JXB Advance Access originally published online on August 1, 2006
Journal of Experimental Botany 2006 57(12):3157-3163; doi:10.1093/jxb/erl077
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
RESEARCH PAPER |
Temporal and spatial pattern of embolism induced by pressure collar techniques in twigs of Picea abies
Institut für Botanik, University Innsbruck, Sternwartestr. 15, A-6020 Innsbruck, Austria
*To whom correspondence should be addressed. E-mail: stefan.mayr{at}uibk.ac.at
Received 23 March 2006; Accepted 8 June 2006
 |
Abstract |
|---|
 Top Abstract IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
The pressure collar technique enables the induction of embolism in plant xylem. This artificial cavitation is based on air seeding processes which occur when specific pressure gradients between the air and water phase of the xylem are exceeded. Standard pressure collars and a new point injection technique, which builds up a local potential gradient, were used to study the time and spatial pattern of this process. On twigs of Norway spruce (Picea abies), the cross-sectional and axial pattern, and the time-course of embolism formation were analysed via conductivity and ultrasonic measurements as well as staining experiments. Furthermore, the release of air from the twig surface was studied by immersing twig sections in water. In cross-sections, embolized areas induced by the point injection technique were smaller compared with the standard collar and restricted to a circle sector. Embolism propagated from the pressure collar towards the nearest distal and proximal nodes but not further. A release of air was also observed predominantly at the internode attached to the pressure collar. Embolism rates increased within minutes and reached
80% loss of conductivity after 10 min treatment with the standard collar. The size of air entry points and embolism rates correlated significantly. Embolism formation in wood therefore depends not only on vulnerability thresholds but also on the extent of air–water interfaces within the xylem and on the time of exposure to pressure gradients. These aspects and the propagation of pressure within samples are crucial for pressure collar experiments. In addition, wood architecture influences the extent and pattern of embolism caused by air seeding processes. Key words: Air entry point, air seeding, air–water interface, cavitation, conifers, embolism, pressure collar, xylem
|
Introduction |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Air–water interfaces are critical areas in the water transport system of plants which is based on metastable water columns transmitting negative pressure to the soil (‘cohesion tension theory’; Boehm, 1893; Dixon and Joly, 1894; Richter, 1972; Jackson and Grace, 1994). Air spaces, always present in the xylem (e.g. as consequence of cracks upon mechanical damage or of herbivory) can destabilize the water columns and consequently induce a breakage of the hydrogen bonds between water molecules, leading to embolism (Tyree et al., 1994). To maintain an intact transport system, plants have to avoid this heterogenous nucleation which usually occurs at the pits of the xylem conduits (air seeding hypothesis; Zimmermann, 1983).
In angiosperms, pit membranes exhibit small pores so that the surface tension of water prevents the entry of air into adjacent water-filled conduits. In contrast, conifer pits exhibit a margo with wide pores which can only stabilize the air–water interface at moderate pressure gradients (Sperry and Tyree, 1990). When these gradients increase, a valve-like aspiration of the margo's central torus to the pit opening protects tracheids from air seeding. Both mechanisms provide an efficient isolation of intact water columns from air spaces, unless pressure gradients exceed species- and xylem-specific thresholds (Tyree et al., 1994; Hacke et al., 2001). In conifer pits, the torus is displaced from its sealing position at these vulnerability thresholds.
Air seeding can be simulated by use of positive pressures (Cochard et al., 1992b). In situ, the xylem sap normally is under substantial negative pressure (low water potential) while air spaces are at atmospheric pressure. The air injection technique is used to raise the pressure in the air phase. The resulting pressure gradient depends on the xylem potential and the applied pressure so that vulnerability thresholds can be reached even when the potential of the xylem sap is zero. This can be done with a pressure chamber enclosing whole twigs (Tyree et al., 1984; Crombie et al., 1985; Cochard et al., 1992a; Jarbeau et al., 1995) or with a pressure collar enclosing just a section of the axes. The latter technique was used by several authors to study vulnerability curves in angiosperms (Cochard et al., 1992b; Sperry and Saliendra, 1994; Alder et al., 1996; Lo Gullo et al., 1997) and conifers (Sperry and Tyree, 1990; Sperry and Ikeda, 1997; Linton et al., 1998; Stout and Sala, 2003). Furthermore, pressure collars were used to induce embolism in situ in Laurus nobilis (Tyree et al., 1999; Salleo et al., 2004) and Salix viminalis (Salleo et al., 1992). Most authors used standard protocols for their pressure collar experiments, focusing on the pressure gradients required to induce embolism. In contrast, knowledge of dynamics and spatial propagation of air seeding in the xylem of twigs and the consequences for the use of the pressure collar technique is still poor.
