The DOI matches its Crossref record; 83 of the 85 references it cites were found in a registry or an index.
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.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“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
Flagged first, then by citations
2 of the 85 references couldn’t be matched to a known paper.
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).
Cited by
Sorted by citations
Items 201–293 of 293
Adaptive Mutation Requires No Mutagenesis—Only Growth Under Selection: A Response
Roth, J. R., Kofoid, E., Roth, F. P., Berg, O. G., Seger, J., & Andersson, D. I. (2003) · Genetics · doi:10.1093/genetics/165.4.2319 · Cited by 6
Mutation and Phenotypic Variation
Hoffmann, A. A., & McKenzie, J. A. (2005) · Elsevier eBooks · doi:10.1016/b978-012088777-4/50011-9 · Cited by 6
Moore, J. M., Wimberly, H., Thornton, P. C., Rosenberg, S. M., & Hastings, P. J. (2012) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2012.06587.x · Cited by 5
Self-citationRecurrence and propagation of past functions through mineral facilitated horizontal gene transfer
Verma, T., Hendiani, S., Moral, C. C., Andersen, S. B., Hammarlund, E. U., Burmølle, M., & Sand, K. K. S. (2024) · Frontiers in Microbiology · doi:10.3389/fmicb.2024.1449094 · Cited by 5
A Creationist Perspective of Beneficial Mutations in Bacteria
Anderson, K. L., & Purdom, G. (2008) · DigitalCommons-Cedarville (Cedarville University) · Cited by 5
Single‐Stranded DNA Binding Protein
Tsurimoto, T. (2002) · Encyclopedia of Molecular Biology · doi:10.1002/047120918x.emb1432 · Cited by 5
Double‐Strand‐Break Repair, Mutagenesis, and Stress
Rogers, E. J., Correa, R., Barreto, B., Núñez, M. A. B., Minnick, P. J., Cruz, D. V., Xia, J., Hastings, P. J., & Rosenberg, S. M. (2016) · Wiley eBooks · doi:10.1002/9781119004813.ch15 · Cited by 5
Self-citationIdentification of a signature of evolutionarily conserved stress-induced mutagenesis in cancer
Cisneros, L. H., Vaske, C. J., & Bussey, K. J. (2022) · Frontiers in Genetics · doi:10.3389/fgene.2022.932763 · Cited by 4
SOS-Inducible DNA Polymerases and Adaptive Mutagenesis
Babynin, E. V. (2004) · Russian Journal of Genetics · doi:10.1023/b:ruge.0000029146.28893.8d · Cited by 4
van den Bergh, J. C. J. M. (2018) · Cambridge University Press eBooks · doi:10.1017/9781108564922.011 · Cited by 3
Ramírez‐Santos, J., García-Mata, V., Poggio, S., Camarena, L., & Gómez‐Eichelmann, M. C. (2008) · Archives of Microbiology · doi:10.1007/s00203-008-0441-z · Cited by 3
Babynin, E. V. (2006) · Microbiology · doi:10.1134/s0026261706040138 · Cited by 4
Moreau, P. L. (2017) · FEMS Microbiology Letters · doi:10.1093/femsle/fnx031 · Cited by 3
Selection and Plasmid Transfer Underlie Adaptive Mutation in Escherichia coli
Maisnier‐Patin, S., & Roth, J. R. (2018) · Genetics · doi:10.1534/genetics.118.301347 · Cited by 3
Genomics-Based Approaches to Novel Antimicrobial Target Discovery
Barrett, J., Dougherty, T. J., & Pucci, M. J. (2003) · CRC Press eBooks · doi:10.1201/9780203911464.ch6 · Cited by 3
Kiran, K., & Patil, K. N. (2023) · The Journal of Biochemistry · doi:10.1093/jb/mvad039 · Cited by 2
Mutagenesis Associated with Repair of DNA Double-Strand Breaks Under Stress
Shee, C., Hastings, P. J., & Rosenberg, S. M. (2013) · Springer eBooks · doi:10.1007/978-1-4614-6280-4_2 · Cited by 3
