Dataset Information

Interplay of Chimeric Mating-Type Loci Impairs Fertility Rescue and Accounts for Intra-Strain Variability in Zygosaccharomyces rouxii Interspecies Hybrid ATCC42981.

ABSTRACT: The pre-whole genome duplication (WGD) Zygosaccharomyces clade comprises several allodiploid strain/species with industrially interesting traits. The salt-tolerant yeast ATCC42981 is a sterile and allodiploid strain which contains two subgenomes, one of them resembling the haploid parental species Z. rouxii. Recently, different mating-type-like (MTL) loci repertoires were reported for ATCC42981 and the Japanese strain JCM22060, which are considered two stocks of the same strain. MTL reconstruction by direct sequencing approach is challenging due to gene redundancy, structure complexities, and allodiploid nature of ATCC42981. Here, DBG2OLC and MaSuRCA hybrid de novo assemblies of ONT and Illumina reads were combined with in vitro long PCR to definitively solve these incongruences. ATCC42981 exhibits several chimeric MTL loci resulting from reciprocal translocation between parental haplotypes and retains two MATa/MAT? expression loci, in contrast to MAT? in JCM22060. Consistently to these reconstructions, JCM22060, but not ATCC42981, undergoes mating and meiosis. To ascertain whether the damage of one allele at the MAT locus regains the complete sexual cycle in ATCC42981, we removed the MAT? expressed locus by gene deletion. The resulting MATa/- hemizygous mutants did not show any evidence of sporulation, as well as of self- and out-crossing fertility, probably because incomplete silencing at the chimeric HML? cassette masks the loss of heterozygosity at the MAT locus. We also found that MAT? deletion switched off a2 transcription, an activator of a-specific genes in pre-WGD species. These findings suggest that regulatory scheme of cell identity needs to be further investigated in Z. rouxii protoploid yeast.

SUBMITTER: Bizzarri M

PROVIDER: S-EPMC6405483 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Interplay of Chimeric Mating-Type Loci Impairs Fertility Rescue and Accounts for Intra-Strain Variability in Zygosaccharomyces rouxii Interspecies Hybrid ATCC42981.

Bizzarri Melissa M Cassanelli Stefano S Bartolini Laura L Pryszcz Leszek P LP Dušková Michala M Sychrová Hana H Solieri Lisa L

Frontiers in genetics 20190301

The pre-whole genome duplication (WGD) Zygosaccharomyces clade comprises several allodiploid strain/species with industrially interesting traits. The salt-tolerant yeast ATCC42981 is a sterile and allodiploid strain which contains two subgenomes, one of them resembling the haploid parental species Z. rouxii. Recently, different mating-type-like (MTL) loci repertoires were reported for ATCC42981 and the Japanese strain JCM22060, which are considered two stocks of the same str ...[more]

PMID: 30881382

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Project description:The mechanism of whole-genome duplication (WGD) in yeast has been intensively studied because it has a large impact on yeast evolution. WGD has shaped the genomic architecture of modern Saccharomyces cerevisiae; however, the mechanism for restoring fertility after interspecies hybridization, which would be involved in the process of WGD, has not been thoroughly elucidated. In this study, we obtained a draft genome sequence of the salt-tolerant yeast Zygosaccharomyces rouxii NBRC110957 and revealed that it is a hybrid lineage of Z. rouxii (allodiploid) with two subgenomes equivalent to NBRC1876. Because this allodiploid yeast can mate with other allodiploid strains and form spores, it can be a good model of restoring fertility after interspecies hybridization. We observed that NBRC110957 and NBRC1876 contain six mating-type-like (MTL) loci. There are no large deletions or deleterious mutations in MTL loci, except for several-base-pair deletions in the X region in certain MTL loci. We also assigned only one mating-type (MAT) locus that exclusively determines mating types from six MTL loci. These results suggest that it is possible to recover mating competence regardless of whether cells lose one MAT locus through random gene loss by mitotically dividing after interspecies hybridization. Moreover, we propose that perturbation of gene expression and substantial breakdown of MAT heterozygosity caused by chromosomal rearrangement at MTL loci play roles in restoring the mating competence of allodiploids. This scenario can provide a mechanism for restoring fertility after interspecies hybridization that is compatible with random gene loss models and suggests genomic plasticity during WGD in yeast.IMPORTANCE A whole-genome duplication occurred in an ancestor of the baker's yeast Saccharomyces cerevisiae The origins of this complex and multifaceted process, which requires intra- or interspecies hybridization followed by dysfunction of one mating-type (MAT) locus to regain mating competence, has not been thoroughly elucidated. In this study, we provide a mechanism for regaining fertility in an interspecies hybrid, Zygosaccharomyces rouxii The draft genome sequence analysis and mating test showed that the Z. rouxii strain used in this study is an intact interspecies hybrid, suggesting that it is possible to recover fertility regardless of whether cells lose one MAT locus.

Project description:In soy sauce manufacturing, Candida versatilis plays a role in the production of volatile flavor compounds, such as volatile phenols, but limited accessible information on its genome has prevented further investigation regarding aroma production and breeding. Although the draft genome sequence data of two strains of C. versatilis have recently been reported, these strains are not similar to each other. Here, we reassess the draft genome sequence data for strain t-1, which was originally reported to be C. versatilis, and conclude that strain t-1 is most probably not C. versatilis but a gamete of hybrid Zygosaccharomyces rouxii Phylogenetic analysis of the D1/D2 region of the 26S ribosomal DNA (rDNA) sequence indicated that strain t-1 is more similar to the genus Zygosaccharomyces than to C. versatilis Moreover, we found that the genome of strain t-1 is composed of haploid genome content and divided into two regions that show approximately 100% identity with the T or P subgenome derived from the natural hybrid Zygosaccharomyces rouxii, such as NBRC110957 and NBRC1876. We also found a chromosome crossing-over signature in the scaffolds of strain t-1. These results suggest that strain t-1 is a gamete of the hybrid Z. rouxii, generated by either meiosis or chromosome loss following reciprocal translocation between the T and P subgenomes. Although it is unclear why strain t-1 was misidentified as C. versatilis, the genome of strain t-1 has broad implications for considering the evolutionary fate of an allodiploid.IMPORTANCE In yeast, crossing between different species sometimes leads to interspecies hybrids. The hybrid generally cannot produce viable spores because dissimilarity of parental genomes prevents normal chromosome segregation during meiotic division, leading to a dead end. Thus, only a few natural cases of homoploid hybrid speciation, which requires mating between 1n gametes of hybrids, have been described. However, a recent study provided strong evidence that homoploid hybrid speciation is initiated in natural populations of the budding yeast, suggesting the potential presence of viable 1n gametes of hybrids. The significance of our study is finding that the strain t-1, which had been misidentified as Candida versatilis, is a viable 1n gamete derived from hybrid Zygosaccharomyces rouxii.

Dataset Information

Interplay of Chimeric Mating-Type Loci Impairs Fertility Rescue and Accounts for Intra-Strain Variability in Zygosaccharomyces rouxii Interspecies Hybrid ATCC42981.

Publications

Interplay of Chimeric Mating-Type Loci Impairs Fertility Rescue and Accounts for Intra-Strain Variability in <i>Zygosaccharomyces rouxii</i> Interspecies Hybrid ATCC42981.

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