Mutational effects and the evolution of new protein functions (original) (raw)
Conant, G. C. & Wolfe, K. H. Turning a hobby into a job: how duplicated genes find new functions. Nature Rev. Genet.9, 938–950 (2008). CASPubMed Google Scholar
Innan, H. & Kondrashov, F. The evolution of gene duplications: classifying and distinguishing between models. Nature Rev. Genet.11, 97–108 (2010). CASPubMed Google Scholar
DePristo, M. A., Weinreich, D. M. & Hartl, D. L. Missense meanderings in sequence space: a biophysical view of protein evolution. Nature Rev. Genet.6, 678–687 (2005). CASPubMed Google Scholar
Pal, C., Papp, B. & Lercher, M. J. An integrated view of protein evolution. Nature Rev. Genet.7, 337–348 (2006). CASPubMed Google Scholar
Dean, A. M. & Thornton, J. W. Mechanistic approaches to the study of evolution: the functional synthesis. Nature Rev. Genet.8, 675–688 (2007). CASPubMed Google Scholar
Tokuriki, N. & Tawfik, D. S. Stability effects of mutations and protein evolvability. Curr. Opin. Struct. Biol.19, 596–604 (2009). CASPubMed Google Scholar
Eyre-Walker, A. & Keightley, P. D. The distribution of fitness effects of new mutations. Nature Rev. Genet.8, 610–618 (2007). CASPubMed Google Scholar
Camps, M., Herman, A., Loh, E. & Loeb, L. A. Genetic constraints on protein evolution. Crit. Rev. Biochem. Mol. Biol.42, 313–326 (2007). CASPubMed Google Scholar
Bloom, J. D. et al. Thermodynamic prediction of protein neutrality. Proc. Natl Acad. Sci. USA102, 606–611 (2005). CASPubMedPubMed Central Google Scholar
Bershtein, S., Segal, M., Bekerman, R., Tokuriki, N. & Tawfik, D. S. Robustness–epistasis link shapes the fitness landscape of a randomly drifting protein. Nature444, 929–932 (2006). CASPubMed Google Scholar
Bershtein, S. & Tawfik, D. S. Ohno's model revisited: measuring the frequency of potentially adaptive mutations under various mutational drifts. Mol. Biol. Evol.25, 2311–2318 (2008). CASPubMed Google Scholar
Hecky, J. & Muller, K. M. Structural perturbation and compensation by directed evolution at physiological temperature leads to thermostabilization of β-lactamase. Biochemistry44, 12640–12654 (2005). CASPubMed Google Scholar
Yue, P. & Moult, J. Identification and analysis of deleterious human SNPs. J. Mol. Biol.356, 1263–1274 (2006). CASPubMed Google Scholar
Tokuriki, N., Oldfield, C. J., Uversky, V. N., Berezovsky, I. N. & Tawfik, D. S. Do viral proteins possess unique biophysical features? Trends Biochem. Sci.34, 53–59 (2009). CASPubMed Google Scholar
Wang, X., Minasov, G. & Shoichet, B. K. Evolution of an antibiotic resistance enzyme constrained by stability and activity trade-offs. J. Mol. Biol.320, 85–95 (2002). CASPubMed Google Scholar
Tokuriki, N., Stricher, F., Serrano, L. & Tawfik, D. S. How protein stability and new functions trade off. PLoS Comput. Biol.4, e1000002 (2008). PubMedPubMed Central Google Scholar
Levin, K. B. et al. Following evolutionary paths to protein–protein interactions with high affinity and selectivity. Nature Struct. Mol. Biol.16, 1049–1055 (2009). CAS Google Scholar
Lindner, A. B., Madden, R., Demarez, A., Stewart, E. J. & Taddei, F. Asymmetric segregation of protein aggregates is associated with cellular aging and rejuvenation. Proc. Natl Acad. Sci. USA105, 3076–3081 (2008). CASPubMedPubMed Central Google Scholar
McLoughlin, S. Y. & Copley, S. D. A compromise required by gene sharing enables survival: implications for evolution of new enzyme activities. Proc. Natl Acad. Sci. USA105, 13497–13502 (2008). CASPubMedPubMed Central Google Scholar
