Evolving responsively: Adaptive mutation

Nature Reviews Genetics

Volumn 2, Issue 7, 2001, Pages 504-515

  Rosenberg, Susan M ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; ANIMAL; BIOLOGICAL MODEL; ESCHERICHIA COLI; GENETIC RECOMBINATION; GENETIC SELECTION; GENETICS; HUMAN; MOLECULAR EVOLUTION; MUTATION; PHYSIOLOGY; REVIEW; SACCHAROMYCES CEREVISIAE; STATISTICAL MODEL;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ESCHERICHIA COLI; EVOLUTION, MOLECULAR; HUMANS; MODELS, GENETIC; MODELS, STATISTICAL; MUTATION; RECOMBINATION, GENETIC; SACCHAROMYCES CEREVISIAE; SELECTION (GENETICS);

EID: 0035404535     PISSN: 14710056     EISSN: None     Source Type: Journal    
DOI: 10.1038/35080556     Document Type: Review

References (129)

1. Adams, D. The Hitch-hiker's Guide to the Galaxy: The Original Radio Scripts (Pan Books, Ltd, London, 1985).
2. Mayr, E. The Growth of Biological Thought, Diversity, Evolution, and Inheritance (Belknap, Cambridge. Massachusetts, 1982).
3. Luria, S. E. & Delbrück, M. Mutations of bacteria from virus sensitivity to virus resistance. Genetics 28, 491-511 (1943).
4. Newcombe, H. B. Origin of bacterial variants. Nature 164, 150-151 (1949).
5. Lederberg, J. & Lederberg, E. M. Replica plating and indirect selection of bacterial mutants. J. Bacteriol. 63, 399-406 (1952).
6. Shapiro, J. A. Observations on the formation of clones containing araB-lacZ fusions. Mol. Gen. Genet. 194, 79-90 (1984).
7. Cairns, J., Overbaugh, J. & Miller, S. The origin of mutants. Nature 335, 142-145 (1988).
8. Novick, A. & Szilard, L. Experiments on spontaneous and chemically induced mutations of bacteria growing in the chemostat. Cold Spring Harbor Symp. Quant. Biol. 16, 337-343 (1951).
9. Ryan, F. J. Distribution of numbers of mutant bacteria in replicate cultures. Nature 169, 882-883 (1952).
10. Ryan, F. Spontaneous mutations in non-dividing bacteria. Genetics 40, 726-738 (1955).
11. Prival, M. J. & Cebula, T. A. Adaptive mutation and slow-growing revertants of an Escherichia coli lacZ amber mutant. Genetics 144, 1337-1341 (1996).
12. Cairns, J. & Foster, P. L. Adaptive reversion of a frameshift mutation in Escherichia coli. Genetics 128, 695-701 (1991).
13. Hastings, P. J., Bull, H. J., Klump, J. R. & Rosenberg, S. M. Adaptive amplification: an inducible chromosomal instability mechanism. Cell 103, 723-731 (2000).
14. Hall, B. G. Adaptive evolution that requires multiple spontaneous mutations. I. Mutations involving an insertion sequence. Genetics 120, 887-897 (1988).
15. Hall, B. G. Spontaneous point mutations that occur more often when advantageous than when neutral. Genetics 126, 5-16 (1990).
16. Boe, L. & Marinus, M. G. Role of plasmid multimers in mutation to tetracycline resistance. Mol. Microbiol. 5, 2541-2545 (1991).
17. Prival, M. J. & Cebula, T. A. Sequence analysis of mutations arising during prolonged starvation of Salmonella typhimurium. Genetics 132, 303-310 (1992).
18. Jayaraman, R. Cairnsian mutagenesis in Escherichia coli: genetic evidence for two pathways regulated by mutS and mutl. genes. J. Genet. 71, 23-41 (1992).
19. Bridges, B. Spontaneous mutation in stationary-phase Escherichia coli WP2 carrying various DNA repair alleles. Mutat. Res. 302, 173-176 (1993).
20. Maenhaut-Michel, G., Blake, C. E., Leach, D. R. & Shapiro, J. A. Different structures of selected and unselected araB-lacZ fusions. Mol. Microbiol. 23. 133-145 (1997).
