Translation rates of individual codons are not correlated with tRNA abundances or with frequencies of utilization in Escherichia coli

We analyzed 12 individual codons, which differed widely with respect to the frequency of use in Escherichia coli and the abundance of the corresponding tRNAs, for their influence on the coupling between transcription and translation. This was probed by determining the effects of codon substitutions in the leader peptide gene on transcription past the pyrE attenuator, as described previously by Bonekamp et al. (F. Bonekamp, H. D. Andersen, T. Christensen, and K. F. Jensen, Nucleic Acids Res. 13:4113-4123, 1985). In principle, the results revealed that either RNA polymerase or the (leading) ribosomes pass the different codon strings at different rates. However, under the assumption that the rate of transcription elongation is unaffected by the sequence changes, the results may be interpreted as indicating that different codons are translated at different rates and that these rates do not generally reflect the concentrations of the corresponding tRNAs or the frequencies with which the codons are used in E. coli. Moreover, it seems that codon synonyms that are served by the same isoaccepting tRNA species can deviate as much from each other in translational behavior as synonymous codons that are served by isoacceptors present in the cell in widely different amounts can.

[1]  K. Jensen,et al.  Hyper-regulation of pyr gene expression in Escherichia coli cells with slow ribosomes. Evidence for RNA polymerase pausing in vivo? , 1988, European journal of biochemistry.

[2]  K. Jensen,et al.  The AGG codon is translated slowly in E. coli even at very low expression levels. , 1988, Nucleic acids research.

[3]  Paul M. Sharp,et al.  Codon usage in yeast: cluster analysis clearly differentiates highly and lowly expressed genes , 1986, Nucleic Acids Res..

[4]  K. Jensen,et al.  Codon-defined ribosomal pausing in Escherichia coli detected by using the pyrE attenuator to probe the coupling between transcription and translation. , 1985, Nucleic acids research.

[5]  T. Ikemura.  Codon usage and tRNA content in unicellular and multicellular organisms. , 1985, Molecular biology and evolution.

[6]  K. Jensen,et al.  Mechanism of UTP‐modulated attenuation at the pyrE gene of Escherichia coli: an example of operon polarity control through the coupling of translation to transcription. , 1984, The EMBO journal.

[7]  K. Jensen,et al.  Studies on the structure and expression of Escherichia coli pyrC, pyrD, and pyrF using the cloned genes. , 1984, European journal of biochemistry.

[8]  C. Alff-Steinberger,et al.  Evidence for a coding pattern on the non-coding strand of the E. coli genome. , 1984, Nucleic acids research.

[9]  M. Gribskov,et al.  The codon preference plot: graphic analysis of protein coding sequences and prediction of gene expression , 1984, Nucleic Acids Res..

[10]  H. Ozeki,et al.  Codon usage and transfer RNA contents: organism-specific codon-choice patterns in reference to the isoacceptor contents. , 1983, Cold Spring Harbor symposia on quantitative biology.

[11]  M. Gouy,et al.  Codon usage in bacteria: correlation with gene expressivity. , 1982, Nucleic acids research.

[12]  J. Fickett.  Recognition of protein coding regions in DNA sequences. , 1982, Nucleic acids research.

[13]  J. Bennetzen,et al.  Codon selection in yeast. , 1982, The Journal of biological chemistry.

[14]  A. D. McLachlan,et al.  Codon preference and its use in identifying protein coding regions in long DNA sequences , 1982, Nucleic Acids Res..

[15]  T. Ikemura.  Correlation between the abundance of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes: a proposal for a synonymous codon choice that is optimal for the E. coli translational system. , 1981, Journal of molecular biology.

[16]  H. Engelberg-Kulka,et al.  UGA suppression by normal tRNA Trp in Escherichia coli: codon context effects. , 1981, Nucleic acids research.

[17]  Manolo Gouy,et al.  Codon catalog usage is a genome strategy modulated for gene expressivity , 1981, Nucleic Acids Res..

[18]  M. Nomura,et al.  DNA sequences from the str operon of Escherichia coli. , 1980, The Journal of biological chemistry.

[19]  M. Gouy,et al.  Codon frequencies in 119 individual genes confirm consistent choices of degenerate bases according to genome type. , 1980, Nucleic acids research.

[20]  P. Dennis,et al.  Nucleotide sequence of the ribosomal protein gene cluster adjacent to the gene for RNA polymerase subunit beta in Escherichia coli. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[21]  A. Fournier,et al.  Adaptation of iso-tRNA concentration to mRNA codon frequency in the eukaryote cell. , 1979, Biochimie.

[22]  S. Adhya,et al.  Control of transcription termination. , 1978, Annual review of biochemistry.

[23]  F. Sanger,et al.  DNA sequencing with chain-terminating inhibitors. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[24]  C. Caskey,et al.  Peptide chain termination. , 1973, Advances in protein chemistry.

[25]  Jeffrey H. Miller.  Experiments in molecular genetics , 1972 .