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Evolutionary Patterns of Codon Usage in the Chloroplast Gene rbcL

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Abstract

In this study we reconstruct the evolution of codon usage bias in the chloroplast gene rbcL using a phylogeny of 92 green-plant taxa. We employ a measure of codon usage bias that accounts for chloroplast genomic nucleotide content, as an attempt to limit plausible explanations for patterns of codon bias evolution to selection- or drift-based processes. This measure uses maximum likelihood-ratio tests to compare the performance of two models, one in which a single codon is overrepresented and one in which two codons are overrepresented. The measure allowed us to analyze both the extent of bias in each lineage and the evolution of codon choice across the phylogeny. Despite predictions based primarily on the low G+C content of the chloroplast and the high functional importance of rbcL, we found large differences in the extent of bias, suggesting differential molecular selection that is clade specific. The seed plants and simple leafy liverworts each independently derived a low level of bias in rbcL, perhaps indicating relaxed selectional constraint on molecular changes in the gene. Overrepresentation of a single codon was typically plesiomorphic, and transitions to overrepresentation of two codons occurred commonly across the phylogeny, possibly indicating biochemical selection. The total codon bias in each taxon, when regressed against the total bias of each amino acid, suggested that twofold amino acids play a strong role in inflating the level of codon usage bias in rbcL, despite the fact that twofolds compose a minority of residues in this gene. Those amino acids that contributed most to the total codon usage bias of each taxon are known through amino acid knockout and replacement to be of high functional importance. This suggests that codon usage bias may be constrained by particular amino acids and, thus, may serve as a good predictor of what residues are most important for protein fitness.

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Acknowledgements

We thank Montgomery Slatkin, Rosalyn Sayman, John Novembre, and the NSF PEET program for its support (NSF DEB-9712347 to Brent D. Mishler [D.P.W] and NSF DEB-9521835 to Jerry Powell and Felix Sperling [J.H]). Our manuscript was greatly improved by comments of Martin Krietman and two anonymous reviewers.

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Authors and Affiliations

  1. Department of Integrative Biology, University of California, Berkeley, Berkeley, CA 94720, USA

    Dennis P. Wall

  2. Division of Insect Biology, University of California, Berkeley, Berkeley, CA 94720, USA

    Joshua T. Herbeck

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  1. Dennis P. Wall
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Correspondence to Dennis P. Wall.

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Wall, D.P., Herbeck, J.T. Evolutionary Patterns of Codon Usage in the Chloroplast Gene rbcL . J Mol Evol 56, 673–688 (2003). https://doi.org/10.1007/s00239-002-2436-8

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