21. Galitski, T. & Roth, J. R. A search for a general phenomenon of adaptive mutability. Genetics 143, 645-659 (1996).
22. Kasak, L., Horak, R. & Kivisaar, M. Promoter-creating mutations in Pseudomonas putida: a model system for the study of mutation in starving bacteria. Proc. Natl Acad. Sci. USA 94, 3134-3139 (1997).
23. Hall, B. G. Adaptive mutagenesis at ebgR is regulated by PhoPQ. J. Bacteriol. 180, 2862-2865 (1998).
24. Massey, R. C., Rainey, P. B., Sheehan, B. J., Keane, O. M. & Dorman, C. J. Environmentally constrained mutation and adaptive evolution in Salmonella. Curr. Biol. 9, 1477-1480 (1999).
25. Wright, B. E., Longacre, A. & Reimers, J. M. Hypermutation in derepressed operons of Escherichia coli K12. Proc. Natl Acad. Sci. USA 96, 5089-5094 (1999).
26. Steele, D. F. & Jinks-Robertson, S. An examination of adaptive reversion in Saccharomyces cerevisiae. Genetics 132, 9-21 (1992).
27. Greene, C. N. & Jinks-Robertson, S. Comparison of spontaneous and adaptive mutation spectra in yeast. J. Genet. 78, 51-55 (1999).
28. Hall, B. G. Selection-induced mutations occur in yeast. Proc. Natl Acad. Sci. USA 89, 4300-4303 (1992).
29. Baranowska, H., Policinska, Z. & Jachymczyk, W. J. Effects of the CDC2 gene on adaptive mutation in the yeast Saccharomyces cerevisiae. Curr. Genet. 28, 521-525 (1995).
30. Heidenreich, E. & Wintersberger, U. Starvation for a specific amino acid induces high frequencies of rhomutants in Saccharomyces cerevisiae. Curr. Genet. 31, 408-413 (1997).
31. Heidenreich, E. & Wintersberger, U. Replication-dependent and selection-induced mutations in respiration-competent and respiration-deficient strains of Saccharomyces cerevisiae. Mol. Gen. Genet. 260, 395-400 (1998).
32. Heidenreich, E. & Wintersberger, U. Adaptive reversion of a frameshift mutation in arrested Saccharomyces cerevisiae cells by simple deletions in mononucleotide repeats. Mutat. Res. 473, 101-107 (2001).
33. Taddei, F., Halliday, J. A., Matic, I. & Radman, M. Genetic analysis of mutagenesis in aging Escherichia coli colonies. Mol. Gen. Genet. 256, 277-281 (1997).
34. Lamrani, S. et al. Starvation-induced Mucts62-mediated coding sequence fusion: a role for CIpXP, Lon, RpoS and Crp. Mol. Microbiol. 32, 327-343 (1999).
35. Friedberg, E. C., Feaver, W. J. & Gertach, V. L. The many faces of DNA polymerases: strategies for mutagenesis and for mutational avoidance. Proc. Natl Acad. Sci. USA 97, 5681-5683 (2000).
36. McKenzie, G. J., Lombardo, M.-J. & Rosenberg, S. M. Recombination-dependent mutation in Escherichia coli occurs in stationary phase. Genetics 149, 1563-1565 (1998).
37. Rosenberg, S. M., Longerich, S., Gee, P. & Harris, R. S. Adaptive mutation by deletions in small mononucleotide repeats. Science 265, 405-407 (1994).
38. Foster, P. L. & Trimarchi, J. M. Adaptive reversion of a frameshift mutation in Escherichia coli by simple base deletions in homopolymeric runs. Science 265, 407-409 (1994).
39. Harris, R. S., Longerich, S. & Rosenberg, S. M. Recombination in adaptive mutation. Science 264, 258-260 (1994).
40. 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 142, 25-37 (1996).
41. 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 142, 681-691 (1996).
42. Kowalczykowski, S. C. Initiation of genetic recombination and recombination-dependent replication. Trends Biochem. Sci. 25, 156-165 (2000).
