JXB Advance Access originally published online on June 4, 2004
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Journal of Experimental Botany, Vol. 55, No. 402, pp. 1569-1575, July 2004
Journal of Experimental Botany, Vol. 55, No. 402, © Society for Experimental Biology 2004; all rights reserved
RESEARCH PAPER |
Changes in pit membrane porosity due to deflection and stretching: the role of vestured pits
1Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts, MA 02138, USA
2Laboratory of Plant Systematics, K.U. Leuven, Institute of Botany and Microbiology, Kasteelpark Arenberg 31, B-3001 Leuven, Belgium
* To whom correspondence should be addressed. Fax: +1 617 496 5854. E-mail: bchoat{at}fas.harvard.edu
Received 10 November 2003; Accepted 7 April 2004
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Abstract |
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The effect of increasing pressure difference (
P) on intervessel pit membrane porosity was studied in two angiosperm tree species with differing pit architecture. Fraxinus americana L. possesses typical angiosperm bordered pit structure while Sophora japonica L. exhibits well-developed vestures in intervessel pit chambers. It was hypothesized (a) that large P across intervessel pits would cause the deflection of pit membranes in the stems of F. americana resulting in significant increases in porosity and thus lower cavitation thresholds, and (b) that the presence of vestures would prevent the deflection of pit membranes in S. japonica. To determine if the porosity of pit membranes increased under mechanical stress, suspensions of colloidal gold, 5 nm and 20 nm in diameter, were perfused across intervessel pit membranes at P ranging from 0.25 MPa to 6.0 MPa. The effect of increasing P on membrane porosity was also tested by comparing air seeding thresholds (Pa) in stems perfused with water or a solution with lower surface tension. Air seeding and colloidal gold experiments indicated that pit membrane porosity increased significantly with P in F. americana. In S. japonica, increases in permeability to colloidal gold with P were small and maximum pore diameters predicted from Pa were independent of P, suggesting that vestures limited the degree to which the membrane can be deflected from the centre of the pit cavity. This provides the first experimental evidence that vestures reduce the probability of air seeding through pit membranes. Key words: Air seeding, cavitation, deflection, pit membranes, porosity, vestures, xylem
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Intervessel pit membranes are modified primary cell walls consisting of tightly interwoven cellulose microfibrils in a matrix of hydrated hemicellulose and pectins (Brett and Waldron, 1996
). The finely porous membranes are designed to allow the flow of water between adjacent vessels while preventing the passage of gas bubbles and pathogens. Vulnerability to water-stress-induced embolism has been related to the porosity of pit membranes by a process known as air seeding (Sperry and Tyree, 1988). When a xylem vessel containing an embolism lies adjacent to a functional vessel containing liquid under tension, a substantial pressure difference can develop across the pit membranes which connect the vessels. At a critical pressure difference that scales inversely with the size of the largest pore, gas will penetrate the pit membrane and the embolism will expand into the previously water-filled vessel (Tyree and Zimmermann, 2002).
A major challenge to understanding water-stress-induced embolism is the discrepancy between empirical measurements of pit membrane pore sizes and those calculated from measurements of air seeding pressure differences (Choat et al., 2003). Electron micrographs of pit membranes often do not reveal pores in the expected size range (Schmid and Machado, 1968; Wheeler, 1983; Sano and Fukazawa, 1994; Choat et al., 2003). While some studies using polystyrene microspheres have shown good correlation between membrane porosity and vulnerability to embolism (Jarbeau et al., 1995), recent experiments with colloidal gold have indicated that pit membrane pores in angiosperm species were smaller than expected based on air seeding thresholds (Shane et al., 2000; Choat et al., 2003). Both particle perfusion experiments and electron micrographs measure membrane pore size in a relaxed state. The possibility that deflection of intervessel pit membranes results in temporarily increased porosity has been suggested to explain the difference in pore diameters calculated from vulnerability curves and those observed using scanning electron microscopy (Hacke and Sperry, 2001; Choat et al., 2003).
