Abstract
Transient exposures to environmental stresses induce altered physiological states in exposed cells that persist after the stresses have been removed. These states, referred to as cellular memory, can even be passed on to daughter cells and may thus be thought of as embodying a form of epigenetic inheritance. We find that meiotically produced spores in the budding yeast S. cerevisiae possess a state of heightened stress resistance that, following their germination, persists for numerous mitotic generations. As yeast meiotic development is essentially a starvation response that a/alpha diploid cells engage, we sought to model this phenomenon by subjecting haploid cells to starvation conditions. We find also that haploid cells exposed to glucose withdrawal acquire a state of elevated stress resistance that persists after the reintroduction of these cells to glucose-replete media. Following release from lengthy durations of glucose starvation, we confirm that this physiological state of enhanced stress resistance is propagated in descendants of the exposed cells through two mitotic divisions before fading from the population. In both haploid starved cells and diploid produced meiotic spores we show that their cellular memories are not attributable to trehalose, a widely regarded stress protectant that accumulates in these cell types. Moreover, the transiently heritable stress resistant state induced by glucose starvation in haploid cells is independent of the Msn2/4 transcription factors, which are known to program cellular memory induced by exposure of cells to NaCl. Our findings identify new developmentally and nutritionally induced states of cellular memory that exhibit striking degrees of persistence and mitotic heritability.
Highlights
Acquired stress resistance is a phenomenon in which the transient exposure of an organism to a mild environmental stress induces in it the capacity to survive subsequent exposure to what would otherwise be lethal stresses
Yeast spores exist in a stress resistant state that persists in their progeny following germination Meiotically produced yeast spores exhibit resistance to a profound degree of environmental stress, a trait largely attributable to their spore coat and likely accounting for their remarkable longevity and durability [13]
As meiotically arrested ndt80∆/∆ cells that were incubated in sporulation medium showed no H2O2 resistance (Figure 1D), our results suggest that the acquired stress resistance of ndt80∆/∆ cells pre-grown in YPA was somehow lost during their meiotic arrest
Summary
Acquired stress resistance is a phenomenon in which the transient exposure of an organism to a mild environmental stress induces in it the capacity to survive subsequent exposure to what would otherwise be lethal stresses. NaCl exposed cells exhibited cross-stress resistance to exposure to H2O2. In all acquired stress resistance and memory experiments, cells maintained as described above represent the naïve state. After wash with ddH2O, treated cells were harvested and resuspended in pre-warmed YPD with NaCl added at a final concentration of 0.7 M stress for 1 hour or grown in YP media without a carbon source at 0.3 OD600 at 30°C. Treated cells were harvested and washed in pre-warmed fresh YPD media. Germinating cells were harvested and exposed to H2O2 ranging from 0 - 8 mM concentrations following 1, 2, 4, or 8 OD doublings of growth in YPD. Carbon starved cells were released from starvation in stress-free YPD media for the indicated number of OD doublings.
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