Global Chromosomal Structural Instability in a Subpopulation of Starving Cells

English version České info

Copy-number variations (CNVs) constitute very common differences between individual humans and possibly all genomes and may therefore be important fuel for evolution, yet how they form remains elusive. In starving Escherichia coli, gene amplification is induced by stress, controlled by the general stress response. Amplification has been detected only encompassing genes that confer a growth advantage when amplified. We studied the structure of stress-induced gene amplification in starving cells in the Lac assay in Escherichia coli by array comparative genomic hybridization (aCGH), with polymerase chain reaction (pcr) and DNA sequencing to establish the structures generated. About 10% of 300 amplified isolates carried other chromosomal structural change in addition to amplification. Most of these were inversions and duplications associated with the amplification event. This complexity supports a mechanism similar to that seen in human non-recurrent copy number variants. We interpret these complex events in terms of repeated template switching during DNA replication. Importantly, we found a significant occurrence (6 out of 300) of chromosomal structural changes that were apparently not involved in the amplification event. These secondary changes were absent from 240 samples derived from starved cells not carrying amplification, suggesting that amplification happens in a differentiated subpopulation of stressed cells licensed for global chromosomal structural change and genomic instability. These data imply that chromosomal structural changes occur in bursts or showers of instability that may have the potential to drive rapid evolution.

Vyšlo v časopise: Global Chromosomal Structural Instability in a Subpopulation of Starving Cells. PLoS Genet 7(8): e32767. doi:10.1371/journal.pgen.1002223
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002223

Souhrn

Zdroje

1. ZhangFGuWHurlesMELupskiJR 2009 Copy number variation in human health, disease, and evolution. Annu Rev Genomics Hum Genet 10 451 481

2. StankiewiczPLupskiJ 2010 Structural variation in the human genome and its role in didease. Annu Rev Med 61 437 455

3. LuXYPhungMTShawCAPhamKNeilSE 2008 Genomic imbalances in neonates with birth defects: high detection rates by using chromosomal microarray analysis. Pediatrics 122 1310 1318

4. RubinCJZodyMCErikssonJMeadowsJRSherwoodE 2010 Whole-genome resequencing reveals loci under selection during chicken domestication. Nature 464 587 591

5. ZhangFCarvalhoCMLupskiJR 2009 Complex human chromosomal and genomic rearrangements. Trends Genet 25 298 307

6. HastingsPJIraGLupskiJR 2009 A Microhomology-mediated Break-Induced Replication Model for the origin of human copy number variation. PLoS Genet 5 e1000327

7. HastingsPJLupskiJRRosenbergSMIraG 2009 Mechanisms of change in gene copy number. Nat Rev Genet 10 551 564

8. KugelbergEKofoidEAnderssonDILuYMellorJ 2010 The tandem inversion-duplications in Salmonella enterica (TID): Selection drives unstable precursors to complete mutation types. Genetics 185 65 80

9. KugelbergEKofoidEReamsABAnderssonDIRothJR 2006 Multiple pathways of selected gene amplification during adaptive mutation. Proc Natl Acad Sci U S A 103 17319 17324

10. SlackAThorntonPCMagnerDBRosenbergSMHastingsPJ 2006 On the mechanism of gene amplification induced under stress in Escherichia coli. PLoS Genetics 2 e48

11. HastingsPJSlackAPetrosinoJFRosenbergSM 2004 Adaptive amplification and point mutation are independent mechanisms: Evidence for various stress-inducible mutation mechanisms. PLoS Biol 2 e399

12. LydeardJRJainSYamaguchiMHaberJE 2007 Break-induced replication and telomerase-independent telomere maintenance require Pol32. Nature 448 820 823

13. PayenCKoszulRDujonBFischerG 2008 Segmental duplications arise from Pol32-dependent repair of broken forks through two alternative replication-based mechanisms. PLoS Genet 4 e1000175

14. PonderRGFonvilleNCRosenbergSM 2005 A switch from high-fidelity to error-prone DNA double-strand break repair underlies stress-induced mutation. Mol Cell 19 791 804

15. SmithCELlorenteBSymingtonLS 2007 Template switching during break-induced replication. Nature 447 102 105

16. CairnsJFosterPL 1991 Adaptive reversion of a frameshift mutation in Escherichia coli. Genetics 128 695 701

17. HastingsPJBullHJKlumpJRRosenbergSM 2000 Adaptive amplification: an inducible chromosomal instability mechanism. Cell 103 723 731