In the present study, the time-course of embolism formation and the axial pattern of the resulting conductivity losses were analysed using a standard pressure collar. The size and number of air entry points was varied to analyse the effects on the extent of conductivity losses. In addition, the release of air from the surface of twigs treated with the pressure collar was estimated. A second, new technique (‘point air injection’) was developed to study the spreading of air seeding from a small air entry point. All the experiments were done on Norway spruce twigs (Picea abies L. Karst), because conifer xylem is very homogenous and therefore an excellent object to study.
|
Materials and methods |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Norway spruce [Picea abies (L.) Karst.] twigs (up to 2 m in length) were harvested at Praxmar, Tyrol (1700 m) and transported to the laboratory in plastic bags. The twigs were re-cut under water and saturated for at least 24 h.
The vulnerability thresholds to drought-induced embolism of twigs at this altitude are at –3.18±0.19 MPa and –3.88±0.06 MPa for 10% and 50% loss of conductivity, respectively (Mayr et al., 2002).
Pressure collar treatment
Twigs were exposed to positive pressures by the use of two techniques. Most experiments were done with a standard pressure collar which completely encloses a section of the twig axes in a chamber. Either the on-limb cavitation chamber (PMS Instrument Company, Corvallis, OR, USA) or a pressure collar, as shown in Fig. 1A, was used. Furthermore, a device was constructed which enables the application of pressure on a small area at the twig's surface, the ‘point air injection’ method. For pressure application, a small metal cone with a borehole, 3.5 mm in diameter, and an O-ring for sealing is pressed on the twig (Fig. 1B).
|
Both techniques were performed on the main axes of whole twigs, whereby sections free of side twigs and up to 15 mm in diameter were selected. The following standard experimental design was used: for the pressure collar, two holes (air entry points), from the upper to the underside and horizontally, were drilled through the twig using a borer, 1 mm in diameter. The twig section was sealed in the chamber with the holes situated in its centre. For the point air injection treatment, a hole, 1 mm in diameter, was drilled through the bark and 1–2 mm into the wood. The device was attached exactly at this air entry point. The pressure collar or point air injection device was connected to a pressure reservoir and the pressure was raised to 4.5 MPa. This pressure was maintained for 15 min.
In additional experiments with the pressure collar, the number (0–10) of boreholes as well as the duration of pressure exposure (0–60 min after reaching 4.5 MPa) were varied. The influence of the borehole depth was studied in twigs 10 mm in diameter, whereby two horizontal holes (depth 0–9 mm at both sides of twigs) were drilled. In an additional experiment with the point air injection device, the time of exposure was varied between 0 and 60 min.
All treatments were ended by slowly (within 5 min) releasing the pressure. The pressure collar or point injection device was removed and axis sections were cut out of the twig distal and proximal to the boreholes. Segments closest to the bore holes and 20 mm in length were used for staining and conductivity analysis. In one experiment with the pressure collar following the standard experimental design, adjacent segments were taken to study the axial embolism pattern.
Dye experiments
After removal of the bark, and re-cutting under water, samples were sealed in silicone tubes connected to a reservoir filled with dye solution [Phloxine B, Sigma Chemical Co., St Louis, MO, USA; 2% (w/v)]. After staining (4 kPa, 5–10 min), cross-sections of samples were prepared.
