Abstract
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 MTLa copies 1 to 3) were recognized, which shared the same MATa1 ORFs but diverged for MATa2 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 a1-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 MATα1 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 a1-α2 heterodimer could be involved in the generation of negative epistasis, contributing to the allodiploid sterility and the dysregulation of cell identity.
Highlights
Ploidy variation has played a major role in the evolution of many extant eukaryotic lineages [1]
To increase the probability of observing conjugated or un-conjugated spore-containing ascii, sporulation was tested by inoculating the early stationary phase culture of ATCC 42981 on five different media [YPD, YPDA, malt extract agar (MEA; Difco), MEA supplemented with 6% (w/v) NaCl (6%NaCl-MEA), and YNB5%GNaCl (1% w/v yeast extract, 5% w/v dextrose, 6.7 g/l yeast nitrogen base, 2.0 M NaCl)] for 3 weeks
Examination under the microscope did not show any evidence of mating reaction of ATCC 42981 cells neither with Z. rouxii CBS 4837 or CBS 4838 tester strains, even after 3 weeks of incubation both on MEA and 6% NaCl-MEA media
Summary
Ploidy variation has played a major role in the evolution of many extant eukaryotic lineages [1]. Numerous studies have demonstrated how variations in the ploidy state took place frequently during evolutionary history [2] [3]. Allodiploid offspring often have strong selective disadvantages due to their sterility [4]. In some instances, the increased genome size and complexity of allodiploids may enhance heterosis and/or adaptive flexibility [5], at the edges of the ancestral species' range, where they are more likely to encounter stress [6] [7]; [8]. Life history models note that there is an intricate interplay between ploidy variation and alterations of mating, meiosis and sporulation patterns [9]. The ploidy state affects the genetic composition at sex-determining loci, giving rise to the ploidy-dependent initiation of dedicated transcriptional programs [10]
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