Hemiascomycetous Yeasts at the Forefront of Comparative Genomics Bernard Dujon
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Hemiascomycetous yeasts at the forefront of comparative genomics Bernard Dujon With more than a dozen species fully sequenced, as many as styles, yeasts form a much diversified group. Further- this partially sequenced, and more in development, yeasts are more, several of them, none more so than S. cerevisiae, are now used to explore the frontlines of comparative genomics of favoured organisms for genetic experiments. Most yeasts eukaryotes. Innovative procedures have been developed to sequenced to date are members of the Hemiascomycete compare and annotate genomes at various evolutionary class, the group of fungi to which budding yeasts belong distances, to identify short cis-acting regulatory elements, to and which, from genome analysis, was recently discov- map duplications, or to align syntenic blocks. Human and plant ered to cover an evolutionary range larger than that of the pathogens, in addition to yeasts that show a variety of entire phylum of Chordates [2]. Other yeasts belonging interesting physiological properties, are included in this to the Archiascomycetes or the Basidiomycetes have also multidimensional comparative survey, which encompasses a been sequenced but will not be discussed here, because very broad evolutionary range. As major steps of the the phylogenetic distances among those fungal groups are evolutionary history of hemiascomycetous genomes emerge, so considerable that it is difficult to compare genomes in precise questions on the general mechanisms of their evolution any detail. By contrast, comparisons within the Hemi- can be addressed, using both experimental and in silico ascomycetes can be performed at various phylogenetic methods. distances, depending on the type of question examined. Addresses The large-scale comparative exploration of hemiascomy- Unite´ de Ge´ ne´ tique mole´ culaire des levures (associated with CNRS cetous genomes started five years ago. Thirteen yeast and University Pierre and Marie Curie), Institut Pasteur, 25, rue du Docteur Roux, F-75724, Paris Cedex 15, France species, selected to sample various branches of the known phylogenetic tree, were sequenced at low coverage, and Corresponding author: Dujon, Bernard ([email protected]) each was compared with S. cerevisiae [3]. The results indicated the power of rapid genome survey to identify conserved or specific genes, to examine the evolution of Current Opinion in Genetics & Development 2005, 15:614–620 functional categories or to compare genetic maps in This review comes from a themed issue on search of the mechanisms of genome evolution. But yeast Genomes and evolution comparative genomics has considerably accelerated over Edited by Stephen J O’Brien and Claire M Fraser the past two years, with the successive publications of the Available online 26th September 2005 complete or high-coverage sequences of a large panel of yeast species, selected on the basis of their intrinsic 0959-437X/$ – see front matter interest and/or for their phylogenetic position. Some # 2005 Elsevier Ltd. All rights reserved. species are major human pathogens; others are used in DOI 10.1016/j.gde.2005.09.005 food processing. Some are able to propagate on a variety of natural substrates; others show specific niche adapta- tion. The novel genomic data were used to examine Introduction questions of general significance regarding eukaryotic Less than ten years have now passed since the first DNA genome evolution, but they also served to explore and sequence of a eukaryotic organism — that of the baker’s develop novel methods and strategies of general applic- yeast, Saccharomyces cerevisiae — was entirely unveiled [1]. ability for comparative genomics. Using the yeast This remarkable achievement quickly contributed to the sequences, a large variety of biological questions can emergence of functional genomics. But rare were those at now be addressed by experimental and/or in silico ana- this time who anticipated that, a few years later, the lyses. This short review only focuses on a limited number genome sequences of many other yeast species would of prominent results obtained during the past two years. also become available, promoting these unicellular fungi to the forefront of comparative genomics. Presently, the Comparative genomics on a short complete, near complete or partial genome sequences of evolutionary range: gene discovery, more than two dozen yeast species have been reported, speciation and identification of conserved offering a collection of genomic information without regulatory sites equal among other eukaryotic groups (Figure 1). The Several species of the Saccharomyces sensu stricto clade have significance of this novel situation, made possible by the been sequenced