Cohesion-tension Theory Research Articles

Safety Factors for Xylem Failure by Implosion and Air-Seeding Within Roots, Trunks and Branches of Young and Old Conifer Trees

The cohesion-tension theory of water transport states that hydrogen bonds hold water molecules together and that they are pulled through the xylem under tension. This tension could cause transport failure in at least two ways: collapse of the conduit walls (implosion), or rupture of the water column through air-seeding. The objective of this research was to elucidate the functional significance of variations in tracheid anatomical features, earlywood to latewood ratios and wood densities with position in young and old Douglas-fir and ponderosa pine trees in terms of their consequences for the safety factors for tracheid implosion and air-seeding. For both species, wood density increased linearly with percent latewood for root, trunk and branch samples. However, the relationships between anatomy and hydraulic function in trunks differed from those in roots and branches. In roots and branches increased hydraulic efficiency was achieved at the cost of increased vulnerability to air-seeding. Mature wood of trunks had earlywood with wide tracheids that optimized water transport and had a high percentage of latewood that optimized structural support. Juvenile wood had higher resistance to air-seeding and cell wall implosion. The two safety factors followed similar axial trends from roots to terminal branches and were similar for both species studied and between juvenile and mature wood.

The transpiration of water at negative pressures in a synthetic tree

Plant scientists believe that transpiration-the motion of water from the soil, through a vascular plant, and into the air-occurs by a passive, wicking mechanism. This mechanism is described by the cohesion-tension theory: loss of water by evaporation reduces the pressure of the liquid water within the leaf relative to atmospheric pressure; this reduced pressure pulls liquid water out of the soil and up the xylem to maintain hydration. Strikingly, the absolute pressure of the water within the xylem is often negative, such that the liquid is under tension and is thermodynamically metastable with respect to the vapour phase. Qualitatively, this mechanism is the same as that which drives fluid through the synthetic wicks that are key elements in technologies for heat transfer, fuel cells and portable chemical systems. Quantitatively, the differences in pressure generated in plants to drive flow can be more than a hundredfold larger than those generated in synthetic wicks. Here we present the design and operation of a microfluidic system formed in a synthetic hydrogel. This synthetic 'tree' captures the main attributes of transpiration in plants: transduction of subsaturation in the vapour phase of water into negative pressures in the liquid phase, stabilization and flow of liquid water at large negative pressures (-1.0 MPa or lower), continuous heat transfer with the evaporation of liquid water at negative pressure, and continuous extraction of liquid water from subsaturated sources. This development opens the opportunity for technological uses of water under tension and for new experimental studies of the liquid state of water.

Negative success in tiny tree

Evaporation of water from the leaves of plants pulls water up from the roots via a passive wick-like action. This 'transpirational pull' generates pressures up to a hundredfold greater than in synthetic wicks. A team from Cornell University has now developed a microfluidic system in a synthetic hydrogel that captures the main attributes — and pulling power — of transpiration in plants. The microfluidic 'synthetic tree' has a root system that extracts liquid water from a subsaturated vapour into negative pressures in the liquid phase. Liquid water flows at large negative pressures through the 'trunk' and the water evaporates through an analagous 'leaf' system. This process validates the cohesion-tension theory of transpiration, and the synthetic tree should also be a useful platform for the study the properties of metastable liquids and a starting point from which to design new technologies for the management of water in chemical processes, heat transfer, and environmental engineering.

