tRNA anticodon shifts in eukaryotic genomes

Embedded in the sequence of each transfer RNA are elements that promote specific interactions with its cognate aminoacyl tRNA-synthetase. Although many such "identity elements" are known, their detection is difficult since they rely on unique structural signatures and the combinatorial action of multiple elements spread throughout the tRNA molecule. Since the anticodon is often a major identity determinant itself, it is possible to switch between certain tRNA functional types by means of anticodon substitutions. This has been shown to have occurred during the evolution of some genomes; however, the scale and relevance of "anticodon shifts" to the evolution of the tRNA multigene family is unclear. Using a synteny-conservation-based method, we detected tRNA anticodon shifts in groups of closely related species: five primates, 12 Drosophila, six nematodes, 11 Saccharomycetes, and 61 Enterobacteriaceae. We found a total of 75 anticodon shifts: 31 involving switches of identity (alloacceptor shifts) and 44 between isoacceptors that code for the same amino acid (isoacceptor shifts). The relative numbers of shifts in each taxa suggest that tRNA gene redundancy is likely the driving factor, with greater constraint on changes of identity. Sites that frequently covary with alloacceptor shifts are located at the extreme ends of the molecule, in common with most known identity determinants. Isoacceptor shifts are associated with changes in the midsections of the tRNA sequence. However, the mutation patterns of anticodon shifts involving the same identities are often dissimilar, suggesting that alternate sets of mutation may achieve the same functional compensation.

[1]  U. RajBhandary,et al.  Mutants of Escherichia coli initiator tRNA that suppress amber codons in Saccharomyces cerevisiae and are aminoacylated with tyrosine by yeast extracts. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[2]  G. Björk,et al.  Three modified nucleosides present in the anticodon stem and loop influence the in vivo aa-tRNA selection in a tRNA-dependent manner. , 1997, Journal of molecular biology.

[3]  T. Pan,et al.  Functional analysis of human tRNA isodecoders. , 2010, Journal of molecular biology.

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

[5]  H. Gross,et al.  Identity elements of human tRNA(Leu): structural requirements for converting human tRNA(Ser) into a leucine acceptor in vitro. , 1995, Nucleic acids research.

[6]  T. Noda,et al.  Human Glycyl-tRNA Synthetase , 1994 .

[7]  Mathias Sprinzl,et al.  Compilation of tRNA sequences and sequences of tRNA genes , 1993, Nucleic Acids Res..

[8]  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.

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

[10]  A. Rich,et al.  Formation of a DNA-soluble RNA hybrid and its relation to the origin, evolution, and degeneracy of soluble RNA. , 1962, Proceedings of the National Academy of Sciences of the United States of America.

[11]  David H. Ardell,et al.  TFAM detects co-evolution of tRNA identity rules with lateral transfer of histidyl-tRNA synthetase , 2006, Nucleic acids research.

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

[13]  Sean R. Eddy,et al.  Infernal 1.0: inference of RNA alignments , 2009, Bioinform..

[14]  M. Deutscher,et al.  Purification of a low molecular weight form of rat liver arginyl-tRNA synthetase. , 1982, The Journal of biological chemistry.

[15]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[16]  J Abelson,et al.  Evolution of a transfer RNA gene through a point mutation in the anticodon. , 1998, Science.

[17]  P. Farabaugh,et al.  Transfer RNA modifications that alter +1 frameshifting in general fail to affect -1 frameshifting. , 2003, RNA.

[18]  Geoffrey J. Barton,et al.  The Jalview Java alignment editor , 2004, Bioinform..

[19]  R. Giegé,et al.  Identity of tRNA for yeast tyrosyl-tRNA synthetase: tyrosylation is more sensitive to identity nucleotides than to structural features. , 2000, Biochemistry.

[20]  H. Gross,et al.  The exchange of the discriminator base A73 for G is alone sufficient to convert human tRNA(Leu) into a serine‐acceptor in vitro. , 1994, The EMBO journal.

[21]  T. Steitz,et al.  Mechanism of transfer RNA maturation by CCA-adding enzyme without using an oligonucleotide template , 2004, Nature.

[22]  Joel Dudley,et al.  TimeTree: a public knowledge-base of divergence times among organisms , 2006, Bioinform..

[23]  Dieter Söll,et al.  Trna: Structure, Biosynthesis, and Function , 1995 .

[24]  S. Eddy,et al.  tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. , 1997, Nucleic acids research.

[25]  Ziniu Yu,et al.  New features of Asian Crassostrea oyster mitochondrial genomes: a novel alloacceptor tRNA gene recruitment and two novel ORFs. , 2012, Gene.

[26]  T. Noda,et al.  Human glycyl-tRNA synthetase. Wide divergence of primary structure from bacterial counterpart and species-specific aminoacylation. , 1994, The Journal of biological chemistry.

[27]  P. Schimmel,et al.  Operational RNA code for amino acids: species-specific aminoacylation of minihelices switched by a single nucleotide. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[28]  Xiujuan Wang,et al.  Gene recruitment--a common mechanism in the evolution of transfer RNA gene families. , 2011, Gene.

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

[30]  C. Florentz,et al.  Identity elements for specific aminoacylation of yeast tRNA(Asp) by cognate aspartyl-tRNA synthetase , 1991, Science.

[31]  U. Englisch,et al.  The modified wobble base inosine in yeast tRNAIle is a positive determinant for aminoacylation by isoleucyl-tRNA synthetase. , 1997, Biochemistry.

