Highly Variable Rates of Genome Rearrangements between Hemiascomycetous Yeast Lineages

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.半子囊菌酵母（Hemiascomycete yeasts）的演化跨度可与整个脊索动物门（Chordata）相媲美。由于该类群目前拥有数量最多的完整基因组序列，因此为解析真核生物基因组组织的演化提供了独一无二的研究契机。我们针对涵盖11个物种的系统发育树的所有分支，推断了基因组不稳定性速率，并计算了物种特异性的基因组重排速率。我们对不同演化分支的6个代表物种之间，同线块（synteny block）内部发生的全部倒位事件进行了系统表征。研究表明，基因顺序的宏观重排与微观重排速率在单个演化分支内呈显著相关，但在不同分支间存在极高的异质性。基因组最不稳定的类群为致病性酵母白色念珠菌（Candida albicans）与光滑念珠菌（Candida glabrata）。即便在那些仍在小同线块中保留了极高比例基因组物理序列的物种之间，染色体图谱也因大量染色体间重排而被广泛打乱。尽管基因位置经历了如此剧烈的重排，但在酿酒酵母（Saccharomyces cerevisiae）基因组中聚集于低重组区域的必需基因，在演化过程中仍倾向于保持同线性。本研究揭示，真核基因组的高度可塑性，源于不同演化分支间以及同一演化分支不同演化阶段的重排速率差异。