Diversity and Postzygotic Evolution of the Mitochondrial Genome in Hybrids of Saccharomyces Species Isolated by Double Sterility Barrier

Abstract

Eukaryotic species are reproductively isolated by sterility barriers that prevent interspecies fertilization (prezygotic sterility barrier) or the fertilization results in infertile offspring (postzygotic sterility barrier). The Saccharomyces species are isolated by postzygotic sterility barriers. Their allodiploid hybrids form no viable gametes (ascospores) and the viable ascospores of the allotetraploids cannot fertilize (conjugate). Our previous work revealed that this mechanism of reproductive isolation differs from those operating in plants and animals and we designated it double sterility barrier (the failure of homeologous chromosomes to pair and the repression of mating by matingtype heterozygosity). Other studies implicated nucleo-mitochondrial incompatibilities in the sterility of the Saccharomyces hybrids, a mechanism assumed to play a central role in the reproductive isolation of animal species. In this project the mitochondrial genomes of 50 cevarum (S. cerevisiae × S. uvarum) hybrids were analyzed. 62% had S. cerevisiae mitotypes, 4% had S. uvarum mitotypes, and 34% had recombinant mitotypes. All but one hybrid formed viable spores indicating that they had genomes larger than allodiploid. Most of these spores were sterile (no sporulation in the clone of vegetative descendants; a feature characteristic of allodiploids). But regardless of their mitotypes, most hybrids could also form fertile alloaneuploid spore clones at low frequencies upon the loss of the MAT-carrying chromosome of the S. uvarum subgenome during meiosis. Hence, the cevarum alloploid nuclear genome is compatible with both parental mitochondrial genomes as well as with their recombinants, and the sterility of the hybrids is maintained by the double sterility barrier (determined in the nuclear genome) rather than by nucleo-mitochondrial incompatibilities. During allotetraploid sporulation both the nuclear and the mitochondrial genomes of the hybrids could segregate but no correlation was observed between the sterility or the fertility of the spore clones and their mitotypes. Nucleo-mitochondrial incompatibility was manifested as respiration deficiency in certain meiotic segregants. As respiration is required for meiosis-sporulation but not for fertilization (conjugation), these segregants were deficient only in sporulation. Thus, the nucleo-mitochondrial incompatibility affects the sexual processes only indirectly through the inactivation of respiration and causes only partial sterility in certain segregant spore clones.

Lager Yeast Design Through Meiotic Segregation of a Saccharomyces cerevisiae × Saccharomyces eubayanus Hybrid

“…As observed in previous studies on allotetraploid yeast (Greig et al, 2002;Sebastiani et al, 2002;Antunovics et al, 2005;Pfliegler et al, 2012;Karanyicz et al, 2017;Szabó et al, 2020;Naseeb et al, 2021) there appeared to be no post-zygotic barrier to reproduction with the F1 hybrid investigated here. The ability to produce viable spores among the F1 spore clones was also limited to tetraploid strains (via endomitosis (Sebastiani et al, 2002) or, as is most likely the case here, self-fertilization of homo-or hemizygous diploid spores).…”

Restoring fertility in yeast hybrids: breeding and quantitative genetics of beneficial traits

“…Mitochondrial-nuclear interactions have been reported as having a major role in phenotypic variation both in intra-species and inter-species yeast hybrids (E. P. Baker et al 2019; Chou et al 2010; Hewitt et al 2020; Hsu and Chou 2017; Lee et al 2008; X. C. Li et al 2019; Paliwal et al 2014), affecting respiration (Albertin et al 2013) fermentation properties (Hewitt et al 2020; Solieri et al 2008), progeny fitness (Zeyl et al 2005; Zeyl 2006), reproductive isolation (Chou and Leu 2010; Lee et al 2008; Szabo et al 2020) and nuclear transcription (Hewitt et al 2020). Studies on inter-species yeast hybrids in the lab have shown a correlation between the origin of the mitochondrial genome and the higher stability of one of the nuclear genomes (Antunovics et al 2005; Karanyicz et al 2017; Peris et al 2020).…”

“…Among these, SKO1, a basic leucine zipper transcription factor, mapped in S. eubayanus alleles of Sc/Sem segregants, has been described having a major role in mediating HOG pathway-dependent osmotic regulation (Rep et al 2001). (Albertin et al 2013) fermentation properties (Hewitt et al 2020;Solieri et al 2008), progeny fitness (Zeyl et al 2005;Zeyl 2006), reproductive isolation (Chou and Leu 2010;Lee et al 2008;Szabo et al 2020) and nuclear transcription (Hewitt et al 2020). Studies on interspecies yeast hybrids in the lab have shown a correlation between the origin of the mitochondrial genome and the higher stability of one of the nuclear genomes (Antunovics et al 2005;Karanyicz et al 2017;Peris et al 2020).…”

Synthetic two-species allodiploid and three-species allotetraploid Saccharomyces hybrids with euploid (complete) parental subgenomes

“…The hybrids usually had parental mitotypes or, less frequently, recombinant mitotypes (e.g. 16,[30][31][32][33][34] ). In this study both types of hybrids were homoplasmic.…”