Measurements of embolism rates
The conductivity of xylem samples was measured with a modified Sperry apparatus (Sperry et al., 1988; Chiu and Ewers, 1993; Vogt, 2001) described in Mayr et al. (2002). Embolism rates are quantified by determination of the increase in hydraulic conductivity after removal of enclosed air by repeated high pressure flushing. Sample preparation was done as described in Mayr et al. (2002). The measurement pressure was set to 4 kPa. The flow rate was determined with a PC-connected balance (Sartorius BP61S, 0.0001 g precision, Sartorius AG, Göttingen, Germany) by weight registration every 10 s and linear regression over 200 s. Flushing (0.13 MPa, 20 min) and conductivity measurements were done with distilled, filtered (0.22 µm), and degassed water containing 0.005% (v/v) ‘Micropur’ (Katadyn Products Inc., Wallisellen, Switzerland) to prevent microbial growth (Sperry et al., 1988). Flushing was repeated until measurements showed no further increase in conductivity. Loss of conductivity as a percentage was calculated from the ratio of initial to maximal conductivity.
Ultrasonic measurements
Ultrasonic measurements were done with a PCI-2 based system (PAC 125 18-bit A/D, 3 kHz–3 MHz PCI2) and 150 kHz resonance sensors (R15/C, 80–400 kHz) connected to a 20/40/60 dB pre-amplifier set to 40 dB (all components: Physical Acoustics, Wolfegg, Germany). The threshold was set to 45 dB; peak definition time, hit definition time, and hit lockout time were 200, 800, and 1000 µs. Registration and analysis of ultrasonic events were done with AEwin software (Mistras Holdings Corp., Princeton, NJ, USA). Sensors were attached to the upper side of the main axes adjacent to the pressure collar and distal or proximal to the next node with side twigs. At these positions, 4 cm2 of the bark was removed and the xylem was covered with silicone grease (to improve the acoustic coupling and prevent transpiration) before attaching the sensors with clamps.
Analysis of air release
The release of air was studied by immersion of a twig section in water while treatment with the pressure collar followed the standard experimental design. The twig section contained two nodes, and the pressure collar was positioned exactly in the middle of the enclosed internode. The cut ends of the twig axes (5 cm outside of the nodes) were plugged with parafilm and a strong tape to prevent air release at the ends of the twig section. Ten minutes after the pressure had reached 4.5 MPa, released air was trapped in a row of water-filled, immersed cuvettes (1x1 cm square cross-section), positioned exactly above the twig for 5–10 min. This allowed a rather rough estimation of the pattern of air release as the number of measurement points (one per cm due to the cuvette size) was low and, especially near the pressure collar, not all air bubbles could be trapped. The volume of trapped air was calculated according to the height of the air column in each cuvette and related to the time during which the air was trapped.
Number of samples and statistics
The axial embolism pattern was analysed from six twigs cavitated with the standard pressure collar and one with the point air injection method. The release of air was studied on five twigs, and ultrasonic measurements were done on three twigs treated with the standard collar. For the analysis of the time-course of embolism formation, 73 samples treated with the standard collar and 23 samples with the point injection were used. The influence of the number of boreholes and of the bore depth was studied on 30 samples, respectively. Differences were tested at the 5% probability level with the Student's t test after checking for normal distribution and variance of the data. Correlation analysis was carried out via Pearson's linear correlation coefficient r at the 5% probability level.
|
Results |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Point air injection method
Twigs treated with the point air injection technique exhibited an overall lower loss of conductivity than those treated with the standard pressure collar due to the restricted area of embolism formation (see below). The technique is difficult to use as a careful adjustment of the force with which the cone (Fig. 1) is attached to the twig is necessary. The sealing is insufficient when the force is too low, but a high force may cause cracks in the wood. However, it enabled several measurements to be made for the analysis of the cross-sectional pattern and time-course of embolism formation.
