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. 1998 Apr;148(4):1453–1459. doi: 10.1093/genetics/148.4.1453

Adaptive mutation: has the unicorn landed?

P L Foster 1
PMCID: PMC1460081  PMID: 9560365

Abstract

Reversion of an episomal Lac- allele during lactose selection has been studied as a model for adaptive mutation. Although recent results show that the mutations that arise during selection are not "adaptive" in the original sense, the mutagenic mechanism that produces these mutations may nonetheless be of evolutionary significance. In addition, a transient mutational state induced in a subpopulation of starving cells could provide a species with a mechanism for adaptive evolution.

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Selected References

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  1. Boe L. Mechanism for induction of adaptive mutations in Escherichia coli. Mol Microbiol. 1990 Apr;4(4):597–601. doi: 10.1111/j.1365-2958.1990.tb00628.x. [DOI] [PubMed] [Google Scholar]
  2. Boyd E. F., Hartl D. L. Recent horizontal transmission of plasmids between natural populations of Escherichia coli and Salmonella enterica. J Bacteriol. 1997 Mar;179(5):1622–1627. doi: 10.1128/jb.179.5.1622-1627.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Boyd E. F., Hill C. W., Rich S. M., Hartl D. L. Mosaic structure of plasmids from natural populations of Escherichia coli. Genetics. 1996 Jul;143(3):1091–1100. doi: 10.1093/genetics/143.3.1091. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bridges B. A. Elevated mutation rate in mutT bacteria during starvation: evidence for DNA turnover? J Bacteriol. 1996 May;178(9):2709–2711. doi: 10.1128/jb.178.9.2709-2711.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cairns J., Foster P. L. Adaptive reversion of a frameshift mutation in Escherichia coli. Genetics. 1991 Aug;128(4):695–701. doi: 10.1093/genetics/128.4.695. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cairns J. Mutation and cancer: the antecedents to our studies of adaptive mutation. Genetics. 1998 Apr;148(4):1433–1440. doi: 10.1093/genetics/148.4.1433. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cairns J., Overbaugh J., Miller S. The origin of mutants. Nature. 1988 Sep 8;335(6186):142–145. doi: 10.1038/335142a0. [DOI] [PubMed] [Google Scholar]
  8. Carter J. R., Patel D. R., Porter R. D. The role of oriT in tra-dependent enhanced recombination between mini-F-lac-oriT and lambda plac5. Genet Res. 1992 Jun;59(3):157–165. doi: 10.1017/s0016672300030433. [DOI] [PubMed] [Google Scholar]
  9. Christensen R. B., Christensen J. R., Lawrence C. W. Conjugation-dependent enhancement of induced and spontaneous mutation in the lacI gene of E. coli. Mol Gen Genet. 1985;201(1):35–37. doi: 10.1007/BF00397983. [DOI] [PubMed] [Google Scholar]
  10. DEMEREC M. SELFER MUTANTS OF SALMONELLA TYPHIMURIUM. Genetics. 1963 Nov;48:1519–1531. doi: 10.1093/genetics/48.11.1519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Escarceller M., Hicks J., Gudmundsson G., Trump G., Touati D., Lovett S., Foster P. L., McEntee K., Goodman M. F. Involvement of Escherichia coli DNA polymerase II in response to oxidative damage and adaptive mutation. J Bacteriol. 1994 Oct;176(20):6221–6228. doi: 10.1128/jb.176.20.6221-6228.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Feng G., Tsui H. C., Winkler M. E. Depletion of the cellular amounts of the MutS and MutH methyl-directed mismatch repair proteins in stationary-phase Escherichia coli K-12 cells. J Bacteriol. 1996 Apr;178(8):2388–2396. doi: 10.1128/jb.178.8.2388-2396.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Foster P. L. Adaptive mutation: the uses of adversity. Annu Rev Microbiol. 1993;47:467–504. doi: 10.1146/annurev.mi.47.100193.002343. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Foster P. L., Cairns J. Mechanisms of directed mutation. Genetics. 1992 Aug;131(4):783–789. doi: 10.1093/genetics/131.4.783. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Foster P. L., Cairns J. The occurrence of heritable Mu excisions in starving cells of Escherichia coli. EMBO J. 1994 Nov 1;13(21):5240–5244. doi: 10.1002/j.1460-2075.1994.tb06855.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Foster P. L. Directed mutation: between unicorns and goats. J Bacteriol. 