The degree of stretching that a pit membrane undergoes will depend upon both the dimensions and mechanical properties of the pit membrane itself as well as the geometry of the pit chamber (Tyree and Zimmermann, 2002; Sperry and Hacke, 2004). Angiosperm vessels possess bordered pits in which the secondary walls overarch the pit membrane (Dickison, 2000). Thus, the shape and dimensions of the pit chamber and the outer pit aperture provide an absolute limit to the extent to which pit membranes can deform under pressure. Some woody angiosperm species possess outgrowths from the secondary cell wall of bordered pits known as vestures (Jansen et al., 1998b), which, when located within the pit cavity, will limit the degree to which pit membranes can be displaced. The distribution of species with vestured pits is skewed toward environments in which high transpiration rates or high xylem tensions are expected, i.e. deserts and tropical, seasonal woodlands (Jansen et al., 2003; S Jansen, unpublished data), leading to the suggestion that vestures might decrease the chances of pit membrane aspiration or rupture by supporting the membrane against large pressure drops (Zweypfenning, 1978; Sperry, 2003). It has also been suggested that vestures may aid in the dissolution of emboli and in the restoration of vessels to a functional state (Carlquist, 1982, 2001; Jansen et al., 2003).
In this study it was investigated how pressure influences the porosity of pit membranes in two angiosperm tree species with differing pit geometry. White ash (Fraxinus americana L.) has the typical bordered pit structure of angiosperm trees, but possesses minutely developed vestures on some intervessel pits, mainly in the narrow latewood vessels (Wheeler, 1981; Baas et al., 1988). The pagoda tree (Sophora japonica L.), has bordered pits that are always distinctly vestured (Ohtani et al., 1984). It was hypothesized that (i) the porosity of pit membranes could be altered by experimentally imposing a range of pressure differences (P) across membranes separating two xylem vessels, and (ii) the extent to which porosity would increase with P would be related to the geometry of the pit chamber and the presence of vestures.
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Materials and methods |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Changes in pit membrane porosity
Branches were collected from F. americana and S. japonica during the growing season of 2003 from mature trees growing at the Arnold Arboretum or on the main campus of Harvard University. The porosity of pit membranes between two adjacent vessels was measured using the microcapillary technique described in Zwieniecki et al. (2001)
. An outline of the experimental procedure used is shown in Fig. 1. Two-year-old stem segments 3–8 cm in length were cut from lateral branches, trimmed with a razor blade at each end, and flushed with filtered (0.22 µm) deionized water. Three or four replicate stem segments were tested for each species. Glass microcapillaries were pulled on a pipette puller (Pul1, World Precision Instruments, Sarasota, FL) and their tips were subsequently broken such that the opening of the capillary was in the same range as vessel diameters of the species used (50–150 µm). The capillary tip was inserted into a vessel lumen in the most recent year's growth using a x50 stereo microscope (SZ-STB2, Olympus, Tokyo) and glued in place using cyanoacrylic glue (Loctite superbond, 409). Air was then pushed through the vessel at low pressure (
0.1 MPa) to determine if the vessel was continuous through the segment. Segments with blocked vessels or ones in which the vessel ended within the segment were discarded. The vessel was stained with 0.01% safranin for identification at the distal end of the segment and then trimmed back with a razor blade at the distal end until a direct connection was observed between the stained vessel and a second vessel. The lumen of the original (stained) vessel was then carefully blocked with glue at the distal end of the segment and a capillary was inserted into the adjacent vessel. This procedure ensured that the perfusing solution only passed through one bordered pit field. The stem segment was then connected to a pressure source by attachment of a compression fitting to the proximal microcapillary and the two vessels were flushed with filtered, deionized water at 2.0 MPa to remove excess stain or residual gas pockets.