43. Mosig, G. The essential role of recombination in phage T4 growth. Annu. Rev. Genet. 21, 347-371 (1987).
44. Skalka, A. in Mechanisms in Recombination (ed. Grell, R. R.) 421-432 (Plenum. New York, 1974).
45. Kogoma, T. Stable DNA replication: interplay between DNA replication, homologous recombination, and transcription. Microbiol. Mol. Biol. Rev. 61, 212-238 (1997).
46. Radding, C. M. (ed.) National Academy of Sciences Colloquium: Links Between Recombination and Replication (Proc. Natl Acad. Sci. USA, 2001, in the press).
47. Kuzminov, A. Collapse and repair of replication forks in Escherichia coli. Mol. Microbiol. 16, 373-384 (1995).
48. Rosenberg, S. M., Harris, R. S., Longerich, S. & Galloway, A. M. Recombination-dependent mutation in non-dividing cells. Mutat. Res. 350, 69-76 (1996).
49. Andersson, D. I., Slechta, E. S. & Roth, J. R. Evidence that gene amplification underlies adaptive mutability of the bacterial lac operon. Science 282, 1133-1135 (1998).
50. Motamedi, M., Szigety, S. K. & Rosenberg, S. M. Double-strand-break repair in Escherichia coli: physical evidence for a DNA replication mechanism in vivo. Genes Dev. 13, 2889-2903 (1999).
51. Holbeck, S. L. & Strathern, J. N. A role for REV3 in mutagenesis during double-strand break repair in Saccharomyces cerevisiae. Genetics 147, 1017-1024 (1997).
52. Ripley, L. S. Frameshift mutation: determinants of specificity. Annu. Rev. Genet 24, 189-213 (1990).
53. 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. USA 92, 7951-7955 (1995).
54. Harris, R. S., Bull, H. J. & Rosenberg, S. M. A direct role for DMA polymerase III in adaptive reversion of a frameshift mutation in Escherichia coli. Mutat. Res. 375, 19-24 (1997).
55. Modrich, P. & Lahue, R. Mismatch repair in replication fidelity, genetic recombination, and cancer. Annu. Rev. Biochem. 65, 101-133 (1996).
56. Fishel, R. Signaling mismatch repair in cancer. Nature Med. 11, 1239-1241 (1999).
57. Longerich, S., Galloway, A. M., Harris, R. S., Wong, C. & Rosenberg, S. M. Adaptive mutation sequences reproduced by mismatch repair deficiency. Proc. Natl Acad. Sci. USA 92, 12017-12020 (1995).
58. Torkelson, J. et al. Genome-wide hypermutation in a subpopulation of stationary-phase cells underlies recombination-dependent adaptive mutation. EMBO J. 16, 3303-3311 (1997).
59. Rosche, W. A. & Foster, P. L. The role of transient hypermutators in adaptive mutation in Escherichia coli. Proc. Natl Acad. Sci. USA 96, 6862-6867 (1999).
60. Harris, R. S. et al. Mismatch repair protein MutL becomes limiting during stationary-phase mutation. Genes Dev. 11, 2426-2437 (1997).
61. Foster, P. L. Are adaptive mutations due to a decline in mismatch repair? The evidence is lacking. Mutat. Res. 436, 179-184 (1999).
62. Harris, R. S. et al. Mismatch repair is diminished during stationary-phase mutation. Mutat. Res. 437, 51-60 (1999).
63. Zhao, J. & Winkler, M. E. Reduction of GC-→TA transversion mutation by overexpression of MutS in Escherichia coli K-12. J. Bacteriol. 182, 5025-5028 (2000).
64. Brègeon, D., Matic, I., Radman, M. & Taddei, F. Mismatch repair: genetic defects and down regulation. J. Genet 78, 21-28 (1999).
65. McKenzie, G. J., Lee, P. L., Lombardo, M.-J., Hastings, P. J. & Rosenberg, S. M. SOS mutator DNA polymerase IV functions in adaptive mutation and not adaptive amplification. Mol. Cell 7, 571-579 (2001).
66. Sutton, M. D., Smith, B. T., Godoy, V. G. & Walker, G. C. The SOS response: recent insights into UmuDC-dependent mutagenesis and DNA damage tolerance. Annu. Rev. Genet. 34, 479-497 (2000).