Cross-sectional pattern of embolism
The standard pressure collar induced embolism in most of the cross-sectional area except for small regions situated in the opposite wood and along the year ring borders (Fig. 2). The use of the point air injection method caused embolized areas restricted to radial segments at the side of pressure application. Borders to fully conductive areas in the rest of the cross-section often were very sharp (Fig. 2). Control samples not treated with the pressure collars showed nearly no embolism. Sometimes small dysfunctional areas were observed in the centre of the samples and in small regions within the compression wood (Fig. 2), which may explain the small uncoloured regions in the compression wood of the sample treated with the point air injection method.
|
Axial pattern of embolism
The axial pattern of induced embolism was closely related to twig morphology. Sections at the air entry points always showed the highest embolism rates (up to 80.6% with the standard pressure collar), while in adjacent sections a slight decrease (–10 to –25%) in loss of conductivity was observed. By contrast, adjacent to proximal and distal nodes an impressive drop to very low or even zero values of embolism occurred in all the twigs studied. Figure 3 shows the typical axial distribution of embolism in three twigs treated with the standard pressure collar. The point air injection revealed an identical pattern (data not shown).
|
This pattern could also be demonstrated using the ultrasonic technique (Fig. 4). Only a sensor mounted near the pressure collar and within the next nodes registered ultrasonic events. The maximum acoustic activity with up to 238 events min–1 was observed within the first minute after reaching 4.5 MPa in the pressure collar. Sensors attached proximal or distal to the nearest nodes showed nearly no acoustic activity.
|
Axial pattern of air release
Air release from the twig surface started a few minutes after a pressure of 4.5 MPa in the standard pressure collar was reached. After 5–10 min, the amount of air released from the twig was constant, whereby air bubbles appeared at dozens of points distributed within the internode to which the pressure collar was attached. The number of air outlet points and the amount of released air (Fig. 3) were highest near the collar and decreased towards the nodes. A lot of air was always released directly at the chamber openings because of incomplete sealing. Air release was hardly visible proximal and distal to the nodes adjacent to the internode at which the pressure collar was attached. There was no extraordinary air release at the nodes.
Time-course of embolism formation
Ultrasonic (Fig. 4) as well as conductivity measurements (Fig. 5) indicate that most cavitation events occur within a few minutes after reaching 4.5 MPa. The standard collar led to 80% loss of conductivity after 10 min; significantly higher embolism rates were observed only in a few samples, even after >30 min. The point air induction method caused an increase of conductivity losses during a longer period and over all lower embolism rates with higher variation. The latter is probably due to differences in air entry at the borehole. Small variations in the depth of the holes and random connections to, for example, cracks in the wood may influence the cavitation efficiency.
|
Influence of the number of boreholes and borehole depth
Embolism rates induced by the standard pressure collar were significantly higher when boreholes were set compared with samples without such air entry points. However, when the number of boreholes was varied between two and 10, no significant influence on embolism rates was observed (Fig. 6). For unknown reasons, loss of conductivity in this measurement series was slightly lower than in others (cf. Fig. 5).
|
The depth of the borehole and loss of conductivity correlated significantly, whereby completely pierced twigs showed >2-fold higher embolism rates than twigs without boreholes (Fig. 7).
|
|
Discussion |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Pressure collar experiments of several previous studies and the present study prove that the formation of drought-induced embolism is based on air seeding processes (Sperry and Tyree, 1990; Cochard et al., 1992b; Salleo et al., 1992; Lo Gullo et al., 1997). Drought as well as the pressure collar causes pressure gradients at air–water interfaces and embolism when vulnerability thresholds are exceeded. Therefore, the pressure collar technique can be used to study experimentally air seeding processes which normally occur only under drought conditions. However, at the twig level, an important difference has to be taken into consideration: while potential gradients built up by the pressure collar are restricted to a small twig section, they are formed throughout the xylem upon dehydration. In consequence, cracks in the wood can lead to a release of air in pressure collar experiments but form additional air entry points in dehydrating twigs. This aspect is relevant for use of the pressure collar technique in vulnerability analysis or embolism induction as well as for the interpretation of spatial and time patterns observed in the present study.
