Patterns of Base Composition Within the Genes of Drosophila melanogaster

Kliman, Richard M.; Eyre‐Walker, Adam

doi:10.1007/pl00006334

Cited by 30 publications

(14 citation statements)

References 35 publications

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“…In D. melanogaster, there seems to be an increase of G ϩ C content at the start of genes followed by an overall decline (28). This decline affects not only exons, but also introns, and may be caused by a within-gene variation of mutational bias.…”

Section: Resultsmentioning

confidence: 99%

Expression pattern and, surprisingly, gene length shape codon usage inCaenorhabditis,Drosophila, andArabidopsis

Duret

Mouchiroud

1999

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

758

693

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We measured the expression pattern and analyzed codon usage in 8,133, 1,550, and 2,917 genes, respectively, from Caenorhabditis elegans, Drosophila melanogaster, and Arabidopsis thaliana. In those three species, we observed a clear correlation between codon usage and gene expression levels and showed that this correlation is not due to a mutational bias. This provides direct evidence for selection on silent sites in those three distantly related multicellular eukaryotes. Surprisingly, there is a strong negative correlation between codon usage and protein length. This effect is not due to a smaller size of highly expressed proteins. Thus, for a same-expression pattern, the selective pressure on codon usage appears to be lower in genes encoding long rather than short proteins. This puzzling observation is not predicted by any of the current models of selection on codon usage and thus raises the question of how translation efficiency affects fitness in multicellular organisms.

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Section: Resultsmentioning

confidence: 99%

Expression pattern and, surprisingly, gene length shape codon usage inCaenorhabditis,Drosophila, andArabidopsis

Duret

Mouchiroud

1999

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

758

693

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“…In particular, there is evidence for variation in the degree of mutation bias both within and between genes (Kliman and Eyre-Walker 1998), variation in the selection coefficient between sites within genes (Akashi 1994), and departure from longterm equilibrium in populations of D. melanogaster (Akashi 1996). Are these factors simply complications, or do they invalidate the whole approach?…”

Section: The Application Of Explicit Population Genetics Models To Emmentioning

confidence: 99%

The Evolution of Codon Preferences in Drosophila: A Maximum-Likelihood Approach to Parameter Estimation and Hypothesis Testing

McVean

Vieira

1999

J Mol Evol

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Synonymous codon usage in related species may differ as a result of variation in mutation biases, differences in the overall strength and efficiency of selection, and shifts in codon preference-the selective hierarchy of codons within and between amino acids. We have developed a maximum-likelihood method to employ explicit population genetic models to analyze the evolution of parameters determining codon usage. The method is applied to twofold degenerate amino acids in 50 orthologous genes from D. melanogaster and D. virilis. We find that D. virilis has significantly reduced selection on codon usage for all amino acids, but the data are incompatible with a simple model in which there is a single difference in the long-term Ne, or overall strength of selection, between the two species, indicating shifts in codon preference. The strength of selection acting on codon usage in D. melanogaster is estimated to be |Nes| approximately 0.4 for most CT-ending twofold degenerate amino acids, but 1.7 times greater for cysteine and 1.4 times greater for AG-ending codons. In D. virilis, the strength of selection acting on codon usage for most amino acids is only half that acting in D. melanogaster but is considerably greater than half for cysteine, perhaps indicating the dual selection pressures of translational efficiency and accuracy. Selection coefficients in orthologues are highly correlated (rho = 0.46), but a number of genes deviate significantly from this relationship.

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“…In contrast, mutational events in D. melanogaster are biased toward A 1 T base pairs (Petrov and Hartl 1999), perhaps because of recombination-driven biased gene conversion (Duret 2002). Mutational bias and codon usage are linked through a sizable and significant correlation between intronic G 1 C content (GC i ) and the G 1 C content at synonymous third codon positions (GC3) (Kliman and Hey 1994;Kliman and Eyre-Walker 1998). Recombination rates have been linked to codon usage bias (Hey and Kliman 2002;Marais and Piganeau 2002), but the effect seems to be small compared to the effects of selection (Bierne and Eyre-Walker 2006).…”

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confidence: 99%

Variable Strength of Translational Selection Among 12 Drosophila Species

Heger

Ponting

2007

Genetics

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Codon usage bias in Drosophila melanogaster genes has been attributed to negative selection of those codons whose cellular tRNA abundance restricts rates of mRNA translation. Previous studies, which involved limited numbers of genes, can now be compared against analyses of the entire gene complements of 12 Drosophila species whose genome sequences have become available. Using large numbers (6138) of orthologs represented in all 12 species, we establish that the codon preferences of more closely related species are better correlated. Differences between codon usage biases are attributed, in part, to changes in mutational biases. These biases are apparent from the strong correlation (r ¼ 0.92, P , 0.001) among these genomes' intronic G 1 C contents and exonic G 1 C contents at degenerate third codon positions. To perform a cross-species comparison of selection on codon usage, while accounting for changes in mutational biases, we calibrated each genome in turn using the codon usage bias indices of highly expressed ribosomal protein genes. The strength of translational selection was predicted to have varied between species largely according to their phylogeny, with the D. melanogaster group species exhibiting the strongest degree of selection.

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Patterns of Base Composition Within the Genes of Drosophila melanogaster

Cited by 30 publications

References 35 publications

Expression pattern and, surprisingly, gene length shape codon usage inCaenorhabditis,Drosophila, andArabidopsis

Expression pattern and, surprisingly, gene length shape codon usage inCaenorhabditis,Drosophila, andArabidopsis

The Evolution of Codon Preferences in Drosophila: A Maximum-Likelihood Approach to Parameter Estimation and Hypothesis Testing

Variable Strength of Translational Selection Among 12 Drosophila Species

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