Plasticity of Mitochondrial DNA Inheritance and its Impact on Nuclear Gene Transcription in Yeast Hybrids

Abstract

Mitochondrial DNA (mtDNA) in budding yeast is biparentally inherited, but colonies rapidly lose one type of parental mtDNA, becoming homoplasmic. Therefore, hybrids between different yeast species possess two homologous nuclear genomes, but only one type of mitochondrial DNA. We hypothesise that the choice of mtDNA retention is influenced by its contribution to hybrid fitness in different environments, and that the allelic expression of the two nuclear subgenomes is affected by the presence of different mtDNAs in hybrids. Here, we crossed Saccharomyces cerevisiae with S. uvarum under different environmental conditions and examined the plasticity of the retention of mtDNA in each hybrid. We showed that on fermentable carbon sources at warm temperatures each parental mtDNA was equally likely to be retained, while at colder temperatures, hybrids preferentially retained mtDNA derived from S.

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

“…The natural hybrid S. pastorianus (hybridized from S. cerevisiae and S. eubayanus ) carries the S. eubayanus mitochondria ( 26 , 27 ), while other industrial hybrids of Saccharomyces species used in wine and cider production have retained S. cerevisiae mitochondrial genome ( 28 ). It has also recently been shown that the type of mitochondria inherited affects the phenotype ( 29 – 31 ) and the transcriptional network ( 18 ) in hybrids. Therefore, here, each of the tetraploid hybrids constructed were also selected for different mitotypes.…”

“…Recently, much work has gone into the generation of de novo yeast hybrids, exploiting their potential for the production of biofuels ( 14 ), brewing ( 15 , 16 ), and winemaking ( 17 ). Interspecies hybrids are not only selected for their capability to combine the advantageous traits of the parent strains, as the genomes from both parents undergo chromosomal rearrangements, mutations, widespread transcriptional changes ( 18 , 19 ), and gene loss and gene duplications, which also impact the nature of protein complexes formed ( 20 ). Hence, new and improved phenotypes can arise thanks to heterosis or hybrid vigor ( 21 ).…”

Patterns of Genomic Instability in Interspecific Yeast Hybrids With Diverse Ancestries

“…This suggests interactions between mtDNA and nuclear DNA or potentially be influenced by the mtDNA itself. Additionally, mitochondrial retention in S. cerevisiae × S. uvarum hybrids was recently shown to be heavily influenced by the effects of mitochondrial genes on nuclear expression and fitness, which in turn often depend on environmental factors (Hewitt et al, 2020). For instance, in rich media at cold temperatures, S. uvarum mitochondria were retained, whereas S. cerevisiae mitochondria were retained on non-fermentable carbon sources regardless of temperature.…”

Hybridization and the origin of new yeast lineages

“…This approach has been used to disentangle cis and trans effects in the evolution of gene regulation (Metzger, Wittkopp and Coolon 2017 ), the effect of different speed of the cellular cycle in the misexpression of genes (Swain Lenz, Riles and Fay 2014 ) or the effect of mitochondrial inheritance in the expression of hybrid nuclear genes (Hewitt et al . 2020 ). We recently directly asked the question of the impact of hybridization on gene expression, by investigating the extent of transcriptional shock in a newly formed Saccharomyces cerevisiae × Saccharomyces uvarum diploid hybrid and its diploid parentals (Hovhannisyan et al .…”