SpringerLink
Log in

Genetic Code Evolution in the RNA World and Beyond

  • Conference paper
Evolution as Computation

Part of the book series: Natural Computing Series ((NCS))

Abstract

Although the translation apparatus presumably arose in an RNA world, subsequent modifications obscure its origins. The genetic code, fixed in the Last Universal Ancestor may contain clues about the types of chemical interaction that led to early correspondences between RNA and protein. The extent to which contemporary translation reflects these primordial influences depends on the processes that have shaped the genetic code since its inception: stereochemical interaction between amino acids and RNA, historical constraints ensuring continuity between successive codes, and optimization to minimize the effects of errors caused by translation and mutation. This chapter explains how these processes, typically presented as mutually antagonistic, may actually be viewed as complementary on different timescales, and I suggest how the “first” codons could have been established in the context of an RNA world.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Similar content being viewed by others

References

  1. Szathmáry, E. & Maynard Smith, J. (1995). The major evolutionary transitions. Nature 374:227–232.

    Article  Google Scholar 

  2. Miller, S.L. (1953). Production of amino acids under possible primitive earth conditions. Science 117:528–529.

    Article  Google Scholar 

  3. Miller, S.L. (1987). Which organic compounds could have occurred on the prebiotic earth? Cold Spring Harbor Symposia on Quantitative Biology LII: 17–27.

    Article  Google Scholar 

  4. Gánti, T. (1975). Organisation of chemical reactions into dividing and metabolizing units: the chemotons. Biosystems 7:189–195.

    Article  Google Scholar 

  5. Crick, F.H.C. (1968). The origin of the genetic code. J. Mol. Biol. 38:367–379.

    Article  Google Scholar 

  6. Knight, R.D., Freeland, S.J. & Landweber, L.F. (1999). Selection, history, and chemistry: the three faces of the genetic code. TiBS, 24:241–247.

    Google Scholar 

  7. Dunnill, P. (1966). Triplet nucleotide-amino acid pairing: A stereochemical basis for the division between protein and nonprotein amino acids. Nature 210:1267–1268.

    Article  Google Scholar 

  8. Pelc, S.R. & Welton, M.G.E. (1966). Stereochemical relationship between coding triplets and amino-acids. Nature 209:868–872.

    Article  Google Scholar 

  9. Gilbert, W. (1986). The RNA world. Nature 319:618.

    Article  Google Scholar 

  10. Yarus, M. (1991). An RNA-amino acid complex and the origin of the genetic code. New Biologist 3:183–189.

    Google Scholar 

  11. Yarus, M. (1998). Amino acids as RNA ligands: A direct-RNA-template theory for the code’s origin. J. Mol. Evol. 47:109–117.

    Article  Google Scholar 

  12. Woese, C.R. (1967). The Genetic Code: The Molecular Basis for Genetic Expression. New York: Harper & Row.

    Google Scholar 

  13. Wong, J.T.-F. (1975). A co-evolution theory of the genetic code. Proc. Natl. Acad. Sci. USA 72:1909–1912.

    Article  Google Scholar 

  14. Dillon, L.S. (1975). The origins of the genetic code. The Botanical Review 39:301–345.

    Article  Google Scholar 

  15. Miseta, A. (1989). The role of protein associated amino acid precursor molecules in the organization of genetic codons. Physiol. Chem. Phys. Med. NMR 21:237–242.

    Google Scholar 

  16. Taylor, F.J.R. & Coates, D. (1989). The code within the codons. Biosystems 22:177–187.

    Article  Google Scholar 

  17. Di Giulio, M. (1989). Some aspects of the organization and evolution of the genetic code. J. Mol. Evol. 29:191–201.

    Article  Google Scholar 

  18. Di Giulio, M. (1998). The historical factor: the biosynthetic relationships between amino acids and their physiochemical properties in the origin of the genetic code. J. Mol. Evol. 46:615–621.