The newly developed point injection method (Fig. 1) demonstrates that the contact area between air and the xylem's water phase is critical for the cross-sectional pattern of embolism. A treatment with the standard collar led to embolism patterns similar to that demonstrated in earlier studies (Sperry and Tyree, 1990; Fig. 2). Small stained areas at some year ring borders indicate that the first earlywood cell rows are less vulnerable than the surrounding xylem. In contrast to the standard pressure collar, the point air injection caused an embolized area restricted to often sharply bordered circular sectors (Fig. 2). As most pits are situated in the radial cell walls, a spreading of embolism within the outer year rings (where the air entry point was set via an up to 2 mm deep borehole) would be expected. It is therefore suggested that radial air spaces present in the wood body enable the propagation of embolism from the air entry point towards the centre on the one hand. On the other hand, air spaces at a distance from the air entry point could be responsible for the sharp borders of embolized areas: a release of pressurized air would lead to a sudden pressure drop and limit the progression of air seeding. These air spaces may be cracks in the wood, possibly along parenchyma rays, but resin ducts may also play a role.
Treatment with the point injection technique also led to lower conductivity losses than with the standard pressure collar (Figs 2, 5) due to the restricted possibility for air to enter the wood body. Accordingly, the size of air entry points in the standard pressure collar (varied via the depth of boreholes) correlated to the amount of embolism (Fig. 7). However, embolism rates could not be increased further by additional boreholes in the standard pressure collar (Fig. 6). This can be explained by the cross-sectional pattern of Fig. 2: when the small air entry point of the point injection method is sufficient to embolize a 90° section of the xylem disc, two boreholes completely pierced through the twig will already enable embolism propagation to all regions of the xylem.
It is concluded that the preparation of sufficient air entry points is a prerequisite for the use of the pressure collar technique. Also Sperry and Saliendra (1994) found in pressure collar experiments with Betula occidentalis that air entry points prepared via overlapping notches at the sample's surface substantially improved the efficiency of the embolization process. The small holes bored in the present experiments (1 mm in diameter) may be another efficient technique to set such entry points without causing much damage to the xylem tissue. In each case, it is recommended that the optimal method should be tested with respect to the species studied and experimental targets.
In the axial direction, the propagation of embolism was found to be strongly influenced by twig architecture: only a moderate decrease of embolism was observed from the air entry point towards the closest nodes (standard pressure collar; Fig. 3), while twig sections outside the nearest distal and proximal nodes were hardly or not embolized. These conductivity measurements corresponded to acoustic analysis (Fig. 4), which showed ultrasonic events near the pressure collar but not at sections separated from the collar by a node. There are two possible reasons for this pattern: first, at nodes, the xylem is less homogenous due to the required reorganization of conduit strands. This may be related to a higher frequency of air-filled cracks, which release applied pressure and avoid further spreading of embolism. Secondly, the reorganization of the xylem may lead to changes in tracheid anatomy and, consequently, in hydraulic safety. A hydraulic architecture (Zimmermann, 1978; Tyree and Ewers, 1991) with higher cavitation resistance at the nodes could stop the embolism from reaching adjacent internodes. The first cause seems unlikely as the analysis of air release by immersion of twigs in water (Fig. 3) revealed no extraordinary escape of air at the nodes. Therefore, embolism was not restricted to internode regions by a sudden pressure drop, but probably by changes in vulnerability. While there are no studies on the vulnerability of conifer nodes available, Salleo and Lo Gullo (1986) demonstrated an even lower vulnerability of nodes compared with internodes for Chorisia insignis. It should also be mentioned that Lo Gullo et al. (1997) observed ultrasonic events in Salix viminalis twigs inside but not outside a pressure collar unless a water flow through the xylem was enabled. This indicates that the pattern of embolism propagation is species specific, which makes a comparison of different species and experimental designs difficult.
