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The Evolutionary Potential of Phenotypic Mutations


The rarity of genetic mutations limits the likelihood of adaptation. However, transcriptional and translational errors, so-called phenotypic mutations, are >105-fold more frequent, thus generating protein mutants from unmodified genes. We provide the first evidence that phenotypic mutations paved the path to what later, after gene duplication, became newly compartmentalized enzymes. Thus, gene duplication followed rather than initiated the divergence of this new trait. Our findings also show that translational infidelity and phenotypic variability comprise the origins of evolutionary innovations, and how selection for enhanced phenotypic variability also promotes the appearance of genetic mutations that lead to the very same outcome.


Vyšlo v časopise: The Evolutionary Potential of Phenotypic Mutations. PLoS Genet 11(8): e32767. doi:10.1371/journal.pgen.1005445
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005445

Souhrn

The rarity of genetic mutations limits the likelihood of adaptation. However, transcriptional and translational errors, so-called phenotypic mutations, are >105-fold more frequent, thus generating protein mutants from unmodified genes. We provide the first evidence that phenotypic mutations paved the path to what later, after gene duplication, became newly compartmentalized enzymes. Thus, gene duplication followed rather than initiated the divergence of this new trait. Our findings also show that translational infidelity and phenotypic variability comprise the origins of evolutionary innovations, and how selection for enhanced phenotypic variability also promotes the appearance of genetic mutations that lead to the very same outcome.


Zdroje

1. Khersonsky O, Tawfik DS (2010) Enzyme promiscuity: a mechanistic and evolutionary perspective. Annu Rev Biochem 79: 471–505. doi: 10.1146/annurev-biochem-030409-143718 20235827

2. O'Brien PJ, Herschlag D (1999) Catalytic promiscuity and the evolution of new enzymatic activities. Chem Biol 6: R91–R105. 10099128

3. Jensen RA (1976) Enzyme recruitment in evolution of new function. Annu Rev Microbiol 30: 409–425. 791073

4. Masel J, Bergman A (2003) The evolution of the evolvability properties of the yeast prion [PSI+]. Evolution 57: 1498–1512. 12940355

5. Tawfik DS (2010) Messy biology and the origins of evolutionary innovations. Nat Chem Biol 6: 692–696. doi: 10.1038/nchembio.441 20852602

6. Whitehead DJ, Wilke CO, Vernazobres D, Bornberg-Bauer E (2008) The look-ahead effect of phenotypic mutations. Biol Direct 3: 18. doi: 10.1186/1745-6150-3-18 18479505

7. Willensdorfer M, Burger R, Nowak MA (2007) Phenotypic mutation rates and the abundance of abnormal proteins in yeast. PLoS Comput Biol 3: e203. 18039025

8. Parker J (1989) Errors and alternatives in reading the universal genetic code. Microbiol Rev 53: 273–298. 2677635

9. Ellis N, Gallant J (1982) An estimate of the global error frequency in translation. Mol Gen Genet 188: 169–172. 6759868

10. Ohno S (1970) Evolution by gene duplication: Springer.

11. Piatigorsky J (2007) Gene Sharing and Evolution: The Diversity of Protein Functions. Cambridge, Massachusetts, USA; London, UK: Harvard Univ. Press.

12. 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. 10101175

13. Hughes AL (1994) The evolution of functionally novel proteins after gene duplication. Proc Biol Sci 256: 119–124. 8029240

14. Soskine M, Tawfik DS (2010) Mutational effects and the evolution of new protein functions. Nat Rev Genet 11: 572–582. doi: 10.1038/nrg2808 20634811

15. Wroe R, Chan HS, Bornberg-Bauer E (2007) A structural model of latent evolutionary potentials underlying neutral networks in proteins. Hfsp J 1: 79–87. doi: 10.2976/1.2739116/10.2976/1 19404462

16. Amitai G, Gupta RD, Tawfik DS (2007) Latent evolutionary potentials under the neutral mutational drift of an enzyme. Hfsp J 1: 67–78. doi: 10.2976/1.2739115/10.2976/1 19404461

17. Hittinger CT, Carroll SB (2007) Gene duplication and the adaptive evolution of a classic genetic switch. Nature 449: 677–681. 17928853

18. Sayou C, Monniaux M, Nanao MH, Moyroud E, Brockington SF, et al. (2014) A promiscuous intermediate underlies the evolution of LEAFY DNA binding specificity. Science 343: 645–648. doi: 10.1126/science.1248229 24436181

19. Coyle SM, Flores J, Lim WA (2013) Exploitation of latent allostery enables the evolution of new modes of MAP kinase regulation. Cell 154: 875–887. doi: 10.1016/j.cell.2013.07.019 23953117

20. Bridgham JT, Carroll SM, Thornton JW (2006) Evolution of hormone-receptor complexity by molecular exploitation. Science 312: 97–101. 16601189