1992 Mar;174(6):1711–1716. doi: 10.1128/jb.174.6.1711-1716.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Foster P. L., Gudmundsson G., Trimarchi J. M., Cai H., Goodman M. F. Proofreading-defective DNA polymerase II increases adaptive mutation in Escherichia coli. Proc Natl Acad Sci U S A. 1995 Aug 15;92(17):7951–7955. doi: 10.1073/pnas.92.17.7951. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Foster P. L. Nonadaptive mutations occur on the F' episome during adaptive mutation conditions in Escherichia coli. J Bacteriol. 1997 Mar;179(5):1550–1554. doi: 10.1128/jb.179.5.1550-1554.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Foster P. L. Population dynamics of a Lac- strain of Escherichia coli during selection for lactose utilization. Genetics. 1994 Oct;138(2):253–261. doi: 10.1093/genetics/138.2.253. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Foster P. L., Trimarchi J. M. Adaptive reversion of a frameshift mutation in Escherichia coli by simple base deletions in homopolymeric runs. Science. 1994 Jul 15;265(5170):407–409. doi: 10.1126/science.8023164. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Foster P. L., Trimarchi J. M. 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):5487–5490. doi: 10.1073/pnas.92.12.5487. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Foster P. L., Trimarchi J. M. Conjugation is not required for adaptive reversion of an episomal frameshift mutation in Escherichia coli. J Bacteriol. 1995 Nov;177(22):6670–6671. doi: 10.1128/jb.177.22.6670-6671.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Foster P. L., Trimarchi J. M., Maurer R. A. Two enzymes, both of which process recombination intermediates, have opposite effects on adaptive mutation in Escherichia coli. Genetics. 1996 Jan;142(1):25–37. doi: 10.1093/genetics/142.1.25. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Galitski T., Roth J. R. A search for a general phenomenon of adaptive mutability. Genetics. 1996 Jun;143(2):645–659. doi: 10.1093/genetics/143.2.645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Galitski T., Roth J. R. Evidence that F plasmid transfer replication underlies apparent adaptive mutation. Science. 1995 Apr 21;268(5209):421–423. doi: 10.1126/science.7716546. [DOI] [PubMed] [Google Scholar]
  26. Harris R. S., Feng G., Ross K. J., Sidhu R., Thulin C., Longerich S., Szigety S. K., Winkler M. E., Rosenberg S. M. Mismatch repair protein MutL becomes limiting during stationary-phase mutation. Genes Dev. 1997 Sep 15;11(18):2426–2437. doi: 10.1101/gad.11.18.2426. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Harris R. S., Longerich S., Rosenberg S. M. Recombination in adaptive mutation. Science. 1994 Apr 8;264(5156):258–260. doi: 10.1126/science.8146657. [DOI] [PubMed] [Google Scholar]
  28. Harris R. S., Ross K. J., Rosenberg S. M. Opposing roles of the holliday junction processing systems of Escherichia coli in recombination-dependent adaptive mutation. Genetics. 1996 Mar;142(3):681–691. doi: 10.1093/genetics/142.3.681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Kasak L., Hõrak R., Kivisaar M. Promoter-creating mutations in Pseudomonas putida: a model system for the study of mutation in starving bacteria. Proc Natl Acad Sci U S A. 1997 Apr 1;94(7):3134–3139. doi: 10.1073/pnas.94.7.3134. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Kogoma T. Stable DNA replication: interplay between DNA replication, homologous recombination, and transcription. Microbiol Mol Biol Rev. 1997 Jun;61(2):212–238. doi: 10.1128/mmbr.61.2.212-238.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Kowalczykowski S. C., Dixon D. A., Eggleston A. K., Lauder S. D., Rehrauer W. M. Biochemistry of homologous recombination in Escherichia coli. Microbiol Rev. 1994 Sep;58(3):401–465. doi: 10.1128/mr.58.3.401-465.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Kunz B. A., Glickman B. W. The infidelity of conjugal DNA transfer in Escherichia coli. Genetics. 1983 Nov;105(3):489–500. doi: 10.1093/genetics/105.3.489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Kuzminov A. Collapse and repair of replication forks in Escherichia coli. Mol Microbiol. 1995 May;16(3):373–384. doi: 10.1111/j.1365-2958.1995.tb02403.x. [DOI] [PubMed] [Google Scholar]
