Dynamics of the yeast transcriptome during wine fermentation reveals a novel fermentation stress response

Abstract

In this study, genome-wide expression analyses were used to study the response of Saccharomyces cerevisiae to stress throughout a 15-day wine fermentation. Forty per cent of the yeast genome significantly changed expression levels to mediate long-term adaptation to fermenting grape must. Among the genes that changed expression levels, a group of 223 genes was identified, which was designated as fermentation stress response (FSR) genes that were dramatically induced at various points during fermentation. FSR genes sustain high levels of induction up to the final time point and exhibited changes in expression levels ranging from four- to 80-fold. The FSR is novel; 62% of the genes involved have not been implicated in global stress responses and 28% of the FSR genes have no functional annotation. Genes involved in respiratory metabolism and gluconeogenesis were expressed during fermentation despite the presence of high concentrations of glucose. Ethanol, rather than nutrient depletion, seems to be responsible for entry of yeast cells into the stationary phase.

Fig. 1

Clustering of genes based on temporal expression profiles. The center graph shows the entire transcriptome plotted with the coefficients calculated from the expression model. The clusters are anchored by the genes numbered in black. The temporal expression of these genes is displayed in the 20 line graphs on the periphery. The dotted lines indicate twofold change in the expression levels. The number of genes in each cluster is circled in the cluster.

Fig. 2

FSR. Venn diagram showing the number of genes associated with two well-known transcriptionally characterized stress responses. ESR – genes induced in the environmental stress response (Gasch et al., 2000), CER – genes induced in the common environmental response (Causton et al., 2001), FSR – fermentation stress response genes. Refer also to supplementary Fig. S1.

Fig. 3

Functional annotations of genes in the FSR using biological process GO Slim Terms from SGD. The distribution of terms for the rest of the yeast genome is shown for comparison.

Fig. 4

Heat map of the association of GO terms to clusters. White represents depletion and enrichment increases with darker squares (based on the χ² statistic).

Fig. 5

Growth of Vin13 in Riesling grape juice containing either 191, 300, 600, or 900mgL⁻¹ N. The nitrogen content of Riesling grape juice containing 191mgL⁻¹ N was adjusted to either 300, 600, or 900mgL⁻¹ N using DAP. ADY of Vin13 was inoculated to 3×10⁶ cells mL⁻¹ in 250- mL Kimax bottles fitted with vapour locks containing 200 mL Riesling grape juice. Ethanol concentrations (% v/v) are indicated on the graph.