Pierre Cruiziat, PIAF-INRA-UBP, France, and Hanno Richter, University of Agricultural Sciences, Vienna

May, 2006

The cohesion-tension theory (CTT) has been advanced to explain the ascent of sap in plants, and especially, in trees. It relies on the physical properties of water, on mechanisms of liquid transport, and on the anatomical features of the xylem, the sap conducting system (see textbook Chapter 4). The CTT embodies the work of several dozen scientists from around the world over the course of a century (see Web Essay 4.2 for historical details). Even if some controversy and unsolved questions remain (see below), the CTT is nevertheless a very well founded explanation of the sap ascent in plants, and has been verified by a large number of experiments.

The CTT theory can be summarized in the following eight statements:

1. Water within the whole plant forms a continuous network of liquid columns from the absorbing surfaces of roots to the evaporating surfaces, mainly but not exclusively, within the leaves. Water columns within the conducting elements (vessels and tracheids) extend over 99% of the whole water pathway (vascular pathway) in a plant. The remaining 1% is constituted by the wall and cytoplasm of living cells, primarily found at the beginning and at the end of the pathway, in root and leaf parenchyma.
2. This vascular pathway has hydraulic continuity from the root-to-soil interface to the different parts and organs of the plant (see textbook Figure 4.1). The primary function of this hydraulic continuity is to transfer instantaneously (sound speed), the variations of tensions or pressure throughout the plant. Hydraulic continuity is highly dependent on the tensile strength of water (see below).
3. The driving force for water movement in the system is generated by surface tension at the evaporating surfaces. The evaporating surface is at the wall of the leaf cells where evaporation takes place. In contrast to a large flat surface of evaporating water, these surfaces are a porous medium. Consequently, evaporation generates a curvature in the water menisci within the pores of the cell wall lined by cellulose microfibrils (see textbook Figure 4.9).
4. The radius of curvature of these menisci is sufficiently small as to be able to support water columns as long as one hundred meters, (approximate size of the highest existing trees). By applying the empirical Jurin law, we find that a radius of 0.12µm supports a column of 120 meters (Zimmermann, 1983).
5. Because of surface tension, and the small radius of curvature of the menisci at the evaporative surfaces, evaporation lowers the water potential of the adjacent regions including the xylem elements. This change is instantaneously transmitted throughout the whole plant.
6. In this way, evaporation establishes gradients of pressure or tension along the pathway in transpiring plants. This causes an inflow of water from the soil to the transpiring surfaces.
   
   The validity of the CTT does not depend on a specific range of xylem tensions, but it nevertheless predicts that "high tensions" could exist in plants. Typical values can be as low as –3 MPa in crop plants, –4 MPa in trees, and –10 MPa in desert species.
   
   It is noteworthy that the well established, linear relation between leaf water potential and transpiration is not predicted by the CTT. Rather, it is a consequence of the fact that in well-watered plants, the water flow through the plant closely approximates the relation: absorption = transpiration (in the absence of significant growth in volume) and the hydraulic resistances remain constant. Water flow through the plant can then be described as an electric current through a circuit of resistances in series:
   
