Reconstruction of Ancestral Metabolic Enzymes Reveals Molecular Mechanisms Underlying Evolutionary Innovation through Gene Duplication

PLoS Biology

Volumn 10, Issue 12, 2012, Pages

  Voordeckers, Karin ^a,b   Brown, Chris A ^a,b,c,d   Vanneste, Kevin ^a,e   van der Zande, Elisa ^a,b   Voet, Arnout ^b   Maere, Steven ^a,e   Verstrepen, Kevin J ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c Fathom Information Design   (United States)

^d HARVARD UNIVERSITY   (United States)

^e GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA GLUCOSIDASE; ISOMALTOSE; MALTOSE;

ARTICLE; ENZYME ACTIVITY; ENZYME STRUCTURE; EVOLUTION; GENE DUPLICATION; GENE MUTATION; MOLECULAR MECHANICS; SACCHAROMYCES CEREVISIAE;

ALPHA-GLUCOSIDASES; AMINO ACIDS; BINDING SITES; EVOLUTION, MOLECULAR; FUNGAL PROTEINS; GENE DOSAGE; GENE DUPLICATION; GENES, DUPLICATE; GLUCOSIDES; HYDROLYSIS; MALTOSE; MODELS, MOLECULAR; MULTIGENE FAMILY; SACCHAROMYCES CEREVISIAE; SELECTION, GENETIC; SUBSTRATE SPECIFICITY;

EID: 84871697209     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001446     Document Type: Article

References (71)