67. McKenzie, G. J., Harris, R. S., Lee, P. L. & Rosenberg, S. M. The SOS response regulates adaptive mutation. Proc. Natl Acad. Sci. USA 97, 6646-6651 (2000).
68. Strauss, B. S., Roberts, R., Francis, L. & Pouryazdanparast, P. Role of the dinB gene product in spontaneous mutation in Escherichia coli with an impaired replicative polymerase. J. Bacteriol. 182, 6742-6750 (2000).
69. Napolitano, R., Janel-Bintz, R., Wagner, J. & Fuchs, R. P. P. All three SOS-inducible DNA polymerases (pol II, pol IV, and pol V) are involved in induced mutagenesis. EMBO J. 19, 6259-6265 (2000).
70. Wagner, J. et al. The dinB gene encodes a novel E. coli DNA polymerase, DNA pol IV, involved in mutagenesis. Mol. Cell 4, 281-286 (1999).
71. Kim, S.-Y, et al. Multiple pathways for SOS-induced mutagenesis in Escherichia coli: an SOS gene product (DinB/P) enhances frameshift mutations in the absence of any exogenous agents that damage DNA Proc. Natl Acad. Sci. USA 94, 13792-13797 (1997).
72. Wagner, J. & Nohmi, T. Escherichia coli DNA polymerase IV mutator activity: genetic requirements and mutational specificity. J. Bacteriol. 182, 4537-4595 (2000).
73. Radman, M. SOS repair hypothesis: phenomenology of an inducible DNA repair which is accompanied by mutagenesis. Basic Life Sci. 5A, 355-367 (1975).
74. Echols, H. SOS functions, cancer and inducible evolution. Cell 25, 1-2 (1981).
75. Schaaper, R. M. & Radman, M. The extreme mutator effect of Escherichia coli mutD5 results from saturation of mismatch repair by excessive DNA replication errors. EMBO J. 8, 3511-3516 (1989).
76. Foster, P. L. Nonadaptive mutations occur in the F' episome during adaptive mutation conditions in Escherichia coli. J. Bacteriol. 179, 1550-1554 (1997).
77. Godoy, V. G., Gizatullin, F. S. & Fox, M. S. Some features of the mutability of bacteria during nonlethal selection. Genetics 154, 49-59 (2000).
78. Rosenberg, S. M., Thulin, C. & Harris, R. S. Transient and heritable mutators in adaptive evolution in the lab and in nature. Genetics 148, 1559-1566 (1998).
79. Bull, H. J., McKenzie, G. J., Hastings, P. J. & Rosenberg, S. M. Evidence that stationary-phase hypermutation in the E. coli chromosome is promoted by recombination. Genetics 154, 1427-1437 (2000).
80. Bull, H. J., McKenzie, G. J., Hastings, P. J. & Rosenberg, S. M. The contribution of transiently hypermutable cells to mutation in stationary phase. Genetics 156, 925-926 (2000).
81. Bull, H. J., Lombardo, M.-J. & Rosenberg, S. M. Stationary-phase mutation in the bacterial chromosome: recombination protein and DNA polymerase IV dependence. Proc. Natl Acad. Sci. USA (2001, in the press).
82. Cairns, J. The contribution of transiently hypermutable cells to mutation in stationary phase. Genetics 156, 923-926 (2000).
83. Rosenberg, S. M. Mutation for survival. Curr. Opin. Genet. Dev. 7, 829-834 (1997).
84. Foster, R. 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. USA 92, 5487-5490 (1995).
85. Radicella, J. P., Park, P. U. & Fox, M. S. Adaptive mutation in Escherichia coli: a role for conjugation. Science 268, 418-420 (1995).
86. Galitski, T. & Roth, J. R. Evidence that F' transfer replication underlies apparent adaptive mutation. Science 268, 421-423 (1995).
87. Foster, P. L. & Trimarchi, J. M. Conjugation is not required for adaptive reversion of an episomal frameshift mutation in Escherichia coli. J. Bacteriol. 177, 6670-6671 (1995).