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The porosity of intervessel pit membranes was quantified by perfusing the samples with suspensions of colloidal gold containing either 5 nm or 20 nm particles (100 µl l–1 as HAuCl4; Sigma Aldrich, St Louis). Samples were first perfused at a pressure of 2.0 MPa. The procedure was then repeated at 4.0 MPa and 6.0 MPa. After this, the samples were perfused at lower pressures of 1.0, 0.5, and 0.25 MPa. Between each perfusion the distal microcapillary was flushed with deionized water. Droplets of exudate (2.5 µl volume) collected at each delivery pressure were dried at ambient temperature on carbon discs. Samples of undiluted suspension were also dried onto carbon discs. Each sample was tested for the presence of gold using energy dispersive X-ray analysis (EDX) in a scanning electron microscope (FEI Quanta 200, Hillsboro, Oregon). Observations were performed through a soft X-ray window at 30 kV and x10 000 magnification. Three measurements were made for each sample droplet.
After exudate samples had been collected at each delivery pressure, the segments were removed from the injection apparatus and the second vessel was stained with toluidine blue (0.01%) from the distal (downstream) end. The stem segment was then sectioned longitudinally to check that there was a direct connection between the two vessels. Preliminary experiments to test whether pit membranes ruptured when exposed to high pressures were conducted using a sequential increase and decrease of perfusion pressures (0.25, 0.5, 1.0, 2.0, 4.0, 6.0, and 0.25 MPa). In no instance was there an increase in the amount of gold in the exudate following the second low-pressure (0.25 MPa) perfusion, indicating that 6.0 MPa did not result in irreversible changes in membrane permeability.
Air seeding threshold
The air seeding threshold (Pa) for intervessel pit membranes was measured in individual vessels for each species (Melcher et al., 2003). To investigate how pit membrane deflection and stretching may affect membrane porosity, liquids of different surface tension (
) were used to alter the Pa of each species. The two liquids used were deionized water (=0.072 N m–1) and 0.1% (w/v) Triton X (=0.031 N m–1). Branches were collected from the same trees used in the gold perfusion experiments and seven to nine replicate stem segments were tested for each treatment. In the laboratory, short segments (length 4–8 cm) were cut from the branches, shaved at each end with a razor blade, and flushed with either deionized water or Triton X. Microcapillaries were glued into two connected vessels as described above. The proximal capillary was filled with either water or Tritonxand connected to the pressure source by a compression fitting. Nitrogen gas was delivered at a pressure of 0.1–0.5 MPa to the proximal capillary. After all of the liquid from the proximal capillary had moved into the distal capillary the system was left for 60 s at a pressure of 0.5 MPa. If no bubbles appeared in the distal capillary, it was assumed that an intact pit field existed between the capillaries. The pressure was then increased in 0.05 MPa steps at 30 s intervals until gas appeared in the distal capillary. This was taken as the threshold pressure for gas penetration of the intervessel pit membranes between the two vessels. Maximum pit membrane pore diameters were calculated from air seeding thresholds for each species using
 | (1) |
P is the pressure difference across the membrane, is the surface tension of the fluid, 
is the contact angle between the air water interface and the pit membrane (assumed to be 0), and D is the diameter of the pore.
Anatomy
Longitudinal and transverse sections were cut with a sliding microtome and observed using scanning electron (SEM) and light microscopy (LM) to determine the geometry of pits for each of the species (Jansen et al., 1998a). Measurements of pit membrane radius (r) and depth of pit chamber (d) were made on LM and SEM images using Carnoy 2.0 software (Schols et al., 2002). The depth of the pit chamber was defined as the distance from the pit membrane to the outer aperture of the pit chamber.
The maximum expansion (stretching) of pit membranes was estimated assuming that the membrane deflection would be limited by the depth (d) of the pit chamber in each species (Fig. 2). It was assumed that the membrane expands to form a segment of a sphere. The increase in surface area (Amax) was calculated as the expansion of a flat membrane of radius r to a segment of a sphere from:
 | (2) |
). Although the inflation of uniform circular diaphragms composed of isotropic materials does not strictly expand into a segment of a sphere (Adkins and Rivlin, 1952), the effect on Amax is small.
