genes Dev. 1997 Sep 15;11(18):2426-37 PMID: 9308969
  64. Microbial genetics. Hypermutation under stress.
    Nature. 1997 Jun 5;387(6633):557-8 PMID: 9177337
  65. Genome organization, natural genetic engineering and adaptive mutation.
    Trends Genet. 1997 Mar;13(3):98-104 PMID: 9066268
  66. The DNA replication protein PriA and the recombination protein RecG bind D-loops.
    J Mol Biol. 1997 Jul 11;270(2):212-21 PMID: 9236123
  67. Evidence that F plasmid transfer replication underlies apparent adaptive mutation.
    Science. 1995 Apr 21;268(5209):421-3 PMID: 7716546
  68. Collapse and repair of replication forks in Escherichia coli.
    Mol Microbiol. 1995 May;16(3):373-84 PMID: 7565099
Article Info
Journal
Genetics
Abbr.
Genetics
ISSN
0016-6731
DOI
10.1093/genetics/154.4.1427
Published
2000-04-00
Pages
1427-37
Language
English
Region
United States
NLM ID
0374636
PMCID
PMC1461015
Subset
IM
Grants
NIAID NIH HHS · R01 AI43917 · United States
NIGMS NIH HHS · R01 GM53158 · United States
Corrections
CommentIn
PMID: 11183859
External Links
PubMed source DOI: 10.1093/genetics/154.4.1427 PMC Full Text View journal details
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