Revisiting the operational RNA code for amino acids: Ensemble attributes and their implications.

It has been suggested that tRNA acceptor stems specify an operational RNA code for amino acids. In the last 20 years several attributes of the putative code have been elucidated for a small number of model organisms. To gain insight about the ensemble attributes of the code, we analyzed 4925 tRNA sequences from 102 bacterial and 21 archaeal species. Here, we used a classification and regression tree (CART) methodology, and we found that the degrees of degeneracy or specificity of the RNA codes in both Archaea and Bacteria differ from those of the genetic code. We found instances of taxon-specific alternative codes, i.e., identical acceptor stem determinants encrypting different amino acids in different species, as well as instances of ambiguity, i.e., identical acceptor stem determinants encrypting two or more amino acids in the same species. When partitioning the data by class of synthetase, the degree of code ambiguity was significantly reduced. In cryptographic terms, a plausible interpretation of this result is that the class distinction in synthetases is an essential part of the decryption rules for resolving the subset of RNA code ambiguities enciphered by identical acceptor stem determinants of tRNAs acylated by enzymes belonging to the two classes. In evolutionary terms, our findings lend support to the notion that in the pre-DNA world, interactions between tRNA acceptor stems and synthetases formed the basis for the distinction between the two classes; hence, ambiguities in the ancient RNA code were pivotal for the fixation of these enzymes in the genomes of ancestral prokaryotes.

[1]  Wei-Yin Loh,et al.  Classification and regression trees , 2011, WIREs Data Mining Knowl. Discov..

[2]  S. Rodin,et al.  On the origin of the genetic code: signatures of its primordial complementarity in tRNAs and aminoacyl-tRNA synthetases , 2008, Heredity.

[3]  R. Alexander,et al.  An operational RNA code for faithful assignment of AUG triplets to methionine. , 2008, Molecular cell.

[4]  Jürgen Brosius,et al.  A novel class of mammalian-specific tailless retropseudogenes. , 2004, Genome research.

[5]  P. Schimmel,et al.  A domain for editing by an archaebacterial tRNA synthetase. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[6]  G. Björk,et al.  Enzymatic conversion of cytidine to lysidine in anticodon of bacterial tRNAIle – an alternative way of RNA editing , 2004 .

[7]  Manuel A. S. Santos,et al.  Driving change: the evolution of alternative genetic codes. , 2004, Trends in genetics : TIG.

[8]  G. Singer,et al.  Thermophilic prokaryotes have characteristic patterns of codon usage, amino acid composition and nucleotide content. , 2003, Gene.

[9]  Paul Schimmel,et al.  Elucidation of tRNA‐dependent editing by a class II tRNA synthetase and significance for cell viability , 2003, The EMBO journal.

[10]  W. McClain,et al.  Genetic perturbations of RNA reveal structure-based recognition in protein-RNA interaction. , 2002, Journal of molecular biology.

[11]  Henri Grosjean,et al.  tRNomics: analysis of tRNA genes from 50 genomes of Eukarya, Archaea, and Bacteria reveals anticodon-sparing strategies and domain-specific features. , 2002, RNA.

[12]  T. Hendrickson Recognizing the D-loop of transfer RNAs , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[13]  O. Nureki,et al.  Structural and mutational studies of the recognition of the arginine tRNA-specific major identity element, A20, by arginyl-tRNA synthetase , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[14]  P. Schimmel,et al.  Aminoacyl-tRNA synthetases: potential markers of genetic code development. , 2001, Trends in biochemical sciences.

[15]  Laura F. Landweber,et al.  How Mitochondria Redefine the Code , 2001, Journal of Molecular Evolution.

[16]  P. Schimmel,et al.  Translocation within the acceptor helix of a major tRNA identity determinant , 2001, The EMBO journal.

[17]  P. Schimmel,et al.  Operational RNA Code for Amino Acids in Relation to Genetic Code in Evolution* , 2001, The Journal of Biological Chemistry.

[18]  P. Schimmel,et al.  Two Classes of tRNA Synthetases Suggested by Sterically Compatible Dockings on tRNA Acceptor Stem , 2001, Cell.

