Transfer RNA paralogs: evidence for genetic code-amino acid biosynthesis coevolution and an archaeal root of life

Xue, Hong; Tong, Ka-Lok; Marck, Christian; Grosjean, Henri; Wong, J. Tze‐Fei

doi:10.1016/s0378-1119(03)00552-3

Cited by 85 publications

(100 citation statements)

References 29 publications

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“…Therefore Phe and Tyr codons are colored both red and green (hashed mode) in Figure 2. Actually, a recent compilation of tRNA sequences has identified the Phe-Tyr pair as the one paralogous pair displaying the highest sequence conservation, in an attempt to identify ''alloacceptors'' (Xue et al 2003). This could be the mark of a recent assignment, or even a codon swapping phenomenon (Szathmary 1991).…”

Section: Asymmetric Pattern In a Colored Codon Tablementioning

confidence: 99%

An asymmetric underlying rule in the assignment of codons: Possible clue to a quick early evolution of the genetic code via successive binary choices

Delarue¹

2006

RNA

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Aminoacyl-tRNA synthetases (aaRSs) are responsible for creating the pool of correctly charged aminoacyl-tRNAs that are necessary for the translation of genetic information (mRNA) by the ribosome. Each aaRS belongs to either one of only two classes with two different mechanisms of aminoacylation, making use of either the 29OH (Class I) or the 39OH (Class II) of the terminal A76 of the tRNA and approaching the tRNA either from the minor groove (29OH) or the major groove (39OH). Here, an asymmetric pattern typical of differentiation is uncovered in the partition of the codon repertoire, as defined by the mechanism of aminoacylation of each corresponding tRNA. This pattern can be reproduced in a unique cascade of successive binary decisions that progressively reduces codon ambiguity. The deduced order of differentiation is manifestly driven by the reduction of translation errors. A simple rule can be defined, decoding each codon sequence in its binary class, thereby providing both the code and the key to decode it. Assuming that the partition into two mechanisms of tRNA aminoacylation is a relic that dates back to the invention of the genetic code in the RNA World, a model for the assignment of amino acids in the codon table can be derived. The model implies that the stop codon was always there, as the codon whose tRNA cannot be charged with any amino acid, and makes the prediction of an ultimate differentiation step, which is found to correspond to the codon assignment of the 22nd amino acid pyrrolysine in archaebacteria.

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Section: Asymmetric Pattern In a Colored Codon Tablementioning

confidence: 99%

An asymmetric underlying rule in the assignment of codons: Possible clue to a quick early evolution of the genetic code via successive binary choices

Delarue¹

2006

RNA

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“…How this set originated is an interesting question that needs to be addressed. A cluster-dispersion model of tRNA evolution has been proposed to account for the generation of new tRNA species by duplication and coadaptation to the genetic code in the ancient lineages of life (Xue et al 2003). An extension of this model could perhaps be used to understand the modern tRNA structure of eubacteria; however, a more extensive analysis, including more distantly related bacteria, is needed in order to work out ancient evolutionary events that led to the formation of the modern tRNA clusters seen in Escherichia spp.…”

Section: Phylogenetic Analysismentioning

confidence: 99%

Archaeology and evolution of transfer RNA genes in the Escherichia coli genome

Withers

Wernisch²,

Reis³

2006

RNA

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Transfer RNA genes tend to be presented in multiple copies in the genomes of most organisms, from bacteria to eukaryotes. The evolution and genomic structure of tRNA genes has been a somewhat neglected area of molecular evolution. Escherichia coli, the first phylogenetic species for which more than two different strains have been sequenced, provides an invaluable framework to study the evolution of tRNA genes. In this work, a detailed analysis of the tRNA structure of the genomes of Escherichia coli strains K12, CFT073, and O157:H7, Shigella flexneri 2a 301, and Salmonella typhimurium LT2 was carried out. A phylogenetic analysis of these organisms was completed, and an archaeological map depicting the main events in the evolution of tRNA genes was drawn. It is shown that duplications, deletions, and horizontal gene transfers are the main factors driving tRNA evolution in these genomes. On average, 0.64 tRNA insertions/duplications occur every million years (Myr) per genome per lineage, while deletions occur at the slower rate of 0.30 per million years per genome per lineage. This work provides a first genomic glance at the problem of tRNA evolution as a repetitive process, and the relationship of this mechanism to genome evolution and codon usage is discussed.

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“…Moreover, with certain chimeric pre-tRNAs, higher eukaryotic tRNA splicing endonucleases, such as the one from Xenopus laevis, can also cleave in a mode that is independent of the mature domain of the tRNA when substrates are able to form the perfect hBHBh splicing motif, the A-I base pair now playing a pivotal role in this process (Fruscoloni et al 2001). Last but not least, from thorough analyses of tRNA populations in 60 fully sequenced genomes, Xue et al (2003) recently argued that both Eukarya and Bacteria probably originated from the phylum Crenarchaeota, whereas the Euryarchaeota evolved from the same ancestor of Crenarchaeota, but independently of Eukarya and Bacteria. Our proposal concerning the independent evolution of the endonucleases found in the three biological domains fits well with this idea.…”

Section: An Ancient Endonuclease From Crenarchaeota Might Be At the Omentioning

confidence: 99%

Identification of BHB splicing motifs in intron-containing tRNAs from 18 archaea: evolutionary implications

Marck¹,

Grosjean²

2003

RNA

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163

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Most introns of archaeal tRNA genes (tDNAs) are located in the anticodon loop, between nucleotides 37 and 38, the unique location of their eukaryotic counterparts. However, in several Archaea, mostly in Crenarchaeota, introns have been found at many other positions of the tDNAs. In the present work, we revisit and extend all previous findings concerning the identification, exact location, size, and possible fit to the proposed bulge-helix-bulge structural motif (BHB, now renamed hBHBh) of the sequences spanning intron-exon junctions in intron-containing tRNAs of 18 archaea. A total of 103 introns were found located at the usual position 37/38 and 33 introns at 14 other different positions, that is, in the anticodon stem and loop, in the D-and T-loops, in the V-arm, or in the amino acid arm. For introns located at 37/38 and elsewhere in the pre-tRNA, canonical hBHBh motifs were not always found. Instead, a relaxed hBH or HBh motif including the constant central 4-bp helix H flanked by one helix (h or h) on either side generating only one bulge could be disclosed. Also, for introns located elsewhere than at position 37/38, the hBHBh (or HBh) structure competes with the three-dimensional structure of the mature tRNA, attesting to important structural rearrangements during the complex multistep maturation-splicing processes. A homotetramer-type of splicing endonuclease (like in all Crenarchaeota) instead of a homodimeric-type of enzyme (as in most Euryarchaeota) appears to best fit the requirement for splicing introns at relaxed hBH or HBh motifs, and may represent the most primitive form of this enzyme.

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Transfer RNA paralogs: evidence for genetic code-amino acid biosynthesis coevolution and an archaeal root of life

Cited by 85 publications

References 29 publications

An asymmetric underlying rule in the assignment of codons: Possible clue to a quick early evolution of the genetic code via successive binary choices

An asymmetric underlying rule in the assignment of codons: Possible clue to a quick early evolution of the genetic code via successive binary choices

Archaeology and evolution of transfer RNA genes in the Escherichia coli genome

Identification of BHB splicing motifs in intron-containing tRNAs from 18 archaea: evolutionary implications

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