MAT heterozygosity and the second sterility barrier in the reproductive isolation of Saccharomyces species

Abstract

The genetic analysis of large numbers of Saccharomyces cerevisiae × S. uvarum (“cevarum”) and S. kudriavzevii × S. uvarum (“kudvarum”) hybrids in our previous studies revealed that these species are isolated by a postzygotic double-sterility barrier. We proposed a model in which the first barrier is due to the abruption of the meiotic process by the failure of the chromosomes of the subgenomes to pair (and recombine) in meiosis and the second barrier is assumed to be the result of the suppression of mating by allospecific MAT heterozygosity. While the former is analogous to the major mechanism of postzygotic reproductive isolation in plants and animals, the latter seems to be Saccharomyces specific. To bolster the assumed involvement of MAT in the second sterility barrier, we produced synthetic alloploid two-species cevarum and kudvarum hybrids with homo- and heterothallic backgrounds as well as three-species S. cerevisiae × S. kudvarum × S. uvarum (“cekudvarum”) hybrids by mass-mating and examined their MAT loci using species- and cassette-specific primer pairs. We found that the allospecific MAT heterozygosity repressed MAT switching and mating in the hybrids and in the viable but sterile spores produced by the cevarum hybrids that had increased (allotetraploid) genomes. The loss of heterozygosity by meiotic malsegregation of MAT-carrying chromosomes in the latter hybrids broke down the sterility barrier. The resulting spores nullisomic for the S. uvarum chromosome produced vegetative cells capable of MAT switching and conjugation, opening the way for GARMe (Genome Autoreduction in Meiosis), the process that leads to chimeric genomes.

Postzygotic reproductive isolation among three Saccharomyces yeast species

“…investigated (Belloch et al, 2009;González et al, 2006González et al, , 2008Morard et al, 2020;Naumov et al, 2013;Naumov et al, 2010;Peris, Lopes, Arias, & Barrio, 2012;Peris, Lopes, Belloch, et al, 2012;Sampaio & Gonçalves, 2008;Sipiczki, 2008Sipiczki, , 2018Sipiczki et al, 2020).…”

Insights on life cycle and cell identity regulatory circuits for unlocking genetic improvement in Zygosaccharomyces and Kluyveromyces yeasts

“…Experimental studies using large numbers of interspecies Saccharomyces hybrids have identified ways by which these barriers can be overcome (Karanyicz et al . 2017 ; Sipiczki, Antunovics and Szabo 2020 ) and it is striking to note that Zygosaccharomyces hybrids use some similar mechanisms. The first sterility barrier can be surmounted if the diploid self-mates to form a tetraploid as this generates two copies of each homologous chromosome that can then pair during prophase-I, allowing the completion of meiosis and the formation of viable diploid progeny.…”

“…Allotetraploids undergo successful meiotic recombination and chromosome segregation leading to diploid hybrid spores. Those spores that contain one copy of each mating type from each parental species will now be sterile hybrid diploids hitting the second sterility barrier (Sipiczki 2018 ; Sipiczki, Antunovics and Szabo 2020 ). However, 50% of diploid spores from such allotetraploid meioses will inherit the same mating type from each parent.…”

Never Change a Brewing Yeast? Why Not, There Are Plenty to Choose From

“…In addition, hybrids can also benefit from a less well-understood effect called heterosis or hybrid vigor, where the resulting hybrid shows a greater fitness than one would expect based on each parental strain ( Lindegren et al, 1953 ; Hebly et al, 2015 ; Bernardes et al, 2017 ). Although hybrids have a huge potential for industrial use, they themselves are usually less suitable for performing genetic crosses since most strains will suffer from hybrid sterility, resulting in very low numbers of viable progeny with a clear mating type ( Sipiczki, 2018 , 2019 ; Ono and Greig, 2020 ; Sipiczki et al, 2020 ). While there were attempts to create novel “lager” strains by crossing meiotic offspring of “lager” yeasts already in the early 1980s ( Gjermansen and Sigsgaard, 1981 ), it was the identification of S. eubayanus that changed the concept of creating novel “lager” yeasts significantly.…”