Self-citationJakkala, K., Sharan, D., Nair, R. R., Paul, A., Pradhan, A., & Ajitkumar, P. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/846378 · Cited by 2
Dobó, V., Homlok, R., Mohácsi‐Farkas, C., & Belák, Á. (2023) · Czech Journal of Food Sciences · doi:10.17221/235/2022-cjfs · Cited by 1
Bayesian learning of nonlinear gene regulatory networks with switching architectures
Vélez-Cruz, N., & Papandreou‐Suppappola, A. (2024) · Frontiers in Signal Processing · doi:10.3389/frsip.2024.1323538 · Cited by 1
Woodland, B., Chowdhury, P. R., O’Rourke, M. B., & Padula, M. P. (2025) · Talanta · doi:10.1016/j.talanta.2025.128480 · Cited by 1
Surbhi, Shau, A. K., Chacko, F. M., & Radhakrishnan, S. K. (2025) · Current Biology · doi:10.1016/j.cub.2025.09.042 · Cited by 1
Varela, E. A., Fuentes, J. L., Herráez, Á., Carro, S., & Prieto, E. (2004) · Revista cubana de investigaciones biomédicas · Cited by 1
Jin, J., Wei, G., Yang, W., Zhang, H., & Gao, P. (2012) · Science China Life Sciences · doi:10.1007/s11427-012-4395-7 · Cited by 1
Effect of the SOS Response on the Mean Fitness of Unicellular Populations: A Quasispecies Approach
Kama, A., & Tannenbaum, E. (2010) · PLoS ONE · doi:10.1371/journal.pone.0014113 · Cited by 1
Origins of cancer symposium 2016: exploring tumor complexity
Harlow, M. L., Lee, K., & Winn, M. E. (2016) · Genes & Cancer · doi:10.18632/genesandcancer.119 · Cited by 1
Shapiro, J. A. (2007) · Biological and medical physics series · doi:10.1007/978-3-540-35306-5_6 · Cited by 1
Free Energies, Landscapes, and Fitness in Evolution Dynamics
Austin, R. H. (2012) · CRC Press eBooks · doi:10.1201/b12676-7 · Cited by 1
Evolution of Social Behaviour in Animals and Humans
van den Bergh, J. C. J. M. (2018) · Cambridge University Press eBooks · doi:10.1017/9781108564922.006 · Cited by 1
Mutagenesis and Translesion Synthesis in Prokaryotes
(2014) · ASM Press eBooks · doi:10.1128/9781555816704.ch15 · Cited by 1
Tuchina, E. S., Kanevsky, M. V., Nidal, E.-K. A., & Slivina, Y. I. (2024) · Izvestiya of Saratov University Chemistry Biology Ecology · doi:10.18500/1816-9775-2024-24-2-196-201 · Cited by 1
van den Bergh, J. C. J. M. (2018) · Cambridge University Press eBooks · doi:10.1017/9781108564922.017 · Cited by 1
Strahilevitz, J., & Hooper, D. C. (2009) · Wiley eBooks · doi:10.1002/9781444308464.ch10 · Cited by 1
Epidemiology and stress responses of Listeria monocytogenes
Markkula, A. (2013) · Työväentutkimus Vuosikirja · Cited by 1
Ndjonka, D., & Bell, C. E. (2009) · AFRICAN JOURNAL OF BIOTECHNOLOGY · doi:10.5897/ajb2009.000-9262 · Cited by 1
How a Large Gene Network Couples Mutagenic DNA Break Repair to Stress inEscherichia Coli
Rogers, E. J., Hastings, P. J., Núñez, M. A. B., & Rosenberg, S. M. (2016) · doi:10.1002/9781119004813.ch54 · Cited by 1
Self-citationAdaptation to Glucosamine Starvation in Borrelia burgdorferi is Mediated by recA
Ryan, G., Janet, A., & David, R. (2012) · InTech eBooks · doi:10.5772/35003
McKenzie, G. J. (2000) · doi:10.21236/ada390995
Self-citationAlhhazmi, A. (2012) · University Library - University of Saskatchewan (University of Saskatchewan)
Mechanism of Mutation in Non-Dividing Cells
Ponder, R. G., & Rosenberg, S. M. (2001) · doi:10.21236/ada396622
Self-citationDNA polümeeraas IV osalus Pseudomonas putida rakkudes toimuvates mutatsiooniprotsessides
Tegova, R. (2004) · DSpace repository (University of Tartu)
Who gives an iota about DNA repair?
