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The SOS response regulates adaptive mutation
Open accessAbstract
Upon starvation some Escherichia coli cells undergo a transient, genome-wide hypermutation (called adaptive mutation) that is recombination-dependent and appears to be a response to a stressful environment. Adaptive mutation may reflect an inducible mechanism that generates genetic variability in times of stress. Previously, however, the regulatory components and signal transduction pathways controlling adaptive mutation were unknown. Here we show that adaptive mutation is regulated by the SOS response, a complex, graded response to DNA damage that includes induction of gene products blocking cell division and promoting mutation, recombination, and DNA repair. We find that SOS-induced levels of proteins other than RecA are needed for adaptive mutation. We report a requirement of RecF for efficient adaptive mutation and provide evidence that the role of RecF in mutation is to allow SOS induction. We also report the discovery of an SOS-controlled inhibitor of adaptive mutation, PsiB. These results indicate that adaptive mutation is a tightly regulated response, controlled both positively and negatively by the SOS system.
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“These data support previous work showing that increases in the mutation rate following DNA damage are due to the action of specific repair machinery, rather than the DNA damage itself (57–60).”
From Staphylococcus aureus Adapts to Oxidative Stress by Producing H 2 O 2 -Resistant Small-Colony Variants via the SOS Response (2015) · cites this paper as [59]
Citations
Cites
Escherichia coli and Salmonella :cellular and molecular biology
Neidhardt, F. C. (1996) · ASM Press eBooks · Cited by 8,197
Friedberg, E. C., Walker, G. C., Siede, W., Wood, R. D., Schultz, R. A., & Ellenberger, T. (2005) · doi:10.1128/9781555816704 · Cited by 5,683
A short course in bacterial genetics
Miller, J. H. (1992) · Cited by 4,391
Bootsma, D., & Hoeijmakers, J. H. J. (1996) · Trends in Genetics · doi:10.1016/0168-9525(96)81408-9 · Cited by 2,285
Cairns, J., Overbaugh, J., & Miller, S. (1988) · Nature · doi:10.1038/335142a0 · Cited by 1,025
SOS Repair Hypothesis: Phenomenology of an Inducible DNA Repair Which is Accompanied by Mutagenesis
Radman, M. (1975) · Springer eBooks · doi:10.1007/978-1-4684-2895-7_48 · Cited by 666
Cleavage of the Escherichia coli lexA protein by the recA protease.
Little, J. W., Edmiston, S. H., Pacelli, L. Z., & Mount, D. W. (1980) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.77.6.3225 · Cited by 546
Nature of the SOS-inducing signal in Escherichia coli
Sassanfar, M., & Roberts, J. W. (1990) · Journal of Molecular Biology · doi:10.1016/0022-2836(90)90306-7 · Cited by 541
DNA-damaging agents stimulate gene expression at specific loci in Escherichia coli.
Kenyon, C. J., & Walker, G. C. (1980) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.77.5.2819 · Cited by 537
UmuD′ 2 C is an error-prone DNA polymerase, Escherichia coli pol V
Tang, M., Shen, X., Frank, E. G., O’Donnell, M. E., Woodgate, R., & Goodman, M. F. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.16.8919 · Cited by 537
Adaptive reversion of a frameshift mutation in Escherichia coli.
