Codon usage in bacteria: correlation with gene expressivity

Gouy, Manolo; Gautier, Christian

doi:10.1093/nar/10.22.7055

Cited by 1,158 publications

(760 citation statements)

References 37 publications

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“…Among codons recognized by different aminoacyl tRNAs, translationally preferred codons tend to be recognized by more abundant isoacceptors. Protein abundance has been shown to correlate strongly with synonymous codon usage in some organisms [40]. Akashi has reported significantly higher frequency of preferred codons at conserved amino acids than at non-conserved ones in fruit flies [41].…”

Section: R E T R a C T E Dmentioning

confidence: 99%

RETRACTED: Why proteins evolve at different rates: The functional hypothesis versus the mistranslation‐induced protein misfolding hypothesis

Park

Choi

2009

FEBS Letters

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Edited by Takashi Gojobori Keywords:Protein evolutionary rate Functional hypothesis Mistranslation-induced protein misfolding hypothesis Translational robustness Expression abundance a b s t r a c t Protein evolutionary rates have been presumed to be mostly determined by the density of functionally important amino acids in a given protein. They have been shown to correlate with variables intuitively related to functional importance of proteins, such as protein dispensability and protein-protein interactions. Surprisingly, the best correlate of the evolutionary rates has turned out to be not the functional importance of a protein, but the expression level of the protein. Drummond and Wilke suggest that the dominant role of expression levels in slowing the rate of protein evolution stems from a selection pressure against mistranslation-induced protein misfolding. We will review current evidence for and against different hypotheses on determining evolutionary rates.

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Section: R E T R a C T E Dmentioning

confidence: 99%

RETRACTED: Why proteins evolve at different rates: The functional hypothesis versus the mistranslation‐induced protein misfolding hypothesis

Park

Choi

2009

FEBS Letters

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“…Adh is a highly expressed gene in D. melanogaster, accounting for Ϸ1-2% of the translational activity of mRNA in adult flies (28). Highly expressed genes have been shown to be positively correlated with levels of codon bias in both bacteria and yeast (29)(30)(31). In multicellular eukaryotes such as Drosophila it is more difficult to quantify expression levels, but it appears that highly expressed Drosophila genes also show high levels of codon bias (27).…”

Section: Discussionmentioning

confidence: 99%

Site-directed mutations reveal long-range compensatory interactions in the Adh gene of Drosophila melanogaster

Parsch

Tanda

Stephan

1997

Proc. Natl. Acad. Sci. U.S.A.

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Long-range interactions between the 5 and 3 ends of mRNA molecules have been suggested to play a role in the initiation of translation and the regulation of gene expression. To identify such interactions and to study their molecular evolution, we used phylogenetic analysis to generate a model of mRNA higher-order structure in the Adh transcript of Drosophila melanogaster. This model predicts long-range, tertiary contacts between a region of the protein-encoding sequence just downstream of the start codon and a conserved sequence in the 3 untranslated region (UTR). To further examine the proposed structure, site-directed mutations were generated in vitro in a cloned D. melanogaster Adh gene, and the mutant constructs were introduced into the Drosophila germ line through P-element mediated transformation. Transformants were spectrophotometrically assayed for alcohol dehydrogenase activity. Our results indicate that transformants containing a silent mutation near the start of the proteinencoding sequence show an Ϸ15% reduction in alcohol dehydrogenase activity relative to wild-type transformants. This activity can be restored to wild-type levels by a second, compensatory mutation in the 3 UTR. These observations are consistent with a higher-order structure model that includes long-range interactions between the 5 and 3 ends of the Adh mRNA. However, our results do not fit the classical compensatory substitution model because the second mutation by itself (in the 3 UTR) did not show a measurable reduction in gene expression.There is a growing body of evidence for functional, long-range interactions between the 5Ј and 3Ј ends of eukaryotic mRNA molecules. Tarun and Sachs (1) have shown that a protein which binds to the 3Ј end of yeast mRNA is involved in the initiation of translation which occurs at the 5Ј end. Similarly, in Drosophila, proteins that bind to an mRNA's 3Ј untranslated region (UTR) have been shown to affect levels of translation (2, 3). In addition to these studies of protein-protein interactions, several sources have suggested direct RNA-RNA pairings between the two ends of mRNA molecules. Konings et al. (4) used a free-energy minimization algorithm to predict folding patterns for 38 eukaryotic mRNAs. Their results indicate a common pattern of mRNA folding, where the 3Ј UTR forms contacts with the coding region just downstream of the start codon. Stephan and Kirby (5) used a phylogenetic comparison method to predict mRNA secondary structures in Drosophila and found evidence for long-range pairings between the 3Ј UTR and the protein-encoding region. These findings raise a number of important questions. For instance, which nucleotides are involved in RNA-RNA interactions and how are they arranged into secondary and tertiary pairing regions? Do the currently available models describe the evolution of compensatory mutations adequately? To begin to address these questions, we have focused on identifying elements of the Adh mRNA higher-order structure in Drosophila melanogaster.Adh produces two deve...

