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Differential translation efficiency of orthologous genes is involved in phenotypic divergence of yeast species

Nature Genetics volume 39, pages 415–421 (2007)Cite this article

A Corrigendum to this article was published on 01 May 2007

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Abstract

A major challenge in comparative genomics is to understand how phenotypic differences between species are encoded in their genomes. Phenotypic divergence may result from differential transcription of orthologous genes, yet less is known about the involvement of differential translation regulation in species phenotypic divergence. In order to assess translation effects on divergence, we analyzed ∼2,800 orthologous genes in nine yeast genomes. For each gene in each species, we predicted translation efficiency, using a measure of the adaptation of its codons to the organism's tRNA pool. Mining this data set, we found hundreds of genes and gene modules with correlated patterns of translational efficiency across the species. One signal encompassed entire modules that are either needed for oxidative respiration or fermentation and are efficiently translated in aerobic or anaerobic species, respectively. In addition, the efficiency of translation of the mRNA splicing machinery strongly correlates with the number of introns in the various genomes. Altogether, we found extensive selection on synonymous codon usage that modulates translation according to gene function and organism phenotype. We conclude that, like factors such as transcription regulation, translation efficiency affects and is affected by the process of species divergence.

NOTE: In the original version of this paper, subpanels 2c and d were switched, resulting in incorrect information in the legend. Figure 2c shows genes of the tricarboxylic acid (TCA) cycle, while Figure 2d shows glycolysis genes. The error has been corrected in the HTML and PDF versions of the article.

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Figure 1: Comparison of the tRNA gene repertoires of S. cerevisiae and Y. lipolytica.
Figure 2: The translation efficiency profiles of mitochondrial and cytosolic ribosomal proteins, glycolysis and the tricarboxylic acid cycle show coherent patterns.
Figure 3: Scheme for testing for a species effect on translation efficiency for a group of genes.
Figure 4: The translation efficiency profiles of genes related to mRNA splicing correlate with the number of introns in the genomes of species.

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  • 28 March 2007

    NOTE: In the original version of this paper, subpanels 2c and d were switched, resulting in incorrect information in the legend. Figure 2c shows genes of the tricarboxylic acid (TCA) cycle, while Figure 2d shows glycolysis genes. The error has been corrected in the HTML and PDF versions of the article.

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Acknowledgements

We thank the Pilpel laboratory for helpful discussions and E. Segal, A. Regev, I. Tirosh, Y. Gilad, N. Barkai, J. Moult and J.L. Sussman for discussions and critical reviews of the manuscript. Y.P. holds the Rothstein Career Development Chair in Genetic Diseases. We thank the Ben May Charitable Trust and EMBRACE, the European Union Network of Excellence in Bioinformatics for grant support.

Author information

Authors and Affiliations

  1. Department of Molecular Genetics, The Weizmann Institute of Science, Rehovot, 76100, Israel

    Orna Man & Yitzhak Pilpel

  2. Department of Structural Biology, The Weizmann Institute of Science, Rehovot, 76100, Israel

    Orna Man

Authors
  1. Orna Man
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  2. Yitzhak Pilpel
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Contributions

Y.P. and O.M. conceived the study, and Y.P. supervised the study. O.M. and Y.P. designed the analyses, O.M. performed the analyses and O.M. and Y.P. wrote the paper.

Corresponding author

Correspondence to Yitzhak Pilpel.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

The relationship between translation efficiency (tAI) and protein levels. (PDF 224 kb)

Supplementary Fig. 2

Physically interacting proteins tend to have similar translation efficiencies across species. (PDF 90 kb)

Supplementary Fig. 3

Clustering of the multispecies translation efficiency profiles. (PDF 407 kb)

Supplementary Fig. 4

Comparison of the effective number of codons (Nc) and the tRNA adaptation index (tAI) for the coding sequences of ten ascomycotic yeast species. (PDF 223 kb)

Supplementary Fig. 5

Translation efficiency profiles of genes related to M-phase of the cell cycle. (PDF 92 kb)

Supplementary Table 1

The tRNA repertoires of the analyzed species. (PDF 76 kb)

Supplementary Table 2

Translation efficiency profiles of orthologous genes across species, their division into 40 clusters, and the functional enrichment within clusters. (PDF 562 kb)

Supplementary Methods (PDF 173 kb)

Supplementary Note (PDF 137 kb)

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Man, O., Pilpel, Y. Differential translation efficiency of orthologous genes is involved in phenotypic divergence of yeast species. Nat Genet 39, 415–421 (2007). https://doi.org/10.1038/ng1967

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