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Results |
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Gold penetration of pit membranes
The amount of gold penetrating between vessels increased with pressure for both 5 nm and 20 nm colloidal particles in both species, however, the increase was much greater in F. americana than in S. japonica (Fig. 3). The small increase in gold penetration observed for S. japonica was not significantly different (P>0.05; Tukey HSD, two-way ANOVA; n=3–4) with 5 nm or 20 nm gold. The amount of 5 nm gold was greater in samples from F. americana than in S. japonica at delivery pressures above 0.5 MPa; particles of this diameter penetrated pit membranes of F. americana to some degree even at the lowest delivery pressures (0.25 MPa). In both species, very little 20 nm gold penetrated below a 2.0 MPa delivery pressure. At 2.0 MPa, there was a significant increase in the amount of 20 nm particles penetrating membranes of F. americana. Measurements of suspensions supplied to the test segments demonstrated that some proportion of colloidal particles was filtered by pit membranes even at high delivery pressures.
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Air seeding pressures
Air seeding thresholds (Pa) obtained using deionized water were higher for S. japonica (2.62±0.18 MPa) than for F. americana (1.92±0.10 MPa), however, Pa was similar for stems perfused with Triton X (Table 1). The mean (±SE) pit membrane pore diameter calculated for F. americana stems perfused with deionized water (152±8 nm; n=7) was significantly wider (P<0.05; t-test) than the mean pore diameter calculated for stems perfused with Triton X (117±13 nm; n=9). By contrast, for S. japonica mean pore diameter was not significantly different (P=0.93; t-test) between deionized water (114±8 nm; n=8) and Triton X (115±10 nm; n=7) treatments. Thus, while pore size increased at higher
P for F. americana, there was no change in estimated pore size for S. japonica between 1.13 MPa and 2.62 MPa.
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Anatomy
F. americana had smaller pits, with a mean membrane radius of 1.95 µm compared with 2.71 µm for S. japonica (Table 2). F. americana also had a smaller pit chamber depth (0.61 µm) than S. japonica (0.84 µm). The vestures in S. japonica vary from small and unbranched to largely branched and widely expanding (Fig. 4). Minutely vestured pits occur in F. americana, especially in the narrow latewood vessels, while intervessel pits of the wide, earlywood vessels have non-vestured pits.
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The calculated maximum pit membrane stretch differed between the species based on the ratio of the depth of the pit chamber to the radius of the pit membrane (d:r). Despite the difference in pit size, the d:r ratio was similar for the two species (0.31) if vestures were not considered (Table 2). However, the presence of vestures results in the effective depth of the pit chamber being very small (
0.2 µm), allowing for little deflection to occur. Thus the maximum increase in surface area as a proportion of the initial pit membrane surface area (Amax) is expected to be larger in F. americana (8.9%) than in S. japonica (0.5%). In addition, it is possible that a greater increase in surface area may occur if the pit membrane stretches through the aperture of the pit chamber in F. americana. It is assumed that vestures would prevent this occurring is S. japonica. |
Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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The principal aim of this study was to determine whether the deformation of intervessel pit membranes plays a significant role in determining the vulnerability of a species to water-stress-induced cavitation. If this is the case then it could (i) explain the difficultly in observing pores in the size range predicted from vulnerability curves and (ii) provide support for the hypothesis that vestures reduce the vulnerability of a species to cavitation by preventing deflection of the membrane.
Data from experiments with colloidal gold indicated that increases in pit membrane porosity with P were greater for F. americana than for S. japonica. This is consistent with the occurrence of stretching in membranes of F. americana and the hypothesis that vestures may limit stretching and deflection of the pit membrane in S. japonica. However, the influence of this increase in porosity on air seeding is complicated by the fact that pore sizes calculated for air seeding for both species were 5–10 times greater than the size of colloidal gold particles used to estimate porosity. Experiments using surfactant to alter the pressure difference at which Pa occurred provided no evidence of an increase in pore diameter caused by stretching in S. japonica; estimated pore diameter for F. americana increased significantly between P of 1.17 MPa and 1.93 MPa. It is proposed that the increase in porosity with P observed in F. americana was a result of deflection and stretching of the pit membranes.