[32]  H. Gross,et al.  Identity determinants of human tRNA(Ser): sequence elements necessary for serylation and maturation of a tRNA with a long extra arm. , 1993, The EMBO journal.

[33]  N. Nameki Identity elements of tRNA(Thr) towards Saccharomyces cerevisiae threonyl-tRNA synthetase. , 1995, Nucleic acids research.

[34]  T. Earnest,et al.  Crystal Structure of the Ribosome at 5.5 Å Resolution , 2001, Science.

[35]  David Sankoff,et al.  The evolving trna molecul , 1981 .

[36]  B. Senger,et al.  The anticodon triplet is not sufficient to confer methionine acceptance to a transfer RNA. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[37]  J. Farris Phylogenetic Analysis Under Dollo's Law , 1977 .

[38]  V. Ramakrishnan,et al.  Recognition of Cognate Transfer RNA by the 30S Ribosomal Subunit , 2001, Science.

[39]  O. Uhlenbeck,et al.  Nucleotides in yeast tRNAPhe required for the specific recognition by its cognate synthetase. , 1989, Science.

[40]  S. Yoshida,et al.  Only one nucleotide insertion to the long variable arm confers an efficient serine acceptor activity upon Saccharomyces cerevisiae tRNA(Leu) in vitro. , 1997, Journal of molecular biology.

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

[42]  O. Uhlenbeck,et al.  Recognition nucleotides for human phenylalanyl-tRNA synthetase. , 1992, Nucleic acids research.

[43]  D. Ardell,et al.  New computational methods reveal tRNA identity element divergence between Proteobacteria and Cyanobacteria. , 2007, Biochimie.

[44]  L. H. Schulman,et al.  The anticodon contains a major element of the identity of arginine transfer RNAs. , 1989, Science.

[45]  Peter F. Stadler,et al.  tRNAdb 2009: compilation of tRNA sequences and tRNA genes , 2008, Nucleic Acids Res..

[46]  Dino Moras,et al.  tRNA aminoacylation by arginyl‐tRNA synthetase: induced conformations during substrates binding , 2000, The EMBO journal.

[47]  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.

[48]  Ian Stansfield,et al.  tRNA properties help shape codon pair preferences in open reading frames , 2006, Nucleic acids research.

[49]  Yann Ponty,et al.  VARNA: Interactive drawing and editing of the RNA secondary structure , 2009, Bioinform..

[50]  L. C. Martin,et al.  Using information theory to search for co-evolving residues in proteins , 2005, Bioinform..

[51]  Casey M. Bergman,et al.  The Evolution of tRNA Genes in Drosophila , 2010, Genome biology and evolution.

[52]  B. Lang,et al.  Transfer RNA gene recruitment in mitochondrial DNA. , 2005, Trends in genetics : TIG.

[53]  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.

[54]  David K. Y. Chiu,et al.  Inferring consensus structure from nucleic acid sequences , 1991, Comput. Appl. Biosci..

[55]  T. Hughes,et al.  Prediction and verification of mouse tRNA gene families , 2009, RNA biology.

[56]  B. Senger,et al.  The presence of a D-stem but not a T-stem is essential for triggering aminoacylation upon anticodon binding in yeast methionine tRNA. , 1995, Journal of molecular biology.

[57]  R. Bieler,et al.  Changing identities: tRNA duplication and remolding within animal mitochondrial genomes , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[58]  K. Musier-Forsyth,et al.  Efficient aminoacylation of tRNA(Lys,3) by human lysyl-tRNA synthetase is dependent on covalent continuity between the acceptor stem and the anticodon domain. , 1999, Nucleic acids research.

[59]  David H. Ardell,et al.  TFAM 1.0: an online tRNA function classifier , 2007, Nucleic Acids Res..

[60]  Dawei Li,et al.  Flavor network and the principles of food pairing , 2011, Scientific reports.

[61]  Toralf Kirsten,et al.  Genomic organization of eukaryotic tRNAs , 2010, BMC Genomics.

[62]  E. Holme,et al.  A novel mitochondrial tRNA Arg mutation resulting in an anticodon swap in a patient with mitochondrial encephalomyopathy , 2012, European Journal of Human Genetics.

[63]  G. Stormo,et al.  Identifying constraints on the higher-order structure of RNA: continued development and application of comparative sequence analysis methods. , 1992, Nucleic acids research.

[64]  J. Jurka,et al.  Repbase Update, a database of eukaryotic repetitive elements , 2005, Cytogenetic and Genome Research.

[65]  H. Himeno,et al.  Escherichia coli tRNA(Asp) recognition mechanism differing from that of the yeast system. , 1992, Biochemical and biophysical research communications.

[66]  J. Conery,et al.  Anticodon-dependent conservation of bacterial tRNA gene sequences. , 2007, RNA.

[67]  J. Frank,et al.  A twisted tRNA intermediate sets the threshold for decoding. , 2003, RNA.

[68]  R. B. Loftfield THE FREQUENCY OF ERRORS IN PROTEIN BIOSYNTHESIS. , 1963, The Biochemical journal.

[69]  B. Dalrymple,et al.  Analysis of the complement and molecular evolution of tRNA genes in cow , 2009, BMC Genomics.

[70]  G. Björk,et al.  Improvement of reading frame maintenance is a common function for several tRNA modifications , 2001, The EMBO journal.

[71]  L. Pallanck,et al.  Anticodon-dependent aminoacylation of a noncognate tRNA with isoleucine, valine, and phenylalanine in vivo. , 1991, Proceedings of the National Academy of Sciences of the United States of America.