JXB Advance Access originally published online on December 6, 2004
Journal of Experimental Botany 2005 56(412):737-744; doi:10.1093/jxb/eri045
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RESEARCH PAPER |
The dependence of leaf hydraulic conductance on irradiance during HPFM measurements: any role for stomatal response?
1USDA Forest Service, Northeastern Experiment Station, 705 Spear St., Burlington, VT 05403, USA
2Dipartimento di Biologia, Università di Trieste, Via L Giorgieri 10, 34127 Trieste, Italia
3Department of Botany, University of Hawaii, 3190 Maile Way, Honolulu, HI 96822, USA
4Departamento de Biologia Vegetal, Universidad de Barcelona, 645 Avda. Diagonal, 08028 Barcelona, Spain
* To whom correspondence should be addressed. Fax: +39 040 568855. E-mail: nardini{at}univ.trieste.it
Received 20 February 2004; Accepted 5 October 2004
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Abstract |
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 Top Abstract Introduction and theoryMaterials and methodsResultsDiscussionReferences |
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This paper examines the dependence of whole leaf hydraulic conductance to liquid water (KL) on irradiance when measured with a high pressure flowmeter (HPFM). During HPFM measurements, water is perfused into leaves faster than it evaporates hence water infiltrates leaf air spaces and must pass through stomates in the liquid state. Since stomates open and close under high versus low irradiance, respectively, the possibility exists that KL might change with irradiance if stomates close tightly enough to restrict water movement. However, the dependence of KL on irradiance could be due to a direct effect of irradiance on the hydraulic properties of other tissues in the leaf. In the present study, KL increased with irradiance for 6 of the 11 species tested. Whole leaf conductance to water vapour, gL, was used as a proxy for stomatal aperture and the time-course of changes in KL and gL was studied during the transition from low to high irradiance and from high to low irradiance. Experiments showed that in some species KL changes were not paralleled by gL changes. Measurements were also done after perfusion of leaves with ABA which inhibited the gL response to irradiance. These leaves showed the same KL response to irradiance as control leaves. These experimental results and theoretical calculations suggest that the irradiance dependence of KL is more consistent with an effect on extravascular (and/or vascular) tissues rather than stomatal aperture. Irradiance-mediated stimulation of aquaporins or hydrogel effects in leaf tracheids may be involved.
Key words: Hydraulic conductance, HPFM, irradiance, leaf conductance, stomates
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Introduction and theory |
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TopAbstractIntroduction and theoryMaterials and methodsResultsDiscussionReferences |
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The high pressure flow meter (HPFM) was first used to measure the hydraulic conductance of whole shoots and its components, i.e. stems, petioles, and leaf blades in Quercus, Acer, and Populus species (Tyree et al., 1993
, 1994; Yang and Tyree, 1994). The hydraulic conductance of leaves, KL, is defined as the water flow rate per unit leaf area divided by the pressure drop driving the flow. The HPFM measures the pressure and the flow rate for the computation of KL. During HPFM measurements water is forced into leaves faster than it evaporates from leaf air spaces, hence leaf air spaces infiltrate with water, which can be seen emerging from stomatal pores (MT Tyree, personal observation; Wei et al., 1999). Hence the HPFM measures the combined hydraulic conductance of the leaf vascular system, extravascular tissues and stomates in an approximately serial pathway.
Leaf hydraulic conductance (KL, kg s–1 m–2 MPa–1) was found to vary from 5x10–3 to 2x10–5 depending on species (Tyree et al., 1999; Nardini, 2001; references above). Tyree et al. (1993) commented on the very low KL values of Acer and Quercus and argued that KL might actually be slightly overestimated by the HPFM (Yang and Tyree, 1994; Tyree et al., 1999) because water flow under positive pressure might follow a higher-conductance, shorter pathway than during evaporation. Yang and Tyree (1994) acknowledged that KL might be underestimated by the HPFM if the conductance of liquid water flow through stomates is sufficiently low, but they discounted the option without providing quantitative justification (see theory below). Assuming KL values for Acer and Quercus are correct, they concluded that water potential gradients in low-KL leaves might be quite large during midday transpiration on sunny days, for example, from 0.5 to 1.5 MPa from base of petiole to the evaporative surfaces.