    Article  Google Scholar 

  19. Sonneborn, T.M. (1965). Degeneracy of the genetic code: extent, nature, and genetic implications. In Evolving Genes and Proteins, V. Bryson and H.J. Vogel, eds. New York: Academic Press, pp. 377–297.

    Google Scholar 

  20. Zuckerkandl, E. & Pauling, L. (1965). Evolutionary divergence and convergence in proteins. In Evolving Genes and Proteins, V. Bryson and H.J. Vogel, eds. New York: Academic Press.

    Google Scholar 

  21. Ardell, D.H. (1998). On error minimization in a sequential origin of the standard genetic code. J. Mol. Evol. 47:1–13.

    Article  Google Scholar 

  22. Haig, D. & Hurst, L.D. (1991). A quantitative measure of error minimization in the genetic code. J. Mol. Evol. 33:412–417.

    Article  Google Scholar 

  23. Freeland, S.J. & Hurst, L.D. (1998). The genetic code is one in a million. J. Mol. Evol. 47:238–48.

    Article  Google Scholar 

  24. Freeland, S.J. & Hurst, L.D. (1998). Load minimization of the code: history does not explain the pattern. Proc. Roy. Soc. Lond. B 265:1–9.

    Article  Google Scholar 

  25. Ring, D., Wolman, Y., Friedmann, N. & Miller, S.L. (1972). Prebiotic synthesis of hydrophobic and protein amino acids. Proc. Natl. Acad. Sci. USA 69:765–768.

    Article  Google Scholar 

  26. Wolman, Y., Haverland, W.J. & Miller, S.L. (1972). Nonprotein amino acids from spark discharges and their comparison with the Murchison meteorite amino acids. Proc. Natl. Acad. Sci. USA 69:809–811.

    Article  Google Scholar 

  27. Weber, A.L. & Miller, S.L. (1981). Reasons for the occurrence of the twenty coded protein amino acids. J. Mol. Evol. 17:273–284.

    Article  Google Scholar 

  28. Kvenvolden, K., Lawless, J.G., et al. (1970). Evidence for extraterrestrial amino-acids and hydrocarbons in the Murchison meteorite. Nature 228:923–926.

    Article  Google Scholar 

  29. Kvenvolden, K.A., Lawless, J.G. & Ponnamperuma, C. (1971). Nonprotein amino acids in the Murchison meteorite. Proc. Natl. Acad. Sci. USA 68:486–490.

    Article  Google Scholar 

  30. Crothers, D.M. (1982). Nucleic acid aggregation geometry and the possible evolutionary origin of ribosomes and the genetic code. J. Mol. Biol. 162:379–391.

    Article  Google Scholar 

  31. Trifonov, E. & Bettecken, T. (1997). Sequence fossils, triplet expansion, and reconstruction of earliest codons. GENE 205:1–6.

    Article  Google Scholar 

  32. Lehmann, U. (1985). Chromatographic separation as selection process for prebiotic evolution and the origin of the genetic code. Biosystems 17:193–208.

    Article  Google Scholar 

  33. Nagyvary, J. & Fendler, J.H. (1974). Origin of the genetic code: a physical-chemical model of primitive codon assignments. Orig. Life 5:357–362.

    Google Scholar 

  34. Woese, C.R., Dugre, D.H., Dugre, S.A., Kondo, M. & Saxinger, W.C. (1966). On the fundamental nature and evolution of the genetic code. Cold Spring Harb. Symp. Quant. Biol. 31:723–736.

    Article  Google Scholar 

  35. Woese, C.R., Dugre, D.H., Saxinger, W.C. & Dugre, S.A. (1966). The molecular basis for the genetic code. Proc. Natl. Acad. Sci. USA 55:966–974.

    Article  Google Scholar 

  36. Weber, A.L. & Lacey, J.C., Jr. (1978). Genetic code correlations: amino acids and their anticodon nucleotides. J. Mol. Evol. 11:199–210.