[19]  Shigeyuki Yokoyama,et al.  Structural Basis for Double-Sieve Discrimination of L-Valine from L-Isoleucine and L-Threonine by the Complex of tRNAVal and Valyl-tRNA Synthetase , 2000, Cell.

[20]  L F Landweber,et al.  Do Proteins Predate DNA? , 1999, Science.

[21]  P. Schimmel,et al.  Atomic Determinants for Aminoacylation of RNA Minihelices and Relationship to Genetic Code , 1999 .

[22]  Manuel A. S. Santos,et al.  Selective advantages created by codon ambiguity allowed for the evolution of an alternative genetic code in Candida spp. , 1999, Molecular microbiology.

[23]  Y. Kawarabayasi,et al.  Substrate recognition by class I lysyl-tRNA synthetases: a molecular basis for gene displacement. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[24]  R Giegé,et al.  Universal rules and idiosyncratic features in tRNA identity. , 1998, Nucleic acids research.

[25]  G. Eriani,et al.  L‐Arginine recognition by yeast arginyl‐tRNA synthetase , 1998, The EMBO journal.

[26]  K. Musier-Forsyth,et al.  Species-specific differences in the operational RNA code for aminoacylation of tRNAPro. , 1998, Biochemistry.

[27]  A. Fersht Sieves in Sequence , 1998, Science.

[28]  D G Vassylyev,et al.  Enzyme structure with two catalytic sites for double-sieve selection of substrate. , 1998, Science.

[29]  W. McClain,et al.  The importance of tRNA backbone-mediated interactions with synthetase for aminoacylation. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[30]  S. Osawa,et al.  Further comments on codon reassignment. , 1997, Journal of molecular evolution.

[31]  P. Schimmel,et al.  Species-specific tRNA recognition in relation to tRNA synthetase contact residues. , 1997, Journal of molecular biology.

[32]  T Suzuki,et al.  The 'polysemous' codon--a codon with multiple amino acid assignment caused by dual specificity of tRNA identity. , 1997, The EMBO journal.

[33]  L. Mosyak,et al.  The crystal structure of phenylalanyl-tRNA synthetase from thermus thermophilus complexed with cognate tRNAPhe. , 1997, Structure.

[34]  J. Sampson,et al.  Variant minihelix RNAs reveal sequence‐specific recognition of the helical tRNA(Ser) acceptor stem by E.coli seryl‐tRNA synthetase. , 1996, The EMBO journal.

[35]  M. Yarus,et al.  On malleability in the genetic code , 1996, Journal of Molecular Evolution.

[36]  M. Giulio Was it an ancient gene codifying for a hairpin RNA that, by means of direct duplication, gave rise to the primitive tRNA molecule? , 1995 .

[37]  C. Francklyn,et al.  Crystal structure of histidyl‐tRNA synthetase from Escherichia coli complexed with histidyl‐adenylate. , 1995, The EMBO journal.

[38]  P. Schimmel,et al.  Transfer RNA: From minihelix to genetic code , 1995, Cell.

[39]  Ya-Ming Hou,et al.  Enzymatic aminoacylation of tRNA acceptor stem helices with cysteine is dependent on a single nucleotide. , 1995, Biochemistry.

[40]  P. Schimmel An operational RNA code for amino acids and variations in critical nucleotide sequences in evolution , 1995, Journal of Molecular Evolution.

[41]  O. Nureki,et al.  Molecular recognition of the identity-determinant set of isoleucine transfer RNA from Escherichia coli. , 1994, Journal of molecular biology.

[42]  W. McClain,et al.  Rules that govern tRNA identity in protein synthesis. , 1993, Journal of molecular biology.

[43]  R Giegé,et al.  An operational RNA code for amino acids and possible relationship to genetic code. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[44]  S. Martinis,et al.  Microhelix aminoacylation by a class I tRNA synthetase. Non-conserved base pairs required for specificity. , 1993, The Journal of biological chemistry.

