Abstract
The genetic code used in nuclear genes is almost universal, but here we report that it changed three times in parallel during the evolution of budding yeasts. All three changes were reassignments of the codon CUG, which is translated as serine (in 2 yeast clades), alanine (1 clade), or the ‘universal’ leucine (2 clades). The newly discovered Ser2 clade is in the final stages of a genetic code transition. Most species in this clade have genes for both a novel tRNASer(CAG) and an ancestral tRNALeu(CAG) to read CUG, but only tRNASer(CAG) is used in standard growth conditions. The coexistence of these alloacceptor tRNA genes indicates that the genetic code transition occurred via an ambiguous translation phase. We propose that the three parallel reassignments of CUG were not driven by natural selection in favor of their effects on the proteome, but by selection to eliminate the ancestral tRNALeu(CAG).
Highlights
The genetic code used in nuclear genes is almost universal, but here we report that it changed three times in parallel during the evolution of budding yeasts
Theoretical models of how a sense codon could be reassigned from one amino acid to another during evolution can be grouped into two broad categories: ambiguous intermediate models, and unassigned codon models[3]
When it was later discovered that the single tRNASer that reads CUG codons in C. albicans is mischarged with leucine instead of serine approximately 3% of the time, the ambiguous intermediate model was extended to include ambiguous charging of a single tRNA species[6,14,15]
Summary
To identify species with modified genetic codes, we systematically examined the genomes of 52 yeast species (including 7 newly sequenced) and two outgroups. Detailed LC–MS/MS and BLAST results for each species are shown in Supplementary Data 1. Examples of LC–MS/MS spectra for species with non-standard codes are shown in Supplementary Fig. 3. Examining the BLAST and mass spectrometry results in the context of the inferred species phylogeny, we conclude that there are five monophyletic groups (clades) that differ in their translations of CUG, which we refer to as the Ala, Ser[1], Ser[2], Leu[1], and Leu[2] clades (Fig. 2), as well as paraphyletic outgroup taxa (Leu0) with the standard code. Ser[2] clade species have few CUG codons in conserved genes and gave conflicting results in the BLAST
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