Diversity of Mating-Type Chromosome Structures in the Yeast Zygosaccharomyces rouxii Caused by Ectopic Exchanges between MAT-Like Loci

Jun Watanabe,Yoshinobu Mogi,Kenji Uehara,Laura N Rusche

doi:10.1371/journal.pone.0062121

Abstract

We investigated sex chromosome diversity in Zygosaccharomyces rouxii (Z. rouxii). In the current study, we show that the organization of the mating-type (MAT) locus is highly variable in the Z. rouxii population, indicating the MAT, HML, and HMR loci are translocation hotspots. Although NBRC1130 and CBS732 were originally two stocks of the type strain of the species, only NBRC1130 retains the original karyotype. A reciprocal translocation between the MAT and HMR loci appears to have occurred during the early passage culture of CBS732, which was used for genome sequencing. In NBRC1733, NBRC0686, NBRC0740 and NBRC1053, the terminal region of the chromosome containing the HMR locus was replaced with the chromosomal region to the left of the MAT or HML loci. The translocation events found in NBRC1733, NBRC0686, NBRC0740, and NBRC1053 were reconstructed under our experimental conditions using the DA2 background, and the reconstruction suggests that the frequency of this type of translocation is approximately 10−7. These results suggest that the MAT and MAT-like loci were the susceptible regions in the genome, and the diversity of mating-type chromosome structures in Z. rouxii was caused by ectopic exchanges between MAT-like loci.

Highlights

Chromosomal rearrangements, which include translocations and large-scale deletions, play key roles in phenotypic variation, genome evolution and genetic disease [1,2]
Isolation of a CBS732-like haploid strain in Z. rouxii Recent studies have shown that various strains originally identified as ‘‘Z. rouxii’’ in yeast culture collections comprise at least three groups: Z. rouxii type strain group, Zygosaccharomyces sp. group, and an allopolyploid group
Solieri et al showed that the group of Z. rouxii-related strains is a complex of haploid and diploid heterogeneous species including: 1) the haploid species Z. rouxii, e.g., CBS732; 2) the diploid species Z. sapae, isolated from high sugar environments; and 3) a diploid mosaic lineage that includes strains retrieved from a salty environment (Fig. S1A) [12,13]

Summary

Introduction

Chromosomal rearrangements, which include translocations and large-scale deletions, play key roles in phenotypic variation, genome evolution and genetic disease [1,2]. During the evolution of the Saccharomycetaceae, translocations have cycled telomere location, and the mating-type (MAT) locus has been a deletion hotspot [3,4]. Based on extensive analysis of yeast sex evolution, mating-type switching has evolved from a two-step process: gain of silent cassettes and HO endonuclease [6]. These two-step events occurred after the ancestor of hemiascomycetous yeast had diverged from other families, such as genus Debaryomyces and Kluyveromyces. The K. lactis gene and the S. castellii gene likely evolved independently of HO, which was acquired late in the evolution of hemiascomycetes [5]. Whether the HO gene was regulated immediately after it was acquired is unknown

Methods

Results

Conclusion