[45]  D. Söll,et al.  Competition of aminoacyl-tRNA synthetases for tRNA ensures the accuracy of aminoacylation. , 1992, Nucleic acids research.

[46]  C. Francklyn,et al.  Enzymatic aminoacylation of an eight-base-pair microhelix with histidine. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[47]  Wen-Hsiung Li,et al.  Fundamentals of molecular evolution , 1990 .

[48]  Olivier Poch,et al.  Partition of tRNA synthetases into two classes based on mutually exclusive sets of sequence motifs , 1990, Nature.

[49]  G. Janssen,et al.  Transfer RNAs for primordial amino acids contain remnants of a primitive code at position 3 to 5. , 1990, Biochimie.

[50]  T. Steitz,et al.  Structure of E. coli glutaminyl-tRNA synthetase complexed with tRNA(Gln) and ATP at 2.8 A resolution. , 1989, Science.

[51]  Paul Schimmel,et al.  Aminoacylation of RNA minihelices with alanine , 1989, Nature.

[52]  A. Matsuda,et al.  A novel lysine-substituted nucleoside in the first position of the anticodon of minor isoleucine tRNA from Escherichia coli , 1989, Journal of Biological Chemistry.

[53]  R. Cedergren,et al.  Tandemly repeated tRNA pseudogenes in photobacterium. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[54]  S. Park,et al.  Evidence for interaction of an aminoacyl transfer RNA synthetase with a region important for the identity of its cognate transfer RNA. , 1988, The Journal of biological chemistry.

[55]  R. Root-Bernstein,et al.  On the origin of the genetic code. , 1982, Journal of theoretical biology.

[56]  J. Ebel,et al.  Incorrect aminoacylations involving tRNAs or valyl-tRNA synthetase from Bacillus stearothermophilus. , 1974, European journal of biochemistry.

[57]  D. Crothers,et al.  Is there a discriminator site in transfer RNA? , 1972, Proceedings of the National Academy of Sciences of the United States of America.

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

[59]  C. Florentz,et al.  Functional idiosyncrasies of tRNA isoacceptors in cognate and noncognate aminoacylation systems. , 2004, Biochimie.

[60]  I. Gruic‐Sovulj,et al.  The Accuracy of Seryl-tRNA Synthesis , 2002 .

[61]  O. Uhlenbeck,et al.  tRNA conformity. , 2001, Cold Spring Harbor symposia on quantitative biology.

[62]  P. Schimmel,et al.  Formation of two classes of tRNA synthetases in relation to editing functions and genetic code. , 2001, Cold Spring Harbor symposia on quantitative biology.

[63]  Dan Graur,et al.  Fundamentals of Molecular Evolution, 2nd Edition , 2000 .

[64]  K. Musier-Forsyth,et al.  Transfer RNA recognition by aminoacyl‐tRNA synthetases , 1999, Biopolymers.

[65]  M. Sherry Point Counter Point Further Comments on Codon Reassignment , 1997 .

[66]  M. Di Giulio,et al.  Was it an ancient gene codifying for a hairpin RNA that, by means of direct duplication, gave rise to the primitive tRNA molecule? , 1995, Journal of theoretical biology.

[67]  S. Martinis,et al.  Small RNA Oligonucleotide Substrates for Specific Aminoacylations , 1995 .

[68]  C. Florentz,et al.  tRNA structure and aminoacylation efficiency. , 1993, Progress in nucleic acid research and molecular biology.

[69]  Daryl Pregibon,et al.  Tree-based models , 1992 .

[70]  L. H. Schulman,et al.  Recognition of tRNAs by aminoacyl-tRNA synthetases. , 1991, Progress in nucleic acid research and molecular biology.

[71]  Freeman J. Dyson,et al.  Infinite in All Directions , 1988 .

[72]  J. Friedman,et al.  Classification and Regression Trees , 1984 .

[73]  Adi Shamir,et al.  A method for obtaining digital signatures and public-key cryptosystems , 1978, CACM.

[74]  W. Gent,et al.  Genetic codes. , 1967, Guy's Hospital reports.