and compared [4,5]. Their sequence progress in sequencing techniques, emerges from the fact divergence is significant but they share very high map- that, despite their similar morphology and common life synteny (see Glossary), interrupted only by a limited Current Opinion in Genetics & Development 2005, 15:614–620 www.sciencedirect.com Hemiascomycetous yeasts at the forefront of comparative genomics Dujon 615 Glossary improved annotation of S. cerevisiae can, in turn, facilitate Allotetraploidy: The status of a cell or an organism having four full annotation of other yeasts and other eukaryotic organ- sets of chromosome complements, two derived from one diploid species, the other two from another, different, diploid species. isms. The novel genes need to be included in future Aneuploidy: The status of a cell or an organism having a non-uniform global functional studies. number of the different chromosomes. This status can be caused, for example, by the loss of one chromosome from a complete diploid set, The Saccharomyces sensu stricto clade was used to evaluate or by the addition of a supernumerary chromosome copy to a the power of comparative genomics to identify novel cis- complete chromosome set. Autotetraploidy: The status of a cell or an organism having four full regulatory sequences, which are otherwise difficult to sets of chromosome complements derived from the duplication of an recognize. Sequence alignments of intergenic regions originally diploid set. between these species, as well as with more distant yeasts, Collinearity: Relates to objects (for example, a gene and its facilitated the identification of numerous novel regulatory corresponding protein, or two chromosomes) having corresponding parts arranged in the same linear order. motifs [4,5]. Elements containing these motifs can then Gene conversion: The process by which a gene sequence be experimentally assayed or compared against the (acceptor) is partially replaced by a copy of another gene sequence sequences recently determined to be bound to transcrip- (donor) from the same genome. In general, the donor and acceptor tional regulators [10]. The recent systematic mapping of sequences must share a sufficient degree of sequence similarity (for transcriptional start sites in S. cerevisiae will also be helpful example, the two alleles in a diploid, or two paralogs). Paralogy: Homology between two non-allelic genes of the same [11]. The success of the comparative methods that have genome, derived by duplication from a common ancestor. been developed [12,13], which are of general interest for Synonymous substitution: A nucleotide substitution, in a gene investigation of many other organisms, obviously depends sequence encoding a protein, that does not result in an amino-acid on the set of sequenced species available [14]. But, change. Synteny: The common presence of genes along a given recently, the procedure has been successfully extended chromosome or chromosomal segment. The notion generally also to larger evolutionary distances, such as those found in implies the order of those genes. Hence, conservation of synteny filamentous fungi [15]. indicates the conservation of the order of homologous genes between two chromosomes or between chromosomal segments of different The broad evolutionary range covered by species. Hemiascomycetes: synteny, genome content, pathway conservation and niche adaptation number of chromosomal translocations and a higher num- Estimated to have separated from the fission yeast, Schi- ber of single gene-deletions [6]. Species definition is zosaccharomyces pombe, between 350 and 1000 million made on the basis of the post-zygotic barrier: viable years ago [16], Hemiascomycetes cover a broad evolu- hybrids easily form and are mitotically stable — some tionary range. Judging by the general distributions of are used for industrial fermentations — but they are conserved amino-acid identities between orthologous generally sterile at meiosis. In artificially produced inter- proteins, Candida glabrata and S. cerevisiae, for example, specific hybrids, the viability of meiotic spores can be are as distant from each other as are man and fishes [2]. partly restored by engineered reconstructions of map And much broader distances from S. cerevisiae exist for collinearity (see Glossary), but a high trend to aneuploidy other clades (for example, from Candida albicans or Yar- (see Glossary) remains [7]. rowia lipolytica; see Figure 1). The considerable reshuf- fling of genetics maps is congruent with these large One of the immediate impacts of genome comparisons evolutionary distances between clades [2,17,18]. between related organisms is the significant improvement When comparing species of different clades, mosaics of of sequence annotation. This has been true even for S. short conserved syntenic blocks, separated by