More recently, Sack et al. (2002) have demonstrated that KL values measured by the HPFM are sensitive to irradiance, i.e. values for Quercus leaves are 1–3x10–4 in high irradiance (>1200 µmol s–1 m–2) versus 2–8x10–5 in ambient room irradiance (<10 µmol s–1 m–2). This observation has been confirmed in some but not in all species in this paper. The results of Sack et al. (2002) make it clear that it is advisable to measure KL in high irradiance if values representative of those in sunlight are desired. Since irradiance has a dramatic effect on stomatal aperture, Sack et al. (2002) suggested that the low KL values measured in low irradiance might be due to stomatal closure. Nevertheless, KL values measured by the HPFM agree with those measured by other hydraulic methods especially when measurements are all done in high irradiance (Tyree et al., 1994; Yang and Tyree, 1994; Tsuda and Tyree, 2000; Sack et al., 2002).
The observed ‘irradiance-effect’ could be explained by stomatal closure if the hydraulic conductance through stomates (KL,s) is about the same as or less than the conductance of vascular and nonvascular tissues (KL,vt). If these conductances can be approximated as conductances in series then
 | (1) |
It could be argued that both KL,s and KL,vt might decrease with decreasing irradiance. If all values of KL,s are >KL,vt at all irradiance levels, then 
and the irradiance dependence of KL would have to be ascribed to that of KL,vt. In this paper, the theoretical and experimental evidence that the irradiance dependence of KL is due either to the irradiance dependence of KL,s or KL,vt is examined.
Theoretical consideration
The purpose of this section is to quantify the theoretical effect of stomatal aperture on conductance of stomates to liquid-water (KL,s) and water-vapour (gs). The following questions will be answered: (i) How tightly do stomates have to close before 
so it could be expected that stomates will dominate KL measurements with an HPFM? (ii) What will the gs values be when 
and can this be confirmed by measurementss of whole leaf conductance to water vapour? (iii) Can stomatal width be confirmed when with a light microscope? To begin with, a simple geometry for stomatal pores will be assumed.
Stomatal pores are closely approximated by an elongated ellipse with a fixed width of the major axis and variable width of the minor axis (Parlange and Waggoner, 1970; Willmer and Fricker, 1996). Quercus rubra leaves have about 150 million stomates per m2 (=N) and stomatal pores with a major axis of about 10.7 µm (=a). If the pores of 15 µm length (=L) are approximated by uniform bores with ‘parallel’ walls, then both hydraulic conductance and water-vapour conductance of stomates can be computed from this simple geometry.
The equation for laminar flow of liquid water through N pipes m–2 with an elliptical cross-section is:
 | (2) |
is the viscosity of water (0.001 Pa s at 20 °C), and 109 is the conversion factor between KL,s in m3 s–1 Pa–1 m–2 and kg s–1 MPa–1 m–2 (Tyree and Zimmermann, 2002).
For the stomatal conductance to water vapour, from Fick's Law and the fact that pores are conductances in series that are additive, it is found that:
 | (3) |
). Equations (2) and (3) are plotted in Fig. 1A and B, respectively. Figure 1A clearly shows that KL,s increases with the pore width (b) to nearly the third power (slope=2.97), and that for most pore widths the value of KL,s is orders of magnitude more than KL of Quercus. From Fig. 1A it can be concluded that KL from equation (1) is due to vessel and tissue properties (KL,vt) for most stomatal apertures. The dashed line in Fig. 1A represents the theoretical value of KL versus pore width assuming KL,vt is constant at 2.5x10–4 kg s–1 MPa–1 m–2 (see below). KL,s has no significant impact on KL until pore width falls below 0.08 µm and does not equal the low-irradiance values observed until width falls to <0.02 µm. Since the resolution of light microscopy is limited to a measurement discrimination of about 0.4 µm, a microscope cannot be used for visual confirmation of the hypothesis that the irradiance effect on KL is due solely to the stomatal closure.