   Flow = Difference of water potential / resistances
   
   This is the well-known Van den Honert approach to the Ohm’s law analogue of sap flow in the soil-plant- atmosphere continuum. The application of the Ohm′s law to sap flow encompasses many phenomena (heat transfer, water transfer in soil, Darcy law, first diffusion law, etc.) and, it is therefore independent of the underlying physical mechanisms and the nature of moving fluid. For example, the electrical approach does not address whether sap is under tension or pressure. For this reason, the description of sap flow by Ohm′s is rather phenomenological. In contrast, the CTT explains specific physical of the water transport in plants.
7. Due to the fact that transpiration "pulls" the sap from the soil to the leaves, water in the xylem is in a metastable state of tension. In this state, the water column is susceptible to cavitation, (i.e., to the appearance of a vapor phase within the liquid phase). Whenever transpiration stops because of the absence of a humidity gradient between the leaf and atmosphere (as in the case when it rains period or in a night with high relative humidity), water will keep moving from the soil to the leaves until the difference of water potential across the water column disappears. The water potential value at this equilibrium is called predawn water potential. Under these conditions there is no more water potential difference between the soil surrounding the roots and the leaves; however if the predawn water potential is different from zero (i.e.: -0.1MPa) the sap will remain under tension. In contrast, if stem pressure (in winter) or root pressure (in spring) exists, water is pushed from the roots to the leaves. Water potential will be positive and sap under pressure.
8. As long as transpiration occurs, the xylem sap is under tension and cavitation could take place. As discussed below, the risk of cavitation has been the most controversial aspect of the CTT. However, both cohesion between water molecules, which gives water its tensile strength, and adhesion of water molecules to xylem walls (see chapter 3 in the textbook), prevent cavitation, to a certain extent. During dry conditions in summer and frost-thaw cycles in winter, air bubbles can enter the xylem and reduce the hydraulic conductivity of the conducting elements. The entry of air into the xylem under dry conditions has been explained by the air-seeding hypothesis. This hypothesis states that xylem cavitation starts when air is pulled through the pit membrane pores (see textbook figure 4.7). This occurs when the air pressure P_a, (usually near zero), minus the xylem pressure P_x (negative under these conditions), across the air-water meniscus at the pore creates a pressure difference sufficient to displace the meniscus. The first phase of this event, the cavitation proper, is an extremely rapid invasion of the conducting element mainly by water vapor. A slower entrance of air, which corresponds to embolism, follows cavitation. Special features of the conducting system design (interconnected conduits much shorter than the tree and pit membrane) and stomatal regulation limit the spread of air.

Winter embolism is best explained by a frost-thaw mechanism. When sap temperature drops a few degrees below 0°C, ice forms, creating air bubbles because gases dissolved in liquid sap are nearly insoluble in ice. It is assumed that during the thaw, when xylem tensions exceed a critical value, air bubbles are progressively released to the liquid phase, and air-water menisci are created. In contrast with summer embolism, winter embolism is highly dependent on the diameter of the conducting elements: the larger the conducting elements, the more likely the occurrence of embolism. Therefore, conifers bearing tracheids are much more resistant than ring-porous trees. This might explain the fact that conifers are much more abundant than broad-leaved trees in many cool areas.

Many experimental results provide strong support for the CTT. However, two arguments have been recently presented against this theory. The first comes from U. Zimmermann (Würzburg University, Germany) and co-workers. Zimmermann’s reasoning against the CTT is as follows:

• The CTT predicts high negative hydrostatic pressures in the xylem.
• Two indirect methods for measuring the xylem water status are available: the pressure chamber and the psychrometric method (correct argument).
• The pressure probe is at present the only direct method (correct argument). (See Web Topic 3.6 for a description of these methods to measure the water status of the xylem.) This method does not yield tensions more negative than ca 0.5 MPa (no longer a valid argument).
Therefore, the indirect methods give wrong results and the CTT that predicts much more negative xylem pressures, is wrong (incorrect argument).

Figure 1   Indirect measurement of cavitation in experiments using a collar pressure chamber in a walnut tree. The collar pressure chamber provides a way to generate external pressure on a portion of a branch. This external pressure, applied for 2 min. intervals in these experiments, is transmitted within the conducting system, and it can induce different degrees of cavitation. During the first day, a pressure of 1 to 2MPa was applied without any effect on the sap flow. On the second day, higher pressure were applied and no changes in sap flow were observed below pressures of 2.4 MPa. For pressures between 2.4 and 2.6 MPa, some cavitation was induced, as shown by the reduction of the sap flow, as compared with the control branches. Around 4 PM a pressure of 3 MPa was applied. For walnut, the vessels are completely cavited at this pressure and no more sap flow occurrs. No sap flow was observed through the pressured branch on the third day, indicated that the discountinuity of the water column caused by cavitation was permanent (Ameglio et al. 1994).

Until a few years ago, it was not possible to measure with a pressure probe xylem tensions higher than 0.6 MPa (corresponding to potentials more negative than –0.6 MPa). The reason behind this limitation is that it is extremely difficult to puncture a vessel with a finely pointed capillary without disturbing the physical state of the water under tension within the vessel. In addition, the relatively large water reservoir in the probe and the materials used for its construction lead to spontaneous cavitations inside the instrument. Recent advances in the pressure probe technique have made it possible to measure pressures as low as –1 MPa. Although these values are not sufficiently negative to make this direct method a suitable alternative to the indirect ones, these findings indicate that the low values previously reported are due to technical limitations of the method. This indicates that Zimmermann’s argument against the CTT was never valid: it dealt with a technical limit of a method, not the validity of the CTT.

