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.

Figure 1. Phylogeny of Hemiascomycete Species

The phylogenetic tree was built on the concatenated sequences of 25 proteins having clear orthologs in all of the 11 studied species. Bootstraps of the tree are given at the branches (out of 1,000). Species whose names are underlined correspond to fully sequenced genomes for which the number of supercontigs is identical to the number of chromosomes. The arrow indicates the place where the whole genome duplication (WGD) event occurred in the tree.

Figure 2. Rates of Genome Instability in Hemiascomycetes

(A) Branch-specific normalized rates of genome rearrangements are indicated either in red or in blue illustrating higher or lower rates than average, respectively. Nodes are numbered from 1 to 9. (B) Cumulated rates of genome instability correspond to the ratios between the sum of the branch-specific GOL and the phylogenetic distance separating each species from node 1 (Table 2).

Figure 3. Branch-Specific Expected Number of Inversions per Gene

The tree topology is deduced from Figure 1. The nodes are numbered from 1 to 4. Calculated inversion numbers are indicated on each branch of the tree.

Figure 4. Chromosomal Map Reorganization between Related Species

The circular representation is adapted from [25]. (A) Chromosome D from S. cerevisiae (Sc_D) is represented in a circle with the 13 chromosomes from C. glabrata (Cg_A to M). Each line joins two orthologs and the color of the lines represents the percentage of similarity between orthologous gene products (green ≤ 50% ≤ cyan ≤ 60% ≤ blue ≤ 70% ≤ magenta ≤ 80% ≤ dark magenta ≤ 90% ≤ red). (B) Same representation between chromosome C of K. lactis (Kl_C) and the seven chromosomes from A. gossypii (Ag_A to G). The diagram shows large uninterrupted regions of conserved synteny between Kl_C and Ag_F or Ag_A, while no such conservation is visible between Sc_D and any of the C. glabrata chromosomes. (C) Distribution of the length of the corresponding syntenic blocks between Sc_D and C. glabrata (black) and Kl_C and A. gossypii (gray).

Figure 5. Proportion of Essential Genes within Conserved Synteny Blocks

(A) The black bar represents the proportion of essential genes in the genome of S. cerevisiae (Sc), as defined in the Comprehensive Yeast Genome Database (http://mips.gsf.de/genre/proj/yeast). The relative proportions of orthologs to these genes among the total number of genes comprised within the syntenic blocks with the genomes of C. glabrata (Cg), K. lactis (Kl), D. hansenii (Dh), and Y. lipolytica (Yl) are represented by dark gray bars. Proportions of essential genes concomitantly conserved within synteny blocks in three, four, and five species are indicated by light gray bars. Error bars represent two standard deviations, and the number of genes considered in each case is indicated in parentheses. (B) Comparison of the proportions of essential genes among syntenic orthologs and among all orthologs at increasing phylogenetic distances. Phylogenetic distances between S. cerevisiae and C. glabrata, S. cerevisiae and K. lactis, S. cerevisiae and D. hansenii, and S. cerevisiae and Y. lipolytica are reported on the x-axis.