Water in trees

Holbrook and Zwieniecki reply: Terry Goldman is correct in suggesting that providing plants with higher carbon dioxide concentrations can result in both water conservation and enhanced photosynthesis. Indeed, CO2 fertilization is already used by many commercial growers. However, enclosed growing systems have huge energy costs associated with cooling and are thus unsuited for large-scale agricultural production.On the planetary scale, we are currently conducting such an experiment, albeit in an uncontrolled fashion. Increased atmospheric CO2 due to human activities such as fossil-fuel combustion and land clearing is estimated to have increased terrestrial photosynthetic output. However, at the same time, rising temperatures due to higher greenhouse gas concentrations increase the water demands placed on plants and are predicted to alter the frequency and intensity of precipitation events. Thus, although elevated CO2 can improve the efficiency of photosynthesis, there appears to be no free lunch.Jean Roy’s letter suggests that our Quick Study on water transport in trees should “teach the controversy,” so to speak. However, there is no scientific controversy regarding the cohesion-tension theory of water transport in plants. In the early 1990s, there was a short-term challenge to the theory due to discrepancies observed by Ulrich Zimmermann using a pressure probe. Subsequent refinements of that measurement technique by Zimmermann and others eliminated those concerns. 1 1. P. J. Melcher, F. C. Meinzer, D. E. Yount, G. Goldstein, U. Zimmermann, J. Exp. Bot. 49, 1757 (1998). https://doi.org/10.1093/jxb/49.327.1757 Since then no xylem water transport data have been found to be inconsistent with the cohesion-tension theory. Nor has any alternative mechanism been proposed that can explain the transport of water in plants. Publication of the reference Roy cites prompted 45 prominent plant biologists to protest. 2 2. G. Angeles et al. , New Phytol. 163, 451 (2004). https://doi.org/10.1111/j.1469-8137.2004.01142.x The editor’s response was that the paper by Zimmermann and coauthors should be perceived as representing the “views and opinions” of the authors and not as a review of the current state of knowledge appropriate for newcomers to the field. 3 3. I. Woodward, New Phytol. 163, 453 (2004). https://doi.org/10.1111/j.1469-8137.2004.01141.x Finally, we stand by our citation of W. F. Pickard’s 1981 work as an outstanding treatment of water transport in plants. That paper is particularly appropriate for the readers of Physics Today because it assumes high literacy in the physical sciences rather than detailed knowledge of plant anatomy. REFERENCESSection:ChooseTop of pageREFERENCES <<1. P. J. Melcher, F. C. Meinzer, D. E. Yount, G. Goldstein, U. Zimmermann, J. Exp. Bot. 49, 1757 (1998). https://doi.org/10.1093/jxb/49.327.1757 , Google ScholarCrossref, CAS2. G. Angeles et al. , New Phytol. 163, 451 (2004). https://doi.org/10.1111/j.1469-8137.2004.01142.x , Google ScholarCrossref3. I. Woodward, New Phytol. 163, 453 (2004). https://doi.org/10.1111/j.1469-8137.2004.01141.x , Google ScholarCrossref© 2008 American Institute of Physics.

Foliar water supply of tall trees: evidence for mucilage-facilitated moisture uptake from the atmosphere and the impact on pressure bomb measurements

The water supply to leaves of 25 to 60 m tall trees (including high-salinity-tolerant ones) was studied. The filling status of the xylem vessels was determined by xylem sap extraction (using jet-discharge, gravity-discharge, and centrifugation) and by (1)H nuclear magnetic resonance imaging of wood pieces. Simultaneously, pressure bomb experiments were performed along the entire trunk of the trees up to a height of 57 m. Clear-cut evidence was found that the balancing pressure (P(b)) values of leafy twigs were dictated by the ambient relative humidity rather than by height. Refilling of xylem vessels of apical leaves (branches) obviously mainly occurred via moisture uptake from the atmosphere. These findings could be traced back to the hydration and rehydration of mucilage layers on the leaf surfaces and/or of epistomatal mucilage plugs. Xylem vessels also contained mucilage. Mucilage formation was apparently enforced by water stress. The observed mucilage-based foliar water uptake and humidity dependency of the P(b) values are at variance with the cohesion-tension theory and with the hypothesis that P(b) measurements yield information about the relationships between xylem pressure gradients and height.

