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Journal of Molecular Evolution

, Volume 77, Issue 4, pp 185–196 | Cite as

The Protein Invasion: A Broad Review on the Origin of the Translational System

  • David W. MorgensEmail author
Review

Abstract

Translation, coded peptide synthesis, arguably exists at the heart of modern cellular life. By orchestrating an incredibly complex interaction between tRNAs, mRNAs, aaRSs, the ribosome, and numerous other small molecules, the translational system allows the interpretation of data in the form of DNA to create massively complex proteins which control and enact almost every cellular function. A natural question then, is how did this system evolve? Here we present a broad review of the existing theories of the last two decades on the origin of the translational system. We attempt to synthesize the wide variety of ideas as well as organize them into modular components, addressing the evolution of the peptide-RNA interaction, tRNA, mRNA, the ribosome, and the first proteins separately. We hope to provide both a comprehensive overview of the literature as well as a framework for future discussions and novel theories.

Keywords

RNA world Origin of translation Origin of the ribosome tRNA evolution 

Notes

Acknowledgments

We are grateful to Andre R. O. Cavalcanti for his support, advice, and critical reading of the manuscript.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Achenbach J, Nierhaus KH (2013) Translocation at work. Nat Struct Mol Biol 20:1019–1022CrossRefGoogle Scholar
  2. Baranov PV, Venin M, Provan G (2009) Codon size reduction as the origin of the triplet genetic code. PLoS ONE 4:e5708. doi: 10.1371/journal.pone.0005708 CrossRefGoogle Scholar
  3. Bernhardt HS (2012) The RNA world hypothesis: the worst theory of the early evolution of life (except for all the others). Biol Direct 7:23CrossRefGoogle Scholar
  4. Bernhardt HS, Tate WP (2010) The transition from noncoded to coded protein synthesis: did coding mRNAs arise from stability-enhancing binding partners to tRNA? Biol Direct 5:16. doi: 10.1186/1745-6150-5-16 CrossRefGoogle Scholar
  5. Bokov K, Sergey V, Steinberg SV (2009) A hierarchical model for evolution of 23S ribosomal RNA. Nature 457:977–980CrossRefGoogle Scholar
  6. Brosius J (1999) Transmutation of tRNA over time. Nat Genet 22(1):8–9CrossRefGoogle Scholar
  7. Brosius J (2001) tRNAs in the spotlight during protein biosynthesis. Trends Biochem Sci 26:653–656. doi: 10.1016/S0968-0004(01)01972-7 CrossRefGoogle Scholar
  8. Cairns-Smith AG (1974) The Methods of Science and the Origins of Life. In: Dose K, Dose K (eds) The Origin of Life and Evolutionary Biochemistry., pp 53–58CrossRefGoogle Scholar
  9. Campbell JH (1991) RNA replisome as the ancestor of the ribosome. J Mol Evol 32(1):3–5CrossRefGoogle Scholar
  10. Crick FH, Brenner S, Klug A, Pieczenik G (1976) A speculation on the origin of protein synthesis. Orig Life 7:389–397. doi: 10.1007/BF00927934 CrossRefGoogle Scholar
  11. Di Giulio M (1997) On the RNA world: evidence in favor of an early ribonucleopeptide world. J Mol Evol 45:571–578CrossRefGoogle Scholar
  12. Di Giulio M (2003) The early phases of genetic code origin: conjectures on the evolution of coded catalysis. Orig Life Evol Biosph 33:479–489CrossRefGoogle Scholar
  13. Di Giulio M (2004) The origin of the tRNA molecule: implications for the origin of protein synthesis. J Theor Biol 226:89–93. doi: 10.1016/j.jtbi.2003.07.001 CrossRefGoogle Scholar
  14. Di Giulio M (2008) Why the genetic code originated: implications for the origin of protein synthesis. the codes of life. Biosemiotics 1:59–67CrossRefGoogle Scholar
  15. Di Giulio M (2009) A comparison among the models proposed to explain the origin of the tRNA molecule: a synthesis. J Mol Evol 69:1–9CrossRefGoogle Scholar
  16. Eigen M, Winkler-Oswatitsch R (1981) Transfer-RNA, an early gene? Naturwissenschaften 68:282–292CrossRefGoogle Scholar
  17. Fox GE (2010) Origin and evolution of the ribosome. Cold Spring Harb Perspect Biol 2(9):a003483. doi: 10.1101/cshperspect.a003483 ReviewCrossRefGoogle Scholar
  18. Gibson TJ, Lamond AI (1990) Metabolic complexity in the RNA world and implications for the origin of protein synthesis. J Mol Evol 31:7–15CrossRefGoogle Scholar
  19. Gordon KH (1995) Were RNA replication and translation directly coupled in the RNA (+protein?) World? J Theor Biol 173(2):179–193CrossRefGoogle Scholar
  20. Knight RD, Landweber LF (2000) Guilt by association: the arginine case revisited. RNA 6:499–510. doi: 10.1017/S1355838200000145 CrossRefGoogle Scholar
  21. Koonin EV (2007) The cosmological model of eternal inflation and the transition from chance to biological evolution in the history of life. Biol Direct 2:15. doi: 10.1186/1745-6150-2-15 CrossRefGoogle Scholar
  22. Krupkin M, Matzov D, Tang H, Metz M, Kalaora R, Kalaora R, Belousoff MJ, Zimmerman E, Bashan A, Yonath A (2011) A vestige of a prebiotic bonding machine is functioning within the contemporary ribosome. Philos Trans R SocLond B BiolSci. doi: 10.1098/rstb.2011.0146 CrossRefGoogle Scholar