Cairns, J., & Foster, P. L. (1991) · Genetics · doi:10.1093/genetics/128.4.695 · Cited by 493
The dinB Gene Encodes a Novel E. coli DNA Polymerase, DNA Pol IV, Involved in Mutagenesis
Wagner, J. E., Grúz, P., Kim, S.-R., Yamada, M., Matsui, K., Fuchs, R. P., & Nohmi, T. (1999) · Molecular Cell · doi:10.1016/s1097-2765(00)80376-7 · Cited by 474
RecA Protein: Structure, Function, and Role in Recombinational DNA Repair
Roca, A. I., & Cox, M. M. (1997) · Progress in nucleic acid research and molecular biology · doi:10.1016/s0079-6603(08)61005-3 · Cited by 426
DNA double‐strand breaks caused by replication arrest
Michel, B., Ehrlich, S. D., & Uzest, M. (1997) · The EMBO Journal · doi:10.1093/emboj/16.2.430 · Cited by 426
Collapse and repair of replication forks in Escherichia coli
Kuzminov, A. (1995) · Molecular Microbiology · doi:10.1111/j.1365-2958.1995.tb02403.x · Cited by 363
Kim, S.-R., Maenhaut-Michel, G., Yamada, M., Yamamoto, Y., Matsui, K., Sofuni, T., Nohmi, T., & Ohmori, H. (1997) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.94.25.13792 · Cited by 343
Mount, D. W., Low, K. B., & Edmiston, S. H. (1972) · Journal of Bacteriology · doi:10.1128/jb.112.2.886-893.1972 · Cited by 304
Matić, I., Rayssiguier, C., & Radman, M. (1995) · Cell · doi:10.1016/0092-8674(95)90501-4 · Cited by 302
Torkelson, J. D., Harris, R. S., Lombardo, M., Nagendran, J., Thulin, C., & Rosenberg, S. M. (1997) · EMBO Journal · doi:10.1093/emboj/16.11.3303 · Cited by 273
Self-citationRecombination in Adaptive Mutation
Harris, R. S., Longerich, S., & Rosenberg, S. M. (1994) · Science · doi:10.1126/science.8146657 · Cited by 262
Self-citationADAPTIVE MUTATION: The Uses of Adversity
Foster, P. L. (1993) · Annual Review of Microbiology · doi:10.1146/annurev.mi.47.100193.002343 · Cited by 262
Inhibition of FtsZ polymerization by SulA, an inhibitor of septation in Escherichia coli
Mukherjee, A., Cao, C., & Lutkenhaus, J. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.6.2885 · Cited by 247
Mount, D. W. (1977) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.74.1.300 · Cited by 230
Adaptive mutation by deletions in small mononucleotide repeats.
Rosenberg, S. M., Longerich, S., Gee, P., & Harris, R. S. (1994) · Science · doi:10.1126/science.8023163 · Cited by 229
Self-citationPlant responses to environmental stress
Vierling, E., & Kimpel, J. A. (1992) · Current Opinion in Biotechnology · doi:10.1016/0958-1669(92)90147-b · Cited by 210
Plant Responses to Environmental Stresses: From Phytohormones to Genome Reorganization
Tudzynski, B. (2001) · Phytochemistry · doi:10.1016/s0031-9422(00)00375-7 · Cited by 209
Homologous Genetic Recombination: The Pieces Begin to Fall into Place
Clark, A. J., & Sandler, S. J. (1994) · Critical Reviews in Microbiology · doi:10.3109/10408419409113552 · Cited by 197
cAMP-dependent SOS induction and mutagenesis in resting bacterial populations.
Taddéi, F., Matić, I., & Radman, M. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.25.11736 · Cited by 197
Foster, P. L., & Trimarchi, J. M. (1994) · Science · doi:10.1126/science.8023164 · Cited by 192
Bacterial SOS Checkpoint Protein SulA Inhibits Polymerization of Purified FtsZ Cell Division Protein
Trusca, D., Scott, S., Thompson, C., & Bramhill, D. (1998) · Journal of Bacteriology · doi:10.1128/jb.180.15.3946-3953.1998 · Cited by 187
χ AND THE RecBC D ENZYME OF ESCHERICHIA COLI
Myers, R. S., & Stahl, F. W. (1994) · Annual Review of Genetics · doi:10.1146/annurev.ge.28.120194.000405 · Cited by 186
Mismatch repair protein MutL becomes limiting during stationary-phase mutationPreprint
Harris, R. S., Feng, G., Ross, K. J., Sidhu, R., Thulin, C., Longerich, S., Szigety, S. K., Winkler, M. E., & Rosenberg, S. M. (1997) · Genes & Development · doi:10.1101/gad.11.18.2426 · Cited by 155
Self-citationFoster, P. L., Trimarchi, J. M., & Maurer, R. (1996) · Genetics · doi:10.1093/genetics/142.1.25 · Cited by 148
Harris, R. S., Ross, K. J., & Rosenberg, S. M. (1996) · Genetics · doi:10.1093/genetics/142.3.681 · Cited by 142
Self-citationControl of recA gene RNA in E. coli: Regulatory and signal genes
McPartland, A., Green, L., & Echols, H. (1980) · Cell · doi:10.1016/0092-8674(80)90319-0 · Cited by 137
The role of transient hypermutators in adaptive mutation in Escherichia coli.