88. Rosenberg, S. M., Harris, R. S. & Torkelson, J. Molecular handles on adaptive mutation. Mol. Microbiol. 18, 185-189 (1995).
89. Lombardo, M.-J., Torkelson, J., Bull, H. J., McKenzie, G. J. & Rosenberg, S. M. Mechanisms of genome-wide hypermutation in stationary phase. Ann. NYAcad. Sci. 870, 275-289 (1999).
90. Yamnolinsky, M. B. Programmed cell death in bacterial populations. Science 267, 836-837 (1995).
91. Firth, N., Ippen-lhler, K. & Skurray, R. H. in Escherichia coli and Salmonella: Cellular and Molecular Biology (eds Neidhardt, F. C. et al.) 2377-2401 (ASM, Washington, DC, 1996).
92. Whoriskey, S. K., Nghiem, V.-H., Leong, R-M., Masson, J.-M. & Miller, J. H. Genetic rearrangement and gene amplification in Escherichia coli: DNA sequences at the junctures of amplified gene fusions. Genes Dev. 1, 227-237 (1987).
93. Tisty, T. D., Margolin, B. H. & Lum, K. Differences in the rates of gene amplification in nontumorigenic and tumorigenic cell lines as measured by Luria-Delbrück fluctuation analysis. Proc. NatlAcad. Sci. USA 86, 9441-9445 (1989).
94. Pipiras, E., Coquelle, A., Bieth, A. & Debatisse, M. Interstitial deletions and intrachromosomal amplification initiated from a double-strand break targeted to a mammalian chromosome. EMBO J. 17, 325-333 (1998).
95. Ono, S. Evolution by Gene Duplication (Springer, Berlin and New York, 1970).
96. Jasin, M. in DNA Damage and Repair. 3. Advances from Phage to Humans (eds Nickoloff, J. A. & Hoekstra, M. F.) 207-235 (Humana, Inc.,Totowa, New Jersey, 1998).
97. Brodeur, G. M. & Hogarty, M. D. in The Genetic Basis of Human Cancer (eds Vogelstein, B. & Kinzler, K. W.) 161-172 (McGraw-Hill, New York, 1998).
98. Coquelle, A., Pipiras, E., Toledo, F., Buttin, G. & Debatisse, M. Expression of fragile sites triggers intrachromosomal mammalian gene amplification and sets boundaries to early amplicons. Cell 89, 215-225 (1997).
99. Deitsch, K. W., Moxon, E. R. & Wellems, T. E. Shared themes of antigenic variation and virulence in bacterial, protozoal, and fungal infections. Microbiol. Mol. Biol. Rev. 61, 281-293 (1997).
100. Saunders, N. J. et al. Repeat-associated phase variable genes in the complete genome sequence of Neisseria meningitidis strain MC58. Mol. Microbiol. 37, 207-215 (2000).
101. Martinez, J. L. & Baquero, F. Mutation frequencies and antibiotic resistance. Antimicrob. Agents Chemother. 44, 1771-1777 (2000).
102. Zambrano, M. M. & Kolter, R. GASPing for life in stationary phase. Cell 86, 181-184 (1996).
103. LeClerc, J. E., Li, B., Payne, W. L. & Cebula, T. A. High mutation frequencies among Escherichia coli and Salmonella pathogens. Science 274, 1208-1211 (1996).
104. Denamur, E. et al. Evolutionary implications of the frequent horizontal transfer of mismatch repair genes. Cell 103, 711-721 (2000).
105. Cashel, M., Gentry, D. R., Hernandez, V. J. & Vinella, D. in Escherichia coli and Salmonella: Cellular and Molecular Biology (eds Neidhardt, F. C. et al.) 1458-1496 (ASM, Washington, DC, 1996).
106. Datta, A. & Jinks-Robertson, S. Association of increased spontaneous mutation rates with high levels of transcription in yeast. Science 268, 1616-1619 (1995).
107. Davis, B. D. Transcriptional bias: a non-Lamarckian mechanism for substrate-induced mutations. Proc. Natl Acad. Sci. USA 86, 5005-5009 (1989).
