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Boyce Thompson Institute, Tower Road, Ithaca, New York 14853-1801
Received for publication September 21, 1998. Accepted for publication February 22, 1999.
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ABSTRACT |
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 TOP ABSTRACT CritiqueLITERATURE CITED |
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Key Words: cohesion theory • compensating pressure theory • tissue pressure • water transport
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Critique |
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TOPABSTRACTCritiqueLITERATURE CITED |
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, 1997a
, b
, 1998a
, b
) as the replacement to the widely accepted adhesion-cohesion-tension theory (Dixon and Joly, 1894
). The compensating pressure theory is presented as an alternative model, which explains water transport without a requirement for large negative pressures (tensions) to be sustained in the xylem of plants, a concept that has been subjected to recent challenges (see Canny, 1995
). Other recent reviews have defended the cohesion tension theory (Tyree, 1997
), pointing out its past and current strength, its robustness in consolidating a large body of data from different techniques, and its internal consistency. Several recent experimental approaches have also verified the reality of tension in the xylem (Holbrook, Burns, and Field, 1995
; Pockman, Sperry, and O'Leary, 1995
; Sperry et al., 1996
; Alder et al., 1997
; see also Stiller and Sperry, this issue). This commentary will not reiterate the findings of these recent works, but will point out some logical failings, inconsistencies, and inaccurate application of concepts in the basic formulation of Canny's theory. While the appearance of several high-profile papers promoting the "compensating pressure" theory has generated a healthy round of experiment and counterexperiment to defend different viewpoints, it has also promoted considerable and unnecessary confusion. As will be argued below, Canny's definition and application of the "compensating pressure" are incompatible with even the basic tenets of water relations that he claims to still accept. Due to several conceptual failings in the compensating pressure theory, there are not two internally consistent theories each waiting for the key experiment to determine which most accurately describes water transport in plants. There is only the cohesion-tension theory on the one hand and, on the other, an increasingly elaborate superstructure of sometimes elusive concepts, many of which cannot bear close scrutiny. Taken individually and apart from the compensating pressure theory, some of Canny's ideas may have merit. However, should the cohesion-tension theory be proven wrong tomorrow, we would be left with no coherent model for water transport at all.
Canny's most recent statement of the theory (Canny, 1998b
) includes the following points (the numbering is mine): (1) Because plant organs are rigid or have rigid outer layers, positive pressure may be contained within them. (2) The maximum pressure is set by the osmotic pressure of the cell sap. (3) The osmotic pressure is balanced by both wall stretching and the general pressing of cells against each other in confined space, the "tissue pressure." (4) For each cell, wall and tissue pressure together make up the turgor pressure. (5) The tissue pressure can be transmitted directly between different tissue regions. In particular, when xylem conduits pass through a tissue possessed of tissue pressure, the positive pressure extends into the xylem compartment. (6) The tissue pressure does not affect flow rates in the xylem, which are set by pumps and one-way valves in both roots and leaves. Since the tissue pressure does not change flux rate, it acts to elevate xylem pressures. (7) Although water flow in the xylem occurs down a pressure gradient even in the compensating pressure theory, the actual pressure measurable in the xylem may not show a gradient if the xylem flows into regions of greater and greater tissue pressure.
The most recent statements of the theory have shifted from emphasizing the compensating gradient in tissue pressure along the flow pathway to speculations that active discharge of capacitance may augment the transpiration stream during the day. There has also been a shift from explaining how cavitating pressures can be avoided to the assertion that cavitation is common, but that active manipulation of tissue pressure in surrounding cells can generate the positive pressures needed to refill xylem even during maximum transpiration rates. The relative weighting of these processes is not important to the arguments below, which focus sharply on the definition and application of tissue and/or compensating pressure as formulated in any of Canny's works. In discussing them, I will refer extensively to the original treatise (Canny, 1995
), which remains the only attempt to rigorously define these terms and is still referenced for detailed development in all later papers (Canny, 1997a
, 1998a
, b
).
To convey the underlying fallacies of this new theory, I begin with basic concepts that Canny and adherents of the cohesion-tension model all claim to agree on. Classic water relations as taught for the last several decades embodies the concept of water potential, where the total water potential is related to the free energy of the water and can be subdivided into several components:
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), but he asserts that at the tissue and organ level, the application of these concepts requires a radical revision.
