Ecological geneticsEcological geneticsЭкологическая генетика1811-09322411-9202Eco-Vector552810.17816/ecogen4320-28ArticlesСтатьиResearch ArticleADAPTIVE MUTAGENESIS IN THE YEAST SACCHAROMYCES CEREVISIAEАДАПТИВНЫЙ МУТАГЕНЕЗ У ДРОЖЖЕЙ SACCHAROMYCES CEREVISIAEBabudriNoraБабудриНораbabudri@upihg.itLucaccioniAngelaЛукачионниАнджелаAchilliAlessandroАчиллиАлессандроachilli@unipg.itUniversity of Perugia, Perugia, ItalyУниверситет Перуджи, Перуджи, ИталияUniversity of Pavia, Pavia, ItalyУниверситет Павии, Павия, Италия1509200643VOL 4, NO3 (2006)ТОМ 4, №3 (2006)202814112016Copyright ©; 2006, Babudri N., Lucaccioni A., Achilli A.Copyright ©; 2006, Бабудри Н., Лукачионни А., Ачилли А.2006Babudri N., Lucaccioni A., Achilli A.Бабудри Н., Лукачионни А., Ачилли А.http://creativecommons.org/licenses/by/4.0https://journals.eco-vector.com/ecolgenet/article/view/5528

The nature of mutation in microorganisms has been debated for a long time. Two theories have been at odds: random spontaneous mutagenesis vs. adaptive mutagenesis. "random mutagenesis" means that mutations occur in proliferating cells before they encountered the selective agent. "adaptive mutagenesis" means that advantageous mutations form in the environment where they have been selected, in non-replicating or poorly replicating cells even though other, non-selected, mutations occur at the same time. In the last 20 years it has been definitely shown that random as well as adaptive mutagenesis occur in bacteria and yeast. microorganisms in nature do not divide or divide poorly because of adverse environmental conditions; therefore adaptive mutations could provide cells with a selective advantage and allow evolution of populations. Here we will focus on some fundamental aspects of adaptive mutagenesis in the yeast Saccharomyces cerevisiae. We begin with a historical overview on the nature of mutation. We then focus on experimental systems aimed at proving or disproving adaptive mutagenesis. We have briefly summarized the results obtained in this field, with particular attention to genetic and molecular mechanisms.

Природа мутаций у микроорганизмов остается дискуссионной темой в течение длительного времени.  Обсуждается две теории: теория о случайной природе  спонтанного мутагенеза и теория адаптивного мутагенеза. В данном случае под «случайным  мутагенезом» понимают процесс возникновения мутаций в делящихся клетках до воздействия на них селективного агента. Термин «адаптивный мутагенез» означает, что мутации возникают именно в тех селективных условиях, в которых они были отобраны,  вне зависимости от того возникают ли параллельно нейтральные мутации.  Адаптивный мутагенез происходит  в неделящихся или медленно растущих клетках. В течение последних 20 лет были получены доказательства того, что и случайные и адаптивные мутации возникают у бактерий и дрожжей. Микроорганизмы в природе не делятся или делятся очень медленно по причине ограничивающих факторов среды. Однако благодаря адаптивным мутациям микроорганизмы могут получить селективное преимущество и стимулировать эволюцию популяции. В данной работе мы обсудим фундаментальные аспекты адаптивного мутагенеза у дрожжей Saccharomyces cerevisiae. В начале мы сосредоточимся на природе адаптивного мутагенеза, затем рассмотрим экспериментальные системы, созданные для доказательства или опровержения адаптивного мутагенеза. Здесь мы кратко обсудили результаты, полученные в области адаптвного мутагенеза, уделив особое внимание генетическим и молекулярным механизмам этого процесса.