    Article  Google Scholar 

  37. Jungck, J.R. (1978). The genetic code as a periodic table. J. Mol. Evol. 11:211–224.

    Article  Google Scholar 

  38. Lacey, J.C., Jr. & Pruitt, K.M. (1969). Origin of the genetic code. Nature 223:799–804.

    Article  Google Scholar 

  39. Saxinger, C. & Ponnamperuma, C. (1971). Experimental investigation on the origin of the genetic code. J. Mol. Evol. 1:63–73.

    Article  Google Scholar 

  40. Raszka, M. & Mandel, M. (1972). Is there a physical chemical basis for the present genetic code? J. Mol. Evol. 2:38–43.

    Article  Google Scholar 

  41. Saxinger, C. & Ponnamperuma, C. (1974). Interactions between amino acids and nucleotides in the prebiotic milieu. Orig. Life 5:189–200.

    Article  Google Scholar 

  42. Lacey, J.C., Jr., Weber, A.L. & White, W.E., Jr. (1975). A model for the coevolution of the genetic code and the process of protein synthesis: review and assessment. Orig. Life 6:273–283.

    Article  Google Scholar 

  43. Reuben, J. & Polk, F.E. (1980). Nucleotide-amino acid interactions and their relation to the genetic code. J. Mol. Evol. 15:103–112.

    Article  Google Scholar 

  44. Podder, S.K. & Basu, H.S. (1984). Specificity of protein-nucleic acid interaction and the biochemical evolution. Orig. Life 14:477–484.

    Article  Google Scholar 

  45. Porschke, D. (1985). Differential effect of amino acid residues on the stability of double helices formed from polyribonucleotides and its possible relation to the evolution of the genetic code. J. Mol. Evol. 21:192–198.

    Article  Google Scholar 

  46. Lacey, J.C., Jr., Wickramasinghe, N.S.M.D., Cook, G.W. & Anderson, G. (1993). Couplings of character and of chirality in the origin of the genetic system. J. Mol. Evol. 37:233–239.

    Article  Google Scholar 

  47. Lacey, J.C., Jr. & Mullins, D.W., Jr. (1983). Experimental studies related to the origin of the genetic code and the process of protein synthesis—a review. Orig. Life 13:3–42.

    Article  Google Scholar 

  48. Lacey, J.C., Jr. (1992). Experimental studies on the origin of the genetic code and the process of protein synthesis: a review update. Orig. Life Evol. Biosph. 22:243–275.

    Article  Google Scholar 

  49. Szathmary, E. (1993). Coding coenzyme handles: a hypothesis for the origin of the genetic code. Proc. Natl. Acad. Sci. USA 90:9916–9920.

    Article  Google Scholar 

  50. Maizels, N. & Weiner, A.M. (1987). Peptide-specific ribosomes, genomic tags, and the origin of the genetic code. Cold Spring Harbor Symp. Quant. Biol. LII:743–749.

    Article  Google Scholar 

  51. Maizels, N. & Weiner, A.M. (1993). The genomic tag hypothesis: modern viruses as molecular fossils of ancient strategies for genomic replication. In The RNA World, R.F. Gesteland and J.F. Atkins, eds. New York: Cold Spring Harbor Laboratory Press, pp. 577–602.

    Google Scholar 

  52. Ralph, R.K. (1968). A suggestion on the origin of the genetic code. Biochem. Biophys. Res. Comm. 33:213–218.

    Article  Google Scholar 

  53. Hopfield, J.J. (1978). Origin of the genetic code: a testable hypothesis based on tRNA structure, sequence, and kinetic proofreading. Proc. Natl. Acad. Sci. USA 75:4334–4338.