A physical analysis of sap flow dynamics in trees

The aim of this thesis was to analyze the water dynamics of trees by using a dynamic modeling approach. The work is of cross-disciplinary nature: tree water issues which is a subject of whole plant physiology is examined by means of physics. From physical principles five different models were derived. First, to study the sap flow and the water pressure dynamics in the xylem of tree stem, the effect of embolism on the sap flow, and the recovery of embolized conduits; and second, to analyze a sap flow measuring system based on the heat balance method. Sap flow and water pressure dynamics are analyzed with two models that are based on the relation between xylem water tension and changes in the diameter of sapwood. This new approach is advantageous because it offers a way to compare the model predictions with the easily measured diameter changes in intact trees. The model results give new insight into the water dynamics in the stem, stating that pressure propagation is fast, but time lags of a few minutes do exist. These time lags are related to the dimensions and radial elasticity of the stem, and to the sapwood permeability. The results are in agreement with the cohesion-tension theory but partly contradict the pipe model theory of a plant form. The embolism recovery model presents a quantitative analysis of the processes that have been suggested to recover embolized conduits while the water in surrounding conduits is under negative pressure. The model analysis reveals that under normal physiological circumstances, e.g., normal xylem water tension, osmotic pressure of living cells, or diffusion distances, the refilling process is possible if the two sides of the same living cell have different transport properties for solutes. The model for analyzing the performance of a sap flow measuring system reveals that the method, that assumes homogenous temperature field inside the stem, is not appropriate for stems with a diameter larger than a few centimeters. This study has shown that relatively simple models, based on physical principles, are useful in increasing our understanding of the processes and behavior of natural objects. Furthermore, model analysis leading to better understanding of dynamic systems, can guide forthcoming research and enhance the development of new instrumentation.

A long drink of water: how xylem changes with depth.

A long drink of water: how xylem changes with depth.

Coordinating stomatal and xylem functioning – an evolutionary perspective

Coordinating stomatal and xylem functioning – an evolutionary perspective

Make your own transpiring tree

In this paper we present a simple set-up that illustrates the mechanism of sap ascent in plants and demonstrates that it can easily draw water up to heights of a few meters. The set-up consists of a tube with the lower end submerged in water and the upper one connected to a filter supported by a standard filter-holder. The evaporation of water from the filter surface causes a tension large enough to pull the water up the column against gravity. The flow of water leaving the system was visualised by continuously weighing the water container with a balance. The set-up worked for at least 4 days before the water column broke, with typical flows of ∼10 mg min-1. Knowledge tests with second year university biology students prior to the activity indicated general ignorance not only of the mechanism of sap ascent but also of transpiration itself. After explaining the mechanism of sap ascent with the aid of the set-up all students were able to explain correctly the main aspects of the cohesion-tension theory. The pedagogical value of the set-up, both at the secondary and university levels, is discussed.

Vulnerability curves from conifer sapwood sections exposed over solutions with known water potentials.

The cohesion-tension (CT) theory requires stability of liquid water in conducting elements under high tensions. This stability has been measured using different methods, some of which yielded contradictory results. In this study a method is presented to establish known tensions in the water inside conifer tracheids, to detect cavitation events under these conditions and to construct vulnerability curves. Tangential sapwood sections of Juniperus virginiana L. were placed closely over the surface of NaCl solutions with water potentials ranging from -0.91 to -7.57 MPa. Water potentials were measured with a thermocouple hygrometer in contact with the section, and ultrasound acoustic emissions (UAE) from the sections were registered with an ultrasound transducer. The emission rate of signals increased with the concentration of the solution. Exposure of 100 microm sections in the airspace over a solution provided optimal conditions for the rupture of the water column: many tracheid walls bordered on air, and water in the lumen came under high tension. Nevertheless, the water remained in the metastable liquid state for periods of many hours. The vulnerability obtained from simultaneous measurements of water potentials and ultrasound acoustic emissions on sapwood sections was substantially higher than from conventionally measured curves of detached branches. It is argued that the isolation of tracheids in a massive organ as well as the rate of potential decline will influence the probability of cavitations at a given water potential and thus the parameters of the vulnerability curve.