Saccharomyces cerevisiaeАДАПТИВНЫЙ МУТАГЕНЕЗНАПРАЫЛЕННЫЙ МУТАГЕНЕЗРЕПАРАЦИЯ ДНКдрожжиНЕДЕЛЯЩИЕСЯ КЛЕТКИHayes W. The Genetics of Bacteria and their Viruses. -Blackwell Scientific Publications, Oxford. -1964. -Vol. 177. -198 p.Luria S.E. and Delbrück M. Mutations of bacteria from virus sensitivity to virus resistance//Genetics. -1943. -Vol. 28. -P. 491-511.Cairns J., Overbaugh J. and Miller S. The origin of mutants//Nature. -1988. -Vol. 335. -P. 142-145.Ryan F.J. Spontaneous mutations in non-dividing bacteria//Genetics. -1955. -Vol. 40. -P. 726-738.Shapiro J.A. Observations on the formation of clones containing araB-lacZ fusions//Mol. Gen. Genet. -1984. -Vol. 194. -P. 79-90.Cairns J. and Foster P.L. Adaptive reversion of a frameshift mutation in Escherichia coli//Genetics. -1991. -Vol. 28. -P. 695-701.Steele D.F. and Jinks-Robertson S. An examination of adaptive reversion in Saccharomyces cerevisiae//Genetics. -1992. -Vol. 132. -P. 9-21.Hall B.G. Spontaneous point mutations that occur more often when advantageous than when neutral//Genetics. -1990. -Vol. 126. -P. 5-16.Hall B.G. Selection induced mutations occur in yeast//Proc. Natl. Acad. Sci. USA. -1992. -Vol. 89. -P. 4300-4303.Achilli A., Pavlov Y.I., Matmati N. et al., The exceptionally high rate of spontaneous mutations in the polymerase delta proof-reading exonuclease deficient S.cerevisiae strains starved for adenina//BMC Genetics. -2004. -Vol. 5. -P. 34-44.Marini A., Morpurgo G. and Matmati N. Starvation in yeast increases non-adaptive mutation//Curr. Genet. -1999. -Vol. 35. -P. 77-81.McPhee D. Is there evidence for directed mutation in bacteria?//Mutagenesis. -1993. -Vol. 8. -P. 3-5.Foster P.L. Adaptive mutation in Escherichia coli//J. Bacteriol. -2004. -Vol. 186. -P. 4846-4852.Foster P.L. Stress responses and genetic variation in bacteria//Mut. Res. -2005. -Vol. 569. -P. 3-11.Rosenberg S.M. Evolving responsively: adaptive mutation//Nat. Rev. Gene. -2001. -Vol. 2. -P. 504-515.Roth J.R., Kugeleberg E., Reams A.B. et al. Origins of Mutations Under Selection: The Adaptive Mutation Controversy//Annu. Rev. Microbiol. -2006. -Vol. 60. -P. 477-501.Foster P.L. Nonadaptive mutations occur on the F' episome during adaptive mutations conditions in Escherichia coli//J. Bacteriol. -1997. -Vol. 174. -P. 1711-1716.Foster P.L. and Cairns J. Adaptive mutation of a lacZ amber allele//Genetics. -1998. -Vol. 150. -P. 1329-1330.Wright B.E. Stress-directed adaptive mutations and evolution//Mol. Microbiol. -2004. -Vol. 52. -P. 643-650.Maki H. Origins of spontaneous mutations: specificity and directionality of base-substitutions, frameshift and sequencesubstitution mutagenesis//Annu. Rev. Genet. -2002. -Vol. 36. -P. 279-303.Barnes D.E. and Lindahl T. Repair and genetic consequences of endogenous DNA base damage in mammalian cells//Annu. Rev. Genet. -2004. -Vol. 38. -P. 445-476.Bridges B.A. Mutation in resting cells: the role of endogenous DNA damage//Cancer Surv. -1996. -Vol. 2. -P. 155-167.Heidenreich E. and Wintersberger U. Starvation for specific aminoacid induces high frequencies of rho-mutants in Saccharomyces cerevisiae//Curr. Genet. -1997. -Vol. 31. -P. 408-413.Prakash S. and Prakash.L. Nucleotide excision repair in yeast//Mut. Res. -2000. -Vol. 451. -P. 13-24.Abdulovic A., Kim N. and Jinks-Robertson S. Mutagenesis and the three R's in yeast//DNA repair. -2006. -Vol. 5. -P. 409-421.Heidenreich E., Holzmann V. and Eisler H. Polymerase zeta dependency of increased adaptive mutation frequencies in nucleotide excision repair-deficient yeast strains//DNA