    Article  Google Scholar 

  54. Root-Bernstein, R.S. (1982). Amino acid pairing. J. Theor. Bio. 94:885–894.

    Article  MathSciNet  Google Scholar 

  55. Root-Bernstein, R.S. (1982). On the origin of the genetic code. J. Theor. Bio. 94:895–904.

    Article  MathSciNet  Google Scholar 

  56. Shimizu, M. (1982). Molecular basis for the genetic code. J. Mol. Evol. 18:297–303.

    Article  MathSciNet  Google Scholar 

  57. Hendry, L.B. & Whitham, F.H. (1979). Stereochemical recognition in nucleic acid-amino acid interactions and its implications in biological coding: a model approach. Perspect. Biol. Med. 22:333–345.

    Google Scholar 

  58. Alberti, S. (1997). The origin of the genetic code and protein synthesis. J. Mol. Evol. 45:352–358.

    Article  Google Scholar 

  59. Keeling, P.J. & Doolittle, W.F. (1997). Widespread and ancient distribution of a noncanonical genetic code in diplomonads. Mol. Biol. Evol. 14(9):895–901.

    Article  Google Scholar 

  60. Lagerkvist, U. (1978). “Two out of three”: an alternative method for codon reading. Proc. Natl. Acad. Sci. USA 75:1759–1762.

    Article  Google Scholar 

  61. Lagerkvist, U. (1980). Codon misreading: a restriction operative in the evolution of the genetic code. American Scientist 68:192–198.

    Google Scholar 

  62. Knight, R.D. & Landweber, L.F. (1998). Rhyme or reason: RNA-arginine interactions and the genetic code. Chem. Biol. 5(9):R215–20.

    Article  Google Scholar 

  63. Ellington, A.D. & Szostak, J.W. (1990). In vitro selection of RNA molecules that bind specific ligands. Nature 346:818–822.

    Article  Google Scholar 

  64. Robertson, D.L. & Joyce, G.F. (1990). Selection in vitro of an RNA enzyme that specifically cleaves single-stranded DNA. Nature 344:467–468.

    Article  Google Scholar 

  65. Tuerk, C. & Gold, L. (1990). Systematic evolution of ligands by exponential enrichment: RNA ligands to bacteriophage T4 DNA polymerase. Science 249:505–510.

    Article  Google Scholar 

  66. Landweber, L.F., Simon, P.J. & Wagner, T.A. (1998). Ribozyme engineering and early evolution. BioScience 48:94–103.

    Article  Google Scholar 

  67. Famulok, M. & Szostak, J.W. (1992). Stereospecific recognition of tryptophan agarose by in vitro selected RNA. J. Am. Chem. Soc. 114:3990–3991.

    Article  Google Scholar 

  68. Majerfeld, I. & Yarus, M. (1994). An RNA pocket for an aliphatic hydrophobe. Nature Struct. Biol. 1:287–292.

    Article  Google Scholar 

  69. Zinnen, S. & Yarus, M. (1995). An RNA pocket for the planar aromatic side chains of phenylalanine and tryptophane. Nucleic Acids Symp. Ser. 33:148–151.

    Google Scholar 

  70. Famulok, M. (1994). Molecular recognition of amino acids by RNA-aptamers: an L-citrulline binding RNA motif and its evolution into an L-arginine binder. J. Am. Chem. Soc. 116:1698–1706.

    Article  Google Scholar 

  71. Majerfeld, I. & Yarus, M. (1998). Isoleucine: RNA sites with essential coding sequences. RNA 4:471–478.

    Google Scholar 

  72. Burgstaller, P., Kochoyan, M. & Famulok, M. (1995). Structural probing and damage selection of citrulline- and arginine-specific RNA aptamers identify base positions required for binding. Nucleic Acids Res. 23:4769–4776.

    Article  Google Scholar 

  73. Connell, G.J., Illangsekare, M. & Yarus, M. (1993). Three small ribooligonucleotides with specific arginine sites. Biochemistry 32:5497–5502.

    Article  Google Scholar 

  74. Connell, G.J. & Yarus, M. (1994). RNAs with dual specificity and dual RNAs with similar specificity. Science 264:1137–1141.