Ultrasonic (Fig. 4) and conductivity measurements (Fig. 5) showed that the induction of embolism by the pressure collar is also time-dependent. About 10 min were required to reach 80% loss of conductivity, whereby most acoustic events occurred within the first minute of pressure application. The high acoustic activity at the beginning may be due to embolism of tracheids in the vulnerable compression wood (Mayr and Cochard, 2003) which do not contribute much to the overall hydraulic conductivity. This may explain the discrepancy in the time-course of the ultrasonic and hydraulic measurements. Other authors exposed their conifer samples for 10 (Sperry and Ikeda, 1997; Linton et al., 1998; Stout and Sala, 2003) or 20 min (Sperry and Tyree, 1990) to positive pressures via the pressure collar. Sperry and Ikeda (1997) suggested that they did not reach 100% loss of conductivity because of an insufficient exposure time. In the present experiments with the standard collar, maximum conductivity losses at 15–20 min exposure were close to the expected embolism rates of 87.5% (according to vulnerability curves in Mayr et al., 2002). In contrast, the point air injection method led to lower conductivity losses and to a smaller slope of the embolism versus time curve (Fig. 5). It is unclear if longer pressure exposure would result in embolism rates comparable with those obtained with the standard collar. Experiments lasting longer were not possible because the incomplete sealing required a permanent adjustment of the pressure by hand. However, this experiment demonstrates that a restricted area of air–water interfaces causes a slowing down of the cavitation process.
Kikuta et al. (2003) also observed a time-course of embolism formation in small xylem sections of Juniperus virginiana and registered ultrasonic emission for several hours. In contrast, the present experiments demonstrate a saturation of the embolization process within 10–20 min, and therefore validate the exposure times used in previous studies (Sperry and Tyree, 1990; Sperry and Ikeda, 1997; Linton et al., 1998; Stout and Sala, 2003). Embolism formation in twigs seems to be a relatively rapid process leading to a fast propagation of dysfunctional areas within the xylem.
Considering not only vulnerability thresholds but also the crucial role of air–water interfaces and the time-course of embolism formation, the pressure collar technique appears to be a very useful tool to study air seeding processes. The observed restriction of embolism propagation to internode sections is one example of findings enabled by this technique.
|
Acknowledgements |
|---|
This study was supported by APART (Austrian Programme for Advanced Research and Technologies), Fonds zur Förderung der wissenschaftlichen Forschung und des wissenschaftlichen Nachwuchses in Tirol, and FWF, ‘Fonds zur Förderung der Wissenschaftlichen Forschung’. We thank Mag. Ing. Birgit Daemon for excellent assistance, and the anonymous referees for thoughtful comments and the idea to study the air release of twigs.
|
References |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Alder NN, Sperry JS, Pockman WT. (1996) Root and stem xylem embolism, stomatal conductance, and leaf turgor in Acer grandidentatum populations along a soil moisture gradient. Oecologia 105:293–301.[CrossRef]
Boehm H. (1893) Capillarität und Saftsteigen. Berichte der Deutschen Botanischen Gesellschaft 11:203–212.
Chiu S and Ewers FW. (1993) The effect of segment length on conductance measurements in Lonicera fragrantissima. Journal of Experimental Botany 44:175–181.
Cochard H, Breda N, Granier A, Aussenac G. (1992a) Vulnerability to air embolism of three European oak species (Quercus petraea (Matt) Liebl,Q. pubescens Willd, Q. robur L.). Annals of Forest Science 49:225–233.
Cochard H, Cruiziat P, Tyree MT. (1992b) Use of positive pressure to establish vulnerability curves. Plant Physiology 100:205–209.
Crombie DS, Milburn JA, Hipkins MF. (1985) Maximum sustainable xylem sap tensions in Rhododendron and other species. Planta 163:27–33.[CrossRef]
Dixon HH and Joly J. (1894) On the ascent of sap. Proceedings of the Royal Society of London 57:3–5.
Hacke UG and Sperry JS. (2001) Functional and ecological xylem anatomy. Perspectives in Plant Ecology, Evolution and Systematics 4:97–115.[CrossRef][ISI]
Jackson GE and Grace J. (1994) Cavitation and water transport in trees. Endeavour 18:50–54.[CrossRef]
Jarbeau JA, Ewers FW, Davis SD. (1995) The mechanism of water-stress-induced embolism in two species of chaparral shrubs. Plant, Cell and Environment 18:189–196.
Kikuta SB, Hietz P, Richter H. (2003) Vulnerability curves from conifer sapwood sections exposed over solutions with known water potentials. Journal of Experimental Botany 54:2149–2155.