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Could confirmation of the hypothesis be obtained from measurements of whole leaf conductance to water vapour as a proxy for stomatal aperture? In Fig. 1B it can be seen that gs varies linearly with pore width that might be concluded from equation (3) with a as a constant. However, the whole leaf conductance to water vapour equals the sum of the cuticular conductance, gc, and the stomatal conductance, gs, in parallel. Since a probable value of gc=2–8 mmol s–1 m–2 in tree leaves (Nobel, 1991
; Sack et al., 2003), the whole leaf conductance will approach a constant value (dashed or solid line in Fig. 1B) about when or a little before pore width begins to limit KL. Given the measurement uncertainty of whole leaf conductance to water vapour, gL=gc+gs, a pore width of less than about 0.02–0.1 µm from gL measurements depending on gc cannot be inferred. Would these conclusions change if a more realistic pore profile was used? In reality the width profile of stomatal pores are uneven, i.e. sometimes narrower near the middle or at the extreme end depending on species. In a more realistic pore shape, the minimum width that would limit KL would be even smaller, hence visual observations with the aid of a microscope would be harder. Confirmations by measurement of gL would still be limited by gc in many species.
Even if gL or pore width could be measured with fairly high resolution, it still could not be proved that KL,s limits KL if allowance is made for patchy stomatal closure. For example, assume that just 0.1% of the stomates remain open in low irradiance and retain a width of 1 µm while the rest have closed to 
0.02 µm width. In this case gs=2.5 mmol s–1 m–2 with patchy closure versus 1.7 mmol s–1 m–2 with uniform closure and gL would equal about 11.5 versus 10.7 mmol s–1 m–2 (with gc=8 mmol s–1 m–2), a difference that would be difficult to resolve experimentally. By contrast, the impact of patchy closure would be much smaller on KL than on gs in the above example. KL,s would be 5.2x10–3 kg s–1 MPa–1 m–2 with just 0.1% of the stomates open at 1 µm and the rest at 0.02 µm width and hence would have a negligible impact on KL, i.e. 2.39x10–4 kg s–1 MPa–1 m–2 with 0.1% of the stomates open at 1 µm width versus 2.50x10–4 kg s–1 MPa–1 m–2 with all stomates open 
1 µm.
On the other hand, there is some value in measuring gL during measurements of KL, because if it can be proved that KL values change in transition from high- to low-irradiance before gL closely approaches gc then this would support the hypothesis that the irradiance dependence of KL is caused by the irradiance dependence of KL,vt. The purpose of this paper is to search for evidence that the irradiance dependence of KL is due to KL,vt. The theoretical relationship between KL and gL is given in Fig. 2; quite low values of gL must be reached before KL declines, i.e. around 10–15 mmol s–1 m–2 in this model. Can irradiance-induced changes in KL be demonstrated at stomatal apertures that yield higher values of gL? Alternatively, can irradiance-induced changes in KL be demonstrated while gL is at low and constant value?
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Materials and methods |
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TopAbstractIntroduction and theoryMaterials and methodsResultsDiscussionReferences |
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All measurements were performed on mature current-year leaves of several temperate deciduous trees: Cercis siliquastrum L. (Fabaceae), Acer pseudoplatanus L. (Sapindaceae), and Juglans regia L. (Juglandaceae) in Trieste, Italy; A. saccharum Marsh. and Quercus rubra L. (Fagaceae) in Burlington, Vermont (nomenclature follows Gleason and Carlquist, 1991
; Tutin et al., 1964; Judd et al., 2002). Leaves of tropical trees were also tested: Schefflera arboricola (Hayata) Merr. (Apiaceae) in a greenhouse in Burlington and Calophyllum longifolium (Clusiaceae), Cordia alliodora (Bignoniaceae), Dendropanax arboreus (Apiaceae), Lindackeria laurina (Achariaceae), and Miconia argentea (Melastomataceae) in tropical lowland rainforest, Barro Colorado Island, Panama (Smithsonian Tropical Research Institute; nomenclature follows Croat, 1978; Judd et al., 2002).