Rosche, W. A., & Foster, P. L. (1999) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.96.12.6862 · Cited by 137
Foster, P. L., & Trimarchi, J. M. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.12.5487 · Cited by 137
Drake, J. W. (1991) · Annual Review of Genetics · doi:10.1146/annurev.ge.25.120191.001013 · Cited by 135
Evidence that F plasmid transfer replication underlies apparent adaptive mutation.
Galitski, T., & Roth, J. R. (1995) · Science · doi:10.1126/science.7716546 · Cited by 133
DNA polymerase II is encoded by the DNA damage-inducible dinA gene of Escherichia coli.
Bonner, C. A., Hays, S. L., McEntee, K., & Goodman, M. F. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.19.7663 · Cited by 130
Brotcorne-Lannoye, A., & Maenhaut-Michel, G. (1986) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.83.11.3904 · Cited by 125
Nucleotide sequence of the lexA gene of E. coli
Horii, T., Ogawa, T., & Ogawa, H. (1981) · Cell · doi:10.1016/0092-8674(81)90432-3 · Cited by 124
Genetic requirements and mutational specificity of the Escherichia coli SOS mutator activity
Fijałkowska, I. J., Dunn, R. L., & Schaaper, R. M. (1997) · Journal of Bacteriology · doi:10.1128/jb.179.23.7435-7445.1997 · Cited by 119
Transient and Heritable Mutators in Adaptive Evolution in the Lab and in Nature
Rosenberg, S. M., Thulin, C., & Harris, R. S. (1998) · Genetics · doi:10.1093/genetics/148.4.1559 · Cited by 114
Self-citationConstruction of a umuDC operon substitution mutation in Escherichia coli
Woodgate, R. (1992) · Mutation Research Letters · doi:10.1016/0165-7992(92)90012-7 · Cited by 112
Proofreading-defective DNA polymerase II increases adaptive mutation in Escherichia coli.
Foster, P. L., Gudmundsson, G., Trimarchi, J. M., Cai, H., & Goodman, M. F. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.17.7951 · Cited by 109
Lin, L.-L., & Little, J. W. (1988) · Journal of Bacteriology · doi:10.1128/jb.170.5.2163-2173.1988 · Cited by 105
The Escherichia coli polB gene, which encodes DNA polymerase II, is regulated by the SOS system
Iwasaki, H., Nakata, A., Walker, G. C., & Shinagawa, H. (1990) · Journal of Bacteriology · doi:10.1128/jb.172.11.6268-6273.1990 · Cited by 93
Nucleotide sequence of the lexA gene of Escherichia coli K-12
Markham, B. E., Little, J. W., & Mount, D. W. (1981) · Nucleic Acids Research · doi:10.1093/nar/9.16.4149 · Cited by 90
Molecular analysis of the recF gene of Escherichia coli.
Blanar, M. A., Sandler, S. J., Armengod, M. E., Ream, L. W., & Clark, A. J. (1984) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.81.15.4622 · Cited by 88
Autodigestion and RecA-dependent cleavage of Ind− mutant LexA proteins
Lin, L.-L., & Little, J. W. (1989) · Journal of Molecular Biology · doi:10.1016/0022-2836(89)90121-6 · Cited by 87
Inhibition of Escherichia coli RecA coprotease activities by DinI
Yasuda, T., Morimatsu, K., Horii, T., Nagata, T., & Ohmori, H. (1998) · The EMBO Journal · doi:10.1093/emboj/17.11.3207 · Cited by 87
Adaptive mutation sequences reproduced by mismatch repair deficiency.
