JXB Advance Access originally published online on July 16, 2003
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Journal of Experimental Botany, Vol. 54, No. 390, pp. 2149-2155,
September 1, 2003
© 2003 Oxford University Press
Vulnerability curves from conifer sapwood sections exposed over solutions with known water potentials
Received 24 January 2003; Accepted 15 May 2003
Institute of Botany, Universität für Bodenkultur Wien, Gregor Mendel Str. 33, A-1180 Vienna, Austria
* To whom correspondence should be addressed. Fax: +43 1 47654 3180. E-mail: silvia.kikuta{at}boku.ac.at
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Abstract |
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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 µm 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.
Key words: Cavitation, cohesion–tension theory, Juniperus virginiana L., sapwood sections, ultrasound acoustic emissions, vulnerability curves, water potentials.
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Introduction |
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Increasing tensions in the liquid water inside conducting xylem elements lead to cavitation (the sudden break of the water column by a rapidly expanding gas bubble), followed by embolization (the entrance of air into tracheae and tracheids). These processes affect the functional integrity of the water transport system and reduce hydraulic conductivity. Differences between species or organs in the resistance of conduits against cavitation and embolization are analysed by constructing vulnerability curves (Tyree and Sperry, 1989; Tyree and Ewers, 1991). Such curves are plots of some quantitative measure for the degree of embolization against the tensions, i.e. against pressure potential in the xylem solution. They may be determined on stems slowly dehydrated by transpiration (Tyree and Sperry, 1989), centrifuged to induce tensions (Pockman et al., 1995; Alder et al., 1997) or subjected to an overpressure of compressed air (Sperry and Saliendra, 1994; Alder et al., 1996; Sperry and Ikeda, 1997; Sperry and Tyree, 1990; Linton et al., 1998), or on detached leaves transpiring on the laboratory bench (Kikuta et al., 1997). Xylem embolization is estimated from the loss of hydraulic conductivity or from the number of ultrasound acoustic emissions (UAE) during cavitation (Lo Gullo and Salleo, 1991). Water potentials are measured with a pressure chamber or a thermocouple hygrometer.
Cavitation events in drying conifer sapwood sections are directly visible under a microscope (Lewis et al., 1994). In the present study vulnerability curves are measured by subjecting such sections to predefined water potentials and quantifying cavitation from UAE. Tangential sections through conifer sapwood are exposed in a small, closed airspace over osmotically active solutions. Water is transferred from the tracheids via the airspace to the solution following the gradient in total water potential, tensions rise and finally cavitations start. A UAE transducer in contact with the xylem section records the number of events during a fixed time span, and this number is compared to the total obtained after exposing the same section to ambient air. The final water potential in the tracheids equals the osmotic potential of the solution, and the course of its establishment may be followed with a thermocouple hygrometer in contact with the section.
This method allows the cavitation resistance of the metastable liquid water in the lumen of tracheids in conifer sapwood sections to be estimated. The vulnerability is low enough to support the cohesion–tension (CT) theory. It is, however, higher than for tracheids in intact stems, which fact requires some discussion on vulnerability curves established by different methods. It seems that both the state of isolation of the conducting xylem elements and the time the water column is exposed to tensions are important and so far ignored factors controlling the vulnerability of the hydraulic system.
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Materials and methods |
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About 20-year-old branches of an adult Juniperus virginiana L. (Cupressaceae) tree were harvested in the Botanical Garden of the Universität für Bodenkultur (BOKU), Vienna. Tangential sections of the fresh sapwood (100 µm thick and 20x20 mm wide) were cut with a sliding microtome (Reichert, Vienna, Austria) and stored in a solution of 14 mM ascorbic acid which had been filtered through a 0.2 µm filter and degassed. This solution prevents microbial growth and hydraulic artefacts ascribed to the swelling of xylem cell walls in distilled water (Zimmermann, 1978; Borghetti et al., 1993; Tognetti and Borghetti, 1994). NaCl solutions with osmotic potentials ranging from – 0.91 to –7.57 MPa were prepared according to Lang (1967).
A section was taken from the ascorbic acid solution, rinsed for a few minutes in filtered and degassed distilled water, blotted with filter paper, and attached to an I15I ultrasound acoustic emission transducer with a diameter of 18 mm connected to a 4516 Drought Stress Monitor (DSM) (Physical Acoustics Corporation, Princeton, NJ, USA). Two types of vessels were used to expose the sections to the atmosphere over an NaCl solution of known osmotic potential.
In the first experiment, when UAE and water potential were measured simultaneously, the rinsed and blotted section was clamped by means of a stiff metal grid under the lid of a shallow aluminium trough filled with NaCl solution (Fig. 1). Holes in the top of the lid held three sensors: (1) an I15I UAE transducer, (2) an L-51 thermocouple hygrometer (Wescor, Logan, UT, USA) calibrated over NaCl solutions of different concentrations; (3) a copper-constantan thermocouple for measuring the temperature of the metal case. Sensors (2) and (3) were connected to an HR 33-T microvoltmeter operated in the dewpoint mode (Wescor, Logan, UT, USA). The UAE transducer and the thermocouple hygrometer were firmly pressed against the sapwood section, sealed in place with a beeswax–lanolin mixture and immobilized with screws.
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The second experiment aimed only at counting UAE during long-term exposure (4 h and 16 h), for which a simpler set-up was used. A close-fitting metal shoe with a central opening of 12.7 mm diameter flattened the section against the ceramic plate of the transducer. The transducer with the section was inserted into a tight-fitting cylindrical vessel filled with 2 ml of NaCl solution. The metal shoe rested on a rim about 2 mm above the solution. Silicon grease between the shoe and the walls of transducer and vessel provided a vapour-tight seal.
In all experiments, the total gain of the ultrasound counter was 70 dB (the monitor amplifier set at 50 dB, the head-stage amplifier at a fixed 20 dB), and UAE were recorded online with a personal computer. To reduce the amount of water which had to be transferred to the solution and to speed up the beginning of ultrasound emissions, the section was exposed to ambient air until the first three to five signals had been registered; this took up to 15 min. Then the lid was sealed over the NaCl trough.
At the end of the preselected time over the solution, the section was removed from the vessel and again exposed to ambient air, which resulted in an immediate surge of emissions. Finally, the signals petered out completely, which took less than 2 h. The total number of signals was different for different sections from a series and even more so for section series cut at different times. This is not surprising, since the number of intact, uncut tracheids of an average length of more than 1 mm will depend on small differences in the alignment between the tracheid axis and the plane of the section. Totals of signals between 6000 and 15 000 were considered acceptable.
The signals emitted from the sapwood section over a given solution were calculated as percentage of the total number of emissions:
%UAE=100 UAEsol/UAEtot
where UAEsol is the number of ultrasound acoustic emissions recorded over the solution, UAEtot the total over the solution and after exposure to ambient air.
In the third experiment, conventional vulnerability curves were measured on detached branches of the same age and collected from the same Juniperus virginiana tree as used in the other experiments. The branches were brought to the laboratory, re-cut under water, covered with plastic bags and kept in a cool and dark room for at least 24 h with their cut ends standing in distilled water. They were then transferred to a room with a temperature of 22.8± 0.1 °C and a relative air humidity of 28.7±0.1%. Bark tissues were peeled from the saturated branches over a length of about 25 mm, and a thin layer of medium-viscous silicon grease was applied to the exposed xylem to prevent dehydration. An I15I ultrasound acoustic emission transducer was clamped to the xylem. The total gain of the ultrasound counter was again set at 70 dB. Peripheral twigs were wrapped in aluminium foil at least 4 h prior to the measurement of xylem water potentials with a pressure chamber (model 3000, Soil Moisture Equipment Corporation, Santa Barbara, CA, USA). The branches took more than a week to dehydrate until UAE stopped. Thus, gradients in water potential in the branch system were probably minimal. Total water potentials were followed to values slightly less negative than –10 MPa, ultrasound signals were counted until they subsided completely.
Four of the sections used in the UAE studies were macerated in Jeffrey’s solution (Jeffrey, 1917). Tracheid lengths were measured under a binocular microscope with a CCD camera connected to a MacIntosh computer, using the NIH-Image analysis system (Wayne Rasband, National Institutes of Health, USA). Values ranged from 626.1 to 1622.4 µm, with a mean of 1037.6±26.5 µm (n=100).
Transverse sections 15 µm thick were cut for the measurement of additional dimensions from the sapwood specimens used for tangential sections, stained with methylene blue and embedded in Euparal (Gerlach, 1984). Lumen diameters and cell wall thickness in a radial direction were measured under a transmission light microscope, again using the NIH system. All lumina and cell walls within 100 µm from a randomly selected starting point were measured, without discrimination between earlywood and latewood. Within this distance of 100 µm, 6–8 layers of tracheids were observed. Their diameters varied between 4.4 and 19.1 µm, with a mean of 13.05±0.29 µm (n=139). Walls were on average 2.65± 0.04 µm thick (n=159), with values from 1.40 to 3.77 µm.
All data were analysed with the SPSS 9.0 statistics package (SPSS Inc., Chicago, IL, USA). Values are means ± standard error. A sigmoid function of the form %UAE=c/(1–exp (bx(MPa–a)) was fitted to vulnerability curves, where a, b and c are parameters obtained with the curve-fitting function of SigmaPlot (V 2.0, SPSS Science, Chicago, IL, USA). This function was used to calculate and compare the tissue water potentials corresponding to 50% UAE.
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Results |
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Figure 2 shows the time-courses of water potentials exposed over NaCl solutions differing in osmotic potentials. Water transfer depends on the vapour pressure gradient, so negative water potentials in the sections were established in shorter times over more concentrated solutions. A plateau value was reached after about 2 h over the strongest and after about 3 h over the weakest NaCl solution. The hygrometer data points at the plateau showed only slightly fluctuating values for tracheid water potentials, and their averages were nearly identical with the potentials of the NaCl solutions: –3.18±0.01 MPa over a solution of –3.21 MPa; –4.14±0.01 over –4.16 MPa; –5.03±0.01 over –5.13 MPa; and –6.54±0.05 over –6.62 MPa.
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The time-courses of UAE over different NaCl solutions were measured for 16 h (Fig. 3). The two strongest solutions (–7.57 MPa, –4.64 MPa) as well as the weakest one (–0.91 MPa) had almost reached an equilibrium after that time. More than 90% of the tracheids had already cavitated over the two strongest solutions, but only 4% in the sections over the –0.91 MPa solution. Signals over the three intermediate solutions continued to increase even after 16 h.
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Percentages of UAE from sections kept over solutions for fixed periods (4 h and 16 h) distinctly depended on the time of exposure (Fig. 4). The difference in %UAE was particularly pronounced over solutions with water potentials of –2.74 and –3.68 MPa. With increasing concentration of the solutions (water potentials of –4.64 and –7.57 MPa) the difference in %UAE between the two treatments diminished.
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Vulnerability curves obtained by exposure over NaCl solutions ranging from –1.82 to –6.62 MPa showed only moderate differences, with a given UAE percentage reached at a higher water potential over the less concentrated NaCl solutions (Fig. 5, solid lines). When the sections reached equilibrium with the solutions, water potentials remained constant, but UAE continued at a low rate for many hours, which is seen as a vertical line at the end of the curves.
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By contrast, vulnerability curves established on whole branches suggested considerably more resistance to cavitation (Fig. 5, closed circles). A low percentage of signals was registered at potentials higher than –4.40±0.30 MPa. 50% UAE activity was reached at –8.25±0.34 MPa.
The average sapwood water potential in sections at 50% UAE was –4.02±1.2 MPa (n=9), but was significantly more negative (Pearson r2=0.66, P <0.01) in sections exposed over stronger solutions, where water loss from the section was faster and a given water potential was reached more rapidly (Fig. 6).
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Discussion |
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Thin tangential sections of conifer sapwood exposed over osmotically active solutions emit acoustic signals which are produced by vibrating tracheid walls after the sudden cavitation of water in the lumen (Milburn and Johnson, 1966; Tyree and Sperry, 1989). In conifer xylem, water-filled structures other than tracheids, which might produce additional signals (Sperry et al., 1988), are absent. If total water potential (
t) in the tissue is less negative than the osmotic potential (o) of the NaCl solution, water is transferred to the solution along the vapour pressure gradient and the tissue potential decreases (Fig. 2). Finally a threshold is reached where cavitations start in the most vulnerable tracheids, presumably those with the widest pit membrane pores bordering on air (Zimmermann, 1983). Cavitating tracheids release some liquid water to their neighbours, so the decline of the water potential in the section will be gradual, with new cavitations added where suitable pit pores are reached by air or where still uncavitated tracheids become vulnerable due to increasing tensions. The sigmoidal shape of the vulnerability curves (Fig. 5) reflects the fact that tracheid vulnerability is distributed along a bell-shaped curve with most of the conducting elements cavitating at medium potentials. A complete stop in tracheid cavitation and signal emission cannot be expected once the water potential of the solution is reached: the water in the lumen is only metastable, and each newly cavitating tracheid will expose the walls of adjacent cells to air contact which in turn may trigger new air seeding. Figure 3 shows that a stable situation will arise only when either all tracheids have cavitated or the tensions are too low to cause an appreciable number of tracheids to cavitate. It obviously takes many hours until optimum conditions for cavitation are established in a thin section for all those tracheids which will eventually cavitate. Any time limit of exposing tissue sections to defined water potentials is thus arbitrary. Keeping the sections over the solutions for 16 h instead of 4 h shifted the vulnerability curves to the right, that is, to higher potentials for a given percentage of embolization. The relationship between exposure time over differently concentrated NaCl solutions and the percentage of UAE recorded followed an exponential function (Fig. 4). This results from the fact that the low cavitation percentages over the most dilute solution were nearly identical after exposure for 4 h and 16 h, while over the strongest solutions a maximum was already approached after 4 h. The most conspicuous differences thus occurred in the middle of the concentration scale.
These results confirm a central premise of the cohesion–tension theory: water filling the lumen of conducting elements comes under tension and is in a metastable state, but tracheids may nevertheless remain uncavitated for a long time. After 16 h of exposure over a solution with a water potential of –0.91 MPa, only 4% of total UAE were measured, and over a solution with a water potential of –1.82 MPa, more than 70% of the tracheids had not yet cavitated (Fig. 3). These facts make superfluous the alternative mechanisms of water transport which have been formulated under the assumption that water in conducting xylem elements cannot sustain pressure potentials more negative than –0.6 to –0.7 MPa for more than a few seconds (Zimmermann et al., 2002; Canny, 1995) and confirm work from the past decade demonstrating the stability of water in the conduits (Alder et al., 1997; Cochard et al., 2000; Comstock, 1999; Holbrook et al., 1995; Pockman et al., 1995; Sperry et al., 1996; Stiller and Sperry, 1999; Tyree, 1999; Wei et al., 1999).
Instead of searching for alternatives to the cohesion–tension theory (Zimmermann et al., 2002) one should concentrate on questions that are still open which will have to be explained in the framework of this old theory (Boehm, 1893; Askenasy, 1895; Dixon and Joly, 1895). Among them is the mechanism for refilling of cavitated and embolized conduits, a phenomenon repeatedly demonstrated (Salleo et al., 1996; Holbrook et al., 2002) but, in the authors’ opinion, not yet convincingly explained. There are, in addition, the impacts of isolation and of exposure time at negative potentials. These two factors influence cavitation events in the conduits, as becomes evident from the data presented here.
There is a large discrepancy between vulnerability curves obtained on sapwood sections after exposure over osmotically active solutions and the ones measured on whole branches from the same tree (Fig. 5). While sections over solutions started to emit an appreciable number of signals at about –1.8 MPa and reached 50% of the total at an average value of –4.0 MPa, the thresholds for incipient and 50% UAE activity of branches were about –4.4 and –8.2 MPa, respectively. The difference is extreme and requires an explanation.
In the authors’ opinion, this explanation has to start from the different exposure to air at the beginning of measurements. The air-seeding hypothesis (Zimmermann, 1983) implies that a conducting element will only cavitate when a suitably porous pit membrane is in contact with bulk air. Sapwood sections consist of only a thin tissue layer, with a large percentage of the tracheids therein bordering on air. The massive sapwood cylinder in an intact conifer stem or branch, on the other hand, includes only a small volume of intercellular spaces and is crossed by few other air-filled structures, such as leaf scars or abscised twigs, so that the great mass of tracheids is isolated from direct air contact and surrounded by other water-filled tracheids. The cambium on the outside of the sapwood provides an additional isolating sheath which, in most cases, lacks intercellular spaces.
It is easy to perceive that air will contact a larger percentage of the tracheids in a shorter time in thin sections than in massive stems or branches. Furthermore, there is speculation that large amounts of gases dissolved in the xylem sap will increase vulnerability (Grace, 1993), although others dismiss this possibility (review by Pickard, 1981). Wood sections exposed to ambient air are probably saturated with gases and thus could be more vulnerable than the interior of stems or branches.
Another factor with consequences for the shape of a vulnerability curve is time. As can be seen from Fig. 4, longer exposures to water potentials more negative than the cavitation threshold will increase the percentage of cavitated tracheids. Rapid water loss over concentrated solutions shifts the point of 50% cavitation towards more negative potentials (Fig. 6), in the authors’ opinion by reducing the impact time of intermediate water potentials. A conventional vulnerability curve, when measured on bench-drying branches as described here, has this time parameter rather undefined. The rate of decline in water potential of such a branch must depend on the ratio between the area of transpiring leaves and the water volume stored in the sapwood. This rate is, therefore, higher in small twigs than in big branches, which means that the impact time of a given water potential is reduced there. The easily standardized but arbitrary periods of exposure used to induce cavitation with the pressure collar and the centrifuge are comparatively short and not identical in all experiments, while the dimensions of the twigs investigated with these methods tend to be small. The vulnerability curves may, therefore, differ from those obtained in bench-drying large branches.
Yet another discrepancy between vulnerability curves from the same object may be due to different indicators for embolization. UAE, which were used in this work, are supposedly a rather direct measure for the number of cavitating conduits (Tyree et al., 1984). The general assumption is that the ratio of true cavitation events to signals emitted is close to 1, so that 50% UAE correspond to 50% cavitated conduits. The percentage loss of hydraulic conductivity, which is often used as a different measure for the degree of cavitation and embolization, is far less directly related to the percentage of cavitation in the sapwood.
The end of the drying process, when the last UAE signal is received by the sensor, will be considered first. It is immediately clear that this signal will be emitted at a water potential lower than needed for the complete loss of conductivity. For maintaining any conductivity at all, not just one tracheid, but an uninterrupted file of tracheids at least, extending from one cut surface to the other of the stem section used in the hydraulic measurement, would be needed. It is, however, extremely unlikely that vulnerabilities of tracheids are distributed and cavitations initiated in such an ordered way; the authors do not think, therefore, that Tyree and Sperry (1989) are right in their belief that the cessation of acoustic emission activity should always correspond in time with the loss of the last vestiges of hydraulic conductivity. Far more plausible seems a scenario where more and more groups of water-filled tracheids become successively isolated amid empty pockets of cavitated tracheids growing from points of contact between walls and air-filled spaces. Water-filled tracheids isolated in this way, while not cavitated and therefore not sensed by the UAE counter, can no longer contribute to water transport. Other pathways between the two cut surfaces will consist of tracheid files with limited contribution to overall conductivity because of high-resistance bottlenecks at the beginning or at the end. Thus it becomes very likely that the percentage loss of conductivity at any water potential beyond the cavitation threshold should, in most cases, be more than the percentage of cavitated tracheids.
There are some literature data from measurements on Juniperus virginiana L. which tend to support this view. Tyree and Sperry (1989) found –4 MPa and –6 MPa for incipient and 50% conductivity loss in a bench-drying experiment. This is exactly intermediate between the low values on sapwood sections and the high values on branches found in this study’s experiments, where cavitation was estimated in both cases from UAE signals.
It may thus be more difficult than hitherto assumed to compare vulnerability curves established with different methods. Furthermore, it is, in the authors’ opinion, not justified to regard the vulnerability data from stems, branches, twigs or even sections exclusively as a result of inherent properties of single conducting elements and their pit membranes. It seems that the structure of the whole sapwood body, from the isolating cambium layer to the volume and the distribution of air-filled spaces and their connection to conducting elements, is of great importance for the stability of the water-conducting system. These problems await further investigation and discussion.
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Acknowledgements |
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We thank Dr Sabine Rosner for help with the measurement of tracheid dimensions, Ulrike Gödl and Mag Jószef Kósa for technical assistance. Suggestions by two anonymous referees helped us to improve an earlier version of this paper.
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