21. Des Marais DL, Rausher MD (2008) Escape from adaptive conflict after duplication in an anthocyanin pathway gene. Nature 454: 762–765. doi: 10.1038/nature07092 18594508

22. Marques AC, Vinckenbosch N, Brawand D, Kaessmann H (2008) Functional diversification of duplicate genes through subcellular adaptation of encoded proteins. Genome Biol 9: R54. doi: 10.1186/gb-2008-9-3-r54 18336717

23. Conant GC, Wolfe KH (2008) Turning a hobby into a job: how duplicated genes find new functions. Nat Rev Genet 9: 938–950. doi: 10.1038/nrg2482 19015656

24. Innan H, Kondrashov F (2010) The evolution of gene duplications: classifying and distinguishing between models. Nat Rev Genet 11: 97–108. doi: 10.1038/nrg2689 20051986

25. 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. 17942681

26. Kisslov I, Naamati A, Shakarchy N, Pines O (2014) Dual-targeted proteins tend to be more evolutionarily conserved. Mol Biol Evol 31: 2770–2779. doi: 10.1093/molbev/msu221 25063438

27. Regev-Rudzki N, Pines O (2007) Eclipsed distribution: a phenomenon of dual targeting of protein and its significance. Bioessays 29: 772–782. 17621655

28. Ast J, Stiebler AC, Freitag J, Bolker M (2013) Dual targeting of peroxisomal proteins. Front Physiol 4: 297. doi: 10.3389/fphys.2013.00297 24151469

29. Williams CC, Jan CH, Weissman JS (2014) Targeting and plasticity of mitochondrial proteins revealed by proximity-specific ribosome profiling. Science 346: 748–751. doi: 10.1126/science.1257522 25378625

30. Freitag J, Ast J, Bolker M (2012) Cryptic peroxisomal targeting via alternative splicing and stop codon read-through in fungi. Nature 485: 522–525. doi: 10.1038/nature11051 22622582

31. Schueren F, Lingner T, George R, Hofhuis J, Dickel C, et al. (2015) Peroxisomal lactate dehydrogenase is generated by translational readthrough in mammals. Elife 3: e03640.

32. Byrne KP, Wolfe KH (2005) The Yeast Gene Order Browser: combining curated homology and syntenic context reveals gene fate in polyploid species. Genome Res 15: 1456–1461. 16169922

33. Ihmels J, Levy R, Barkai N (2004) Principles of transcriptional control in the metabolic network of Saccharomyces cerevisiae. Nat Biotechnol 22: 86–92. 14647306

34. Henke B, Girzalsky W, Berteaux-Lecellier V, Erdmann R (1998) IDP3 encodes a peroxisomal NADP-dependent isocitrate dehydrogenase required for the beta-oxidation of unsaturated fatty acids. J Biol Chem 273: 3702–3711. 9452501

35. Gould SJ, Keller GA, Hosken N, Wilkinson J, Subramani S (1989) A conserved tripeptide sorts proteins to peroxisomes. J Cell Biol 108: 1657–1664. 2654139

36. Brocard C, Hartig A (2006) Peroxisome targeting signal 1: is it really a simple tripeptide? Biochim Biophys Acta 1763: 1565–1573. 17007944

37. Lu Q, McAlister-Henn L (2010) Peroxisomal localization and function of NADP+-specific isocitrate dehydrogenases in yeast. Arch Biochem Biophys 493: 125–134. doi: 10.1016/j.abb.2009.10.011 19854152

38. Stiebler AC, Freitag J, Schink KO, Stehlik T, Tillmann BA, et al. (2014) Ribosomal readthrough at a short UGA stop codon context triggers dual localization of metabolic enzymes in Fungi and animals. PLoS Genet 10: e1004685. doi: 10.1371/journal.pgen.1004685 25340584

39. Rockah-Shmuel L, Toth-Petroczy A, Sela A, Wurtzel O, Sorek R, et al. (2013) Correlated occurrence and bypass of frame-shifting insertion-deletions (InDels) to give functional proteins. PLoS Genet 9: e1003882. doi: 10.1371/journal.pgen.1003882 24204297

40. Tamas I, Wernegreen JJ, Nystedt B, Kauppinen SN, Darby AC, et al. (2008) Endosymbiont gene functions impaired and rescued by polymerase infidelity at poly(A) tracts. Proc Natl Acad Sci U S A 105: 14934–14939. doi: 10.1073/pnas.0806554105 18815381

41. Wagner LA, Weiss RB, Driscoll R, Dunn DS, Gesteland RF (1990) Transcriptional slippage occurs during elongation at runs of adenine or thymine in Escherichia coli. Nucleic Acids Res 18: 3529–3535. 2194164

