Abstract
Identifying the mechanisms of eukaryotic genome evolution by comparative genomics is often complicated by the multiplicity of events that have taken place throughout the history of individual lineages, leaving only distorted and superimposed traces in the genome of each living organism. The hemiascomycete yeasts, with their compact genomes, similar lifestyle and distinct sexual and physiological properties, provide a unique opportunity to explore such mechanisms. We present here the complete, assembled genome sequences of four yeast species, selected to represent a broad evolutionary range within a single eukaryotic phylum, that after analysis proved to be molecularly as diverse as the entire phylum of chordates. A total of approximately 24,200 novel genes were identified, the translation products of which were classified together with Saccharomyces cerevisiae proteins into about 4,700 families, forming the basis for interspecific comparisons. Analysis of chromosome maps and genome redundancies reveal that the different yeast lineages have evolved through a marked interplay between several distinct molecular mechanisms, including tandem gene repeat formation, segmental duplication, a massive genome duplication and extensive gene loss.
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Acknowledgements
We thank M. Tichit, S. Duthoy, S. Ferry and N. Zidane for technical assistance; A. Louis for help and expertise in the use of the INFOBIOGEN computational facilities; O. Jaillon, H. Roest-Crollius and their colleagues for sharing unpublished results on Tetraodon negroviridis; and A. Goffeau, H. Feldmann, A. Nicolas, N. Huu-Vang, J.-P. Latgé, I. Moszer and M. Vergassola for discussions and advice. This work was supported by the Consortium National de Recherche en Génomique (to Génoscope and to Institut Pasteur Génopole), the CNRS (GDR 2354, Génolevures sequencing consortium) and the ‘Conseil Régional d'Aquitaine’. B.D. is a member of Institut Universitaire de France.
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Supplementary information
Supplementary Table S1
List of centromeres for C. glabrata, K. lactis and Y. lipolytica with coordinates, sequences and flanking genes. (PDF 141 kb)
Supplementary Table S2
List of telomeric repeats and proteins of the telomerase complex of C. glabrata, K. lactis, D. hansenii and Y. lipolytica. (PDF 70 kb)
Supplementary Table S3
Full table of codon usage and number of tRNA genes in S. cerevisiae, C. glabrata, K. lactis, D. hansenii and Y. lipolytica. (PDF 147 kb)
Supplementary Table S4
Full list of introns in tRNA genes of S. cerevisiae, C. glabrata, K. lactis, D. hansenii and Y. lipolytica with their size (in nucleotides). (PDF 102 kb)
Supplementary Table S5
List of potentially co-transcribed tRNA gene pairs in C. glabrata, K. lactis, D. hansenii and Y. lipolytica with nature of gene involved, size of intergene and number of occurences in each genome. (PDF 63 kb)
Supplementary Table S6
List of all identified non-coding RNA genes in C. glabrata, K. lactis, D. hansenii and Y. lipolytica, with type, size of molecules, gene name, and chromosomal location. (PDF 70 kb)
Supplementary Figure S7
Phylogenetic tree of Hemisaacomycete yeast species derived from 25S rDNA sequences. (PDF 91 kb)
Supplementary Table S8
Full list of genes encountered in tandem arrays in any of the yeasts S. cerevisiae, C. glabrata, K. lactis, D. hansenii and Y. lipolytica with indication of gene number, protein family number and functional annotation. (PDF 137 kb)
Supplementary Table S9
A list of all recognized ancient duplication blocks in the genome of C. glabrata, with the names of paralogous gene duplicates involved, their map coordinates, and the corresponding ancient duplication blocks in the genome of S. cerevisiae, when coinciding. (PDF 82 kb)
Supplementary Table S10
List of S. cerevisiae genes with their functional annotation which are specifically absent in only one of the four yeast species C. glabrata, K. lactis, D. hansenii and Y. lipolytica (but present in the three others). (PDF 111 kb)
Supplementary Table S11
List of genes identified in the genomes of K. lactis, D. hansenii and Y. lipolytica, without homolog in other eucaryotes, including other yeasts and that probably correspond to horizontal gene transfer from bacterial origin. (PDF 108 kb)
Supplementary Methods S12
Details the successive steps followed in the classifiaction of the 34,824 proteins of S. cerevisiae, C. glabrata, K. lactis, D. hansenii and Y. lipolytica. (PDF 91 kb)
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Dujon, B., Sherman, D., Fischer, G. et al. Genome evolution in yeasts. Nature 430, 35–44 (2004). https://doi.org/10.1038/nature02579
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DOI: https://doi.org/10.1038/nature02579
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