Compensatory Genetic and Transcriptional Cytonuclear Coordination in Allopolyploid Lager Yeast (Saccharomyces pastorianus)

Abstract

Cytonuclear coordination between biparental nuclear genomes and uniparental cytoplasmic organellar genomes in plants is often resolved by genetic and transcriptional cytonuclear responses. Whether this mechanism also acts in allopolyploid members of other kingdoms is not clear. Additionally, cytonuclear coordination of interleaved allopolyploid cells/individuals within the same population is underexplored. The yeast Saccharomyces pastorianus provides the opportunity to explore cytonuclear coevolution during different growth stages and from novel dimensions. Using S. pastorianus cells from multiple growth stages in the same environment, we show that nuclear mitochondria-targeted (NMT) genes have undergone both asymmetric gene conversion and growth stage-specific biased expression favoring genes from the mitochondrial genome donor (S. eubayanus). Our results suggest that cytonuclear coordination in allopolyploid lager yeast species entails an orchestrated and compensatory genetic and transcriptional evolutionary regulatory shift. The common as well as unique properties of cytonuclear coordination underlying allopolyploidy between unicellular yeasts and higher plants offers novel insights into mechanisms of cytonuclear evolution associated with allopolyploid speciation.

Development of a genome-scale metabolic model for the lager hybrid yeast S. pastorianus to understand the evolution of metabolic pathways in industrial settings

“…Additionally, among the initial 56 genes removed from Yeast8, the mitochondrial genes ATP8 , ATP6 , COB , OLI1 , COX1 , COX2 , and COX3 were present ( Table S2 ), because only the nuclear genomic data of S. pastorianus were available. Given that the presence of functional mitochondrial DNA in S. pastorianus cells has been confirmed ( 28 ), the Yeast8 mitochondrial reactions, initially removed, were investigated to understand whether they could be supported by existing S. pastorianus enzymes. As a result, four reactions were re-introduced: (i) as S. pastorianus CBS1513 genome contains the S. eubayanus -like gene APA2 (ID: SPGP0Y01780) that supports the ATP adenylyltransferase reaction (ID: r_0222), the reaction and gene were both added to iSP_1513; (ii) the mitochondrial ATP synthase “r_0226” reaction was reintroduced as ATP6 , ATP8 , and OLI1 genes are encoded by the mitochondrion and all the other subunits of this protein complex are present (i .…”

Development of a genome scale metabolic model for the lager hybrid yeastS. pastorianusto understand evolution of metabolic pathways in industrial settings

“…Additionally, among the initial 56 genes removed from Yeast8, the mitochondrial genes ATP8 , ATP6 , COB , OLI1 , COX1 , COX2 and COX3 were present (Supplementary Table 2), since only the nuclear genomic data of S. pastorianus was available. Given that the presence of functional mitochondrial DNA in S. pastorianus cells has been confirmed (Zhang et al , 2022), the Yeast8 mitochondrial reactions, initially removed, were investigated to understand whether they could be supported by existing S. pastorianus enzymes. As result, four reactions were re-introduced: i. as S. pastorianus CBS1513 genome contains the S. eubayanus -like gene APA2 (ID: SPGP0Y01780) that supports the ATP adenylyltransferase reaction (ID: r_0222), the reaction and gene were both added to iSP_1513; ii.…”

Cytonuclear Interactions and Subgenome Dominance Shape the Evolution of Organelle-Targeted Genes in the Brassica Triangle of U

“…The other dimension of the main possible explanation was that both plastids and mitochondrial genomes undergo heteroplasmic sorting to fix variations among multiple copies within cells, and plastids had a faster sorting rate than that of mitochondrial genomes, often within a single generation ( Broz et al 2022 ). Therefore, the fixation of nuclear genome variations may compensate for plastid variations rapidly ( Osada and Akashi 2012 ; Havird et al 2015 ; Hill 2020 ; Zhang et al 2022 ). Furthermore, we assumed that the interactive strength between organelle-targeted genes and organelles depended on whether they coencode complexes.…”