Abstract
Many interspecies hybrids have been discovered in yeasts, but most of these hybrids are asexual and can replicate only mitotically. Whole-genome duplication has been proposed as a mechanism by which interspecies hybrids can regain fertility, restoring their ability to perform meiosis and sporulate. Here, we show that this process occurred naturally during the evolution of Zygosaccharomyces parabailii, an interspecies hybrid that was formed by mating between 2 parents that differed by 7% in genome sequence and by many interchromosomal rearrangements. Surprisingly, Z. parabailii has a full sexual cycle and is genetically haploid. It goes through mating-type switching and autodiploidization, followed by immediate sporulation. We identified the key evolutionary event that enabled Z. parabailii to regain fertility, which was breakage of 1 of the 2 homeologous copies of the mating-type (MAT) locus in the hybrid, resulting in a chromosomal rearrangement and irreparable damage to 1 MAT locus. This rearrangement was caused by HO endonuclease, which normally functions in mating-type switching. With 1 copy of MAT inactivated, the interspecies hybrid now behaves as a haploid. Our results provide the first demonstration that MAT locus damage is a naturally occurring evolutionary mechanism for whole-genome duplication and restoration of fertility to interspecies hybrids. The events that occurred in Z. parabailii strongly resemble those postulated to have caused ancient whole-genome duplication in an ancestor of Saccharomyces cerevisiae.
Highlights
A whole-genome duplication (WGD) occurred more than 100 million years ago in the common ancestor of 6 yeast genera in the ascomycete family Saccharomycetaceae, including Saccharomyces [1, 2]
It has recently been proposed that the whole-genome duplication (WGD) event that occurred during evolution of an ancestor of the yeast S. cerevisiae was the result of a hybridization between 2 parental yeast species that were significantly divergent in DNA sequence, followed by a doubling of the genome content to restore the hybrid’s ability to make viable spores
The molecular details of how genome doubling could occur in a hybrid were unclear because most known interspecies hybrid yeasts have no sexual cycle
Summary
A whole-genome duplication (WGD) occurred more than 100 million years ago in the common ancestor of 6 yeast genera in the ascomycete family Saccharomycetaceae, including Saccharomyces [1, 2]. The WGD had a profound effect on the genome, proteome, physiology, and cell biology of the yeasts that are descended from it, but the genomes of these yeasts have changed substantially in the time since the WGD occurred, with extensive chromosomal rearrangement, deletion of duplicate gene copies, and sequence divergence between ohnologs (pairs of paralogous genes produced by the WGD). These changes have made it difficult to ascertain the molecular details of how the WGD occurred. Ancient hybridizations are rare in fungi (or at least difficult to detect [4]), but numerous relatively recent hybridizations have been identified using genomics, in the ascomycete genera Saccharomyces [5, 6], Zygosaccharomyces [7,8,9], Candida [10,11,12], and Millerozyma [13]
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