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

Watanabe, Jun; Uehara, Kenji; Mogi, Yoshinobu

doi:10.1371/journal.pone.0062121

Cited by 25 publications

(64 citation statements)

References 27 publications

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“…S2) and placed the peak signal from chromosome 3 at position 897 kb, which is 3 kb from the leftmost IR and 5 kb from the MATalpha genes. The centromeric region is transcriptionally silent (SI Appendix, (3,4,(12)(13)(14)(15)(16)(17)(18). Saccharomycotina, Pezizomycotina, and Taphrinomycotina are subphyla within phylum Ascomycota (19).…”

Section: Resultsmentioning

confidence: 99%

Mating-type switching by chromosomal inversion in methylotrophic yeasts suggests an origin for the three-locusSaccharomyces cerevisiaesystem

Hanson

Byrne

Wolfe

2014

Proc. Natl. Acad. Sci. U.S.A.

150

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Saccharomyces cerevisiae has a complex system for switching the mating type of haploid cells, requiring the genome to have three mating-type (MAT)-like loci and a mechanism for silencing two of them. How this system originated is unknown, because the threelocus system is present throughout the family Saccharomycetaceae, whereas species in the sister Candida clade have only one locus and do not switch. Here we show that yeasts in a third clade, the methylotrophs, have a simpler two-locus switching system based on reversible inversion of a section of chromosome with MATa genes at one end and MATalpha genes at the other end. In Hansenula polymorpha the 19-kb invertible region lies beside a centromere so that, depending on the orientation, either MATa or MATalpha is silenced by centromeric chromatin. In Pichia pastoris, the orientation of a 138-kb invertible region puts either MATa or MATalpha beside a telomere and represses transcription of MATa2 or MATalpha2. Both species are homothallic, and inversion of their MAT regions can be induced by crossing two strains of the same mating type. The three-locus system of S. cerevisiae, which uses a nonconservative mechanism to replace DNA at MAT, likely evolved from a conservative two-locus system that swapped genes between expression and nonexpression sites by inversion. The increasing complexity of the switching apparatus, with three loci, donor bias, and cell lineage tracking, can be explained by continuous selection to increase sporulation ability in young colonies. Our results provide an evolutionary context for the diversity of switching and silencing mechanisms.Hansenula polymorpha | Pichia pastoris | yeast genetics | comparative genomics M ating-type switching in yeasts is a highly regulated process that converts a haploid cell of one mating type into a haploid of the opposite type (1-5). Switching involves the complete deactivation of one set of regulatory genes and activation of an alternative set, but, unlike most regulatory changes, the switch is achieved by physically replacing the DNA at an expression site that is shared by both types of cell. In Saccharomyces cerevisiae the switching system uses a menagerie of molecular components (3) including three mating-type (MAT)-like loci (the expressed MAT locus and the silent loci HML and HMR); an endonuclease (HO) that creates a double-strand break at the MAT locus, which then is repaired using HMLalpha or HMRa as a donor; a mechanism (Sir1 and Sir2/3/4 proteins) for repressing transcription and HO cleavage at the silent loci; two triplicated sequences (the Z and X regions) that guide repair of the dsDNA break; a donorbias mechanism (the recombination enhancer, RE) to ensure that switching happens in the correct direction; and a cell lineagetracking mechanism (Ash1 mRNA localization) to ensure that switching occurs only in particular cells. Most of these components have no function other than facilitating switching.

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Section: Resultsmentioning

confidence: 99%

Mating-type switching by chromosomal inversion in methylotrophic yeasts suggests an origin for the three-locusSaccharomyces cerevisiaesystem

Hanson

Byrne

Wolfe

2014

Proc. Natl. Acad. Sci. U.S.A.

