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Evolution of +1 Programmed Frameshifting Signals and Frameshift-Regulating tRNAs in the Order Saccharomycetales

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Abstract

Programmed translational frameshifting is a ubiquitous but rare mechanism of gene expression in which mRNA sequences cause the translational machinery to shift reading frames with extreme efficiency, up to at least 50%. The mRNA sequences responsible are deceptively simple; the sequence CUU-AGG-C causes about 40% frameshifting when inserted into an mRNA in the yeast Saccharomyces cerevisiae. The high efficiency of this site depends on a set of S. cerevisiae tRNA isoacceptors that perturb the mechanism of translation to cause the programmed translational error. The simplicity of the system might suggest that it could evolve frequently and perhaps be lost as easily. We have investigated the history of programmed +1 frameshifting in fungi. We find that frameshifting has persisted in two structural genes in budding yeasts, ABP140 and EST3 for about 150 million years. Further, the tRNAs that stimulate the event are equally old. Species that diverged from the lineage earlier both do not employ frameshifting and have a different complement of tRNAs predicted to be inimical to frameshifting. The stability of the coevolution of protein coding genes and tRNAs suggests that frameshifting has been selected for during the divergence of these species.

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Acknowledgments

This work was supported by a grant from the National Institute of General Medical Sciences (GM 29480-24). Part of the work was performed while P.J.F. was a visiting scientist at the Universite‘ Paris XI, Orsay, France, supported by the Centre Nationale de la Recherche Scientifique.

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Authors and Affiliations

  1. Department of Biological Sciences and Program in Molecular and Cell Biology, University of Maryland Baltimore County, Baltimore, Maryland, 21250, USA

    Philip J. Farabaugh, Emily Kramer, Haritha Vallabhaneni & Ana Raman

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  1. Philip J. Farabaugh
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  2. Emily Kramer
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  3. Haritha Vallabhaneni
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  4. Ana Raman
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Correspondence to Philip J. Farabaugh.

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Farabaugh, P.J., Kramer, E., Vallabhaneni, H. et al. Evolution of +1 Programmed Frameshifting Signals and Frameshift-Regulating tRNAs in the Order Saccharomycetales. J Mol Evol 63, 545–561 (2006). https://doi.org/10.1007/s00239-005-0311-0

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