Highly Variable Rates of Genome Rearrangements between Hemiascomycetous Yeast Lineages

Abstract

Hemiascomycete yeasts cover an evolutionary span comparable to that of the entire phylum of chordates. Since this group currently contains the largest number of complete genome sequences it presents unique opportunities to understand the evolution of genome organization in eukaryotes. We inferred rates of genome instability on all branches of a phylogenetic tree for 11 species and calculated species-specific rates of genome rearrangements. We characterized all inversion events that occurred within synteny blocks between six representatives of the different lineages. We show that the rates of macro- and microrearrangements of gene order are correlated within individual lineages but are highly variable across different lineages. The most unstable genomes correspond to the pathogenic yeasts Candida albicans and Candida glabrata. 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 Saccharomyces cerevisiae, tend to remain syntenic during evolution. This work reveals that the high plasticity of eukaryotic genomes results from rearrangement rates that vary between lineages but also at different evolutionary times of a given lineage. The yeast Saccharomyces cerevisiae has proved to be a very powerful model organism for deciphering the molecular functioning of our cells. It also is the first eukaryote (the domain of life that includes human) whose genome has been completely sequenced in 1996. There are hundreds of species of yeast covering a tremendous genetic diversity. Almost ten years after the release of the first complete eukaryotic genome sequence, yeasts are still at the forefront of the field of genomics as they represent the monophyletic group of eukaryotes for which the largest number of complete genome sequences has been unveiled. The comparative analysis of their organization now provides an exquisite tool to dissect the mechanistic underpinnings of the process of genome evolution. This study reveals the extraordinary plasticity of the eukaryotic genomes. It also shows that genomes get rearranged at different rates both between the different lineages but also at the different evolutionary times of a given lineage. Finally, in spite of their distant phylogenetic relationship, pathogenic yeasts such as the two main causatives of human candidiasis, Candida albicans and Candida glabrata species, harbor the most unstable genomes of all lineages.