There was some disparity between data collected from gas penetration and gold perfusion experiments. For instance, penetration of 5 nm gold particles through the pit membranes of S. japonica increased with P (Fig. 3), but this increase was not apparent in air seeding experiments. This disparity is likely to relate to the different ways in which these methods estimate membrane pore size. Because air seeding will always occur first at the largest pore, the values obtained from gas penetration experiments represent the diameters of the largest wetted pores in the membranes (Tyree and Zimmermann, 2002). Assuming that there is a normal distribution of pore diameters within a population of pit membranes that connects two vessels, it is only the very tail of this distribution that would be responsible for air seeding events. Membrane porosity measured with colloidal gold should be more sensitive to the mean pore size, as the amount of gold allowed through the membrane by a small number of large pores is likely to be below the limits of detection by EDX.
From the few studies that have examined the structure of angiosperm intervessel pit membranes in detail, it appears that the membranes consist of a number of distinct layers of microfibrils on either side of the middle lamella (Schmid, 1965; Schmid and Machado, 1968). The layers of microfibrils have different orientations, with layers formed prior to cell expansion having a primarily parallel orientation, while those formed after cell expansion exhibit a random orientation. Based on this arrangement of cell wall components, it is apparent that most pathways through the membrane would be complex and tortuous rather than straight channels. Electron micrographs also suggest that the majority of pit membranes pores have an effective diameter of 5–20 nm, close to that of primary cell walls from living cells (Wheeler, 1981, 1983; Choat et al., 2003). While the experimental data presented here support the interpretation that there is a temporary increase in the porosity of pit membranes with increasing P, they do not indicate that a small (5–20 nm) pore would expand to a 100–150 nm pore across the range of pressures at which air seeding occurred. It is likely that the large pores responsible for air seeding would be visible, even in a relaxed state, at the resolutions obtainable with an SEM, i.e. 50–100 nm in diameter. Therefore, the most likely explanation for the difficulty in direct observation of large pores is that they are rare enough to avoid detection and occur in only a few of the thousands of pit membranes which connect two vessels.
An increase in porosity was not observed in the pit membranes of S. japonica by either experimental method used. Thus, the data presented here provide the first experimental evidence that vestures reduce the vulnerability of plants to water-stress-induced cavitation, a function long postulated by wood anatomists concerned with ecological aspects of xylem anatomy (Zweypfenning, 1978; Carlquist, 1982; Jansen et al., 2003). However, confirmation of this hypothesis will require further experimentation involving a greater sample size of species with vestured and non-vestured pits. It is also clear that other factors, relating to the size and frequency of larger pores, are equally if not more important than the potential for deflection and stretching of pit membranes in determining the underlying vulnerability to cavitation of a species. This is highlighted by the fact that the presence of vestures is not an essential trait for drought tolerance, and many species existing in arid regions lack vestures but maintain high cavitation thresholds (Jansen et al., 1998b). Finally, it is presumed that some cost will accompany the benefits bestowed by vestures, most likely in the form of increased resistance to flow through the bordered pit chamber. Further study is required to determine the constraints that such structures may place on water transport.
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Acknowledgements |
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We thank Richard Schalek for assistance with electron microscopy and EDX analysis. This research was supported by grants from the Andrew W Mellon Foundation, the USDA (NRICGP 2001-35100-10615), and the National Science Foundation (IBN 0078155). Steven Jansen is a postdoctoral fellow of the Fund for Scientific Research, Flanders (Belgium) (FWO, Vlaanderen) and his visit to Harvard University was supported by a grant from the FWO, Vlaanderen.
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