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Programmed and unprogrammed genomic rearrangements during the evolution of yeast species

Final Report Summary - CHROMARRANGE (Programmed and unprogrammed genomic rearrangements during the evolution of yeast species)

The goal of the project was to study particular rearrangements in the genomes of yeast species, with the specific aims of (1) understanding evolutionary processes that affect the organization of chromosomes, and (2) identifying ongoing processes that affect genome structure. We made substantial progress on both of these aspects:
1 – Evolutionary mechanisms: We discovered that the mating-type (MAT) locus is a hotspot of chromosomal rearrangement, and that its emergence as a hotspot coincides with the origin of the ‘copy-and-paste’ mechanism of mating-type switching that is used by some species including Saccharomyces cerevisiae. The hotspot activity is attributed to occasional errors that occur during switching, resulting in deletions and/or transpositions of DNA that previously flanked the MAT locus. We established that loss of the MAT locus gene MATa2 coincided with the occurrence of the whole-genome duplication in family Saccharomycetaceae. We identified dramatic reorganizations of centromere structure in the yeast genus Naumovozyma, and we identified a new type of centromere in the methylotrophic yeast Pichia pastoris.
2 – Ongoing processes of genome rearrangement: We discovered that a recurring inversion polymorphism of a large chromosomal region in several methylotrophic yeast species is caused by an unusual process of mating-type switching. We found the same mechanism in Ascoidea rubescens, a distantly related yeast that is an outgroup both to methylotrophs and to the Saccharomyces clade, indicating that this mechanism of switching-by-inversion is an evolutionary ancestor of the copy-and-paste mechanism of switching used by Saccharomyces. Separately, we characterized an analogous recurring inversion polymorphism in Saccharomyces.