Sayers, J. R., & Patel, D. (2001) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(01)01802-3
Ndjonka, D. (2010) · AFRICAN JOURNAL OF BIOTECHNOLOGY
Effects of Growth Inhibition on the Ability of Escherichia coli to Survive UV Irradiation
Pang, P. Y. T., Cheong, S. K. W., Lai, D. Y. N., & Lee, J. P. T. (2026) · Open Collections · doi:10.14288/ujemi.v7.204163
TARTU ÜLIKOOL BIOLOOGIA-GEOGRAAFIA TEADUSKOND MOLEKULAAR- JA RAKUBIOLOOGIA INSTITUUT
Verhovtsova, P. (2006)
Starvation-Induced Reproductive Isolation in Yeast
Kroll, E., Rosenzweig, R. F., & Dunn, B. L. (2010) · Springer eBooks · doi:10.1007/978-3-642-12340-5_3
Xiaobo, L. (2007) · National University of Singapore
Wigle, T. J. (2019) · Carolina Digital Repository (University of North Carolina at Chapel Hill) · doi:10.17615/r266-2c09
Varela, E. A., Fuentes, J. L., Herráez, Á., Carro, S., & Prieto, E. (2004) · Revista cubana de investigaciones biomédicas
Environmental Cues Regulate Virulence and Biofilm Formation
Pace, J., & Frey, S. (2005) · CRC Press eBooks · doi:10.1201/9781420028232.ch14
Krašovec, R., Jerman, I., & Jan, L. (2010) · Acta Biologica Slovenica · doi:10.14720/abs.53.1.15492
Peterson, E. J. R. (2019) · Carolina Digital Repository (University of North Carolina at Chapel Hill) · doi:10.17615/da0x-y275
The Role of RecN in DNA Recombination and Repair in Escherichia coli
Feulner, C. J. (2008) · Digital WPI
Molecular and Cellular Levels of Biological Evolution
Radman, M. (2005) · Kluwer Academic Publishers eBooks · doi:10.1007/0-306-48662-8_14
Understanding Bacterial Resistance and Dissemination: The Impact of Biocide Priming
Adkin, O. P. (2020) · DMU Open Research Archive (De Montfort University)
Industrialisation and Technological History
van den Bergh, J. C. J. M. (2018) · Cambridge University Press eBooks · doi:10.1017/9781108564922.013
Pre-Darwinism, Darwinism and Neo-Darwinism
van den Bergh, J. C. J. M. (2018) · Cambridge University Press eBooks · doi:10.1017/9781108564922.004
Prehistory Until the Rise of Agriculture
van den Bergh, J. C. J. M. (2018) · Cambridge University Press eBooks · doi:10.1017/9781108564922.012
Evolutionary Theories of Human Culture
van den Bergh, J. C. J. M. (2018) · Cambridge University Press eBooks · doi:10.1017/9781108564922.008
Improving cyanobacteria productivity: From theory to assay
Shabestary, K. (2020) · KTH Publication Database DiVA (KTH Royal Institute of Technology)
Advanced Ideas in Evolutionary Biology and Genetics
van den Bergh, J. C. J. M. (2018) · Cambridge University Press eBooks · doi:10.1017/9781108564922.005
Marinus, M. (2005) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.1023621.277665
Faculty Opinions recommendation of Cell death in Pseudomonas aeruginosa biofilm development.
Hengge, R. (2003) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.1014684.195861
Response of Foodborne Pathogens to Cold Plasma
Liao, X., Ding, T., Xiang, Q., & Feng, J. (2022) · Springer eBooks · doi:10.1007/978-3-030-90578-1_10
Faculty Opinions recommendation of The dinB operon and spontaneous mutation in Escherichia coli.