Longerich, S., Galloway, A. M., Harris, R. S., Wong, C., & Rosenberg, S. M. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.26.12017 · Cited by 81
Self-citationBagdasarian, M. M., Bailone, A., Angulo, J. F., Scholz, P., Bagdasarian, M., & Devoret, R. (1992) · Molecular Microbiology · doi:10.1111/j.1365-2958.1992.tb01539.x · Cited by 78
Motamedi, M. R., Szigety, S. K., & Rosenberg, S. M. (1999) · Genes & Development · doi:10.1101/gad.13.21.2889 · Cited by 77
Self-citationSomatic hypermutation and the three R's: repair, replication and recombination
Harris, R. S., Kong, Q., & Maizels, N. (1999) · Mutation Research/Reviews in Mutation Research · doi:10.1016/s1383-5742(99)00003-4 · Cited by 74
Self-citationHypermutation in derepressed operons of Escherichia coli K12
Wright, B. E., Longacre, A., & Reimers, J. M. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.9.5089 · Cited by 73
Zhang, Q.-M., Ishikawa, N., Nakahara, T., & Yonei, S. (1998) · Nucleic Acids Research · doi:10.1093/nar/26.20.4669 · Cited by 72
Rosenberg, S. M. (1997) · Current Opinion in Genetics and Development · doi:10.1016/s0959-437x(97)80047-0 · Cited by 70
Self-citationMismatch repair is diminished during stationary-phase mutation.
Harris, R. S., Feng, G., Ross, K. J., Sidhu, R., Thulin, C., Longerich, S., Szigety, S. K., Hastings, P. J., Winkler, M. E., & Rosenberg, S. M. (1999) · PubMed · Cited by 68
Self-citationGenetic analysis of mutagenesis in aging Escherichia coli colonies
Taddéi, F., Halliday, J. A., Matić, I., & Radman, M. (1997) · Molecular and General Genetics MGG · doi:10.1007/s004380050570 · Cited by 67
Reconstitution of an SOS Response Pathway
Anderson, D. G., & Kowalczykowski, S. C. (1998) · Cell · doi:10.1016/s0092-8674(00)81721-3 · Cited by 66
Embryonic Encyclopedia of Life Sciences
Gilmour, R. (2001) · Reference Reviews · doi:10.1108/rr.2001.15.2.36.96 · Cited by 62
Some Features of the Mutability of Bacteria During Nonlethal Selection
Godoy, V. G., Gizatullin, F., & Fox, M. S. (2000) · Genetics · doi:10.1093/genetics/154.1.49 · Cited by 60
Bull, H. J., McKenzie, G. J., Hastings, P. J., & Rosenberg, S. M. (2000) · Genetics · doi:10.1093/genetics/154.4.1427 · Cited by 60
Self-citationMolecular handles on adaptive mutation
Rosenberg, S. M., Harris, R. S., & Torkelson, J. D. (1995) · Molecular Microbiology · doi:10.1111/j.1365-2958.1995.mmi_18020185.x · Cited by 56
Self-citationHarris, R. S., Bull, H. J., & Rosenberg, S. M. (1997) · Mutation research · doi:10.1016/s0027-5107(96)00244-8 · Cited by 52
Self-citationATP Hydrolysis and DNA Binding by the Escherichia coli RecF Protein
Webb, B. L., Cox, M. M., & Inman, R. B. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.22.15367 · Cited by 50
Hypermutability in Carcinogenesis
Strauss, B. S. (1998) · Genetics · doi:10.1093/genetics/148.4.1619 · Cited by 49
Bridges, B. A. (1997) · Nature · doi:10.1038/42370 · Cited by 48
The effect of the stringent response on mutation rates in Escherichia coli K‐12
Wright, B. E. (1996) · Molecular Microbiology · doi:10.1046/j.1365-2958.1996.367892.x · Cited by 39
Recombination-dependent mutation in Escherichia coli occurs in stationary phase.