Linton MJ, Sperry JS, Williams DG. (1998) Limits to water transport in Juniperus osteosperma and Pinus edulis: implications for drought tolerance and regulation of transpiration. Functional Ecology 12:906–911.[CrossRef]
Lo Gullo MA, Zhang S, Kikuta SB, Richter H. (1997) Xylem embolization by the pressure collar in Salix viminalis L: sites for embolization and ultrasound acoustic emission. Plant's Biosystems 131:23–32.
Mayr S and Cochard H. (2003) A new method for vulnerability analysis of small xylem areas reveals that compression wood of Norway spruce has lower hydraulic safety than opposite wood. Plant, Cell and Environment 26:1365–1371.[CrossRef]
Mayr S, Wolfschwenger M, Bauer H. (2002) Winter-drought induced embolism in Norway spruce (Picea abies) at the Alpine timberline. Physiologia Plantarum 115:74–80.[CrossRef][Medline]
Richter H. (1972) Wie entstehen Saugspannungsgradienten in Bäumen? Berichte der Deutschen Botanischen Gesellschaft 85:341–351.
Salleo S, Hinckley TM, Kikuta SB, Lo Gullo MA, Weilgony P, Yoon TM, Richter H. (1992) A method for introducing xylem embolism in situ: experiments with a field-grown tree. Plant, Cell and Environment 15:491–497.[CrossRef]
Salleo S and Lo Gullo MA. (1986) Xylem cavitation in nodes and internodes of whole Chorisia insignis H.B. et K. plants subjected to water stress: relations between xylem conduit size and cavitation. Annals of Botany 58:431–441.
Salleo S, Lo Gullo MA, Trifilo P, Nardini A. (2004) New evidence for a role of vessel-associated cells and phloem in the rapid xylem refilling of cavitated stems of Laurus nobilis L. Plant, Cell and Environment 27:1065–1076.[CrossRef]
Sperry JS, Donnelly JR, Tyree MT. (1988) A method for measuring hydraulic conductivity and embolism in xylem. Plant, Cell and Environment 11:35–40.[CrossRef]
Sperry JS and Ikeda T. (1997) Xylem cavitation in roots and stems of Douglas-fir and white fir. Tree Physiology 17:275–280.[ISI][Medline]
Sperry JS and Saliendra NZ. (1994) Intra- and inter-plant variation in xylem cavitation in Betula occidentalis. Plant, Cell and Environment 17:1233–1241.[CrossRef]
Sperry JS and Tyree MT. (1990) Water-stress-induced xylem embolism in three species of conifers. Plant, Cell and Environment 13:427–436.
Stout DL and Sala A. (2003) Xylem vulnerability to cavitation in Pseudotsuga menziesii and Pinus ponderosa from contrasting habitats. Tree Physiology 23:43–50.[ISI][Medline]
Tyree MT, Davis SD, Cochard H. (1994) Biophysical perspectives of xylem evolution: is there a tradeoff of hydraulic efficiency for vulnerability to dysfunction? IAWA Journal 15:335–360.
Tyree MT, Dixon MA, Thompson RG. (1984) Ultrasonic acoustic emissions from the sapwood of Thuja occidentalis measured inside a pressure bomb. Plant Physiology 74:1046–1049.
Tyree MT and Ewers FW. (1991) The hydraulic architecture of trees and other woody plants. New Phytologist 119:345–360.[CrossRef][ISI]
Tyree MT, Salleo S, Nardini A, LoGullo MA, Mosca R. (1999) Refilling of embolized vessels in young stems of laurel. Do we need a new paradigm? Plant Physiology 120:11–21.
Vogt UK. (2001) Hydraulic vulnerability, vessel refilling, and seasonal courses of stem water potential of Sorbus aucuparia L. and Sambucus nigra L. Journal of Experimental Botany 52:1527–1536.
Zimmermann MH. (1978) Hydraulic architecture of some diffuse-porous trees. Canadian Journal of Botany 56:2286–2295.
Zimmermann MH. (1983) Xylem structure and the ascent of sap Berlin Springer Verlag.
CiteULike 
Connotea 
Del.icio.us What's this?
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||