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A novel nuclear genetic code alteration in yeasts and the evolution of codon reassignment in eukaryotes.

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Mühlhausen,  S.
Research Group of Systems Biology of Motor Proteins, MPI for Biophysical Chemistry, Max Planck Society;

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Findeisen,  P.
Research Group of Systems Biology of Motor Proteins, MPI for Biophysical Chemistry, Max Planck Society;

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Plessmann,  U.
Research Group of Bioanalytical Mass Spectrometry, MPI for biophysical chemistry, Max Planck Society;

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Urlaub,  H.
Research Group of Bioanalytical Mass Spectrometry, MPI for biophysical chemistry, Max Planck Society;

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Kollmar,  M.
Research Group of Systems Biology of Motor Proteins, MPI for Biophysical Chemistry, Max Planck Society;

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2310354-Suppl.pdf
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Citation

Mühlhausen, S., Findeisen, P., Plessmann, U., Urlaub, H., & Kollmar, M. (2016). A novel nuclear genetic code alteration in yeasts and the evolution of codon reassignment in eukaryotes. Genome Research, 26(7), 945-955. doi:10.1101/gr.200931.115.


Cite as: https://hdl.handle.net/11858/00-001M-0000-002A-FDFE-9
Abstract
The genetic code is the cellular translation table for the conversion of nucleotide sequences into amino acid sequences. Changes to the meaning of sense codons would introduce errors into almost every translated message and are expected to be highly detrimental. However, reassignment of single or multiple codons in mitochondria and nuclear genomes, although extremely rare, demonstrates that the code can evolve. Several models for the mechanism of alteration of nuclear genetic codes have been proposed (including "codon capture," "genome streamlining," and "ambiguous intermediate" theories), but with little resolution. Here, we report a novel sense codon reassignment in Pachysolen tannophilus, a yeast related to the Pichiaceae. By generating proteomics data and using tRNA sequence comparisons, we show that Pachysolen translates CUG codons as alanine and not as the more usual leucine. The Pachysolen tRNACAG is an anticodon-mutated tRNA(Ala) containing all major alanine tRNA recognition sites. The polyphyly of the CUG-decoding tRNAs in yeasts is best explained by a tRNA loss driven codon reassignment mechanism. Loss of the CUG-tRNA in the ancient yeast is followed by gradual decrease of respective codons and subsequent codon capture by tRNAs whose anticodon is not part of the aminoacyl-tRNA synthetase recognition region. Our hypothesis applies to all nuclear genetic code alterations and provides several testable predictions. We anticipate more codon reassignments to be uncovered in existing and upcoming genome projects.