Hydraulic architecture of trees: main concepts and results

Since about twenty years, hydraulic architecture (h.a.) is, doubtless, the major trend in the domain of plants (and especially trees) wa- ter relations. This review encompasses the main concepts and results concerning the hydraulic of architecture of trees. After a short paragraph about the definition of the h.a., the qualitative and quantitative characteristics of the h.a. are presented. This is an occasion to discuss the pipe mo- del from the h.a. point of view. The second part starts with the central concept of embolism and give a review of important experimental results and questions concerning summer and winter The last part deals with the coupling between hydraulic and stomatal conductances. It discusses the theoretical and experimental relationships between transpiration and leaf water potential during a progressive soil drought, the in- crease of soil-root resistance and its consequences in term of xylem vulnerability, the factors controlling the daily maximum transpiration and how stomates can prevent run away embolism. In conclusion different kinds of unsolved questions of h.a., which can be a matter of future in- vestigations, are presented in addition with a classification of trees behaviour under drought conditions. To end, an appendix recalls the notions of water potential, pressure and tension. hydraulic architecture / cohesion-tension theory / summer embolism / winter embolism / drought resistance

THE COHESION-TENSION MECHANISM AND THE ACQUISITION OF WATER BY PLANT ROOTS.

The physical basis and evidence in support of the cohesion-tension theory of the ascent of sap in plants are reviewed. The focus is on the recent discussion of challenges to the cohesion-tension mechanism based on measurements with the pressure probe. Limitations of pressure probes to measure tensions (negative pressures) in intact transpiring plants are critically assessed. The possible role of the cohesion-tension mechanism during the acquisition of water and solutes by plant roots is discussed.

The essentials of direct xylem pressure measurement

ABSTRACTThis paper discusses the essentials of the oil‐filled pressure probe technique in the measurement of negative xylem pressures, focusing in particular on the technique and physics underlying our recent, successful experiment which has rekindled the debate on the validity of the Cohesion–Tension theory. We illustrate a number of general problems associated with the cell pressure probe and xylem pressure probe techniques, and propose appropriate criteria for micropipette construction. We enumerate factors dealing with the cavitation problem and suggest methods for eliminating air seeds in the system. We introduce reliable criteria for the successful measurement of xylem pressure, and emphasize the importance of the probe pressure relaxation test. Several problems regarding the controversy over the Cohesion–Tension theory are also discussed. We discuss the correlation between xylem pressure and the transpiration rate, the existence of absolute negative xylem pressure in intact plants, the most negative values of xylem pressure measured by the pressure probe, the agreement between the pressure probe and pressure bomb techniques, and the vulnerability to cavitation (tensile strength) of pressure probes.

Cryo-scanning electron microscopy observations of vessel content during transpiration in walnut petioles. Facts or artifacts?

The current controversy about the "cohesion-tension" of water ascent in plants arises from the recent cryo-scanning electron microscopy (cryo-SEM) observations of xylem vessels content by Canny and coworkers (1995). On the basis of these observations it has been claimed that vessels were emptying and refilling during active transpiration in direct contradiction to the previous theory. In this study we compared the cryo-SEM data with the standard hydraulic approach on walnut (Juglans regia) petioles. The results of the two techniques were in clear conflict and could not both be right. Cryo-SEM observations of walnut petioles frozen intact on the tree in a bath of liquid nitrogen (LN(2)) suggested that vessel cavitation was occurring and reversing itself on a diurnal basis. Up to 30% of the vessels were embolized at midday. In contrast, the percentage of loss of hydraulic conductance (PLC) of excised petiole segments remained close to 0% throughout the day. To find out which technique was erroneous we first analyzed the possibility that PLC values were rapidly returned to zero when the xylem pressures were released. We used the centrifugal force to measure the xylem conductance of petiole segments exposed to very negative pressures and established the relevance of this technique. We then analyzed the possibility that vessels were becoming partially air-filled when exposed to LN(2). Cryo-SEM observations of petiole segments frozen shortly after their xylem pressure was returned to atmospheric values agreed entirely with the PLC values. We confirmed, with water-filled capillary tubes exposed to a large centrifugal force, that it was not possible to freeze intact their content with LN(2). We concluded that partially air-filled conduits were artifacts of the cryo-SEM technique in our study. We believe that the cryo-SEM observations published recently should probably be reconsidered in the light of our results before they may be used as arguments against the cohesion-tension theory.