42. Warnecke T, Hurst LD (2011) Error prevention and mitigation as forces in the evolution of genes and genomes. Nat Rev Genet 12: 875–881. doi: 10.1038/nrg3092 22094950

43. Drummond DA, Wilke CO (2009) The evolutionary consequences of erroneous protein synthesis. Nat Rev Genet 10: 715–724. doi: 10.1038/nrg2662 19763154

44. Kunze M, Hartig A (2013) Permeability of the peroxisomal membrane: lessons from the glyoxylate cycle. Front Physiol 4: 204. doi: 10.3389/fphys.2013.00204 23966945

45. Neuberger G, Maurer-Stroh S, Eisenhaber B, Hartig A, Eisenhaber F (2003) Prediction of peroxisomal targeting signal 1 containing proteins from amino acid sequence. J Mol Biol 328: 581–592. 12706718

46. Aharoni A, Gaidukov L, Khersonsky O, Mc QGS, Roodveldt C, et al. (2005) The 'evolvability' of promiscuous protein functions. Nat Genet 37: 73–76. 15568024

47. Kondrashov FA (2005) In search of the limits of evolution. Nat Genet 37: 9–10. 15624013

48. Small I, Wintz H, Akashi K, Mireau H (1998) Two birds with one stone: genes that encode products targeted to two or more compartments. Plant Mol Biol 38: 265–277. 9738971

49. Danpure CJ (1995) How can the products of a single gene be localized to more than one intracellular compartment? Trends Cell Biol 5: 230–238. 14732127

50. Kochetov AV (2008) Alternative translation start sites and hidden coding potential of eukaryotic mRNAs. Bioessays 30: 683–691. doi: 10.1002/bies.20771 18536038

51. Chang KJ, Wang CC (2004) Translation initiation from a naturally occurring non-AUG codon in Saccharomyces cerevisiae. J Biol Chem 279: 13778–13785. 14734560

52. Rajon E, Masel J (2011) Evolution of molecular error rates and the consequences for evolvability. Proc Natl Acad Sci U S A 108: 1082–1087. doi: 10.1073/pnas.1012918108 21199946

53. True HL, Lindquist SL (2000) A yeast prion provides a mechanism for genetic variation and phenotypic diversity. Nature 407: 477–483. 11028992

54. Brachmann CB, Davies A, Cost GJ, Caputo E, Li J, et al. (1998) Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14: 115–132. 9483801

55. Wach A, Brachat A, Pohlmann R, Philippsen P (1994) New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10: 1793–1808. 7747518

56. Taxis C, Knop M (2006) System of centromeric, episomal, and integrative vectors based on drug resistance markers for Saccharomyces cerevisiae. Biotechniques 40: 73–78. 16454043

57. Miyazaki K (2003) Creating random mutagenesis libraries by megaprimer PCR of whole plasmid (MEGAWHOP). Methods Mol Biol 231: 23–28. 12824598

58. Wapinski I, Pfeffer A, Friedman N, Regev A (2007) Natural history and evolutionary principles of gene duplication in fungi. Nature 449: 54–61. 17805289

59. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792–1797. 15034147

60. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696–704. 14530136

61. Wach A, Brachat A, Alberti-Segui C, Rebischung C, Philippsen P (1997) Heterologous HIS3 marker and GFP reporter modules for PCR-targeting in Saccharomyces cerevisiae. Yeast 13: 1065–1075. 9290211

62. Rozen S, Tieri A, Ridner G, Stark AK, Schmaler T, et al. Exposing the subunit diversity within protein complexes: a mass spectrometry approach. Methods 59: 270–277. doi: 10.1016/j.ymeth.2012.12.013 23296018

63. Kimura Y, Saeki Y, Yokosawa H, Polevoda B, Sherman F, et al. (2003) N-Terminal modifications of the 19S regulatory particle subunits of the yeast proteasome. Arch Biochem Biophys 409: 341–348. 12504901

64. Huh WK, Falvo JV, Gerke LC, Carroll AS, Howson RW, et al. (2003) Global analysis of protein localization in budding yeast. Nature 425: 686–691. 14562095

65. Edelman I, Culbertson MR (1991) Exceptional codon recognition by the glutamine tRNAs in Saccharomyces cerevisiae. Embo J 10: 1481–1491. 2026145

66. Chittum HS, Lane WS, Carlson BA, Roller PP, Lung FD, et al. (1998) Rabbit beta-globin is extended beyond its UGA stop codon by multiple suppressions and translational reading gaps. Biochemistry 37: 10866–10870. 9692979

67. Rottensteiner H, Kal AJ, Filipits M, Binder M, Hamilton B, et al. (1996) Pip2p: a transcriptional regulator of peroxisome proliferation in the yeast Saccharomyces cerevisiae. Embo J 15: 2924–2934. 8670793

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