Repair. -2004. -Vol. 3. -P. 395-402.Storchová Z., Rohas A.P., Janderová B., et al. The involvement of the RAD6 gene in starvation-induced reverse mutations in Saccharomyces cerevisiae//Mol. Gen. Genet. -1998. -Vol. 258. -P. 546-552.Ceiká P., Vondrejs V., Storchová S. Dissection of the functions of the Saccharomyces cerevisiae RAD6 postreplicative repair group in mutagenesis and UV sensitivity//Genetics -2001. -Vol. 159. -P. 953-963.Prakash L. The structure and function of RAD6 and RAD18 DNA repair genes of Saccharomyces cerevisiae//Genome. -1989. -Vol. 31. -P. 597-600.Lawrence C. The RAD6 DNA repair pathway in Saccharomyces cerevisiae: what does it do, and how does it do it?//Bioessays. -1994. -Vol. 16. -P. 253-258.Watts F.Z. Sumoylation of PCNA: Wrestling with recombination at stalled replication forks//DNA Repair. -2006. -Vol. 5. -P. 399-403.Ulrich H.D. Mutual interactions between the SUMO and ubiquitin systems: a plea of no contest//Trends Cell Biol. -2005. -Vol. 15. -P. 525-532.Ulrich H.D. The RAD6 pathway: control of DNA damage bypass and mutagenesis by ubiquitin and SUMO//Chembiochem. -2005. -Vol. 6. -P. 1735-1743.Baranowska H., Policinska Z. and Jachymezyk W.Y. Effects of the CDC2 gene on adaptive mutation in the yeast Saccharomyces cerevisiae//Curr. Genet. -1995. -Vol. 28. -P. 521-525.Babudri N., Pavlov Y.I., Matmati N., et al. Stationary-phase mutations in proofreading exonuclease-deficient strains in the yeast Saccharomyces cerevisiae//Mol. Gen. Genomics. -2001. -Vol. 265. -P. 362-366.Halas A., Baranowska H., Policinska Z. The influence of the mismatch-repair system on stationary-phase mutagenesis in the yeast Saccharomyces cerevisiae//Curr. Genet. -2002. -Vol. 42. -P. 140-146.Modrich P. and Lahue R. Mismatch repair in replication fidelity, genetic recombination, and cancer biology//Ann. Rev. Biochem. -1996. -Vol. 65. -P. 101-133.Harfe B.D. and Jinks-Robertson S. DNA mismatch repair and genetic instability//Ann. Rev. Genet. -2000. -Vol. 34. -P. 359-399.Kunkel T.A. and Erie D.A. DNA mismatch repair//Ann. Rev. Biochem. -2005. -Vol. 74. -P. 681-710.Storchov Z. and Vondrejs V. Starvation-associated mutagenesis in yeast Saccharomyces cerevisiae is affected by Ras2/cAMP signaling pathway//Mut. Res. -1999. -Vol. 16. -P. 59-67.Thevelein J.M. and de Winde J.H. Novel sensing mechanisms and targets for the cAMP -protein kinase A pathway in the yeast Saccharomyces cerevisiae//Mol. Microbiol. -1999. -Vol. 33. -P. 904-918.Estruch F. Stress-controlled transcription factors, stressinduced genes and stress tolerance in budding yeast//FEMS Microbiol. Rev. -2000. -Vol. 24. -P. 469-486.Bresson A. and Fuchs R.P. Lesion bypass in yeast cells: Pol eta participates in a multi-DNA polymerases process//EMBO J. -2002. -Vol. 21. -P. 3881-3887.Zhang H. and Siede W. UV-induced TC transition at a TT photoproduct site is dependent on Saccharomyces cerevisiae polymerase eta in vivo//Nucleic Acid Res. -2002. -Vol. 30. -P. 1262-1267.Kozmin S.G., Pavlov Y.I., Kunkel T.A., et al. Roles of Saccharomyces cerevisiae DNA polymerases Poleta and polzeta in response to irradiation by simulated sunlight//Nucleic Acid Res. -2003. -Vol. 31. -P. 4541-4552.Heidenreich E., Eiser H. and Steinboeck F. Epistatic participation of REV1 and REV3 in the formation of UVinduced frameshift mutations in cell cycle arrested cells//Mut. Res. -2006. -Vol. 593. -P. 187-195.Abdulovic A.L. and Jinks-Robertson S. The in vivo characterization of translesion synthesis across UV-induced lesions in Saccharomyces cerevisiae: insights into Pol