As mentioned in the example above, the presence of the plant cell wall is necessary for the development of a large turgor in response to osmosis. Both introductory (Salisbury and Ross, 1985
) and advanced treatments (Nobel, 1991
) of cellular water relations generally point out that, at equilibrium, opposing force vectors must cancel at the fluid-wall boundary. Some texts introduce the term "wall pressure" when describing the inwardly directed force vectors imposed by the solid phase (e.g., Raven, Evert, and Curtis, 1981
). For our isolated cell in the preceding example, these inward force vectors at the wall surface derive from tension in the wall. It is the tensile strength of the wall that allows large turgor to exist without causing the membranes to expand and ultimately rupture, but the wall mechanics themselves are not a water potential component.
Canny correctly points out that, in real plants, we are not necessarily dealing with just the structural rigidity of a single wall, but rather the packed structure of all the cells in a tissue. In packed tissue, most cell walls are bounded by protoplasts on both sides, and it is then possible that force applied by adjacent protoplasts to a single wall will cancel out, while the wall experiences compression rather than tension. For this situation to occur, the individual cell walls must be elastic, but whole tissues must be contained within less elastic boundaries, which ultimately constrain and balance the expansive forces within. While this condition may reasonably be called a tissue pressure, we must accept it only with the following caveats: (1) tissue pressure, like wall pressure, is a description of mechanical forces in the solid phase, not a water potential component. (2) Tissue pressure is part of the balance of forces acting within a bounded tissue, and not a force that one tissue may impose upon another existing outside the rigid outer layer.
Canny's estimates of the magnitude of tissue pressure also deserve scrutiny. He claims they commonly reach values between 1 and 3 MPa, and further asserts that cavitation vulnerability curves, frequently reaching full cavitation only at 6–8 MPa, are in fact measuring the limits to tissue pressure development (Canny, 1998b
, but see Stiller and Sperry, this issue). This means the tension in the outer constraining layer would typically need to balance an outward pressure of 1–3 MPa, and even greater pressures under stress. The implications of this are easily quantified using La Place's Law for circumferential stresses (as would be used in determining needed wall thicknesses when designing pressure chambers):
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; Niklas, 1992
). The lower value, measured against the grain, is likely to be more relevant to our concern with circumferential stresses, and indicates that, at the tissue level, the cohesion of cells can be more limiting than wall strength itself. In contrast, the same pressure in a spherical parenchyma cell with a radius of 50 µm and wall thickness of 0.5 µm is only 100 MPa. The lower value compared to the stem example arises because even a thin-walled parenchyma cell achieves a more favorable ratio of wall thickness to total radius. Further, the stress may be compared to the tensile strength measured not at the gross tissue level but per individual wall cross-sectional area. Tensile strength of walls in live carrot cells was 450 MPa (Carpita, 1985
), which agrees favorably with that of pure cellulose fibers (Vogel, 1988
; Niklas, 1992
). Let us return again to consideration of a whole stem. For the same 1 cm diameter stem above, what if the constraining layer is an extended cortical collenchyma with radial thickness of 150–200 µm, as might be found in a mature tomato? Such a tissue layer might be seven cells deep, each cell having two tangential walls, and each wall with an average thickness as great as 2 µm. At 2 MPa tissue pressure, the stress in these tangential walls (total tangential wall thickness of 28 µm for the whole collenchyma layer) would be over 700 MPa, and, even if we assume that only wall strength and not cell cohesion is limiting, the tissue would fail at this still moderate pressure. From these estimates, it seems very likely that most of the turgor pressure is balanced by wall tension at the cellular level, with a relatively small contribution by tension across whole extended tissues. This is why the epidermis of tomatoes is so commonly ruptured after a rain—the tensile strength of the epidermis is not sufficient to withstand the internal pressure created by swelling cells. Canny's model depends upon not one but many such organ-level force barriers, justified in many cases by observation of a single outer cell layer with moderately thickened walls.
Canny repeatedly (1995, 1997a, 1998a, b) states that "turgor pressure is made up of wall and tissue pressure," and expresses this formally as (Canny, 1995
, Eq. 1):
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Let us consider Canny's only published example illustrating exactly how tissue pressure is supposed to work (Fig. 1, reproduced from Canny's fig. 12 of Canny, 1995
). In panel A, we see a parenchyma tissue with a 
total of 0 MPa, which is in contact with a xylem element that has a total of +;t10.8 MPa. Canny states emphatically that this is an "equilibrium state." How can this be? Only because he is projecting the "tissue pressure" from the parenchyma into the xylem compartment. He goes on to consider how this situation changes under transpiration (Fig. 1B), and we have parenchyma at total = -0.8 MPa in "equilibrium" with xylem at total = 0. It is hard to tell from this example why the concept of "compensating pressure" ("P" in Canny's figure) is introduced at all, since it is defined as -total and is therefore a redundant term. Xylem pressure is assumed to always equal tissue pressure of the surrounding tissues, and compensating pressure is not a separate force or action but merely a bookkeeping ledger of how much tissue pressure has been lost as total water potential and turgor drop.
