tRNA properties help shape codon pair preferences in open reading frames

J Ross Buchan, Lorna Sharman Aucott, Ian Stansfield (Corresponding Author)

Research output: Contribution to journalArticle

61 Citations (Scopus)

Abstract

Translation elongation is an accurate and rapid process, dependent upon efficient juxtaposition of tRNAs in the ribosomal A- and P-sites. Here, we sought evidence of A- and P-site tRNA interaction by examining bias in codon pair choice within open reading frames from a range of genomes. Three distinct and marked effects were revealed once codon and dipeptide biases had been subtracted. First, in the majority of genomes, codon pair preference is primarily determined by a tetranucleotide combination of the third nucleotide of the P-site codon, and all 3 nt of the A-site codon. Second, pairs of rare codons are generally under-used in eukaryotes, but over-used in prokaryotes. Third, the analysis revealed a highly significant effect of tRNA-mediated selection on codon pairing in unicellular eukaryotes, Bacillus subtilis, and the gamma proteobacteria. This was evident because in these organisms, synonymous codons decoded in the A-site by the same tRNA exhibit significantly similar P-site pairing preferences. Codon pair preference is thus influenced by the identity of A-site tRNAs, in combination with the P-site codon third nucleotide. Multivariate analysis identified conserved nucleotide positions within A-site tRNA sequences that modulate codon pair preferences. Structural features that regulate tRNA geometry within the ribosome may govern genomic codon pair patterns, driving enhanced translational fidelity and/or rate.
Original languageEnglish
Pages (from-to)1015-1027
Number of pages13
JournalNucleic Acids Research
Volume34
Issue number3
DOIs
Publication statusPublished - 2006

Fingerprint

Transfer RNA
Codon
Open Reading Frames
Nucleotides
Eukaryota
Genome
Gammaproteobacteria
Dipeptides
Bacillus subtilis
Ribosomes
Multivariate Analysis

Keywords

  • Bacillus subtilis
  • Bacteria
  • Base Pairing
  • Cluster Analysis
  • Codon
  • Gammaproteobacteria
  • Genomics
  • Open Reading Frames
  • RNA, Transfer
  • Yeasts

Cite this

tRNA properties help shape codon pair preferences in open reading frames. / Buchan, J Ross; Aucott, Lorna Sharman; Stansfield, Ian (Corresponding Author).

In: Nucleic Acids Research, Vol. 34, No. 3, 2006, p. 1015-1027.

Research output: Contribution to journalArticle

@article{7d5c4b97ef204b2896793a84a30f52b8,
title = "tRNA properties help shape codon pair preferences in open reading frames",
abstract = "Translation elongation is an accurate and rapid process, dependent upon efficient juxtaposition of tRNAs in the ribosomal A- and P-sites. Here, we sought evidence of A- and P-site tRNA interaction by examining bias in codon pair choice within open reading frames from a range of genomes. Three distinct and marked effects were revealed once codon and dipeptide biases had been subtracted. First, in the majority of genomes, codon pair preference is primarily determined by a tetranucleotide combination of the third nucleotide of the P-site codon, and all 3 nt of the A-site codon. Second, pairs of rare codons are generally under-used in eukaryotes, but over-used in prokaryotes. Third, the analysis revealed a highly significant effect of tRNA-mediated selection on codon pairing in unicellular eukaryotes, Bacillus subtilis, and the gamma proteobacteria. This was evident because in these organisms, synonymous codons decoded in the A-site by the same tRNA exhibit significantly similar P-site pairing preferences. Codon pair preference is thus influenced by the identity of A-site tRNAs, in combination with the P-site codon third nucleotide. Multivariate analysis identified conserved nucleotide positions within A-site tRNA sequences that modulate codon pair preferences. Structural features that regulate tRNA geometry within the ribosome may govern genomic codon pair patterns, driving enhanced translational fidelity and/or rate.",
keywords = "Bacillus subtilis, Bacteria, Base Pairing, Cluster Analysis, Codon, Gammaproteobacteria, Genomics, Open Reading Frames, RNA, Transfer, Yeasts",
author = "Buchan, {J Ross} and Aucott, {Lorna Sharman} and Ian Stansfield",
year = "2006",
doi = "10.1093/nar/gkj488",
language = "English",
volume = "34",
pages = "1015--1027",
journal = "Nucleic Acids Research",
issn = "0305-1048",
publisher = "Oxford University Press",
number = "3",

}

TY - JOUR

T1 - tRNA properties help shape codon pair preferences in open reading frames

AU - Buchan, J Ross

AU - Aucott, Lorna Sharman

AU - Stansfield, Ian

PY - 2006

Y1 - 2006

N2 - Translation elongation is an accurate and rapid process, dependent upon efficient juxtaposition of tRNAs in the ribosomal A- and P-sites. Here, we sought evidence of A- and P-site tRNA interaction by examining bias in codon pair choice within open reading frames from a range of genomes. Three distinct and marked effects were revealed once codon and dipeptide biases had been subtracted. First, in the majority of genomes, codon pair preference is primarily determined by a tetranucleotide combination of the third nucleotide of the P-site codon, and all 3 nt of the A-site codon. Second, pairs of rare codons are generally under-used in eukaryotes, but over-used in prokaryotes. Third, the analysis revealed a highly significant effect of tRNA-mediated selection on codon pairing in unicellular eukaryotes, Bacillus subtilis, and the gamma proteobacteria. This was evident because in these organisms, synonymous codons decoded in the A-site by the same tRNA exhibit significantly similar P-site pairing preferences. Codon pair preference is thus influenced by the identity of A-site tRNAs, in combination with the P-site codon third nucleotide. Multivariate analysis identified conserved nucleotide positions within A-site tRNA sequences that modulate codon pair preferences. Structural features that regulate tRNA geometry within the ribosome may govern genomic codon pair patterns, driving enhanced translational fidelity and/or rate.

AB - Translation elongation is an accurate and rapid process, dependent upon efficient juxtaposition of tRNAs in the ribosomal A- and P-sites. Here, we sought evidence of A- and P-site tRNA interaction by examining bias in codon pair choice within open reading frames from a range of genomes. Three distinct and marked effects were revealed once codon and dipeptide biases had been subtracted. First, in the majority of genomes, codon pair preference is primarily determined by a tetranucleotide combination of the third nucleotide of the P-site codon, and all 3 nt of the A-site codon. Second, pairs of rare codons are generally under-used in eukaryotes, but over-used in prokaryotes. Third, the analysis revealed a highly significant effect of tRNA-mediated selection on codon pairing in unicellular eukaryotes, Bacillus subtilis, and the gamma proteobacteria. This was evident because in these organisms, synonymous codons decoded in the A-site by the same tRNA exhibit significantly similar P-site pairing preferences. Codon pair preference is thus influenced by the identity of A-site tRNAs, in combination with the P-site codon third nucleotide. Multivariate analysis identified conserved nucleotide positions within A-site tRNA sequences that modulate codon pair preferences. Structural features that regulate tRNA geometry within the ribosome may govern genomic codon pair patterns, driving enhanced translational fidelity and/or rate.

KW - Bacillus subtilis

KW - Bacteria

KW - Base Pairing

KW - Cluster Analysis

KW - Codon

KW - Gammaproteobacteria

KW - Genomics

KW - Open Reading Frames

KW - RNA, Transfer

KW - Yeasts

U2 - 10.1093/nar/gkj488

DO - 10.1093/nar/gkj488

M3 - Article

VL - 34

SP - 1015

EP - 1027

JO - Nucleic Acids Research

JF - Nucleic Acids Research

SN - 0305-1048

IS - 3

ER -