The second challenge to the CTT was presented by M. J. Canny and his group at the RSBC, Canberra, Australia. Canny proposed a different scheme for water movement, the compensating pressure theory. This theory claims that due to the fact that plant organs are rigid or have rigid outer layers, positive pressure may exist within them. The maximum pressure would be set by the osmotic pressure of the cell sap, and the osmotic pressure would be balanced by both wall stretching and the pressing of cells against each other in a confined space, the so called "tissue pressure." For each cell, the wall and tissue pressure together would make up the turgor pressure. This tissue pressure could be transmitted directly between different tissue regions; in particular, when xylem conduits pass through a tissue having tissue pressure, the positive pressure would extend into the xylem compartment. The tissue pressure would not affect flow rates in the xylem, which, according to Canny’s theory, 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 (Canny 1998, Canny 2001, Comstock 1999). The main objection to Canny’s suggested mechanism is that it is physically untenable and violates basic principles of thermodynamics (Tyree 1999, Comstock 1999). Canny’s opinion mainly comes from his cryo-scanning electron microscopy experiments. However, all present evidence suggests that the observed diurnal fluctuations in the filling state of frozen vessels are artifacts (Richter 2001, Tyree et al. 2002). Although Canny’s ideas are inconsistent with basic physical laws and lack experimental support, they have nevertheless stimulated a large number of critical experiments, raising interesting questions concerning refilling processes (Steudle 2001).

A recent synthesis of the main features of the CTT and the electrical analogy used for modeling water transport in the soil-plant-atmosphere continuum has led to a new approach to plant and tree water relations: the hydraulic architecture approach. This approach considers a plant, and especially a tree, as a hydraulic system. All hydraulic systems (dams, irrigation systems for crops or houses, the human blood vascular system) are composed of the same basic elements: a driving force, pipes, reservoirs and regulating systems. So described, the hydraulic architecture is a powerful tool to study the hydraulic characteristics of the conducting tissues under a whole range of natural conditions. Important questions subject to study with the hydraulic architecture approach include: What are the dynamics of cavitation? Does the microstructure of vessels (e.g., mechanical properties of pit membranes) affect water transfer and vulnerability to cavitation? What is the hydraulic specificity of the leaves? How important is the extravascular pathway, as compared to the vascular pathway? Can vulnerability curves provide a better understanding of the drought responses of trees?

References

Améglio, T., Cruiziat, P., and Bodet, C. (1994) A pressure chamber to reduce and control embolism in situ: consequence on the sap flow. Plant Sciences, Saint Malo (FR) Meeting of the SFPV, 1994/10/12-14. University of Rennes I, p. 281.

Canny, M. J. (1998) Applications of the compensating pressure theory of water transport. Am. J. Bot. 84: 1223-1230.

Canny, M. J., Huang, G. C., and McCully, M. (2001) The cohesion theory debate continues. Trends in Plant Science 6: 454-455.

Comstock, J. P. (1999) Why Canny’s theory doesn’t hold water. Am. J. Bot. 86: 1077-1081.

Cruiziat, P., Cochard, H., and Améglio, T. (2002) Hydraulic architecture of trees: Main concepts and results. Ann. For. Sci. 59: 723–752.

Richter, H. (2001) The cohesion theory debate continues: The pitfalls of cryobiology. Trends in Plant Science 6: 456–457.

Steudle, E. (2001) The cohesion-tension mechanism and the acquisition of water by plant roots. Annu. Rev. Plant Physiol. Mol. Biol. 52: 847–75.

Tyree, M. T. (1997) The cohesion-tension theory of sap ascent: Current controversies. J. Exp. Bot. 48: 1753–1765.

Tyree, M. T. (1999) The forgotten component of plant water potential: A reply—Tissue pressures are not additive in the way M. J. Canny suggests. Plant Biology 1: 598-601.

Tyree, M. T., and Zimmermann, M. H. (2002) Xylem Structure and the Ascent of Sap, 2nd ed. Springer, Berlin.

Tyree, M. T., Cochard, H., and Cruiziat, P. (2002) The water-filled versus air-filled status of vessels cut open in air: The "Scholander assumption" revisited. Plant Cell and Environment 26: 613–621.