Direct measurement of xylem pressure in leaves of intact maize plants. A test of the cohesion-tension theory taking hydraulic architecture into consideration

The water relations of maize (Zea mays L. cv Helix) were documented in terms of hydraulic architecture and xylem pressure. A high-pressure flowmeter was used to characterize the hydraulic resistances of the root, stalk, and leaves. Xylem pressure measurements were made with a Scholander-Hammel pressure bomb and with a cell pressure probe. Evaporation rates were measured by gas exchange and by gravimetric measurements. Xylem pressure was altered by changing the light intensity, by controlling irrigation, or by gas pressure applied to the soil mass (using a root pressure bomb). Xylem pressure measured by the cell pressure probe and by the pressure bomb agreed over the entire measured range of 0 to -0.7 MPa. Experiments were consistent with the cohesion-tension theory. Xylem pressure changed rapidly and reversibly with changes in light intensity and root-bomb pressure. Increasing the root-bomb pressure increased the evaporation rate slightly when xylem pressure was negative and increased water flow rate through the shoots dramatically when xylem pressure was positive and guttation was observed. The hydraulic architecture model could predict all observed changes in water flow rate and xylem. We measured the cavitation threshold for oil- and water-filled pressure probes and provide some suggestions for improvement.

Water ascent in plants: do ongoing controversies have a sound basis?

The cohesion-tension theory of the ascent of sap in plants is fundamental to the understanding of water movement in plants. According to the theory, water is pulled upwards by high tensions (low negative pressures) created in the xylem vessels and tracheids of higher plants by the evaporation of water vapour from leaves. However, much lower tensions (less negative pressures) have been found from direct measurements using a pressure probe. These do not appear to be compatible with the cohesion-tension theory. As a consequence, the validity of the cohesion-tension theory has been questioned and alternative mechanisms for sap ascent have been proposed. Recent experiments show that the conclusions drawn from the pressure probe work were premature. New direct measurements of xylem pressure support the cohesion-tension theory and the previous indirect measurements of xylem pressure.

Comparative measurements of xylem pressure in transpiring and non-transpiring leaves by means of the pressure chamber and the xylem pressure probe

proposed more than 100 years ago by Dixon and Joly (1894). According to this theory, long-distance water Simultaneous measurements were made with the transport in xylem is driven by tension (negative pressure) xylem pressure probe on exposed, transpiring leaves gradients generated by the evaporation of water from and with the Scholander pressure chamber on both leaves and transmitted through continuous water columns transpiring and covered, non-transpiring leaves of from the leaf apoplast to the roots. Evidence supporting sugarcane and maize plants. Xylem tensions inferred the Cohesion-Tension theory consists largely of thousands from pressure chamber balancing pressures on non- of indirect estimates of xylem pressure obtained in excised transpiring leaves were similar to those measured leaves and branches with the Scholander pressure chamdirectly with the xylem pressure probe in transpiring ber (Scholander et al., 1965). The recent development of leaves. However, tensions inferred with the pressure the xylem pressure probe (xylem probe) by Balling and chamber on transpiring leaves that were placed in Zimmermann (1990) has allowed the direct measurement plastic bags just prior to excision were up to 0.6 MPa of xylem pressure in single vessels of intact plants. greater than those measured concurrently with the Measurements with the xylem probe have confirmed xylem pressure probe. These findings suggest that the existence of tensions in the xylem of both transpiring relatively large differences in water potential between and non-transpiring plants, but the values obtained are the xylem and bulk leaf tissue can exist during periods often substantially smaller than those inferred from indirof rapid transpiration, and they confirm that the ect techniques, such as the pressure chamber and psychrobalance pressure of an excised, previously transpiring meter (Balling and Zimmermann, 1990; Zimmermann leaf is only a measure of the bulk average equilibrium et al., 1991, 1994a, b). This has led some researchers to leaf water potential and not of the true xylem pressure question the validity of estimates of xylem tension that existed prior to excision. obtained with the pressure chamber and to postulate that the currently accepted hundred-year-old Cohesion