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Some of these confusing contradictions are caused by coining misleading and unnecessary new terminology. Tissue pressure as Canny defines it is real, but its effects can all be explained in terms of standard principles, and its magnitude is probably far less than he suggests, except possibly in very small local regions. It is not valid to project the tissue pressure between tissues as Canny suggests, but one could define a system in which the xylem and parenchyma were, together, within a common, constraining outer layer. If this layer really had the strength to contain the pressures postulated by Canny, how would swelling parenchyma affect the water relations of the xylem? If it pressed only on the walls of the xylem, but the lumen did not compress, then not at all. If, on the other hand, swelling parenchyma compressed the xylem conduits, then there would be a transient acceleration of water leaving the xylem, after which it would take larger forces than before to move the same flux through the now crimped pipes!
Canny is aware that these would be the predictions of classic water relations theory, and so he has added to his model an elaborate pumping system to replace the simple concept of flow driven by pressure gradients and suction generated during evaporation from the leaves. Canny's model actually requires that the flow through the xylem be completely indifferent to both absolute pressures and pressure gradients within the xylem. The xylem, in his model, is a contained volume, which can be pressurized by surrounding tissues, and all flow characteristics are set entirely and solely by an active water pump in the roots and a one-way, regulating valve in the leaves. This assemblage of valves and pumps ensures that the flow rate through the xylem is completely independent of the action of tissue pressure on the middle of the pathway (Canny, 1998b
). It also ensures that the tissue pressure cannot squeeze water out of the pipes, but merely pressurizes them.
This is a truly astounding concept. The requirement of perfect coordination between separate water pumps below and self-regulating check valves above should cause some doubts. Canny's ideas for the root pump are complex and as radical as all other parts of his theory. Without endorsing them in any way, I will accept a root pump for the sake of argument and, in the interests of brevity, focus attention on the much simpler mechanism of the proposed valve in the leaves. Canny states that a one-way valve, with a flux-rate completely independent of xylem pressure characteristics, exists inherently in the final, gas-phase portion of the transpiration pathway (Canny, 1998a
). Water evaporates from the cell walls bordering the air spaces and diffuses out of the leaf as a gas through stomatal pores. This leaves a water deficit in the evaporating walls, and the remaining water retreats into the pores of the wall producing sharply curved menisci. It is in these bent water surfaces that energy is stored (Canny, 1995
), which can then pull water out of the xylem (in the cohesion tension theory, of course, they pull water out of the soil and all the way through the plant).
Canny's assertion that this process guarantees a liquid flux rate independent of xylem pressures seems to be a misapplication of an important concept first presented by Gradmann (1928)
and formalized by van den Honert (1948)
. This concept states that, in the catena of resistances comprising the soil–plant–atmosphere continuum, the greatest resistance is found in the epidermis and is regulated by stomatal aperture changes, and the greatest water potential drop is that between the vapor phase in the leaf air spaces and the external atmosphere. As Canny correctly states, this means that the stomata exert almost full control over the transpiration rate, while the hydraulic conductance of the xylem and other tissues serve primarily to determine the water-potential gradients within the liquid phase. These gradients are important for their influence on cavitation and the relative water contents of all tissues, but, contrary to Canny's argument, only if the whole water-transport pathway is in steady state will water uptake from the soil and transport rates throughout the xylem all equal the transpiration rate. The amount of time plants actually spend under steady state transport conditions varies tremendously depending on succulence, wood volume, tissue elasticity, and environmental constancy, but there is no fixed relationship between transpiration and xylem flux rate.
Even when xylem flux and transpiration are equal, this steady-state is due to passive equilibration of capacitance, hydraulic conductance, and the water potential gradient through the plant, and not to rate-regulating valves controlling the liquid pathway. Control of transpiration always occurs at the stomates where water is already in the gas phase, but this control in no case implies a limiting valve at the evaporative sites. The lack of a regulating valve anywhere in the leaf mesophyll is made particularly obvious by hydraulic conductance measurement techniques in which water is pushed into the xylem of a severed twig under positive pressure. Under these conditions, water readily moves through the leaf tissue, floods the normally gas-filled intercellular spaces, and drips as a liquid from each stomatal pore (Yang and Tyree, 1994
). Thus, the water flux leaving the xylem is always dependent on the water potential gradient between xylem and leaf tissues and not directly on the transpiration rate. Any successful squeezing of the xylem conduits that compresses the vessel lumen will only cause a transient efflux. We see, then, that the requirements of this pump system are untenable, and no viable mechanisms have been identified to meet them.
