The Coevolution of Genes and Genetic Codes: Crick’s Frozen Accident Revisited

The standard genetic code is the nearly universal system for the translation of genes into proteins. The code exhibits two salient structural characteristics: it possesses a distinct organization that makes it extremely robust to errors in replication and translation, and it is highly redundant. The origin of these properties has intrigued researchers since the code was first discovered. One suggestion, which is the subject of this review, is that the code’s organization is the outcome of the coevolution of genes and genetic codes. In 1968, Francis Crick explored the possible implications of coevolution at different stages of code evolution. Although he argues that coevolution was likely to influence the evolution of the code, he concludes that it falls short of explaining the organization of the code we see today. The recent application of mathematical modeling to study the effects of errors on the course of coevolution, suggests a different conclusion. It shows that coevolution readily generates genetic codes that are highly redundant and similar in their error-correcting organization to the standard code. We review this recent work and suggest that further affirmation of the role of coevolution can be attained by investigating the extent to which the outcome of coevolution is robust to other influences that were present during the evolution of the code.

[1]  D. Payne Posttranslational Modification of Proteins by ADP-ribosylation , 1984 .

[2]  J. Wong,et al.  Coevolution theory of the genetic code at age thirty. , 2005, BioEssays : news and reviews in molecular, cellular and developmental biology.

[3]  D. Petrov,et al.  Patterns of nucleotide substitution in Drosophila and mammalian genomes. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[4]  M. Hecht,et al.  Binary patterning of polar and nonpolar amino acids in the sequences and structures of native proteins , 1995, Protein science : a publication of the Protein Society.

[5]  S. Freeland,et al.  The Case for an Error Minimizing Standard Genetic Code , 2003, Origins of life and evolution of the biosphere.

[6]  F. Crick Origin of the Genetic Code , 1967, Nature.

[7]  C. Alff-Steinberger,et al.  The genetic code and error transmission. , 1969, Proceedings of the National Academy of Sciences of the United States of America.

[8]  C. Francklyn,et al.  Aminoacyl-tRNA synthetases: versatile players in the changing theater of translation. , 2002, RNA.

[9]  E. Freese Transitions and transversions induced by depurinating agents. , 1961, Proceedings of the National Academy of Sciences of the United States of America.

[10]  K. Hawkes,et al.  African populations and the evolution of human mitochondrial DNA. , 1991, Science.

[11]  W. Brown,et al.  A comparison of the small ribosomal RNA genes from the mitochondrial DNA of the great apes and humans: sequence, structure, evolution, and phylogenetic implications. , 1986, Molecular biology and evolution.

[12]  Laurence D. Hurst,et al.  A quantitative measure of error minimization in the genetic code , 1991, Journal of Molecular Evolution.

[13]  W. Gilbert,et al.  STREPTOMYCIN, SUPPRESSION, AND THE CODE. , 1964, Proceedings of the National Academy of Sciences of the United States of America.

[14]  The coevolution theory of the origin of the genetic code , 2004 .

[15]  R. Krishna,et al.  Post-translational modification of proteins. , 1993, Advances in enzymology and related areas of molecular biology.

[16]  S. Osawa,et al.  Recent evidence for evolution of the genetic code , 1992, Microbiological reviews.

[17]  T. Jukes,et al.  Arginine as an evolutionary intruder into protein synthesis. , 1973, Biochemical and biophysical research communications.

[18]  W. Fitch An improved method of testing for evolutionary homology. , 1966, Journal of molecular biology.

[19]  L. H. Bradley,et al.  Protein design by binary patterning of polar and nonpolar amino acids. , 1993, Methods in molecular biology.

[20]  M. Eigen,et al.  The Hypercycle: A principle of natural self-organization , 2009 .

[21]  G. Sella,et al.  The Impact of Message Mutation on the Fitness of a Genetic Code , 2002, Journal of Molecular Evolution.

[22]  C. Kannicht Posttranslational Modification of Proteins , 2002 .

[23]  M. D. Topal,et al.  Complementary base pairing and the origin of substitution mutations , 1976, Nature.

[24]  C. Woese The universal ancestor. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[25]  L F Landweber,et al.  Guilt by association: the arginine case revisited. , 2000, RNA.