The Cohesion-Tension theory of sap ascent: current controversies

In recent years, the Cohesion-Tension (C-T) theory of sap ascent in plants has come under question because of work published by Professor Ulrich Zimmermann and colleagues at the University of Wurzburg, Germany. The purpose of this review is to (1) state the essential and testable elements of the C-T theory, (2) summarize the negative evidence for the C-T theory, and (3) review critically the positive evidence for the C-T theory and the evidence that the ScholanderHammel pressure bomb measures xylem pressure potential (Px) correctly, because much of the evidence for the C-T theory depends on pressure bomb data. Much of the current evidence negates the conclusions drawn by Zimmermann from studies using the xylem pressure probe (XPP), but it is not yet clear in every instance why the XPP results disagree with those of other methods for estimating xylem pressure. There is no reason to reject the XPP as a useful new tool for studying xylem tensions in the range of 0 to -0.6 MPa. Additional research is needed to test the C-T theory with both the XPP and traditional methods.

Cohesion Transport Theory of Water Movement in Plants: Some Anomalous Results Provided by Xylophagous Leafhoppers

The Cohesion Tension Theory, first in 1894 introduced by Dixon and Joly is the theory most often invoked to explain water movement in a transpiring plant. The pressure chamber technique has provided the strongest indirect evidence for this theory. However, controversy remains because 1) the necessary pressure gradients in xylem vessels have never been measured directly; 2) it is uncertain how continuous water columns under great tensions could persist in a metastable state for extended periods of time, and; 3) direct pressure probe measurements on individual xylem vessels have not been indicative of the extreme negative pressures obtained with the pressure chamber. Xylem fluid is an energy-limited resource containing the lowest available carbon (energy content = 2 to 15 J/cm3) of any plant tissue. However, many species of xylophagous leafhoppers subsist entirely on this dilute food source, despite the negative pressures thought to occur in xylem vessels. Carbon limitations of leafhoppers were underscored by 1) high feeding rates; 2) an unprecedented assimilation efficiency of organic compounds (i.e., &gt;99%); 3) ammonotelism, and; 4) synchronization of feeding to optimum host nutrient content both seasonally and diurnally. The maximum tension that can be generated by the cibarial pumping mechanism of an insect based on anatomy and biochemistry is about 0.3 to 0.6 MPa, far below the purported xylem tensions occurring during most daylight hours. By contrast, we have shown that feeding has been usually independent of xylem tensions, as measured with a pressure chamber, and instead was a function of the amide content of xylem fluid. Moreover, the calculated net energy gain of insect feeding (or that contained within insect biomass) on xylem fluid of a given composition under a given tension have also been an a paradox. Experiments will be described that provide insight into the energetics of xylem fluid extraction.

Sustained and significant negative water pressure in xylem

DESPITE two centuries of research, the mechanism of water transport in plants is still debated1–8.The prevailing cohesion–tension theory2,3, which states that water is pulled upwards by capillarity in cell-wall pores, remains vulnerable to challenge because its corollary is difficult to prove: that large negative pressures exist in xylem conduits4–7. Recent xylem pressure-probe and z-tube experiments suggest that cavitation limits xylem pressures to above −0.5 MPa, despite the much more negative pressures predicted by the cohesion–tension theory and measured with the standard pressure-chamber method4,5,9,10. Here we show, using centrifugal force to induce negative pressure between −0.5 and −3.5 MPa in intact stems, that xylem conduits remained water-filled and conductive to species-specific pressures ranging from −1.2 to below −3.5 MPa. Results were consistent when stems were air-dried or injected with air. Agreement among these techniques demonstrates that xylem can support large negative pressures, that the pressure chamber reliably measures these pressures, and that cavitation is nucleated by air entry through conduit wall pores.