18. GodoyVGGizatullinFSFoxMS 2000 Some features of the mutability of bacteria during nonlethal selection. Genetics 154 49 59

19. TorkelsonJHarrisRSLombardoM-JNagendranJThulinC 1997 Genome-wide hypermutation in a subpopulation of stationary-phase cells underlies recombination-dependent adaptive mutation. EMBO J 16 3303 3311

20. RoscheWAFosterPL 1999 The role of transient hypermutators in adaptive mutation in Escherichia coli. Proc Natl Acad Sci U S A 96 6862 6867

21. GalhardoRSHastingsPJRosenbergSM 2007 Mutation as a stress response and the regulation of evolvability. Crit Rev Biochem Mol Biol 42 399 435

22. GonzalezCHadanyLPonderRGPriceMHastingsPJ 2008 Mutability and importance of a hypermutable cell subpopulation that produces stress-induced mutants in Escherichia coli. PLoS Genet 4 e1000208

23. LupskiJRWeinstockGM 1992 Short, interspersed repetitive DNA sequences in prokaryotic genomes. J Bacteriol 174 4525 4529

24. PetoRPikeMCArmitagePBreslowNECoxDR 1977 Design and analysis of randomized clinical trials requiring prolonged observation of each patient. II. analysis and examples. Br J Cancer 35 1 39

25. LeeJACarvalhoCMLupskiJR 2007 A DNA replication mechanism for generating nonrecurrent rearrangements associated with genomic disorders. Cell 131 1235 1247

26. FisherRA 1922 On the interpretation of χ2 from contingency tables, and the calculation of P. Journal of the Royal Statistical Society 85 87 94

27. FisherRA 1954 Statistical Methods for Research Workers Edinburgh Oliver and Boyd

28. LaytonJCFosterPL 2003 Error-prone DNA polymerase IV is controlled by the stress-response sigma factor, RpoS, in Escherichia coli. Mol Microbiol 50 549 561

29. LombardoM-JAponyiIRosenbergSM 2004 General stress response regulator RpoS in adaptive mutation and amplification in Escherichia coli. Genetics 166 669 680

30. GibsonJLLombardoM-JThorntonPCHuKGalhardoRS 2010 The σE stress response is required for stress-induced mutagenesis in Escherichia coli. Mol Micro 77 415 430

31. DongTKirchhofMGSchellhornHE 2008 RpoS regulation of gene expression during exponential growth of Escherichia coli K12. Mol Genet Genomics 279 267 277

32. AlbertiniAMHoferMCalosMPMillerJH 1982 On the formation of spontaneous deletions: the importance of short sequence homologies in the generation of large deletions. Cell 29 319 328

33. FarabaughPJSchmeissnerUHoferMMillerJH 1978 Genetic studies of the lac repressor. VII. On the molecular nature of spontaneous hotspots in the lacI gene of Escherichia coli. J Mol Biol 126 847 857

34. BachellierSGilsonEHofnungMHillCW 1996 Repeated sequences. CurtissRIIIIngrahamJLLinECCLowKBMagasanikB Escherichia coli and Salmonella Cellular and Molecular Biology. 2nd ed Washington, D.C. ASM Press 2012 2040

35. LovettSTHurleyRLSuteraVAJrAubuchonRHLebedevaMA 2002 Crossing over between regions of limited homology in Escherichia coli. RecA-dependent and RecA-independent pathways. Genetics 160 851 859

36. ShenPHuangHV 1986 Homologous recombination in Escherichia coli: dependence on substrate length and homology. Genetics 112 441 457

37. BacollaAWojciechowskaMKosmiderBLarsonJEWellsRD 2006 The involvement of non-B DNA structures in gross chromosomal rearrangements. DNA Repair (Amst) 5 1161 1170

38. VoineaguINarayananVLobachevKSMirkinSM 2008 Replication stalling at unstable inverted repeats: interplay between DNA hairpins and fork stabilizing proteins. Proc Natl Acad Sci U S A 105 9936 9941

39. McKenzieGJHarrisRSLeePLRosenbergSM 2000 The SOS response regulates adaptive mutation. Proc Natl Acad Sci U S A 97 6646 6651

40. HarrisRSRossKJRosenbergSM 1996 Opposing roles of the Holliday junction processing systems of Escherichia coli in recombination-dependent adaptive mutation. Genetics 142 681 691

41. KofoidEBergthorssonUSlechtaESRothJR 2003 Formation of an F′ plasmid by recombination between imperfectly repeated chromosomal Rep sequences: a closer look at an old friend (F′(128) pro lac). J Bacteriol 185 660 663