Vick, J. E., Schmidt, D. M. & Gerlt, J. A. Evolutionary potential of (β/α)8-barrels: in vitro enhancement of a 'new' reaction in the enolase superfamily. Biochemistry44, 11722–11729 (2005). CASPubMed Google Scholar
Khersonsky, O. & Tawfik, D. S. Enzyme promiscuity: a mechanistic and evolurtionary perpective. Ann. Rev. Biochem.79, 471–505 (2010). CASPubMed Google Scholar
Aharoni, A. et al. The 'evolvability' of promiscuous protein functions. Nature Genet.37, 73–76 (2005). CASPubMed Google Scholar
Tokuriki, N. & Tawfik, D. S. Protein dynamism and evolvability. Science324, 203–207 (2009). CASPubMed Google Scholar
Scannell, D. R. & Wolfe, K. H. A burst of protein sequence evolution and a prolonged period of asymmetric evolution follow gene duplication in yeast. Genome Res.18, 137–147 (2008). CASPubMedPubMed Central Google Scholar
Kaessmann, H. Genetics. More than just a copy. Science325, 958–959 (2009). PubMed Google Scholar
Parker, H. G. et al. An expressed fgf4 retrogene is associated with breed-defining chondrodysplasia in domestic dogs. Science325, 995–998 (2009). CASPubMedPubMed Central Google Scholar
Andersson, D. I. & Hughes, D. Gene amplification and adaptive evolution in bacteria. Annu. Rev. Genet.43, 167–195 (2009). CASPubMed Google Scholar
Schimke, R. T. Gene amplification in cultured cells. J. Biol. Chem.263, 5989–5992 (1988). CASPubMed Google Scholar
Papp, B., Pal, C. & Hurst, L. D. Metabolic network analysis of the causes and evolution of enzyme dispensability in yeast. Nature429, 661–664 (2004). CASPubMed Google Scholar
Perry, G. H. et al. Diet and the evolution of human amylase gene copy number variation. Nature Genet.39, 1256–1260 (2007). CASPubMed Google Scholar
Fablet, M., Bueno, M., Potrzebowski, L. & Kaessmann, H. Evolutionary origin and functions of retrogene introns. Mol. Biol. Evol.26, 2147–2156 (2009). CASPubMed Google Scholar
Jablonka, E. & Lamb, M. J. Epigenetic Inheritance and Evolution: The Lamarckian Dimension (Oxford Univ. Press, Oxford, UK, 1995). Google Scholar
Steele, E. J., Lindley, R. A. & Blanden, R. V. Lamarck's Signature: How Retrogenes Are Changing Darwin's Natural Selection Paradigm, (Allen & Unwin; Perseus Books, Australia, 1988). Google Scholar
Chen, G. K. et al. Preferential expression of a mutant allele of the amplified MDR1 (ABCB1) gene in drug-resistant variants of a human sarcoma. Genes Chromosomes Cancer34, 372–383 (2002). PubMed Google Scholar
Goldsmith, M. & Tawfik, D. S. Potential role of phenotypic mutations in the evolution of protein expression and stability. Proc. Natl Acad. Sci. USA106, 6197–6202 (2009). CASPubMedPubMed Central Google Scholar
Siu, L. K., Ho, P. L., Yuen, K. Y., Wong, S. S. & Chau, P. Y. Transferable hyperproduction of TEM-1 β-lactamase in Shigella flexneri due to a point mutation in the pribnow box. Antimicrob. Agents Chemother.41, 468–470 (1997). CASPubMedPubMed Central Google Scholar
Hall, B. G. The EBG system of E. coli: origin and evolution of a novel β-galactosidase for the metabolism of lactose. Genetica118, 143–156 (2003). CASPubMed Google Scholar
Stoebel, D. M., Dean, A. M. & Dykhuizen, D. E. The cost of expression of Escherichia coli lac operon proteins is in the process, not in the products. Genetics178, 1653–1660 (2008). CASPubMedPubMed Central Google Scholar
Wagner, A. Energy constraints on the evolution of gene expression. Mol. Biol. Evol.22, 1365–1374 (2005). CASPubMed Google Scholar
Vavouri, T., Semple, J. I., Garcia-Verdugo, R. & Lehner, B. Intrinsic protein disorder and interaction promiscuity are widely associated with dosage sensitivity. Cell138, 198–208 (2009). CASPubMed Google Scholar
