Artificial chromosome reorganization reveals high plasticity of the budding and fission yeast genomes

The genome of a eukaryotic cell is usually organized on a set of chromosomes. Recently, karyotype engineering has been applied to various organisms, but whether and to what extent a naturally evolved genome can resist or tolerate massive artificial manipulations remains unexplored. Using unicellular yeast models of both Saccharomyces cerevisiae and Schizosaccharomyces pombe, we deliberately construct dozens of single-chromosome strains with different chromosome architectures. Three S. cerevisiae strains have the individual chromosomes fused into a single chromosome, but with the individual chromosomes in different orders. Eighteen S. cerevisiae strains have a single chromosome but with different centromeric sequences. Fifteen S. cerevisiae strains have a single chromosome with the centromere at different distances relative to the telomeres. Two S. pombe strains have a single, circular chromosome, and three strains have a single, linear chromosome with the centromere at different distances relative to the telomeres. All of these single-chromosome strains are viable, but the strains with an acrocentric or a telocentric chromosome have abnormal cell morphologies, and grow more slowly than those with a metacentric or sub-metacentric chromosome, and show increased genome instability with chromosome segregation abnormalities or genome diploidization. The functional genomes of both the evolutionarily distant yeasts S. cerevisiae and S. pombe are highly tolerant of diversified genome organizations. The phenotypic abnormalities and increased genome instability of the acrocentric/telocentric single-chromosome yeasts suggest that yeasts with metacentric chromosomes have an evolutionary advantage.