Abstract
BackgroundYeast cells live in a highly fluctuating environment with respect to temperature, nutrients, and especially osmolarity. The Hog1 mitogen-activated protein kinase (MAPK) pathway is crucial for the adaption of yeast cells to external osmotic changes.Methodology/Principal FindingsTo better understand the osmo-adaption mechanism in the budding yeast Saccharomyces cerevisiae, we have developed a mathematical model and quantitatively investigated the Hog1 response to osmotic stress. The model agrees well with various experimental data for the Hog1 response to different types of osmotic changes. Kinetic analyses of the model indicate that budding yeast cells have evolved to protect themselves economically: while they show almost no response to fast pulse-like changes of osmolarity, they respond periodically and are well-adapted to osmotic changes with a certain frequency. To quantify the signal transduction efficiency of the osmo-adaption network, we introduced a measure of the signal response gain, which is defined as the ratio of output change integral to input (signal) change integral. Model simulations indicate that the Hog1 response gain shows bell-shaped response curves with respect to the duration of a single osmotic pulse and to the frequency of periodic square osmotic pulses, while for up-staircase (ramp) osmotic changes, the gain depends on the slope.Conclusions/SignificanceThe model analyses suggest that budding yeast cells have selectively evolved to be optimized to some specific types of osmotic changes. In addition, our work implies that the signaling output can be dynamically controlled by fine-tuning the signal input profiles.
Highlights
Cells have evolved to sense and respond to various changes of their environmental conditions such as hormones, nutrients, temperature and osmotic stresses
One of the well-studied examples is the adaption of budding yeast cells (Saccharomyces cerevisiae) to high external osmolarity: information about the osmotic stress is transmitted through the high-osmolarity glycerol (HOG) mitogen-activated protein kinase (MAPK) signaling pathway [1]
To better understand how budding yeast cells respond to different types of osmotic changes, we developed a mathematical model to investigate the dynamics of the Hog1 response to different scenarios of stress signals: simple step increase, single pulse, periodic square pulses and up-staircase increase of osmotic changes (Figure 1B)
Summary
Cells have evolved to sense and respond to various changes of their environmental conditions such as hormones, nutrients, temperature and osmotic stresses. One of the well-studied examples is the adaption of budding yeast cells (Saccharomyces cerevisiae) to high external osmolarity: information about the osmotic stress is transmitted through the high-osmolarity glycerol (HOG) mitogen-activated protein kinase (MAPK) signaling pathway [1]. The increase of external osmolarity is recognized by two osmosensing proteins, Sln and Sho, which in turn independently lead to the phosphorylation of the MAPK kinase (MAPKK) Pbs. The Sho branch triggers the activation of a distinct MAPKKK Ste, which activates Pbs. Activated Hog accumulates in the nucleus and regulates different processes to increase glycerol accumulation, thereby compensating the increase of external osmolarity [1,2,3]. The Hog mitogen-activated protein kinase (MAPK) pathway is crucial for the adaption of yeast cells to external osmotic changes
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