Veitia, R. A. Gene dosage balance: deletions, duplications and dominance. Trends Genet.21, 33–35 (2005). CASPubMed Google Scholar
Drummond, D. A., Bloom, J. D., Adami, C., Wilke, C. O. & Arnold, F. H. Why highly expressed proteins evolve slowly. Proc. Natl Acad. Sci. USA102, 14338–14343 (2005). CASPubMedPubMed Central Google Scholar
Fares, M. A., Ruiz- González, M. X., Moya, A., Elena, S. F. & Barrio, E. Endosymbiotic bacteria: GroEL buffers against deleterious mutations. Nature417, 398 (2002). CASPubMed Google Scholar
Rutherford, S., Hirate, Y. & Swalla, B. J. The Hsp90 capacitor, developmental remodeling, and evolution: the robustness of gene networks and the curious evolvability of metamorphosis. Crit. Rev. Biochem. Mol. Biol.42, 355–372 (2007). CASPubMed Google Scholar
Cowen, L. E. & Lindquist, S. Hsp90 potentiates the rapid evolution of new traits: drug resistance in diverse fungi. Science309, 2185–2189 (2005). CASPubMed Google Scholar
Parent, K. N., Ranaghan, M. J. & Teschke, C. M. A second-site suppressor of a folding defect functions via interactions with a chaperone network to improve folding and assembly in vivo. Mol. Microbiol.54, 1036–1050 (2004). CASPubMed Google Scholar
Tokuriki, N. & Tawfik, D. S. Chaperonin overexpression promotes genetic variation and enzyme evolution. Nature459, 668–673 (2009). CASPubMed Google Scholar
Zhang, L. & Watson, L. T. Analysis of the fitness effect of compensatory mutations. HFSP J.3, 47–54 (2009). PubMed Google Scholar
Bershtein, S., Goldin, K. & Tawfik, D. S. Intense neutral drifts yield robust and evolvable consensus proteins. J. Mol. Biol.379, 1029–1044 (2008). CASPubMed Google Scholar
Hecky, J., Mason, J. M., Arndt, K. M. & Muller, K. M. A general method of terminal truncation, evolution, and re-elongation to generate enzymes of enhanced stability. Methods Mol. Biol.352, 275–304 (2007). CASPubMed Google Scholar
Kather, I., Jakob, R. P., Dobbek, H. & Schmid, F. X. Increased folding stability of TEM-1 β-lactamase by in vitro selection. J. Mol. Biol.383, 238–251 (2008). CASPubMed Google Scholar
Marciano, D. C. et al. Genetic and structural characterization of an L201P global suppressor substitution in TEM-1 β-lactamase. J. Mol. Biol.384, 151–164 (2008). CASPubMedPubMed Central Google Scholar
Kimura, M. The role of compensatory neutral mutations in molecular evolution. J. Genet.64, 7–19 (1985). CAS Google Scholar
Bloom, J. D., Labthavikul, S. T., Otey, C. R. & Arnold, F. H. Protein stability promotes evolvability. Proc. Natl Acad. Sci. USA103, 5869–5874 (2006). CASPubMedPubMed Central Google Scholar
McIntosh, B. E., Hogenesch, J. B. & Bradfield, C. A. Mammalian Per-Arnt-Sim proteins in environmental adaptation. Annu. Rev. Physiol.72, 625–645 (2010). CASPubMed Google Scholar
Lynch, M. Genomics. Gene duplication and evolution. Science297, 945–947 (2002). CASPubMed Google Scholar
Beckmann, J. S., Estivill, X. & Antonarakis, S. E. Copy number variants and genetic traits: closer to the resolution of phenotypic to genotypic variability. Nature Rev. Genet.8, 639–646 (2007). CASPubMed Google Scholar
Hastings, P. J., Lupski, J. R., Rosenberg, S. M. & Ira, G. Mechanisms of change in gene copy number. Nature Rev. Genet.10, 551–564 (2009). CASPubMed Google Scholar
Liao, B. Y. & Zhang, J. Null mutations in human and mouse orthologs frequently result in different phenotypes. Proc. Natl Acad. Sci. USA105, 6987–6992 (2008). CASPubMedPubMed Central Google Scholar