Leaves were harvested early in the morning from adult trees or shrubs and transported to the laboratory while keeping the petiole immersed in a 10 mM KCl solution. Leaves were then connected to the HPFM (Tyree et al., 1995) via the petiole using compression fittings. Leaves were immersed in distilled water to stop transpiration and to prevent leaf overheating upon illumination (see below). Leaves were perfused at 0.3–0.5 MPa with a 10 mM KCl solution for 50 min. Leaf hydraulic conductance (KL) was measured every 2 s and saved as means every 30 to 60 s under ambient laboratory irradiance (PAR <6 µmol m–2 s–1). The temperature of the water bath (Tw) was also recorded at the same time interval using a thermocouple thermometer (Digi-Sense model 91100–40, Cole-Parmer Instrument Co., Vernon Hills, IL, USA). Leaves were then illuminated at a PAR of 1000–1200 µmol m–2 s–1 using a slide projector or floodlight (as used in Panama). In order to avoid excessive heating of the water bath, irradiance from the projector was reflected by a mirror before striking the leaves. This way, water temperature never increased more than 2 °C during the following 30 min. During the high irradiance period, both KL and Tw were recorded every 60 s. Then, irradiance was returned to ambient and both KL and Tw were measured for 30 min more. Overall, each experiment lasted 115 min. Control experiments were performed where KL was measured on leaves connected to the HPFM for 115 min and never illuminated. At the end of each experiment, leaf surface area (AL) was measured for KL calculation using a leaf area meter (LI-3000A, Li-Cor Inc., Lincoln, NE, USA) and KL was scaled by AL. All KL measurements were corrected for eventual temperature changes to account for changes in water viscosity.
Because Sack et al. (2002) had suggested that the irradiance response of KL might be due to stomatal opening, changes in stomatal aperture were monitored during the dark and high irradiance periods. Leaves were connected to the HPFM and pressurized at 0.02 MPa, in order to prevent leaf desiccation while avoiding substantial infiltration of leaf air spaces. Leaves were not immersed in water but kept in air. The time-course of the experiment was the same as for KL measurements but, in this case, leaf conductance to water vapour (gL) was measured every 2 min, using a steady-state porometer (LI-1600, Li-Cor Inc.) in Trieste or with a LI-6400 (Li-Cor Inc.) in Burlington. It was confirmed that both porometers gave values of gL near zero when leaves were replaced by plastic sheets, i.e. 0.1±0.2 mmol s–1 m–2 for the LI-1600 and 1.4±2.3 mmol s–1 m–2 for the LI-6400 (mean ±sd).
To investigate the generality of the irradiance response of KL, less detailed experiments of a confirmatory nature were performed for tropical species. KL values were compared either for given leaves before and after changing from low to high irradiance, or for different leaves sampled from the same branch held constantly at low versus high irradiance. Leaves of tropical species were not tested for gL responses.
In all cases, differences between KL measured in the dark or after illumination were tested for statistical significance using One-way-ANOVA.
ABA experiments
In order to investigate the response to irradiance of leaves whose stomatal irradiance response had been inhibited, leaves of J. regia were collected early in the morning and transported to the laboratory as described above. Here, they were rehydrated for 2 h with either 10 mM KCl solution (controls) or with a solution of 10 mM KCl+0.5 mM abscisic acid solution (ABA, Sigma-Aldrich S.r.l.). The plant hormone ABA is well known for its effects on stomatal movements. In particular, ABA is known to inhibit the irradiance-induced stomatal opening at low concentrations (10–3 mM, Trejo et al., 1993). Control and ABA-treated samples were then measured for KL changes under low or high irradiance conditions as described above. Preliminary experiments were performed to assess the effect of ABA on stomatal aperture; leaf conductance to water vapour of control or ABA-treated leaves was measured under conditions similar to experiments described above. In particular, leaves rehydrated with either KCl or KCl+ABA solutions were connected to the HPFM and pressurized at 0.02 MPa, in order to avoid substantial infiltration of air spaces. Leaves were immersed in water and kept for 15 min under normal laboratory irradiance (see above). Leaves were taken out of water, carefully dried with filter paper and their leaf conductance to water vapour (gL) was measured using a steady-state porometer (LI-1600, Li-Cor Inc.). Leaves were immersed again in water and illuminated as described above. After 30 min, leaf surface was dried again and leaves were re-measured for gL.
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Results |
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TopAbstractIntroduction and theoryMaterials and methodsResultsDiscussionReferences |
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Sack et al. (2002)
measured the irradiance response of KL on only two species (Quercus rubra and Hedera helix). In the former they found a large irradiance response when measured with the HPFM, but no significant effect on the latter when measured with the vacuum chamber method. The results of Sack et al. (2002) were replicated on Q. rubra and also on Acer saccharum. A. saccharum (n=12) had a smaller effect than Q. rubra (n=29). After 50 min in ambient irradiance A. saccharum and Q. rubra had KL values that did not differ significantly, i.e. 3.66±0.46x10–5 (mean±sem) and 3.57±0.31x10–5, respectively (Fig. 3); but KL increased after 33 min in high irradiance by 64% and 392% for A. saccharum and Q. rubra, respectively. KL values in high irradiance were lower by about a 30–50% than those shown in Fig. 2 of Sack et al. (2002). The differences may be genetic or environmental in origin or may be due to the time of year (measurements were made in May–June versus August in Sack et al., 2002). In both studies the leaves were exposed to high irradiance for about the same time period (20–35 min) prior to recording KL values.
