Evolutionary remodeling of chromosomes maps in yeasts
Unité de Génétique Moléculaire des Levures, Institut Pasteur, 25, rue du Docteur Roux, 75724 Paris Cedex 15
The Génolevures I program represented the fist attempt to explored the genetic diversity present within a whole class of eukaryotes, the hemiascomycetous yeasts (Souciet et al., FEBS Letters, 2000). The second phase of the Génolevures program lead to the release of 4 complete genome sequences of species covering the entire evolutionary range present within this group (Dujon et al., Nature, 2004). Presently, the (nearly) complete genome sequences of about two dozen yeast species have been reported, allowing the development of powerful comparative approaches to decipher the mechanisms of genome evolution. The level of genetic diversity spanned by these species is often unsuspected. For instance, the average protein divergence of more than 50% found between Saccharomyces cerevisiae and Yarrowia lipolytica, an alkane-using yeast, reveals that Hemiascomycetes are molecularly as diverse as the entire phylum of chordate. We used the complete (or nearly complete) genome sequences of 11 yeast species covering the entire clade to quantify the rates of gene order changes in the different branches of the Hemiascomycete tree. We also identified all inversion events that occurred within synteny blocks conserved between pairwise comparisons of 6 fully sequenced genomes corresponding to representative species from the different lineages. We showed that the rates of macro- and microrearrangements of gene order are correlated within individual lineages but are highly variable across the different lineages. The most unstable genomes correspond to yeasts adapted to a particular host, like pathogens, followed by the ones that have inherited a whole genome duplication event. We found a tremendous level of chromosomal reorganization outside of the Saccharomyces sensu stricto¹ species. Chromosomal maps have been intensively shuffled by numerous interchromosomal rearrangements, even between species that have retained a very high physical fraction of their genomes within small synteny blocks. Despite this intensive reshuffling of gene positions, essential genes, which cluster in low recombination regions in the genome of S. cerevisiae, tend to remain adjacent during evolution, indicating selective constraints onto gene order preservation. This work suggests that these constraints might be alleviated by increased genome redundancy and decreased effective population sizes.