Ohno, S. Evolution by Gene Duplication (Allen & Unwin; Springer, New York, 1970). Google Scholar
Kimura, M. & Ota, T. On some principles governing molecular evolution. Proc. Natl Acad. Sci. USA71, 2848–2852 (1974). CASPubMedPubMed Central Google Scholar
Zhang, J. Evolution by gene duplication: an update. Trends Ecol. Evol.18, 292–298 (2003). Google Scholar
Hughes, A. L. Adaptive evolution after gene duplication. Trends Genet.18, 433–434 (2002). CASPubMed Google Scholar
Lynch, M. & Katju, V. The altered evolutionary trajectories of gene duplicates. Trends Genet.20, 544–549 (2004). CASPubMed Google Scholar
Kondrashov, F. A. & Koonin, E. V. A common framework for understanding the origin of genetic dominance and evolutionary fates of gene duplications. Trends Genet.20, 287–290 (2004). CASPubMed Google Scholar
Bergthorsson, U., Andersson, D. I. & Roth, J. R. Ohno's dilemma: evolution of new genes under continuous selection. Proc. Natl Acad. Sci. USA104, 17004–17009 (2007). CASPubMedPubMed Central Google Scholar
Kondrashov, F. A. In search of the limits of evolution. Nature Genet.37, 9–10 (2005). CASPubMed Google Scholar
Boehr, D. D., Nussinov, R. & Wright, P. E. The role of dynamic conformational ensembles in biomolecular recognition. Nature Chem. Biol.5, 789–796 (2009). CAS Google Scholar
Piatigorsky, J. et al. Gene sharing by D-crystallin and argininosuccinate lyase. Proc. Natl Acad. Sci. USA85, 3479–3483 (1988). CASPubMedPubMed Central Google Scholar
Piatigorsky, J. Gene Sharing and Evolution: The Diversity of Protein Functions, (Harvard Univ. Press, Cambridge, Massachusetts, USA; London, UK, 2007). Google Scholar
Lee, Y. N., Nechushtan, H., Figov, N. & Razin, E. The function of lysyl-tRNA synthetase and Ap4A as signaling regulators of MITF activity in FceRI-activated mast cells. Immunity20, 145–151 (2004). CASPubMed Google Scholar
Sedlak, T. W. & Snyder, S. H. Messenger molecules and cell death: therapeutic implications. JAMA295, 81–89 (2006). CASPubMed Google Scholar
Rosenberg, H. F. RNase A ribonucleases and host defense: an evolving story. J. Leukoc. Biol.83, 1079–1087 (2008). CASPubMed Google Scholar
Jensen, R. A. Enzyme recruitment in evolution of new function. Annu. Rev. Microbiol.30, 409–425 (1974). Google Scholar
O'Brien, P. J. & Herschlag, D. Catalytic promiscuity and the evolution of new enzymatic activities. Chem. Biol.6, R91–R105 (1999). CASPubMed Google Scholar
Palmer, D. R. et al. Unexpected divergence of enzyme function and sequence: '_N_-acylamino acid racemase' is _o_-succinylbenzoate synthase. Biochemistry38, 4252–4258 (1999). CASPubMed Google Scholar
James, L. C. & Tawfik, D. S. Catalytic and binding poly-reactivities shared by two unrelated proteins: the potential role of promiscuity in enzyme evolution. Protein Sci.10, 2600–2607 (2001). CASPubMedPubMed Central Google Scholar
Afriat, L., Roodveldt, C., Manco, G. & Tawfik, D. S. The latent promiscuity of newly identified microbial lactonases is linked to a recently diverged phosphotriesterase. Biochemistry45, 13677–13686 (2006). CASPubMed Google Scholar
Copley, S. D. Evolution of efficient pathways for degradation of anthropogenic chemicals. Nature Chem. Biol.5, 559–566 (2009). CAS Google Scholar
Copley, S. D. Comprehensive Natural Products II: Chemistry and Biology (eds Mander, L. & Liu, H.-W.) (Elsevier, Oxford, 2010). Google Scholar
Hughes, A. L. The evolution of functionally novel proteins after gene duplication. Proc. Biol. Sci.256, 119–124 (1994). CASPubMed Google Scholar
