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 genes have undergone both asymmetric gene conversion and growth stage-specific biased expression favoring genes from the mitochondrial genome donor (Saccharomyces 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.

Keywords: allotetraploid lager yeast; cytonuclear coevolution; nuclear mitochondria-targeted gene.

Fig. 1.

Nonsynonymous to synonymous substitution ratios (d_N/d_S) of mitochondrial and nuclear genes. (A) d_N/d_S ratios (y-axis) of homologous mitochondrial genes (mtDNA genes; x-axis) in S. pastorianus and S. eubayanus are summarized; (B) Each panel summarizes the d_N/d_S ratios of all single-copy NMT and non-NMT genes characterized in diploid orthologs of S. eubayanus and S. cerevisiae and subgenomic homoeologs of allopolyploid S. pastorianus.

Fig. 2.

Genetic cytonuclear coordination in three allopolyploid S. pastorianus strains. (A) Schematic diagram illustrating the S. cerevisiae-to-S. eubayanus (S. c.-to-S. e.) and S. eubayanus-to-S. cerevisiae (S. e.-to-S. c.) gene conversions (in right and left dotted boxes). Single-copy gene orthologs and homoeologs (C and E subgenomes) are aligned into quartets. Changes of amino acids and nucleotides involved in gene conversion are specified in each box. Labels 1-8 describe the criteria of defining nonsynonymous gene conversions among homoeologs (see Materials and Methods); (B) Number and relative percentage of S. cerevisiae-to-S. eubayanus (S. c.-to-S. e.) and S. eubayanus-to-S. cerevisiae (S. e.-to-S. c.) gene conversions in NMT and non-NMT homoeologs in three S. pastorianus strains are summarized in each column. (C) Density distribution of gene conversion levels of identified S. cerevisiae-to-S. eubayanus (S. c.-to-S. e.) gene conversions in each S. pastorianus strain.

Fig. 3.

Transcriptional cytonuclear coordination in S. pastorianus strain WS 34/70. (A) Microaerobic growth experiment design, in which three parallel replicates (R1 to R3) are used for sampling at each time point (T1 to T37); (B) Dynamic transcriptional expression bias for S. eubayanus homoeologs at each sampling point in the growth process. The sampling time points are denoted in x-axis; the absorbance value at OD₆₀₀ for each sample and its respective expression bias of S. eubayanus homoeologs are denoted on the left and right y-axis, respectively. The dashed curve represents the growth curve; the solid curves fit the expression bias of S. eubayanus NMT and non-NMT genes in the time course, respectively; (C) The log₂ transformed fold changes of transcripts per million (TPM) for NMT homoeolog pair categorized in Cluster 0; (D) Expression levels (TPMs) of S. cerevisiae and S. eubayanus homoeologs categorized in cluster 0 within the exponential growth phase (T1–T17 sampling points). The left and right panels represent the S. eubayanus and S. cerevisiae homoeologs, respectively. The horizontal dashed lines represent the maximum median and minimum median TPM values in all samples.

Fig. 4.

Compensatory cytonuclear coordination between genetic and transcriptional responses in S. pastorianus strain WS 34/70. (A) Dynamic transcriptional expression bias for S. eubayanus homoeologs with high and low gene conversion levels (abbreviated as high and low at each sampling point in the growth process. The solid curves illustrate linear fitting of expression bias of S. eubayanus NMT homoeologs in each homoeolog group for different gene conversion levels, respectively; (B) GO term enrichments (biological process [BP], cellular component [CC], and molecular function [MF]) for homoeologs with high and low conversion levels (high and low). GO terms specifically enriched in homoeologous groups of high or low conversion level are specified in the diagram; (C) The density distribution of S. cerevisiae-to-S. eubayanus gene conversion levels for homoeologs categorized in Cluster 0 and for all other NMT genes identified in S. pastorianus strain (background).