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“…The correlation between codon usage and tRNA content has been observed extensively (Chavancy et al, 1979;Post & Nomura, 1980;Bennetzen & Hall, 1982;Gouy & Gautier, 1982;Ikemura & Ozeki, 1983;Ikemura, 1985;. Codon usage has been used to detect coding regions in DNA (Ficket, 1982;Staden & McLachlan, 1982), to predict the levels of protein production from genes (Gribskov et al, 1984;Sharp & Li, 1987), and to suggest which codons are optimal for the translation system of a given organism (Ikemura & Ozeki, 1983;Ikemura, 1981).…”

Section: Implications For Studies On Codon Usagementioning

confidence: 99%

Ribosome‐mediated translational pause and protein domain organization

1996

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Because regions on the messenger ribonucleic acid differ in the rate at which they are translated by the ribosome and because proteins can fold cotranslationally on the ribosome, a question arises as to whether the kinetics of translation influence the folding events in the growing nascent polypeptide chain. Translationally slow regions were identified on mRNAs for a set of 37 multidomain proteins from Escherichia coli with known three-dimensional structures. The frequencies of individual codons in mRNAs of highly expressed genes from E. coli were taken as a measure of codon translation speed. Analysis of codon usage in slow regions showed a consistency with the experimentally determined translation rates of codons; abundant codons that are translated with faster speeds compared with their synonymous codons were found to be avoided; rare codons that are translated at an unexpectedly higher rate were also found to be avoided in slow regions. The statistical significance of the occurrence of such slow regions on mRNA spans corresponding to the oligopeptide domain termini and linking regions on the encoded proteins was assessed. The amino acid type and the solvent accessibility of the residues coded by such slow regions were also examined. The results indicated that protein domain boundaries that mark higher-order structural organization are largely coded by translationally slow regions on the RNA and are composed of such amino acids that are stickier to the ribosome channel through which the synthesized polypeptide chain emerges into the cytoplasm. The translationally slow nucleotide regions on mRNA possess the potential to form hairpin secondary structures and such structures could further slow the movement of ribosome. The results point to an intriguing correlation between protein synthesis machinery and in vivo protein folding. Examination of available mutagenic data indicated that the effects of some of the reported mutations were consistent with our hypothesis.Keywords: codon usage; domain linkers; peptide channel; protein folding; ribosome; translation The rate of protein translation is nonuniform along the mRNA (Varenne et al., 1984). Ribosomes seem to pause as well as stack at specific regions on mRNA (Chaney & Morris, 1979;Wolin &Walter, 1988;Kim et al., 1991;Kim & Hollingsworth, 1992). Two of the mRNA features that slow the ribosome during translation are the presence of slow codons (Varenne et al., 1984;Bonekamp et al., 1985;Wolin & Walter, 1988) and the formation of higher order nucleotide structures (Chaney & Morris, 1979;Tu et al., 1992). The resultant translational pause may temporally separate the adjacent regions on the growing nascent polypeptide. Given that proteins can fold cotranslationally with the possible involvement of the ribosome (Phillips, 1966;Baldwin, 1975;Yonath, 1992;Kudlicki et al., 1994;Wiedmann et al., 1994;Brimacombe, 1995), the temporal separation might exert a phenotypic effect on the structural organization of the encoded protein. We show that as much as 70% of the do...

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Codon usage in bacteria: correlation with gene expressivity

Cited by 1,158 publications

References 37 publications

RETRACTED: Why proteins evolve at different rates: The functional hypothesis versus the mistranslation‐induced protein misfolding hypothesis

RETRACTED: Why proteins evolve at different rates: The functional hypothesis versus the mistranslation‐induced protein misfolding hypothesis

Site-directed mutations reveal long-range compensatory interactions in the Adh gene of Drosophila melanogaster

Ribosome‐mediated translational pause and protein domain organization

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