zeta-and Pol eta-dependent frameshift mutagenesis//Genetics. -2006. -Vol. 172. -P. 1487-1498.Lawrence C.W. and Maher V.M. Eukaryotic mutagenesis and translesion replication dependent on DNA polymerases zeta and Rev1 protein//Biochem. Soc. Trans. -2001. -Vol. 29. -P. 187-191.Daley J.M., Palmbos P.L., Wu D. et al., Nonhomologous end joining in yeast//Annu. Rev. Genet. -2005. -Vol. 39. -P. 431-451.Heidenreich E., Novotny R., Kneidinger B., et al. Non-homologous end joining as an important mutagenic process in cell cycle-arrested cells.//EMBO J. -2003. -Vol. 22. -2274-2283.Krog B.O. and Symington L.S. Recombination proteins in yeast//Annu. Rev. Genet. -2004. -Vol. 38. -P. 233-271.Aylon Y. and Kupiec M. DSB repair: the yeast paradigm//DNA Repair. -2004. -Vol. 3. -P. 797-815.Heidenreich E. and Eisler H. Non-homologous end joining dependency of gamma-irradiation induced adaptive frameshift mutation formation in cell cycle-arrested yeast cells.//Mut. Res. -2004. -Vol. 556. -P. 201-208.Xiao W., Chow B.L., Broomfield S., et al. The Saccharomyces cerevisiae RAD6 group is composed of an error-prone and two error-free postreplication repair pathways//Genetics. -2000. -Vol. 155. -P. 1633-1641.Heidenreich E. and Wintersberger U. Adaptive reversions of a frameshift mutation in arrested Saccharomyces cerevisiae cells by simple deletions in mononucleotide repeats//Mut. Res. -2001. -Vol. 473. -P. 101-107.Wright B.E., Longacre A. and Reimers J.M. Hypermutation in derepressed operons of Escherichia coli K12//Proc. Natl. Acad. Sci. USA. -1999. -Vol. 96. -P. 5089-5094.Wright B.E. A biochemical mechanism for non-random mutations and evolution//J. Bacteriol. -2000. -Vol. 182. -P. 2993-3001.Reimers J.M., Schmidt K.H., Longacre A. Increased transcription rates correlate with increased reversion rates in leuB and argH Escherichia coli auxotrophs//Microbiology. -2004. -Vol. 150. -P. 1457-1466.Datta A. and Jinks-Robertson S. Association of increased spontaneous mutation rates with high levels of transcription in yeast//Science. -1995. -Vol. 26. -P. 1616-1619.Morey N.J., Greene C.N. and Jinks-Robertson S. Genetic analysis of transcription-associated mutations in Saccharomyces cerevisiae//Genetics. -2000. -Vol. 154. -P. 109-120.Lippert M.J., Freedman J.A., Barber M.A. et al. Identification of a distinctive mutation spectrum associated with high levels of transcription in yeast//Mol. Cell. Biol. -2004. -Vol. 24. -P. 4801-4809.Doetsch P.W. Translesion sythesis by RNA polymerases: occurrence and biological implications for transcriptional mutagenesis//Mut. Res. -2002. -Vol. 510. -P. 131-140.Viswanathan A., You H.J. and Doetsch P.W. Phenotypic change caused by transcriptional bypass of uracil in nondividing cells//Science. -1999. -Vol. 284. -P. 159-162.Pimpinelli S., Marini A., Babudri N. et al. 6-N-hydroxylaminopurine (HAP)-induced accumulation of variability in haploid and diploid strains of Aspergillus nidulans//Curr. Genet. -1997. -Vol. 32. -P. 331-336.Kivisaar M. Stationary phase mutagenesis: mechanisms that accelerate adaptation of microbial populations under environmental stress//Envirom. Microbiol. -2003. -Vol. 5. -P. 814-827.Roth J.R., Andersson D.I. Adaptive mutations: how growth under selection stimulates Lac(-) reversion by increasing target copy number//J. Bacteriol. -2004. -Vol. 186. -P. 4855-4860.Roth J.R., Andersson D.I. Adaptive mutation: how growth under selection contributes to the origin of genetic diversity and explains the phenomenon of adaptive mutations//Res. Microbiol. -2004. -Vol. 155. -P. 342-351.