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Two out of the three species studied in Trieste showed an irradiance-induced increase of KL. In particular, KL of Cercis siliquastrum did not respond to irradiance level, but Acer pseudoplatanus and Juglans regia showed marked responses to illumination in that their KL increased by about 150% and 300% (for J. regia and A. pseudoplatanus, respectively, Fig. 4). In the latter two species KL increased gradually upon illumination, but remained relatively constant after lights were turned off in contrast to the behaviour of A. saccharum and Q. rubra where KL fell slowly after returning to ambient irradiance. In the case of C. siliquastrum, KL did not differ in control or illuminated leaves, thus suggesting that irradiance had no effect on KL in this species. The analysis of stomatal kinetics (Fig. 4, triangles) showed that stomata opened in response to high irradiance stimulus and closed in low irradiance, as expected for all species. However, gL changes did not parallel KL changes. In fact, in the case of A. pseudoplatanus and J. regia, stomatal opening followed KL increase upon illumination with a delay of 5–10 min. Moreover, after irradiance was turned off, gL markedly decreased to its previous levels in low irradiance but KL did not. In the case of C. siliquastrum, gL increased after illumination of the leaf but KL remained constant.
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Both control and ABA-rehydrated leaves of J. regia showed similar dark values of gL (about 8–10 mmol m–2 s–1, Fig. 5B). In high irradiance, gL of control leaves increased to about 55 mmol m–2 s–1 while that of ABA-treated leaves remained at the same values as measured in the dark. The kinetics of KL response to illumination was the same for control and ABA-treated leaves (Fig. 5A).
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Two of the six tropical species in this study changed KL in response to irradiance. Table 1 gives KL values in low and high irradiance conditions.
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Discussion |
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TopAbstractIntroduction and theoryMaterials and methodsResultsDiscussionReferences |
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In all species KL decreased with time after the onset of perfusion with the HPFM. This initial decrease may be of no functional significance since it is probably due to non-steady-state conditions that will exist until leaves, initially dehydrated, become fully hydrated. Not all species showed a statistically significant response in leaf hydraulic conductance to irradiance when measured with the HPFM; five species did not respond to irradiance and six species did. This is consistent with Sack et al. (2002)
who reported an irradiance response in one of two species during measurements of KL with the HPFM or vacuum chamber. Irradiance effects on KL were not replicated as much in some species as others, hence the statistical power to resolve changes were unequal in these studies. Therefore, the effects of irradiance on leaf hydraulic properties might be more ubiquituous. It is tentatively concluded that these data are most consistent with the hypothesis that the irradiance dependence of KL is due more to a dependence of the leaf blade tissues accounted for in the vessel+tissue component (KL,vt) than in the stomatal component (KL,s). When stomatal response to irradiance is inhibited by the application of ABA, the irradiance response to KL remains unchanged (Fig. 5). The ABA-response might still be consistent with the hypothesis that stomates control KL in low irradiance if it is assumed that ABA does not cause complete stomatal closure and prevents further response of stomates to irradiance. In A. pseudoplatanus and J. regia the kinetics of the irradiance response of gL and KL (Fig. 4) are not what is expected from the theory (Figs 1, 2) if stomatal conductance were driving the KL response. Theory would predict a rapid increase in KL to a maximum value with a negligible change in gL immediately after the lights are turned on (Fig. 2). What is found is a gradual increase in KL as gL increases gradually. In addition, it would be expected that the decrease in KL would mirror the decrease in gL when the lights are turned off. Instead, it was found that KL remained relatively constant while gL falls back almost to the original, dark-adapted value in A. pseudoplatanus and J. regia (Fig. 4). Furthermore, no irradiance response is observed in C. siliquastrum even though gL is varying over the same range as the other two species.
