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Molecular evidence for an ancient duplication of the entire yeast genome

Abstract

Gene duplication is an important source of evolutionary novelty1,2. Most duplications are of just a single gene, but Ohno1 proposed that whole-genome duplication (polyploidy) is an important evolutionary mechanism. Many duplicate genes have been found in Saccharomyces cerevisiae, and these often seem to be phenotypically redundant3,4,5,6,7. Here we show that the arrangement of duplicated genes in the S. cerevisiae genome is consistent with Ohno's hypothesis. We propose a model in which this species is a degenerate tetraploid resulting from a whole-genome duplication that occurred after the divergence of Saccharomyces from Kluyveromyces. Only a small fraction of the genes were subsequently retained in duplicate (most were deleted), and gene order was rearranged by many reciprocal translocations between chromosomes. Protein pairs derived from this duplication event make up 13% of all yeast proteins, and include pairs of transcription factors, protein kinases, myosins, cyclins and pheromones. Tetraploidy may have facilitated the evolution of anaerobic fermentation in Saccharomyces.

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Figure 1: Locations of similar genes on chromosomes X and XI.
Figure 2: Locations of 55 duplicated chromosomal regions.
Figure 3: Phylogenetic analysis of S.cerevisiae gene pairs and their K. lactis or K. marxianus homologues.

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Acknowledgements

We thank our colleagues in the yeast genome project; J. I. Garrels for use of the YPD database, which was central to this study; G. Butler, A. T. Lloyd, L. Skrabanek, C. Seoighe, B. Baum and R.Rothstein for comments; and S. Kossida, M. Lewis and R. Keogh for initial work on this project. Yeast genome sequencing in our laboratory was supported by the European Union. In silico analysis is supported by the European Union and Forbairt (to K.H.W.) and the Wellcome Trust (to D.C.S.).

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Correspondence to Kenneth H. Wolfe.

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Wolfe, K., Shields, D. Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387, 708–713 (1997). https://doi.org/10.1038/42711

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