Barkman, T. & Zhang, J. Evidence for escape from adaptive conflict? Nature462, e1; discussion e2–e3 (2009). CASPubMed Google Scholar
Des Marais, D. L. & Rausher, M. D. Escape from adaptive conflict after duplication in an anthocyanin pathway gene. Nature454, 762–765 (2008). CASPubMed Google Scholar
Lynch, M. & Force, A. The probability of duplicate gene preservation by subfunctionalization. Genetics154, 459–473 (2000). CASPubMedPubMed Central Google Scholar
Dykhuizen, D. & Hartl, D. L. Selective neutrality of 6PGD allozymes in E. coli and the effects of genetic background. Genetics96, 801–817 (1980). CASPubMedPubMed Central Google Scholar
Force, A. et al. Preservation of duplicate genes by complementary, degenerative mutations. Genetics151, 1531–1545 (1999). CASPubMedPubMed Central Google Scholar
Wagner, A. Robustness and Evolvability in Living Systems (Princeton Univ. Press, Princeton, USA, 2005). Google Scholar
Schuster, P. & Fontana, W. Chance and necessity in evolution: lessons from RNA. Physica D133, 427–452 (1999). CAS Google Scholar
Wroe, R., Chan, H. S. & Bornberg-Bauer, E. A structural model of latent evolutionary potentials underlying neutral networks in proteins. HFSP J.1, 79–87 (2007). CASPubMedPubMed Central Google Scholar
Klassen, J. L. Pathway evolution by horizontal transfer and positive selection is accommodated by relaxed negative selection upon upstream pathway genes in purple bacterial carotenoid biosynthesis. J. Bacteriol.191, 7500–7508 (2009). CASPubMedPubMed Central Google Scholar
Wloch, D. M., Szafraniec, K., Borts, R. H. & Korona, R. Direct estimate of the mutation rate and the distribution of fitness effects in the yeast Saccharomyces cerevisiae. Genetics159, 441–452 (2001). CASPubMedPubMed Central Google Scholar
Kivisaar, M. Degradation of nitroaromatic compounds: a model to study evolution of metabolic pathways. Mol. Microbiol.74, 777–781 (2009). CASPubMed Google Scholar
Wackett, L. P. Questioning our perceptions about evolution of biodegradative enzymes. Curr. Opin. Microbiol.12, 244–251 (2009). CASPubMed Google Scholar
Newcomb, R. D., Gleeson, D. M., Yong, C. G., Russell, R. J. & Oakeshott, J. G. Multiple mutations and gene duplications conferring organophosphorus insecticide resistance have been selected at the Rop-1 locus of the sheep blowfly, Lucilia cuprina. J. Mol. Evol.60, 207–220 (2005). CASPubMed Google Scholar
Patzoldt, W. L., Hager, A. G., McCormick, J. S. & Tranel, P. J. A codon deletion confers resistance to herbicides inhibiting protoporphyrinogen oxidase. Proc. Natl Acad. Sci. USA103, 12329–12334 (2006). CASPubMedPubMed Central Google Scholar
O'Maille, P. E. et al. Quantitative exploration of the catalytic landscape separating divergent plant sesquiterpene synthases. Nature Chem. Biol.4, 617–623 (2008). CAS Google Scholar
Lozovsky, E. R. et al. Stepwise acquisition of pyrimethamine resistance in the malaria parasite. Proc. Natl Acad. Sci. USA106, 12025–12030 (2009). CASPubMedPubMed Central Google Scholar
Poelwijk, F. J., Kiviet, D. J., Weinreich, D. M. & Tans, S. J. Empirical fitness landscapes reveal accessible evolutionary paths. Nature445, 383–386 (2007). CASPubMed Google Scholar
Kondrashov, A. S., Sunyaev, S. & Kondrashov, F. A. Dobzhansky–Muller incompatibilities in protein evolution. Proc. Natl Acad. Sci. USA99, 14878–14883 (2002). CASPubMedPubMed Central Google Scholar
Weinreich, D. M., Delaney, N. F., Depristo, M. A. & Hartl, D. L. Darwinian evolution can follow only very few mutational paths to fitter proteins. Science312, 111–114 (2006). CASPubMed Google Scholar