    Article  Google Scholar 

  75. Tao, J. & Frankel, A.D. (1996). Arginine-binding RNAs resembling TAR identified by in vitro selection. Biochemistry 35:2229–2238.

    Article  Google Scholar 

  76. Yang, Y., Kochoyan, M., Burgstaller, P., Westhof, E. & Famulok, F. (1996). Structural basis of ligand discrimination by two related RNA aptamers resolved by NMR spectroscopy. Science 272:1343–1346.

    Article  Google Scholar 

  77. Tao, J. & Frankel, A. (1992). Specific binding of arginine to TAR RNA. Proc. Natl. Acad. Sci. 89:2723–2726.

    Article  Google Scholar 

  78. Yarus, M. (1989). Specificity of arginine binding by the tetrahymena intron. Biochemistry 28:980–988.

    Article  Google Scholar 

  79. Maizels, N. & Weiner, A.M. (1994). Phylogeny from function: Evidence from the molecular fossil record that tRNA originated in replication, not translation. Proc. Natl. Acad. Sci. USA 91:6729–6734.

    Article  Google Scholar 

  80. Jay, D.G. & Gilbert, W. (1987). Basic protein enhances the incorporation of DNA into lipid vesicles: model for the formation of primordial cells. Proc. Natl. Acad. Sci. USA 84:1978–1980.

    Article  Google Scholar 

  81. Herschlag, D., Khosla, M., Tsuchihashi, Z. & Karpel, R.L. (1994). An RNA chaperone activity of non-specific RNA binding proteins in hammerhead ribozyme catalysis. Embo J. 13:2913–24.

    Google Scholar 

  82. Alff-Steinberger, C. (1969). The genetic code and error transmission. Proc. Natl. Acad. Sci. USA 64:584–591.

    Article  Google Scholar 

  83. Osawa, S. (1995). Evolution of the Genetic Code. Oxford: Oxford University Press.

    Google Scholar 

  84. Tourancheau, A.B., Tsao, N., Klobutcher, L.A., Pearlman, R.E. & Adoutte, A. (1995). Genetic code deviations in the ciliates: evidence for multiple and independent events. EMBO J. 14:3262–3267.

    Google Scholar 

  85. Hayashi-Ishimaru, Y., Ehara, M., Inagaki, Y. & Ohama, T. (1997). A deviant mitochondrial genetic code in prymnesiophytes (yellow-algae): UGA codon for tryptophan. Curr. Genet. 32:296–299.

    Article  Google Scholar 

  86. Hayashi-Ishimaru, Y., Ohama, T., Kawatsu, Y., Nakamura, K. & Osawa, S. (1996). UAG is a sense codon in several chlorophyceas mitochondria. Curr. Genet. 30:29–33.

    Article  Google Scholar 

  87. Knight, R.D. & Landweber, L.F. (2000). Guilt by Association: The Arginine Case Revisited. RNA. 6:499–510.

    Article  Google Scholar 

  88. Knight, R.D., Freeland, S.J. & Landweber, L.F. (2001). Rewiring the Keyboard: Evolvability of the Genetic Code. Nature Reviews Genetics. 2:49–58.

    Article  Google Scholar 

Download references

Authors
  1. Robin D. Knight
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ, 08544, USA

    Laura F. Landweber

  2. Computer Science and Computation and Neural Systems, Caltech, Pasadena, CA, 91125, USA

    Erik Winfree

Rights and permissions

Reprints and permissions

Copyright information

© 2002 Springer-Verlag Berlin Heidelberg

About this paper

Cite this paper

Knight, R.D. (2002). Genetic Code Evolution in the RNA World and Beyond. In: Landweber, L.F., Winfree, E. (eds) Evolution as Computation. Natural Computing Series. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-55606-7_8

Download citation

  • DOI: https://doi.org/10.1007/978-3-642-55606-7_8

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-63081-1

  • Online ISBN: 978-3-642-55606-7

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation