Biophysical properties of Saccharomyces cerevisiae and their relationship with HOG pathway activation

Theoretical Biophysics, Humboldt University, Invaliden Str 42, 10115 Berlin, Germany.
Biophysics of Structure and Mechanism (Impact Factor: 2.47). 10/2010; 39(11):1547-56. DOI: 10.1007/s00249-010-0612-0
Source: PubMed

ABSTRACT Parameterized models of biophysical and mechanical cell properties are important for predictive mathematical modeling of cellular processes. The concepts of turgor, cell wall elasticity, osmotically active volume, and intracellular osmolarity have been investigated for decades, but a consistent rigorous parameterization of these concepts is lacking. Here, we subjected several data sets of minimum volume measurements in yeast obtained after hyper-osmotic shock to a thermodynamic modeling framework. We estimated parameters for several relevant biophysical cell properties and tested alternative hypotheses about these concepts using a model discrimination approach. In accordance with previous reports, we estimated an average initial turgor of 0.6 ± 0.2 MPa and found that turgor becomes negligible at a relative volume of 93.3 ± 6.3% corresponding to an osmotic shock of 0.4 ± 0.2 Osm/l. At high stress levels (4 Osm/l), plasmolysis may occur. We found that the volumetric elastic modulus, a measure of cell wall elasticity, is 14.3 ± 10.4 MPa. Our model discrimination analysis suggests that other thermodynamic quantities affecting the intracellular water potential, for example the matrix potential, can be neglected under physiological conditions. The parameterized turgor models showed that activation of the osmosensing high osmolarity glycerol (HOG) signaling pathway correlates with turgor loss in a 1:1 relationship. This finding suggests that mechanical properties of the membrane trigger HOG pathway activation, which can be represented and quantitatively modeled by turgor.

Electronic supplementary material
The online version of this article (doi:10.1007/s00249-010-0612-0) contains supplementary material, which is available to authorized users.

Download full-text


Available from: Stefan Hohmann, Jul 05, 2015
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: The growing pollen tube is central to plant reproduction and is a long-standing model for cellular tip growth in biology. Rapid osmotically driven growth is maintained under variable conditions, which requires osmosensing and regulation. This study explores the mechanism of water entry and the potential role of osmosensory regulation in maintaining pollen growth. The osmotic permeability of the plasmalemma of Lilium pollen tubes was measured from plasmolysis rates to be 1.32±0.31×10(-3) cm s(-1). Mercuric ions reduce this permeability by 65%. Simulations using an osmotic model of pollen tube growth predict that an osmosensor at the cell membrane controls pectin deposition at the cell tip; inhibiting the sensor is predicted to cause tip bursting due to cell wall thinning. It was found that adding mercury to growing pollen tubes caused such a bursting of the tips. The model indicates that lowering the osmotic permeability per se does not lead to bursting but rather to thickening of the tip. The time course of induced bursting showed no time lag and was independent of mercury concentration, compatible with a surface site of action. The submaximal bursting response to intermediate mercuric ion concentration was independent of the concentration of calcium ions, showing that bursting is not due to a competitive inhibition of calcium binding or entry. Bursting with the same time course was also shown by cells growing on potassium-free media, indicating that potassium channels (implicated in mechanosensing) are not involved in the bursting response. The possible involvement of mercury-sensitive water channels as osmosensors and current knowledge of these in pollen cells are discussed.
    Journal of Experimental Botany 10/2013; 64(16). DOI:10.1093/jxb/ert311 · 5.79 Impact Factor
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: The elastic modulus of the Baker's yeast (Saccharomyces cerevisiae) cell wall reported in studies using atomic force microscopy (AFM) is two orders of magnitude lower than that obtained using whole cell compression by micromanipulation. Using finite element modelling, it is shown that Hertz-Sneddon analysis cannot be applied to AFM indentation data for single layer core-shell structures. In addition, the Reissner solution for shallow homogeneous spheres is not appropriate for thick walls such as those of yeast cells. In order to explain yeast compression measurements at different length scales, a double layer wall model is presented considering a soft external layer composed of mannoproteins, and a stiff inner layer of β-glucan fibres and chitin. Under this model, previous AFM studies using sharp indenters provide reasonable estimates of the external layer elastic modulus, while micromanipulation provides the total stiffness of the cell wall. Data from both measurements are combined to estimate the mechanical properties of the inner stiff layer.
    Biophysics of Structure and Mechanism 05/2013; DOI:10.1007/s00249-013-0909-x · 2.47 Impact Factor
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: All living cells respond to external stimuli and execute specific physiological responses through signal transduction pathways. Understanding the mechanisms controlling signalling pathways is important for diagnosing and treating diseases and for reprogramming cells with desired functions. Although many of the signalling components in the budding yeast Saccharomyces cerevisiae have been identified by genetic studies, many features concerning the dynamic control of pathway activity, cross-talk, cell-to-cell variability or robustness against perturbation are still incompletely understood. Comparing the behaviour of engineered and natural signalling pathways offers insight complementary to that achievable with standard genetic and molecular studies. Here, we review studies that aim at a deeper understanding of signalling design principles and generation of novel signalling properties by engineering the yeast mitogen-activated protein kinase (MAPK) pathways. The underlying approaches can be applied to other organisms including mammalian cells and offer opportunities for building synthetic pathways and functionalities useful in medicine and biotechnology.
    Molecular Microbiology 03/2013; 88(1). DOI:10.1111/mmi.12174 · 5.03 Impact Factor