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

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.

Contrasting Patterns of rDNA Homogenization within the Zygosaccharomyces rouxii Species Complex

“…The Z . rouxii species complex encompasses both asexual and sexual populations which could undergo different homogenization rates [ 35 , 76 ]. For category I, we can speculate that homogenized chimeric rDNA arrays sorted after meiosis, when putative hybrid ancestors produced rare viable spores with recombinant rDNA-containing chromosomes ( Fig 7 ).…”

“…In plants, epigenetic silencing of rDNA loci also influences evolutionary patterns of rDNA homogenization, because silenced arrays are less prone to concerted evolution than those actively transcribed [ 76 ]. Given that rRNA genes are highly transcribed and tightly controlled, any genomic modifications at rRNA loci (such as differential upregulation/suppression of rRNA variants) will translate into “extra-coding functions” affecting a multitude of cellular processes [ 78 ].…”

Draft Genome Sequences of the Highly Halotolerant Strain Zygosaccharomyces rouxii ATCC 42981 and the Novel Allodiploid Strain Zygosaccharomyces sapae ATB301 T Obtained Using the MinION Platform

“…The halotolerant yeasts of the genus Zygosaccharomyces find relevant applications in food spoilage and fermentation ( 1 ). They exhibit high diversity in response to high solute concentrations, tendency to hybridization, and ectopic recombination at the mating type loci, leading to ploidy and karyotype variation ( 2 , 3 ). Zygosaccharomyces rouxii ATCC 42981 is an allodiploid strain isolated from Japanese miso, which grows at NaCl and dextrose concentrations up to 3.0 M and 70% (wt/vol), respectively ( 4 ).…”

“…Under standard conditions, ATCC 42981 produces more glycerol than does ABT301 T and better retains it in the cell under conditions of salt stress ( 6 ). ATCC 42981 is thought to have arisen from hybridization between two divergent parents ( 3 , 5 , 7 – 9 ), while no evidence about the origin of strain ABT301 T is available. Here, we present the draft genome sequences of ATCC 42981 and ABT301 T .…”

Recent Advances in Understanding Yeast Genetics of Sex Determination

“…Furthermore, translocation events make the MTL flanking regions variable in strains of the same species. Finally in the Z. sapae type strain ABT301 T , with aααα genotype, an unusual cassette configuration without a HMR silent cassette [11], makes difficult the αa switching and dys-regulates cell-type identity [21].…”