Friedberg, E. C. (2003) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.1014044.192545
Evolving Solutions for Climate Change
van den Bergh, J. C. J. M. (2018) · Cambridge University Press eBooks · doi:10.1017/9781108564922.015
van den Bergh, J. C. J. M. (2018) · Cambridge University Press eBooks · doi:10.1017/9781108564922.019
Evolutionary Policy and Politics
van den Bergh, J. C. J. M. (2018) · Cambridge University Press eBooks · doi:10.1017/9781108564922.016
van den Bergh, J. C. J. M. (2018) · Cambridge University Press eBooks · doi:10.1017/9781108564922.018
The World According to Evolution
van den Bergh, J. C. J. M. (2018) · Cambridge University Press eBooks · doi:10.1017/9781108564922.003
Group Selection in Biology and the Social Sciences
van den Bergh, J. C. J. M. (2018) · Cambridge University Press eBooks · doi:10.1017/9781108564922.007
Making the Improbable Probable
van den Bergh, J. C. J. M. (2018) · Cambridge University Press eBooks · doi:10.1017/9781108564922.002
Evolution of Organisations and Institutions
van den Bergh, J. C. J. M. (2018) · Cambridge University Press eBooks · doi:10.1017/9781108564922.010
van den Bergh, J. C. J. M. (2018) · Cambridge University Press eBooks · doi:10.1017/9781108564922.001
Mapping the dynamics of epigenetic adaptation during heterochromatin misregulationPreprint
Larkin, A., Kunze, C., Seman, M., Levashkevich, A., Curran, J., Morris-Evans, D., Lemieux, S., Khalil, A. S., & Ragunathan, K. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.07.10.548368
Adaptive mutation: shall we survive bacterial genetic skills?
Krašovec, R., & Jerman, I. (2002) · Acta Biologica Slovenica · doi:10.14720/abs.45.2.16628
Using N2 as a final electron receptor in yeast to produce NH3 in bioreactors
Gaballah, Y. (2024) · Research Ideas and Outcomes · doi:10.3897/rio.10.e124020
Expression of dnaE2 promotes genetic diversity in mycobacterial biofilms
Salini, S., Bhat, S. G., Nijisha, M., Paritosh, K., Ramachandran, R., Nikolas, N., Naz, S., & Kurthkoti, K. (2025) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2025.1647744
Lifespan-extending downregulation of insulin signalling reduces germline mutation loadPreprint
Duxbury, E., Godden, A. M., de Coriolis, J., Carlsson, H., Immler, S., & Maklakov, A. A. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2025.12.05.692572
On the role of dcm and vsr in Escherichia coli adaptive mutation
Minda, R., Ramchandani, J., Bindal, G., Rath, D., Kodgire, P., Makde, R. D., & Bhattacharjee, S. (2025) · Molecular Genetics and Genomics · doi:10.1007/s00438-025-02320-z
Tantoso, E., Eisenhaber, B., Kirsch, M., Shitov, V., Zhao, Z., & Eisenhaber, F. (2022) · Figshare · doi:10.6084/m9.figshare.20087966
Tantoso, E., Eisenhaber, B., Kirsch, M., Shitov, V., Zhao, Z., & Eisenhaber, F. (2022) · Figshare · doi:10.6084/m9.figshare.20087975
Tantoso, E., Eisenhaber, B., Kirsch, M., Shitov, V., Zhao, Z., & Eisenhaber, F. (2022) · Figshare · doi:10.6084/m9.figshare.20087969
Atakgayeva, G., Porco, N., Rudovskaya, S., Sarkar, M., Tomlinson, M., Huynh, R., Pucadyil, T., Botelho, R. J., & McPhee, J. B. (2026) · bioRxiv · doi:10.64898/2026.01.29.702582
Ripandelli, R. A. A., Wood, E. A., Robinson, A., van Oijen, A. M., & Cox, M. M. (2026) · PLoS Genetics · doi:10.1371/journal.pgen.1012110
Implications of oxidative stress on microbial evolution
Kumari, A., & Singh, K. (2026) · Elsevier eBooks · doi:10.1016/b978-0-443-42857-9.00015-3
Mapping Griselimycin Functional Group Roles in Sliding Clamp Binding and Antimycobacterial Activity
Clemente, A. F., Koness, K. J., O’Neal, L. G., Jabaley, I. E. Z., Klassen, K. M., Thrall, E. S., & Sawyer, N. (2026) · ACS Chemical Biology · doi:10.1021/acschembio.6c00396
Carcinogens Target Cell Respiration and Induce Glycolysis
Schwartz, L. H. (2004) · Springer eBooks · doi:10.1007/978-3-642-18543-4_9
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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review