[26]  S. Pestka,et al.  On the Coding of Genetic Information , 1963 .

[27]  J. Wakeley,et al.  The excess of transitions among nucleotide substitutions: new methods of estimating transition bias underscore its significance. , 1996, Trends in ecology & evolution.

[28]  L. Hurst,et al.  The Genetic Code Is One in a Million , 1998, Journal of Molecular Evolution.

[29]  L F Landweber,et al.  Selection, history and chemistry: the three faces of the genetic code. , 1999, Trends in biochemical sciences.

[30]  T. M. Sonneborn Degeneracy of the Genetic Code: Extent, Nature, and Genetic Implications , 1965 .

[31]  D. Sankoff,et al.  Evolution of 5S RNA and the non-randomness of base replacement. , 1973, Nature: New biology.

[32]  Guy Sella,et al.  On the Evolution of Redundancy in Genetic Codes , 2001, Journal of Molecular Evolution.

[33]  W. Fitch Evidence suggesting a partial, internal duplication in the ancestral gene for heme-containing globins. , 1966, Journal of molecular biology.

[34]  The phylogeny of trnas seems to confirm the predictions of the coevolution theory of the origin of the genetic code , 1995, Origins of life and evolution of the biosphere.

[35]  A. Goldberg,et al.  Genetic Code: Aspects of Organization , 1966, Science.

[36]  C. Woese,et al.  Evolution of the genetic code , 2004, The Science of Nature.

[37]  Takashi Gojobori,et al.  Patterns of nucleotide substitution in pseudogenes and functional genes , 2005, Journal of Molecular Evolution.

[38]  M Yarus,et al.  RNA-ligand chemistry: a testable source for the genetic code. , 2000, RNA.

[39]  C. Woese,et al.  On the fundamental nature and evolution of the genetic code. , 1966, Cold Spring Harbor symposia on quantitative biology.

[40]  P. Marlière,et al.  Reassigning cysteine in the genetic code of Escherichia coli. , 1998, Genetics.

[41]  David H. Ardell,et al.  On Error Minimization in a Sequential Origin of the Standard Genetic Code , 1998, Journal of Molecular Evolution.

[42]  H. Khorana,et al.  A further study of misreading of codons induced by streptomycin and neomycin using ribopolynucleotides containing two nucleotides in alternating sequence as templates. , 1966, Journal of molecular biology.

[43]  L. I. Woolf The Genetic Code. The Molecular Basis for Genetic Expression , 1968 .

[44]  J. Parker,et al.  Errors and alternatives in reading the universal genetic code. , 1989, Microbiological reviews.

[45]  S. Louda Differential predation pressure: A general mechanism for structuring plant communities along complex environmental gradients? , 1989 .

[46]  W. Fitch,et al.  The phylogeny of tRNA sequences provides evidence for ambiguity reduction in the origin of the genetic code. , 1987, Cold Spring Harbor symposia on quantitative biology.

[47]  Stephen J. Freeland,et al.  The Darwinian Genetic Code: An Adaptation for Adapting? , 2002, Genetic Programming and Evolvable Machines.

[48]  V. Bryson,et al.  Evolving Genes and Proteins. , 1965, Science.

[49]  F. Taylor,et al.  The code within the codons. , 1989, Bio Systems.

[50]  J. Wong A co-evolution theory of the genetic code. , 1975, Proceedings of the National Academy of Sciences of the United States of America.

[51]  Guy Sella,et al.  No accident: genetic codes freeze in error-correcting patterns of the standard genetic code. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[52]  L. Pauling,et al.  Evolutionary Divergence and Convergence in Proteins , 1965 .

[53]  R. Swanson A unifying concept for the amino acid code. , 1984, Bulletin of mathematical biology.

[54]  J. Wong,et al.  Transfer RNA paralogs: evidence for genetic code-amino acid biosynthesis coevolution and an archaeal root of life. , 2003, Gene.

[55]  F. H. C. CRICK,et al.  Origin of the Genetic Code , 1967, Nature.

[56]  J. Wong,et al.  Role of minimization of chemical distances between amino acids in the evolution of the genetic code. , 1980, Proceedings of the National Academy of Sciences of the United States of America.