1. Ohno S (1970) Evolution by gene duplication, Berlin: Springer-Verlag.
2. Hahn MW, (2009) Distinguishing among evolutionary models for the maintenance of gene duplicates. J Hered 100: 605-617.
3. Taylor JS, Raes J, (2004) Duplication and divergence: the evolution of new genes and old ideas. Annu Rev Genet 38: 615-643.
4. Force A, Lynch M, Pickett FB, Amores A, Yan YL, et al. (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151: 1531-1545.
5. Hughes AL, (1994) The evolution of functionally novel proteins after gene duplication. Proc Biol Sci 256: 119-124.
6. Kondrashov FA, Rogozin IB, Wolf YI, Koonin EV, (2002) Selection in the evolution of gene duplications. Genome Biol 3: RESEARCH0008.
7. Cheung J, Wilson MD, Zhang J, Khaja R, MacDonald JR, et al. (2003) Recent segmental and gene duplications in the mouse genome. Genome Biol 4: R47.
8. Lynch M, Force A, (2000) The probability of duplicate gene preservation by subfunctionalization. Genetics 154: 459-473.
9. Wapinski I, Pfeffer A, Friedman N, Regev A, (2007) Natural history and evolutionary principles of gene duplication in fungi. Nature 449: 54-61.
10. Lynch M, Conery JS, (2000) The evolutionary fate and consequences of duplicate genes. Science 290: 1151-1155.
11. Piatigorsky J, Wistow G, (1991) The recruitment of crystallins: new functions precede gene duplication. Science 252: 1078-1079.
12. Wistow G, Piatigorsky J, (1987) Recruitment of enzymes as lens structural proteins. Science 236: 1554-1556.
13. Conant GC, Wolfe KH, (2008) Turning a hobby into a job: how duplicated genes find new functions. Nat Rev Genet 9: 938-950.
14. Innan H, Kondrashov F, (2010) The evolution of gene duplications: classifying and distinguishing between models. Nat Rev Genet 11: 97-108.
15. He X, Zhang J, (2005) Rapid subfunctionalization accompanied by prolonged and substantial neofunctionalization in duplicate gene evolution. Genetics 169: 1157-1164.
16. Des Marais DL, Rausher MD, (2008) Escape from adaptive conflict after duplication in an anthocyanin pathway gene. Nature 454: 762-765.
17. Hittinger CT, Carroll SB, (2007) Gene duplication and the adaptive evolution of a classic genetic switch. Nature 449: 677-681.
18. Hughes AL, (2005) Gene duplication and the origin of novel proteins. Proc Natl Acad Sci U S A 102: 8791-8792.
19. Rueffler C, Hermisson J, Wagner GP, (2012) Evolution of functional specialization and division of labor. Proc Natl Acad Sci U S A 109: E326-E335.
20. Bergthorsson U, Andersson DI, Roth JR, (2007) Ohno's dilemma: evolution of new genes under continuous selection. Proc Natl Acad Sci U S A 104: 17004-17009.
21. Francino MP, (2005) An adaptive radiation model for the origin of new gene functions. Nat Genet 37: 573-577.
22. Hendrickson 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 U S A 99: 2164-2169.
23. Bridgham JT, Carroll SM, Thornton JW, (2006) Evolution of hormone-receptor complexity by molecular exploitation. Science 312: 97-101.
24. Carroll SM, Ortlund EA, Thornton JW, (2011) Mechanisms for the evolution of a derived function in the ancestral glucocorticoid receptor. PLoS Genet 7: e1002117 doi:10.1371/journal.pgen.1002117.
25. Chandrasekharan UM, Sanker S, Glynias MJ, Karnik SS, Husain A, (1996) Angiotensin II-forming activity in a reconstructed ancestral chymase. Science 271: 502-505.
26. Gaucher EA, Govindarajan S, Ganesh OK, (2008) Palaeotemperature trend for Precambrian life inferred from resurrected proteins. Nature 451: 704-707.
27. Jermann TM, Opitz JG, Stackhouse J, Benner SA, (1995) Reconstructing the evolutionary history of the artiodactyl ribonuclease superfamily. Nature 374: 57-59.
28. Malcolm BA, Wilson KP, Matthews BW, Kirsch JF, Wilson AC, (1990) Ancestral lysozymes reconstructed, neutrality tested, and thermostability linked to hydrocarbon packing. Nature 345: 86-89.
29. Thomson JM, Gaucher EA, Burgan MF, De Kee DW, Li T, et al. (2005) Resurrecting ancestral alcohol dehydrogenases from yeast. Nat Genet 37: 630-635.
30. Zhang J, Dyer KD, Rosenberg HF, (2002) RNase 8, a novel RNase A superfamily ribonuclease expressed uniquely in placenta. Nucleic Acids Res 30: 1169-1175.
31. Wouters MA, Liu K, Riek P, Husain A, (2003) A despecialization step underlying evolution of a family of serine proteases. Mol Cell 12: 343-354.
32. Brown CA, Murray AW, Verstrepen KJ, (2010) Rapid expansion and functional divergence of subtelomeric gene families in yeasts. Curr Biol 20: 895-903.
33. Teste MA, Francois JM, Parrou JL, (2010) Characterization of a new multigene family encoding isomaltases in the yeast Saccharomyces cerevisiae, the IMA family. J Biol Chem 285: 26815-26824.
34. Yamamoto K, Miyake H, Kusunoki M, Osaki S, (2010) Crystal structures of isomaltase from Saccharomyces cerevisiae and in complex with its competitive inhibitor maltose. Febs J 277: 4205-4214.
35. Kurtzman CP, Robnett CJ, (2003) Phylogenetic relationships among yeasts of the 'Saccharomyces complex' determined from multigene sequence analyses. FEMS Yeast Res 3: 417-432.
36. Huelsenbeck JP, Ronquist F, (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754-755.
37. Guindon S, Gascuel O, (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704.
