Abstract
Creation of new genes and functions is a central feature of evolution. Duplication of existing genes has long been assumed to be the source of new genes, but the precise mechanism has remained unclear. One suggestion is that new genes are created via temporary amplifications, which simultaneously increase both the selective advantage of weak, pre-existing secondary functions and the target for optimizing mutations. This paper examines the amplification model by formalizing it into a mathematical framework. This framework is used to perform stochastic (Monte Carlo) simulations. In addition, experimental data from Salmonella typhimurium LT2 are used to support the modelling, by providing estimates for parameter values. The results show that amplification of tandem repeats is likely to contribute to creation of new genes in nature.
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References
Anderson RP, Roth JR (1977) Tandem genetic duplications in phage and bacteria. Annu Rev Microbiol 31:473–505. doi:10.1146/annurev.mi.31.100177.002353
Anderson RP, Roth JR (1981) Spontaneous tandem genetic duplications in Salmonella typhimurium arise by unequal recombination between ribosomal RNA (rrn) cistrons. Proc Natl Acad Sci USA 78:3113–3117. doi:10.1073/pnas.78.5.3113
Berg OG, Kurland CG (2002) Evolution of microbial genomes: sequence acquisition and loss. Mol Biol Evol 19:2265–2276
Bergthorsson U, Andersson DI, Roth JR (2007) Ohno’s Dilemma: Evolution of new genes under continuous selection. Proc Natl Acad Sci USA. doi:10.1073/pnas.0707158104
Cairns J, Overbaugh J, Miller S (1988) The origin of mutants. Nature 335:142–145. doi:10.1038/335142a0
Cairns J, Foster PL (1991) Adaptive reversion of a frameshift mutation in Escherichia coli. Genetics 128:1091–1100
Dunham MJ, Baderane H, Ferea T, Adams J, Brown PO, Rosenzweig F et al (2002) Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae. Proc Natl Acad Sci USA 99(25):16144–16149. doi:10.1073/pnas.242624799
El-Sayed NM, Myler PJ, Bartholomeu DC, Nilsson D, Aggarwal G, Tran AN et al (2005) The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309:409–415. doi:10.1126/science.1112631
Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlewaith J (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531–1545
Francino MP (2005) An adaptive radiation model for the origin of new gene functions. Nat Genet 37:573–577. doi:10.1038/ng1579
Guillemand T, Raymond M, Tsagkarakou A, Bernard C, Rochard P, Pasteur N (1999) Quantitative variation and selection of esterase gene amplification in Culex pipiens. Heredity 83:87–99. doi:10.1038/sj.hdy.6885370
Hendricksson H, Slechta ES, Bergthorsson U, Andersson DI, Roth JR (2002) Amplification-mutagenesis: evidence that “directed” adaptive mutation and general hypermutability result from growth with a selected gene amplification. Proc Natl Acad Sci USA 99:2164–2169. doi:10.1073/pnas.032680899
Hooper SD, Berg OG (2002) On the nature of gene innovation: duplication patterns in microbial genomes. Mol Biol Evol 20:945–954. doi:10.1093/molbev/msg101
Hooper SD, Berg OG (2003) Duplication is more common among laterally transferred genes than among indigenous genes. Genome Biol 4:R48. doi:10.1186/gb-2003-4-8-r48
Kugelberg E, Kofoid E, Reams AB, Andersson DI, Roth JR (2006) Multiple pathways of selected gene amplifications during adaptive mutation. Proc Natl Acad Sci USA 103:17319–17324. doi:10.1073/pnas.0608309103
Lynch M, Force A (2000) The Probability of duplicate gene preservation by subfunctionalization. Genetics 154:459–473
Lynch M, O’Hely M, Walsh B, Force A (2001) The probability of preservation of a newly arisen gene duplicate. Genetics 159:1789–1804
Matsamura I, Ellington AD (2001) In vitro evolution of beta-glucuronidase into a beta- galactosidase proceeds through non-specific intermediates. J Mol Biol 305:331–339. doi:10.1006/jmbi.2000.4259
Meyer A, Würsten M, Schmid A, Kohler HE, Witholt B (2002) Hydroxylation of indole by laboratory-evolved 2-hydroxybiphenyl 3-monooxygenase. J Biol Chem 277:34161–34167. doi:10.1074/jbc.M205621200
Nilsson AI, Zorzet A, Kanth A, Dahlstöm S, Berg OG, Andersson DI (2006) Reducing the fitness cost of antibiotic resistance by amplification of initiator tRNA genes. Proc Natl Acad Sci USA 103:6976–6981. doi:10.1073/pnas.0602171103
Ohno S, Wolf U, Atkin NB (1968) Evolution from fish to mammals by gene duplication. Hereditas 59:169–187
Ohno S (1970) Evolution by gene duplication. Springer-Verlag, New York
Ohta T (1980) Evolution and variation of multigene families. Lecture Notes in Biomathematics, vol 37. Springer-Verlag, New York
Ohta T (1983) On the evolution of multigene families. Theor Popul Biol 23:216–240. doi:10.1016/0040-5809(83)90015-1
Ohta T (1987) Simulating evolution by gene duplication. Genetics 115:207–213
Ohta T (2002) Usefulness of the identity coefficients for assessing evolutionary forces. In: Slatkin M, Veuille M (eds) Modern Development in Theoretical Population Genetics - The Legacy of Gustave Malecot, pp 37–49. University Press, Oxford
Pál C, Papp B, Lercher MJ (2005) Adaptive evolution of bacterial metabolic networks by horizontal gene transfer. Nat Genet 37:1372–1375. doi:10.1038/ng1686
Pettersson ME, Andersson DI, Roth JR, Berg OG (2005) The amplification model for adaptive mutation–simulation and analysis. Genetics 169:1105–1115. doi:10.1534/genetics.104.030338
Romero D, Martinezsalazar J, Girard L, Brom S, Davila G, Palacios R et al (1995) Discrete amplifiable regions (amplicons) in the symbiotic plasmid of Rhizobium-ETLI CFN42. J Bacteriol 177:973–980
Roth JR, Andersson DI (2004) Amplification-mutagenesis–how growth under selection contributes to the origin of genetic diversity and explains the phenomenon of adaptive mutation. Res Microbiol 155:342–351. doi:10.1016/j.resmic.2004.01.016
Walsh B (2003) Population-genetic models of the fate of duplicate genes. Genetica 118:279–294. doi:10.1023/A:1024194802441
Winfield SL, Falkinham JO (1981) Effect of recA and polA mutations on gene duplication in Salmonella typhimurium. Mutat Res 91:15–20. doi:10.1016/0165-7992(81)90063-4
Wong K, deLeeuw K, Dosanjh RJ, Kimm NS, Cheng LR, Horsman Z et al (2007) A comprehensive analysis of common copy-number variations in the human genome. Am J Hum Genet 80:91–104. doi:10.1086/510560
Acknowledgements
This work was supported by the Swedish Research Council (MEP, OGB and DIA) and the 7th EU framework programme (DIA).
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Pettersson, M.E., Sun, S., Andersson, D.I. et al. Evolution of new gene functions: simulation and analysis of the amplification model. Genetica 135, 309–324 (2009). https://doi.org/10.1007/s10709-008-9289-z
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DOI: https://doi.org/10.1007/s10709-008-9289-z