  34. Maenhaut-Michel G., Shapiro J. A. The roles of starvation and selective substrates in the emergence of araB-lacZ fusion clones. EMBO J. 1994 Nov 1;13(21):5229–5239. doi: 10.1002/j.1460-2075.1994.tb06854.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Mao E. F., Lane L., Lee J., Miller J. H. Proliferation of mutators in A cell population. J Bacteriol. 1997 Jan;179(2):417–422. doi: 10.1128/jb.179.2.417-422.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Mittler J. E., Lenski R. E. Experimental evidence for an alternative to directed mutation in the bgl operon. Nature. 1992 Apr 2;356(6368):446–448. doi: 10.1038/356446a0. [DOI] [PubMed] [Google Scholar]
  37. Mittler J. E., Lenski R. E. New data on excisions of Mu from E. coli MCS2 cast doubt on directed mutation hypothesis. Nature. 1990 Mar 8;344(6262):173–175. doi: 10.1038/344173a0. [DOI] [PubMed] [Google Scholar]
  38. Modrich P., Lahue R. Mismatch repair in replication fidelity, genetic recombination, and cancer biology. Annu Rev Biochem. 1996;65:101–133. doi: 10.1146/annurev.bi.65.070196.000533. [DOI] [PubMed] [Google Scholar]
  39. Ninio J. Transient mutators: a semiquantitative analysis of the influence of translation and transcription errors on mutation rates. Genetics. 1991 Nov;129(3):957–962. doi: 10.1093/genetics/129.3.957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Radicella J. P., Park P. U., Fox M. S. Adaptive mutation in Escherichia coli: a role for conjugation. Science. 1995 Apr 21;268(5209):418–420. doi: 10.1126/science.7716545. [DOI] [PubMed] [Google Scholar]
  41. Rangarajan S., Gudmundsson G., Qiu Z., Foster P. L., Goodman M. F. Escherichia coli DNA polymerase II catalyzes chromosomal and episomal DNA synthesis in vivo. Proc Natl Acad Sci U S A. 1997 Feb 4;94(3):946–951. doi: 10.1073/pnas.94.3.946. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Reddy M., Gowrishankar J. A genetic strategy to demonstrate the occurrence of spontaneous mutations in nondividing cells within colonies of Escherichia coli. Genetics. 1997 Nov;147(3):991–1001. doi: 10.1093/genetics/147.3.991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Richards B., Zhang H., Phear G., Meuth M. Conditional mutator phenotypes in hMSH2-deficient tumor cell lines. Science. 1997 Sep 5;277(5331):1523–1526. doi: 10.1126/science.277.5331.1523. [DOI] [PubMed] [Google Scholar]
  44. Sniegowski P. D. A test of the directed mutation hypothesis in Escherichia coli MCS2 using replica plating. J Bacteriol. 1995 Feb;177(4):1119–1120. doi: 10.1128/jb.177.4.1119-1120.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Stahl F. W. Bacterial genetics. A unicorn in the garden. Nature. 1988 Sep 8;335(6186):112–113. doi: 10.1038/335112a0. [DOI] [PubMed] [Google Scholar]
  46. Strathern J. N., Shafer B. K., McGill C. B. DNA synthesis errors associated with double-strand-break repair. Genetics. 1995 Jul;140(3):965–972. doi: 10.1093/genetics/140.3.965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Taddei F., Matic I., Radman M. cAMP-dependent SOS induction and mutagenesis in resting bacterial populations. Proc Natl Acad Sci U S A. 1995 Dec 5;92(25):11736–11740. doi: 10.1073/pnas.92.25.11736. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Torkelson J., Harris R. S., Lombardo M. J., Nagendran J., Thulin C., Rosenberg S. M. Genome-wide hypermutation in a subpopulation of stationary-phase cells underlies recombination-dependent adaptive mutation. EMBO J. 1997 Jun 2;16(11):3303–3311. doi: 10.1093/emboj/16.11.3303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. West S. C. The RuvABC proteins and Holliday junction processing in Escherichia coli. J Bacteriol. 1996 Mar;178(5):1237–1241. doi: 10.1128/jb.178.5.1237-1241.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Whitby M. C., Ryder L., Lloyd R. G. 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):341–350. doi: 10.1016/0092-8674(93)80075-p. [DOI] [PubMed] [Google Scholar]
  51. Zahrt T. C., Maloy S. Barriers to recombination between closely related bacteria: MutS and RecBCD inhibit recombination between Salmonella typhimurium and Salmonella typhi. Proc Natl Acad Sci U S A. 1997 Sep 2;94(18):9786–9791. doi: 10.1073/pnas.94.18.9786. [DOI] [PMC free article] [PubMed] [Google Scholar]

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