Topic 3.5 Can Negative Turgor Pressures Exist in Living Cells?
One of the challenging aspects of understanding plant water relations is the remarkable range of pressures, both positive and negative, that occur within the bodies of plants. Negative pressures (or tensions), which depend upon the cohesive strength of water coupled with the strength of lignified cell walls to resist deformation, play an important role in water transport through the xylem. Positive pressures, which depend upon the semipermeable nature of the plasma membrane and the elastic nature of primary cell walls, occur in all hydrated living plants cells but can be especially large in sieve tubes and guard cells. Living plant cells are typically assumed to have only positive pressures (e.g., textbook Figure 3.11). However, there appears to be no reason that negative pressures could not also occur within the cytoplasm of living plant cells. This web topic explores the existence and potential role of negative turgor pressures in plants.
When a cell loses water in air, turgor declines and solute concentrations increase. At the turgor loss point (Ψp = 0), the hydrostatic pressure in the cell sap is equal to atmospheric pressure, meaning that no net force is exerted on the cell wall. If water continues to be lost from the cell, the pressure within the cytoplasm drops below atmospheric pressure, resulting in a force imbalance that collapses the cell wall. The deformation of living cells upon desiccation is called cytorrhysis. Note that the plasma membrane is pressed against the cell wall throughout desiccation (i.e., plasmolysis does not occur) because the hydrostatic pressure in cytoplasm remains greater than the hydrostatic pressure in apoplast (see also textbook Figure 3.10).
In the living cells described above, a decrease in cell water potential below the turgor loss point is balanced by an increase in solute concentration as the volume of the cell decreases. Thus, true "negative" pressures do not develop. In contrast, xylem conduits have rigid cell walls that resist deformation, allowing them to sustain negative pressures without imploding. This raises the question of what happens when water is lost from living cells that have thick walls or are embedded in a rigid matrix of cells (e.g., xylem parenchyma). Might these cells resist deformation and thus develop negative turgor pressures?
It is important to emphasize that this is a controversial area, due in large part to the absence of direct measurements of negative turgor pressures within cells (Tyree 1976). However, before reviewing the evidence for negative turgor pressures, it is worthwhile to consider what physiological effects might result from the development of such negative pressures in living cells. The major outcome of negative turgor is that it allows stiff-walled cells to decrease in water potential without undergoing major changes in cell volume or osmotic concentration. Because cytorrhysis might cause physical damage to the wall and/or cell membranes, while the high concentrations of solutes resulting from the reduction in cell volume might adversely affect the conformation of membranes and proteins, it is possible to imagine a physiological role or benefit for the development of negative turgor pressures in plant cells.
We now turn this around and ask if there are any downsides to the generation of negative turgor pressures in living cells? In the xylem, the primary issue associated with negative pressures is cavitation; could this also be a concern for living cells? The primary mechanism for cavitation in plants is air seeding (see textbook Chapter 4), reflecting the fact that the probability of the de novo formation of gas voids in water (either by homogeneous or heterogeneous nucleation) is extremely low (Pickard 1983). In air seeding, air is sucked in through the cell wall, where it then “nucleates” the transition to the vapor phase. For air seeding to occur in a living cell experiencing negative pressures, air would have to be pulled through the very small pores of the cell wall. While one can imagine this happening, the movement of air across the cell wall would result in plasmolysis and thus the immediate release of any tension in the cytoplasm because the plasma membrane is not capable of withstanding any significant pressure.
Other costs associated with the ability of living cells to generate negative pressures include the metabolic costs of producing rigid cell walls, as well as any limitations lignified walls might place on physiological function. In addition, a strategy for avoiding cell damage due to desiccation via the generation of negative pressures might impose limitations on cell size. The strength of a cell to withstand collapse (and thus generate negative pressures) is inversely proportional to cell size.
Evidence for negative turgor pressure in plants is limited, in part reflecting the fact that few researchers have devoted much attention to this issue. Living cells with flexible (unlignified) cell walls deform relatively easily upon desiccation and thus do not appear to support negative pressures. However, measurements of the forces needed to collapse cell walls suggest that living cells with thick walls can withstand forces in the range of 1.0 MPa (Oertli et al. 1990). Visual examination of tissues adapted to withstand very cold temperatures also provides indirect evidence for negative turgor. For example, frozen ray parenchyma cells often do not exhibit significant deformation, despite the very strong desiccatory effects (low water potential) of extracellular ice. One can hypothesize that the existence of negative pressures within these cells acts to balance the water potential gradient across the cell membrane (i.e., between the cytoplasm and ice formed within the apoplast).
In summary, negative turgor pressure remains an intriguing but little-studied area of plant water relations. While it does not appear to form in cells such as the leaf mesophyll, that can deform easily, its existence in living cells with either lignified cell walls or where the cell is embedded in a matrix of lignified tissues (e.g., living cells within wood) cannot be ruled out. The potential benefits of negative turgor pressures in terms of preventing mechanical and osmotic damage associated with severe desiccation makes this topic worthy of further study.