Contrasting modes of macro and microsynteny evolution in a eukaryotic subphylum

Examination of the changes in order and arrangement of homologous genes is key for understanding the mechanisms of genome evolution in eukaryotes. Previous comparisons between eukaryotic genomes have revealed considerable conservation across species that diverged hundreds of millions of years ago (e.g., vertebrates,1-3 bilaterian animals,4,5 and filamentous fungi6). However, understanding how genome organization evolves within and between eukaryotic major lineages remains underexplored. We analyzed high quality genomes of 120 representative budding yeast species (subphylum Saccharomycotina) spanning-400 million years of eukaryotic evolution to examine how their genome organization evolved and to compare it with the evolution of animal and plant genome organization.7 We found that the decay of both macrosynteny (the conservation of homologous chromosomes) and microsynteny (the conservation of local gene content and order) was strongly associated with evolutionary divergence across budding yeast major clades. However, although macrosynteny decayed very fast, within-100 million years, the microsynteny of many genes-especially genes in metabolic clusters (e.g., in the GAL gene cluster8)-was much more deeply conserved both within major clades and across the subphylum. We further found that when genomes with similar evolutionary divergence times were compared, budding yeasts had lower macrosynteny conservation than animals and filamentous fungi but higher conservation than angiosperms. In contrast, budding yeasts had levels of microsynteny conservation on par with mammals, whereas angiosperms exhibited very low conservation. Our results provide new insight into the tempo and mode of the evolution of gene and genome organization across an entire eukaryotic subphylum.

Automated summary

Examining the changes in order and arrangement of homologous genes is crucial for understanding genome evolution in eukaryotes. This study analyzed 120 high quality genomes of budding yeast species to investigate the evolution of genome organization and compared it with animals and plants. The decay of macrosynteny and microsynteny was strongly associated with evolutionary divergence in the budding yeast major clades. However, the microsynteny of many genes, especially in metabolic clusters, was deeply conserved within major clades and across subphylum. Comparing genomes with similar divergence times, budding yeasts showed lower conservation in macrosynteny compared to animals and filamentous fungi, but higher conservation than angiosperms. In contrast, they exhibited similar levels of microsynteny conservation with mammals, while angiosperms had very low conservation.