150

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“…Such events of unusual recombination can cause changes in breeding systems from heterothallism to homothallism as observed in Aspergillus nidulans (Paoletti et al , 2007), Neurospora spp. (Ellison et al , 2011; Gioti et al , 2012), S. sclerotiorum (Chitrampalam et al , 2013), Grosmannia clavigera (Tsui et al , 2013), and Zygosaccharomyces rouxii (Watanabe et al , 2013). Meiotic crossing-over events that reorganize the mating-type locus as a step toward homothallism likely occurred between the homologous chromosomes bearing the mating-type regions.…”

Section: Three Impacts Of Recombination Associated With Mating Typementioning

confidence: 99%

Contrasted patterns in mating-type chromosomes in fungi: Hotspots versus coldspots of recombination

Idnurm

Hood

Johannesson

et al. 2015

Fungal Biology Reviews

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It is striking that, while central to sexual reproduction, the genomic regions determining sex or mating-types are often characterized by suppressed recombination that leads to a decrease in the efficiency of selection, shelters genetic load, and inevitably contributes to their genic degeneration. Research on model and lesser-explored fungi has revealed similarities in recombination suppression of the genomic regions involved in mating compatibility across eukaryotes, but fungi also provide opposite examples of enhanced recombination in the genomic regions that determine their mating types. These contrasted patterns of genetic recombination (sensu lato, including gene conversion and ectopic recombination) in regions of the genome involved in mating compatibility point to important yet complex processes occurring in their evolution. A number of pieces in this puzzle remain to be solved, in particular on the unclear selective forces that may cause the patterns of recombination, prompting theoretical developments and experimental studies. This review thus points to fungi as a fascinating group for studying the various evolutionary forces at play in the genomic regions involved in mating compatibility.

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“…To summarize, the first round of long-range PCR was done with high-fidelity DNA polymerase (Phusion, Thermofisher) and the external primers 1, 2, 3, A, B, B′, C (Watanabe et al 2013), and DownMATa1R1 (this study) in 20 µL of reaction volume, following the manufacturer’s instructions. Subsequently, a seminested PCR amplification was done using a 1:20 dilution of the previous PCR and internal MTL locus-specific primers.…”

Section: Methodsmentioning

confidence: 99%

Sex-Determination System in the Diploid Yeast Zygosaccharomyces sapae

Solieri

Dakal

Giudici

et al. 2014

G3 Genes|Genomes|Genetics

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Sexual reproduction and breeding systems are driving forces for genetic diversity. The mating-type (MAT) locus represents a mutation and chromosome rearrangement hotspot in yeasts. Zygosaccharomyces rouxii complex yeasts are naturally faced with hostile low water activity (aw) environments and are characterized by gene copy number variation, genome instability, and aneuploidy/allodiploidy. Here, we investigated sex-determination system in Zygosaccharomyces sapae diploid strain ABT301T, a member of the Z. rouxii complex. We cloned three divergent mating type-like (MTL) α-idiomorph sequences and designated them as ZsMTLα copies 1, 2, and 3. They encode homologs of Z. rouxii CBS 732T MATα2 (amino acid sequence identities spanning from 67.0 to 99.5%) and MATα1 (identity range 81.5–99.5%). ABT301T possesses two divergent HO genes encoding distinct endonucleases 100% and 92.3% identical to Z. rouxii HO. Cloning of MATa-idiomorph resulted in a single ZsMTLa locus encoding two Z. rouxii-like proteins MATa1 and MATa2. To assign the cloned ZsMTLα and ZsMTLa idiomorphs as MAT, HML, and HMR cassettes, we analyzed their flanking regions. Three ZsMTLα loci exhibited the DIC1-MAT-SLA2 gene order canonical for MAT expression loci. Furthermore, four putative HML cassettes were identified, two containing the ZsMTLα copy 1 and the remaining harboring ZsMTLα copies 2 and 3. Finally, the ZsMTLa locus was 3′-flanked by SLA2, suggesting the status of MAT expression locus. In conclusion, Z. sapae ABT301T displays an aααα genotype missing of the HMR silent cassette. Our results demonstrated that mating-type switching is a hypermutagenic process in Z. rouxii complex that generates genetic diversity de novo. This error-prone mechanism could be suitable to generate progenies more rapidly adaptable to hostile environments.

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

Cited by 25 publications

References 27 publications

Mating-type switching by chromosomal inversion in methylotrophic yeasts suggests an origin for the three-locusSaccharomyces cerevisiaesystem

Mating-type switching by chromosomal inversion in methylotrophic yeasts suggests an origin for the three-locusSaccharomyces cerevisiaesystem

Contrasted patterns in mating-type chromosomes in fungi: Hotspots versus coldspots of recombination

Sex-Determination System in the Diploid Yeast Zygosaccharomyces sapae

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