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Allodiploidization is a fundamental yet evolutionarily poorly characterized event, which impacts genome evolution and heredity, controlling organismal development and polyploid cell-types. In this study, we investigated the sex determination system in the allodiploid and sterile ATCC 42981 yeast, a member of the  Zygosaccharomyces rouxii  species complex, and used it to study how a chimeric mating-type gene repertoire contributes to hybrid reproductive isolation. We found that ATCC 42981 has 7  MAT -like ( MTL ) loci, 3 of which encode α-idiomorph and 4 encode  a -idiomorph. Two phylogenetically divergent  MAT  expression loci were identified on different chromosomes, accounting for a hybrid  a /α genotype. Furthermore, extra  a -idimorph-encoding loci (termed  MTL  a  copies 1 to 3) were recognized, which shared the same  MAT  a 1 ORFs but diverged for  MAT  a 2 genes. Each  MAT  expression locus was linked to a  HML  silent cassette, while the corresponding  HMR  loci were located on another chromosome. Two putative parental sex chromosome pairs contributed to this unusual genomic architecture: one came from an as-yet-undescribed taxon, which has the NCYC 3042 strain as a unique representative, while the other did not match any  MAT - HML  and  HMR  organizations previously described in  Z .  rouxii  species. This chimeric rearrangement produces two copies of the  HO  gene, which encode for putatively functional endonucleases essential for mating-type switching. Although both  a  and α coding sequences, which are required to obtain a functional cell-type  a 1-α2 regulator, were present in the allodiploid ATCC 42981 genome, the transcriptional circuit, which regulates entry into meiosis in response to meiosis-inducing salt stress, appeared to be turned off. Furthermore, haploid and α-specific genes, such as  MAT α1 and  HO , were observed to be actively transcribed and up-regulated under hypersaline stress. Overall, these evidences demonstrate that ATCC 42981 is unable to repress haploid α-specific genes and to activate meiosis in response to stress. We argue that sequence divergence within the chimeric  a 1-α2 heterodimer could be involved in the generation of negative epistasis, contributing to the allodiploid sterility and the dysregulation of cell identity.

Chimeric Sex-Determining Chromosomal Regions and Dysregulation of Cell-Type Identity in a Sterile Zygosaccharomyces Allodiploid Yeast