  23. Ma W (2010) The scenario on the origin of translation in the RNA world: in principle of replication parsimony. Biol Direct 5:65CrossRefGoogle Scholar
  24. Maizels N, Weiner AM (1994) Phylogeny from function: Evidence from the molecular fossil record that tRNA originated in replication, not translation. Proc Natl Acad Sci USA 91:156729–156734CrossRefGoogle Scholar
  25. Milner-White EJ, Russell MJ (2008) Predicting the conformations of peptides and proteins in early evolution. A review article submitted to biology direct. Biol Direct 3:3. doi: 10.1186/1745-6150-3-3 ReviewCrossRefGoogle Scholar
  26. Noller HF (2004) The driving force for molecular evolution of translation. RNA 10:1833–1837CrossRefGoogle Scholar
  27. Noller HF (2010) Evolution of protein synthesis from an RNA world. Cold Spring Harb Perspect Biol 7:7Google Scholar
  28. Orgel LE (1989) The origin of polynucleotide-directed protein synthesis. J Mol Evol 29:465–474CrossRefGoogle Scholar
  29. Penny D (2005) An interpretive review of the origin of life research. Philos Biol 20:633–671. doi: 10.1007/s10539-004-7342-6 CrossRefGoogle Scholar
  30. Penny D, Hoeppner MP, Poole AM, Jeffares DC (2009) An overview of the introns-first theory. J Mol Evol 13(5):527–540CrossRefGoogle Scholar
  31. Poole AM, Jeffares DC, Penny D (1998) The path from the RNA world. J Mol Evol 46:1–17. doi: 10.1007/PL00006275 CrossRefGoogle Scholar
  32. Rodin AS, Szathmáry E, Rodin SN (2011) On origin of genetic code and tRNA before translation. Biol Direct 6:14CrossRefGoogle Scholar
  33. Roth A, Breaker RR (1998) An amino acid as a cofactor for a catalytic polynucleotide. Proc Natl Acad Sci USA 95(11):6027–6031CrossRefGoogle Scholar
  34. Schimmel P, Henderson B (1994) Possible role of aminoacyl-RNA complexes in noncoded peptide synthesis and origin of coded synthesis. Proc Natl Acad Sci USA 91(24):11283–11286CrossRefGoogle Scholar
  35. Szathmary E (1993) Coding coenzyme handles: a hypothesis for the origin of the genetic code. Proc Natl Acad Sci USA 90:9916–9920. doi: 10.1073/pnas.90.21.9916 CrossRefGoogle Scholar
  36. Szathmary E (1999) The origin of the genetic code: amino acids as cofactors in an RNA world. Trends Genet 15:223–229. doi: 10.1016/S0168-9525(99)01730-8 CrossRefGoogle Scholar
  37. Szathmary E, Maynard Smith J (1997) From replicators to reproducers: the first major transitions leading to life. J Theor Biol 187:555–571. doi: 10.1006/jtbi.1996.0389 CrossRefGoogle Scholar
  38. Voordeckers K, Brown CA, Vanneste K, van der Zande E, Voet A et al (2012) Reconstruction of ancestral metabolic enzymes reveals molecular mechanisms underlying evolutionary innovation through gene duplication. PLoS Biol 10(12):e1001446. doi: 10.1371/journal.pbio.1001446 CrossRefGoogle Scholar
  39. Weiner AM, Maizels N (1987) 3′ terminal tRNA-like structures tag genomic RNA molecules for replication: implications for the origin of protein synthesis. Proc Natl Acad Sci USA 84:7383–7387. doi: 10.1073/pnas.84.21.7383 CrossRefGoogle Scholar
  40. Weiner AM, Maizels N (1999) The genomic tag hypothesis: modern viruses as molecular fossils of ancient strategies for genomic replication, and clues regarding the origin of protein synthesis. Biol Bull 196:327–328. doi: 10.2307/1542962 CrossRefGoogle Scholar
  41. Wetzel R (1995) Evolution of the aminoacyl-trna synthetases and the origin of the genetic code. J Mol Evol 40(5):545–550CrossRefGoogle Scholar
  42. White HB (1976) Coenzymes as fossils of an earlier metabolic state. J Mol Evol 7:101–104CrossRefGoogle Scholar
  43. White HB (1982) Evolution of Coenzymes and the Origin of Pyridine Nucleotides. In: Everse J, Anderson B, You KS (eds) The Pyridine Nucleotide Coenzymes. Academic Press, New York, pp 1–17Google Scholar
  44. Wolf YI, Koonin EV (2007) On the origin of the translation system and the genetic code in the RNA world by means of natural selection, exaptation, and subfunctionalization. Biology Direct; 2(14)Google Scholar
  45. Wong JT (1991) Origin of genetically encoded protein synthesis a model based on selection for RNA peptidation. Orig Life Evol Biosph 21:165–176CrossRefGoogle Scholar
  46. Yakhnin AV (2007) A model for the origin of protein synthesis as coreplicational scanning of nascent RNA. Orig Life Evol Biosph 37:523–536. doi: 10.1007/s11084-007-9108-z CrossRefGoogle Scholar
  47. Yarus M (1998) Amino acids as RNA ligands: a direct-RNA-template theory for the code’s origin. J Mol Evol 47:109–117. doi: 10.1007/PL00006357 CrossRefGoogle Scholar
  48. Yarus M, Widmann JJ, Knight R (2009) RNA-amino acid binding: a stereochemical era for the genetic code. J Mol Evol 69:406–429. doi: 10.1007/s00239-009-9270-1 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Biology DepartmentPomona CollegeClaremontUSA

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