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On the Possible Role of tRNA Base Modifications in the Evolution of Codon Usage: Queuosine and Drosophila

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Abstract

The best documented selection-based hypothesis to explain unequal usage of codons is based on the relative abundance of isoaccepting tRNAs. In unicellular organisms the most used codons are optimally translated by the most abundant tRNAs. The chemical bonding energies are affected by modification of the four traditional bases, in particular in the first anti-codon corresponding to the third codon position. One nearly universal modification is queuosine (Q) for guanine (G) in tRNAHis, tRNAAsp, tRNAAsn, and tRNATyr; this changes the optimal binding from codons ending in C to no preference or a slight preference for U-ending codons. Among species of Drosophila, codon usage is constant with the exception of the Drosophila willistoni lineage which has shifted primary usage from C-ending codons to U/T ending codons only for these four amino acids. In Drosophila melanogaster Q containing tRNAs only predominate in old adults. We asked the question whether in D. willistoni these Q containing tRNAs might predominate earlier in development. As a surrogate for levels of modification we studied the expression of the gene (tgt) coding for the enzyme that catalyzes the substitution of Q for G in different life stages of D. melanogaster, D. pseudoobscura, and D. willistoni. Unlike the other two species, the highest tgt expression in D. willistoni is in young females producing eggs. Because tRNAs laid down in eggs persist through the early stages of development, this implies that Q modification occurs earlier in development in D. willistoni than in other Drosophila.

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Acknowledgments

We are thankful to Aditya Paul for helping with the RNA quantification, to Julien Claude for helping with the statistical analyses, and to Dieter Söll and Erick Kubli for discussion of Drosophila tRNAs. Two reviewers made helpful comments. NIH grant RO1 GM077533 (to JRP) provided financial support for this study. AP was supported by a Marie Curie Outgoing International Fellowship (Contract No. MOIF-CT-2006-021357). This is the publication #ISEM 2010-010 of YC.

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Author notes

  1. Ylenia Chiari

    Present address: Institut des Sciences de l’Evolution, CNRS-UMR no. 5554, CC 064, Université Montpellier 2, 2, Place Eugène Bataillon, 34095, Montpellier Cedex 5, France

  2. James Colborn

    Present address: Epidemic Intelligence Service, Centers for Disease Control and Prevention, Atlanta, GA, 30333, USA

  3. Aristeidis Parmakelis

    Present address: Department of Ecology and Taxonomy, Faculty of Biology, University of Athens, Panepistimioupoli Zografou, 15784, Athens, Greece

Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, Yale University, 21 Sachem St, New Haven, CT, 06520-8106, USA

    Ylenia Chiari, Kirstin Dion, James Colborn, Aristeidis Parmakelis & Jeffrey R. Powell

  2. Idaho Department of Health and Welfare, 450 W. State St. 4th Floor, Boise, ID, 83720, USA

    James Colborn

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  1. Ylenia Chiari
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  2. Kirstin Dion
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  5. Jeffrey R. Powell
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Correspondence to Jeffrey R. Powell.

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Ylenia Chiari, Kirstin Dion, and James Colborn contributed equally.

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Chiari, Y., Dion, K., Colborn, J. et al. On the Possible Role of tRNA Base Modifications in the Evolution of Codon Usage: Queuosine and Drosophila . J Mol Evol 70, 339–345 (2010). https://doi.org/10.1007/s00239-010-9329-z

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  • DOI: https://doi.org/10.1007/s00239-010-9329-z

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