108. Strauss, B. S. The origin of point mutations in human tumor cells. Cancer Res. 52, 249-253 (1992).
109. Hall, B. G. Adaptive mutations in Escherichia coli as a model for the multiple mutational origins of cancer. Proc. Natl Acad. Sci. USA 92, 5669-5673 (1995).
110. Finch, C. E. & Goodman, M. F. Relevance of 'adaptive' mutations arising in non-dividing cells of microorganisms to age-related changes in mutant phenotypes of neurons. Trends Neurosci. 20, 501-507 (1997).
111. Drake, J. W. Spontaneous mutation. Annu. Rev. Genet. 25, 125-146 (1991).
112. Walter, C. A., Intano, G. W., McCarrey, J. R., McMahan, C. A. & Walter, R. B. Mutation frequency declines in spermatogenesis in young mice but increases in old mice. Proc. Natl Acad. Sci. USA 95, 10015-10019 (1998).
113. Swanson, W. J., Yang, Z., Wolfner, M. F. & Aquadro, C. F. Positive Darwinian selection drives the evolution of several female reproductive proteins in mammals. Proc. Natl Acad. Sci. USA 98, 2509-2514 (2001).
114. Harris, R. S., Kong, Q. & Maizels, N. Somatic hypermutation and the three R's: repair, replication and recombination. Mutat Res. 436, 157-178 (1999).
115. Jacobs, H., Rajewsky, K., Fukita, Y. & Bross, L. Indirect and direct evidence for DNA double-strand breaks in hypermutating immunoglobulin genes. Phil. Trans. R. Soc. Lond. B 356, 119-125 (2001).
116. McDonald, J. P. et al. DNA polymerase iota and related Rad30-like enzymes. Phil. Trans. R. Soc. Lond. B 356, 53-60 (2001).
117. True, H. L & Lindquist, S. L. A yeast prion provides a mechanism for genetic variation and phenotypic diversity. Nature 407, 477-483 (2000).
118. Delbrück, M. Cold Spring Harbor Symp. Quant. Biol. 11, 154 (1946).
119. Stewart, F. M., Gordon, D. M. & Levin, B. R. Fluctuation analysis: the probability distribution of the number of mutants under different conditions. Genetics 124 (1990).
120. Higgins, N. P., Kato, K. & Strauss, B. J. A model for replication repair in mammalian cells Mol. Biol. 101, 417-125 (1976).
121. Louarn, J.-M., Louam, J., Francois, V. & Patte, J. Analysis and possible role of hyperrecombination in the terminus region of the Escherichia coli chromosome. J. Bacteriol. 173, 5096-5104 (1991).
122. Seigneur, M., Bidnenko, V., Ehrlich, S. D. & Michel, B. RuvAB acts at arrested replication forks. Cell 95, 419-430 (1998).
123. Powell, S. C. & Wartell, R. M. Different characteristics distinguish early versus late arising adaptive mutations in Escherichia coli FC40. Mutat. Res. 473, 219-228 (2001).
124. Akerlund, T., Nordstrom, K. & Bernander, R. Analysis of cell size and DNA content in exponentially growing and stationary-phase batch cultures of Escherichia coli. J. Bacteriol. 177, 6791-6797 (1995).
125. Anderson, R. P. & Roth, J. R. Spontaneous tandem duplications in Salmonella typhimurium arise by unequal recombination between rRNA (rrn) cistrons. Proc. Natl Acad. Sci. USA 78, 3113-3117 (1981).
126. Zan, H. et al. The translesion DNA polymerase zeta plays a major role in lg and bcl-6 somatic hypermutation. Immunity 14, 643-653 (2001).
127. Rogozin, I. B., Pavlov, Y. I., Bebenek, K., Matsuda, T. & Kunkel, T. A. Somatic mutation hotspots correlate with DNA polymerase eta error spectrum. Nature Immunol. 2, 530-536 (2001).
128. Zeng, X. et al. DNA polymerase eta is an A-T mutator in somatic hypermutation of immunoglobulin variable genes. Nature Immunol. 2, 537-541 (2001).
129. Chicurel, M. Can organisms speed their own evolution? Science 292, 1824-1827 (2001).