Opinion
Life under pressure: hydrostatic pressure in cell growth and function

https://doi.org/10.1016/j.tplants.2007.01.006Get rights and content

H2O is one of the most essential molecules for cellular life. Cell volume, osmolality and hydrostatic pressure are tightly controlled by multiple signaling cascades and they drive crucial cellular functions ranging from exocytosis and growth to apoptosis. Ion fluxes and cell shape restructuring induce asymmetries in osmotic potential across the plasma membrane and lead to localized hydrodynamic flow. Cells have evolved fascinating strategies to harness the potential of hydrodynamic flow to perform crucial functions. Plants exploit hydrodynamics to drive processes including gas exchange, leaf positioning, nutrient acquisition and growth. This paradigm is extended by recent work that reveals an important role for hydrodynamics in pollen tube growth.

Section snippets

The pivotal role of water in the origin, function and proliferation of cellular life

Life is all about aqueous chemistry and reactions that occur at surfaces and interfaces. The unique physical properties of water not only promoted the emergence of cellular life but also set limits on effective cell dimensions within which viability and reproduction can be maintained [1]. It was crucial for cell function that osmolality, membrane tension and hydrostatic pressure (see Glossary) were tightly controlled. Thus, early in evolution, cells were confronted with the problem of how to

Mechanosensitive ion channels

Water surrounds cells, penetrates into the plasma membrane and cytosol, and affects the local geometry of the lipid bilayer and membrane proteins [15]. Ions or osmolytes perturb the aqueous network and affect membrane tension and osmotic potential. In bacteria, milli-osmolar changes in water concentration are sufficient to shift the osmotic pressure across the plasma membrane and generate stretch and compression forces along the plane of the lipid bilayer [16]. These forces gate

Hydrodynamic flow drives crucial cellular functions

Cell volume crucially affects membrane tension and curvature, molecular crowding in the cytosol, and intracellular ionic strength 40, 41, 42. Because of this, processes ranging from growth and proliferation to necrosis and apoptosis are controlled by cell volume in Bacteria and Eukarya 2, 3. Furthermore, many cell types have evolved fascinating strategies that enable them to harness the potential of osmotic gradients and hydrodynamic flow to drive crucial cellular functions. Some functions

Vectorial hydrodynamic flow and hydrostatic pressure surges can trigger localized cell expansion and growth

There is increasing evidence that cell shape restructuring and polarized growth are initiated by transiently non-equilibrated hydrostatic pressure surges pushing against the cell boundary 9, 12, 13, 14. Recent work in animal and bacterial cells indicates that the cytoplasm is highly non-uniform and structured as a porous contractile elastic network composed of cytoskeletal filaments and organelles, infiltrated with an electrolytic interstitial fluid, similar to a fluid-filled sponge 12, 42. It

Conclusions and perspectives

Hydrodynamics and hydrostatic pressure are among the most fundamental physical properties that determine cell form and function. Cells rapidly respond to changes in volume and osmotic potential differences across the plasma membrane. Hydrostatic pressure changes can generate stretch or compression forces along the plasma membrane and activate mechanosensitive ion channels. This simple switch is postulated to be one of the oldest sensory transduction processes that evolved with the onset of

Acknowledgements

We apologize to scientists whose work could not be cited due to space limitations. We thank Michel Haring for critical reading of the manuscript. Research in T.M.'s laboratory is currently supported by the Netherlands Organization for Scientific Research (NWO 813.06.003, 863.04.004 and 864.05.001).

Glossary

Anisotropic
exhibiting unequal properties along different axes.
Electro-osmosis
the movement of a polar fluid through a selectively permeable membrane or porous material, or along a charged surface, under the influence of an electric field.
Hydraulic conductivity
the movement of fluid through pores or confined spaces under pressure, depending on the intrinsic permeability of the material and on the degree of saturation.
Hydrodynamics
the dynamics of fluids in motion; the forces exerted by fluids in

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      The hydrostatic pressure gradient is balanced by the mechanical tension on the cell surface (cytoskeleton network at the cortex, tension in the plasma membrane, and cell surface protein network such as glycoproteins - reviewed in [19]). In contrast to animal cells, plant cells maintain an incredibly high hydrostatic pressure in their cytoplasm due to the presence of stiff cell walls [21–24]. The pressure inside a single plant cell is on the order of a few (0.5–4) megapascals, which is much higher than a car tire at 0.2 megapascals [21,24–26].

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