The importance of regulated resource reallocation during dynamic environmental shifts in yeast

Many organisms maintain generalized stress responses activated by adverse conditions. A common theme is the induction of stress-defense proteins with reduced production of growth-promoting proteins, including ribosomes. Yet the precise roles of these coupled programs are difficult to dissect. Here, we investigated Saccharomyces cerevisiae responding to salt as a model stressor. We used molecular, genomic, and single-cell microfluidic methods to examine the interplay between transient induction of stress-defense genes and coordinated repression of growth-promoting genes in the yeast environmental stress response (ESR). Loss of transcriptional inducers Msn2/4 accelerates growth during multiple mild stress doses, at the expense of acquired tolerance to subsequent severe stresses. In contrast, loss of Dot6/Tod6 repressors of growth-promoting genes delays stress acclimation, showing that gene repression accommodates the cost of the Msn2/4 response. Msn2/4 bind the DOT6 promoter, influence Dot6 abundance and activation dynamics, and are required for full repression of Dot6 targets and other growth-promoting genes. Thus, Msn2/4 participate in regulating resource reallocation needed to induce their transcripts, underscoring a common theme in stress responses utilized in other organisms.