McKenzie, G. J., Lombardo, M., & Rosenberg, S. M. (1998) · Genetics · doi:10.1093/genetics/149.2.1163 · Cited by 39
Self-citationRecombination-dependent mutation in non-dividing cells.
Rosenberg, S. M., Harris, R. S., Longerich, S., & Galloway, A. (1996) · Mutation research · doi:10.1016/0027-5107(95)00092-5 · Cited by 37
Self-citationHigashitani, N., Higashitani, A., Roth, A., & HORIUCHI, K. (1992) · Journal of Bacteriology · doi:10.1128/jb.174.5.1612-1618.1992 · Cited by 36
Adaptive Mutagenesis at ebgR Is Regulated by PhoPQ
Hall, B. G. (1998) · Journal of Bacteriology · doi:10.1128/jb.180.11.2862-2865.1998 · Cited by 35
Evidence that rnmB is the operator of the Escherichia coli recA gene.
Volkert, M. R., Margossian, L. J., & Clark, A. J. (1981) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.78.3.1786 · Cited by 35
Finch, C. E., & Goodman, M. F. (1997) · Trends in Neurosciences · doi:10.1016/s0166-2236(97)01143-0 · Cited by 30
(1999) · Mutation Research/Reviews in Mutation Research · doi:10.1016/s1383-5742(99)00064-2 · Cited by 30
Hall, B. G. (1992) · Current Opinion in Genetics and Development · doi:10.1016/s0959-437x(05)80120-0 · Cited by 26
Tomer, G., Reuven, N. B., & Livneh, Z. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.24.14106 · Cited by 23
Timms, A. R., Muriel, W. J., & Bridges, B. A. (1999) · Mutation Research/DNA Repair · doi:10.1016/s0921-8777(99)00035-x · Cited by 21
Mechanisms of Genome‐Wide Hypermutation in Stationary Phasea
Lombardo, M., Torkelson, J. D., Bull, H. J., McKenzie, G. J., & Rosenberg, S. M. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb08888.x · Cited by 19
Self-citationHypermutation in stationary-phaseE. coli: tales from thelac operon
Lombardo, M., & Rosenberg, S. M. (1999) · Journal of Genetics · doi:10.1007/bf02994698 · Cited by 10
Self-citation
Research works printed but not linked: 2
- M Radman Basic Life Sci 5A, 355–367 (1975).
- R S Harris Ph.D. Thesis (University of Alberta, Edmonton, Alberta, Canada, 1997).
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Metadata
- Authors
- McKenzie, G. J., Harris, R. S., Lee, P. L., & Rosenberg, S. M.
- Affiliations
- University of Alberta (CA)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2000-05-30
- Volume
- 97
- Issue
- 12
- Pages
- 6646-6651
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC18688
- OpenAlex
- W2037722651
- Cited by
- 295
- References
- 85
- Citations by year
- 2026: 5 · 2025: 8 · 2024: 12 · 2023: 16 · 2022: 16 · 2021: 9 · 2020: 8 · 2019: 12 · 2018: 28 · 2017: 6 · 2016: 12 · 2015: 3 · 2014: 6 · 2013: 7 · 2012: 12
- FWCI
- 8.70
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- U.S. Department of Defense
- Fondation pour la Recherche Médicale
- National Institutes of Health (5r01ai043917-05)
- National Institute of General Medical Sciences (R01GM053158)
- National Institute of Allergy and Infectious Diseases (R01-AI43917)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Keywords
- adaptive mutation, SOS response, Escherichia coli, starvation, recF, RecA, DNA damage response, signal transduction regulation
- MeSH terms
- LexA Repressor Protein, Adaptation, Physiological, Bacterial Proteins, DNA Repair, DNA-Binding Proteins, Mutation, Serine Endopeptidases, SOS Response, Genetics, Signal Transduction, Regulon, Escherichia coli Proteins
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