These results might still be consistent with the irradiance dependence of KL being caused by irradiance dependence of KL,s but it would have to be supposed that there are differences in the kinetics of stomatal response to irradiance in the HPFM experiments versus the gas exchange experiments. It would probably be necessary to invoke hysteresis in the kinetics of gL changes upon change in irradiance and it might have to be supposed that gL changes over different ranges of values in the HPFM and gas exchange experiments. These possibilities cannot totally be discounted, especially if it is taken into account that experimental conditions during KL measurements (leaf immersed in water) and gL measurements (leaf kept in air) were not the same.
Because these results are less consistent with the hypothesis that stomatal opening is responsible for the irradiance-mediated increase of KL than with the hypothesis that there is an irradiance-mediated response of tissues (KL,vt), possible alternative explanations have to be sought. Several studies suggest that leaf hydraulic resistance is dominated by the extravascular component (Tyree and Cheung, 1977; Tyree et al., 2001; Salleo et al., 2003; Trifilò et al., 2003). Water flow across cell membranes is known to be enhanced (by over three times) by the presence of aquaporins (Maurel, 1997). Hence, it is conceivable that rapid irradiance-mediated increase of leaf hydraulic conductance is due to the de novo expression of aquaporins or, more likely, to the up-regulation of pre-existing water channels. Irradiance-mediated circadian regulation of aquaporin expression has been shown to be involved in the regulation of root water permeability (Henzler et al., 1999; Lopez et al., 2003) and in the pulvinar movements of Samanea saman (Moshelion et al., 2002). Post-translational regulation of aquaporin activity through phosphorylation has also been reported (Maurel et al., 1995; Johnsson et al., 1998, 2000; Eckert et al., 1999; Chaumont et al., 2000; Baiges et al., 2002). It is therefore conceivable that the increase of KL observed in the present study might be due to irradiance-mediated activity of specific kinases which, in turn, would lead to up-regulation of aquaporins and consequent enhanced water transport through the bundle sheath and/or mesophyll. Although there is no experimental evidence supporting this mechanism, it is felt that this hypothesis represents an interesting starting point for future studies addressed at elucidating the role of aquaporin regulation in mediating the response of KL to environmental stimuli.
Some recent studies (Zwieniecki et al., 2002; Sack et al., 2004) reported a dominance of vascular hydraulic resistance on KL in some species. If this were the case, then irradiance-induced changes of KL might be mediated by changes in the hydraulic properties of the leaf venation system as well. In turn, these changes might be caused by modifications of xylem sap composition (Zwieniecki et al., 2001) possibly mediated by the phloem (Zwieniecki et al., 2004). However, previous work on A. saccharum and Q. rubra has shown KL to be invariant with large changes in the ion composition of the flow solution (i.e. KL was the same when measured with deionized filtered water as with 10 mM KCl; see ‘Materials and methods’ in Sack et al., 2004). For such species, at least, it is suggested that the irradiance response is localized in the extravascular portion of the water flow pathway.
It has to be pointed out that all results presented in this study and related discussion might only apply to leaves when measured with the HPFM. Eventual irradiance-mediated KL changes in the field were not measured and it is felt that methods to measure KL directly would be difficult to devise on intact plants. However, it is considered that such changes might be of adaptive value if KL increases during the central part of the day, when PAR and evaporative demand is highest, thus allowing plants to sustain high transpiration rates while buffering leaf water potential above critical values inducing xylem cavitation (Bond and Kavanagh, 1999; Nardini and Salleo, 2000). Moreover, the relative magnitude of KL response to irradiance might depend on several factors like the relative contribution of the vascular and extravascular compartments to leaf hydraulics or the abundance of aquaporins in leaf tissues. Aquaporins would only influence the hydraulic conductance of the extravascular tissues, and not the xylem. Thus, if aquaporins are involved in the irradiance response, a stronger irradiance effect would be expected for leaves in which the extravascular tissue is a more important determinant of KL (Tyree et al., 2001; Salleo et al., 2003). Apparently, the response of KL to irradiance is highly variable across species, and it is also possible that the exact mechanisms may vary among species. However, because the irradiance effect is common and substantial, it is recommended that KL measurements be conducted under the irradiance most relevant to the biological application. Clearly, the functional and ecological implications of the phenomenon described in this paper invite further studies.
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Acknowledgements |
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Lawren Sack was supported by a Putnam Fellowship at the Arnold Arboretum of Harvard University and a Short-Term Fellowship at the Smithsonian Tropical Research Institute. We are grateful to John Bennink for technical assistance.
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