In summary, Canny's theory suffers from fatal flaws at almost every step. (1) His attempt to alter xylem pressures by the application of tissue pressure violates basic tenets that he elsewhere admits are valid. Tissue pressures may exist, but will be much better understood if analyzed using traditional water relations concepts. (2) Tissue pressure is likely to be ubiquitous but small. Extreme reinforcement would be needed to sustain the tissue pressures postulated in the model, not just one or two cell layers with thickened walls. (3) The postulated pump-and-valve system, essential to the working of the model, is untenable.
Only by making these serious errors is Canny able to attribute water transport in plants to active processes supported by compensating pressure. Stiller and Sperry (this issue), however, have shown that living cells are irrelevant to many of the contested phenomena. In particular, Canny claims that there is no tension in the xylem because it has been compensated. This and similar claims must be dismissed as flawed conclusions of faulty premises.
Some isolated components of Canny's proposed theory are not, in themselves, impossible. Reverse osmosis and active manipulations of capacitance volumes in particular tissues are theoretically possible. Whether or not such things actually happen could be the legitimate subject of future experiments. The entire concept of "compensating pressure" and its application is not a legitimate subject. It has no coherent basis. While the cohesion-tension theory, as we now employ it, may not be complete or perfect in every particular, it has proven itself robust and extremely consistent to a wide range of experimental and technical approaches. None of Canny's several recent studies is compelling enough to reject it, and it is likely to remain the central paradigm of water transport in plants for a long time to come.
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FOOTNOTES |
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LITERATURE CITED |
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TOPABSTRACTCritiqueLITERATURE CITED |
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Canny, M. J. 1995 A new theory for the ascent of sap—cohesion supported by tissue pressure. Annals of Botany 75: 343–357.
———. 1997a Vessel contents of leaves after excision—a test of Scholander's assumption. American Journal of Botany 84: 1217–1222.[Abstract]
———. 1997b Vessel contents during transpiration—embolisms and refilling. American Journal of Botany 84: 1223–1230.[Abstract]
———. 1998a Transporting water in plants. American Scientist 86: 152–159.[CrossRef]
———. 1998b Applications of the compensating pressure theory of water transport. American Journal of Botany 85: 897–909.[Abstract]
Carpita, N. C. 1985 Tensile strength of cell walls of living cells. Plant Physiology 79: 485–488.
Dixon, H. H., and J. Joly. 1894 On the ascent of sap. Philosophical Transactions of the Royal Society of London B. 186: 563–576.[CrossRef]
Gradmann, H. 1928 Untersuchungen über die Wasserverhältnisse des Bodens als Grundlage des Pflanzenwachstums. I. Jahrbücher für Wissenschaft Botanik 69: 1–100.
Holbrook, N. M., M. J. Burns, and C. B. Field. 1995 Negative xylem pressures in plants: a test of the balancing pressure technique. Science 270: 1193–1194.
Niklas, K. J. 1992 Plant biomechanics. University of Chicago Press, Chicago, IL.
Nobel, P. S. 1991 Physicochemical and environmental plant physiology. Academic Press, San Diego, CA.
Pockman, W. T., Sperry, J. S., and J. W. O'Leary. 1995 Sustained and significant negative water pressure in xylem. Nature 378: 715–716.[CrossRef][Web of Science]
Raven, P. H., R. F. Evert, and H. Curtis. 1981 Biology of plants, 3d ed. Worth, New York, NY.
Salisbury, F. B., and C. W. Ross. 1985 Plant physiology, 3d ed. Wadsworth, Belmont, CA.
Sperry, J. S., N. Z. Saliendra, W. T. Pockman, H. Cochard, P. Cruiziat, S. D. Davis, F. W. Ewers, and M. T. Tyree. 1996 New evidence for large negative xylem pressures and their measurement by the pressure chamber method. Plant, Cell and Environment 19: 427–436.[CrossRef]
Stiller, V., and J. S. Sperry. 1999 Canny's compensating pressure theory fails the test. American Journal of Botany 86: 1082–1086.
Tyree, M. T. 1997 The cohesion-tension theory of sap ascent: current controversies. Journal of Experimental Botany 48: 1753–1765.
van den Honert, T. H. 1948 Water transport in plants as a catenary process. Discussions of the Faraday Society 3: 146–153.[CrossRef][Web of Science]
Vogel, S. 1988 Life's devices. Princeton University Press, Princeton, NJ.
Yang, S., and M. T. Tyree. 1994 Hydraulic architecture of Acer saccharum and A. rubrum: comparison of branches to whole trees and the contribution of leaves to hydraulic resistance. Journal of Experimental Botany 45: 271–186.
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0, which is consistent with most data