38. Low NH, Sporns P, (1988) Analysis and Quantitation of Minor Di- and Trisaccharides in Honey, Using Capillary Gas Chromatography. Journal of Food Science 53: 558-561.
39. Yamamoto K, Miyake H, Kusunoki M, Osaki S, (2011) Steric hindrance by 2 amino acid residues determines the substrate specificity of isomaltase from Saccharomyces cerevisiae. J Biosci Bioeng 112: 545-550.
40. Yamamoto K, Nakayama A, Yamamoto Y, Tabata S, (2004) Val216 decides the substrate specificity of alpha-glucosidase in Saccharomyces cerevisiae. Eur J Biochem 271: 3414-3420.
41. Pond SL, Frost SD, (2005) A genetic algorithm approach to detecting lineage-specific variation in selection pressure. Mol Biol Evol 22: 478-485.
42. Zhang J, Nielsen R, Yang Z, (2005) Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol Biol Evol 22: 2472-2479.
43. Kosakovsky Pond SL, Murrell B, Fourment M, Frost SD, Delport W, et al. (2011) A random effects branch-site model for detecting episodic diversifying selection. Mol Biol Evol 28: 3033-3043.
44. Hughes AL, (2007) Looking for Darwin in all the wrong places: the misguided quest for positive selection at the nucleotide sequence level. Heredity (Edinb) 99: 364-373.
45. Nozawa M, Suzuki Y, Nei M, (2009) Reliabilities of identifying positive selection by the branch-site and the site-prediction methods. Proc Natl Acad Sci U S A 106: 6700-6705.
46. Suzuki Y, Nei M, (2001) Reliabilities of parsimony-based and likelihood-based methods for detecting positive selection at single amino acid sites. Mol Biol Evol 18: 2179-2185.
47. Suzuki Y, Nei M, (2002) Simulation study of the reliability and robustness of the statistical methods for detecting positive selection at single amino acid sites. Mol Biol Evol 19: 1865-1869.
48. Barkman T, Zhang J, (2009) Evidence for escape from adaptive conflict? Nature 462: E1 discussion E2-E3.
49. Zhai W, Nielsen R, Goldman N, Yang Z, (2012) Looking for Darwin in Genomic Sequences-Validity and Success of Statistical Methods. Mol Biol Evol.
50. Deng C, Cheng CH, Ye H, He X, Chen L, (2010) Evolution of an antifreeze protein by neofunctionalization under escape from adaptive conflict. Proc Natl Acad Sci U S A 107: 21593-21598.
51. Huang R, Hippauf F, Rohrbeck D, Haustein M, Wenke K, et al. (2012) Enzyme functional evolution through improved catalysis of ancestrally nonpreferred substrates. Proc Natl Acad Sci U S A 109: 2966-2971.
52. Sobreira TJ, Marletaz F, Simoes-Costa M, Schechtman D, Pereira AC, et al. (2011) Structural shifts of aldehyde dehydrogenase enzymes were instrumental for the early evolution of retinoid-dependent axial patterning in metazoans. Proc Natl Acad Sci U S A 108: 226-231.
53. Des Marais DL, Rausher MD, (2008) Reply to: Barkman T. and Zhang J. Nature 462: E2-E3.
54. Bridgham JT, Ortlund EA, Thornton JW, (2009) An epistatic ratchet constrains the direction of glucocorticoid receptor evolution. Nature 461: 515-519.
55. Khersonsky O, Tawfik DS, (2010) Enzyme promiscuity: a mechanistic and evolutionary perspective. Annu Rev Biochem 79: 471-505.
56. Copley SD, (2003) Enzymes with extra talents: moonlighting functions and catalytic promiscuity. Curr Opin Chem Biol 7: 265-272.
57. van Hoof A, (2005) Conserved functions of yeast genes support the duplication, degeneration and complementation model for gene duplication. Genetics 171: 1455-1461.
58. Afriat L, Roodveldt C, Manco G, Tawfik DS, (2006) The latent promiscuity of newly identified microbial lactonases is linked to a recently diverged phosphotriesterase. Biochemistry 45: 13677-13686.
59. Aharoni A, Gaidukov L, Khersonsky O, Mc QGS, Roodveldt C, et al. (2005) The 'evolvability' of promiscuous protein functions. Nat Genet 37: 73-76.
60. Bone R, Silen JL, Agard DA, (1989) Structural plasticity broadens the specificity of an engineered protease. Nature 339: 191-195.
61. Wolfe KH, Shields DC, (1997) Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387: 708-713.
62. Friis EM, Pedersen KR, Crane PR, (2005) When Earth started blooming: insights from the fossil record. Curr Opin Plant Biol 8: 5-12.
63. Abascal F, Zardoya R, Posada D, (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21: 2104-2105.
64. Nylander JA, Wilgenbusch JC, Warren DL, Swofford DL, (2008) AWTY (are we there yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics 24: 581-583.
65. Yang Z, (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586-1591.
66. Pond SL, Frost SD, Muse SV, (2005) HyPhy: hypothesis testing using phylogenies. Bioinformatics 21: 676-679.
67. Arnegard ME, Zwickl DJ, Lu Y, Zakon HH, (2010) Old gene duplication facilitates origin and diversification of an innovative communication system-twice. Proc Natl Acad Sci U S A 107: 22172-22177.
68. Yang Z, Nielsen R, (2002) Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol Biol Evol 19: 908-917.
69. Anisimova M, Yang Z, (2007) Multiple hypothesis testing to detect lineages under positive selection that affects only a few sites. Mol Biol Evol 24: 1219-1228.
70. Yang Z, Wong WS, Nielsen R, (2005) Bayes empirical bayes inference of amino acid sites under positive selection. Mol Biol Evol 22: 1107-1118.
71. Brown CA, Brown KS, (2010) Validation of coevolving residue algorithms via pipeline sensitivity analysis: ELSC and OMES and ZNMI, oh my!. PLoS One 5: e10779 doi:10.1371/journal.pone.0010779.