Journal of Experimental Botany, Vol. 52, No. 357, pp. 739-745,
April 15, 2001
© 2001 Oxford University Press
Original Papers |
Metabolic inhibition of root water flow in red-osier dogwood (Cornus stolonifera) seedlings
Department of Renewable Resources, 4-42 Earth Sciences Bldg., University of Alberta, Edmonton, Alberta, Canada
Received 7 June 2000; Accepted 17 October 2000
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Abstract |
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The short-term effects of sodium azide (NaN3) on water flow in red-osier dogwood (Cornus stolonifera Michx.) seedlings were examined in excised roots at a constant pressure of 0.3 MPa. NaN3 significantly decreased root water flow rates (Qv). It also induced a significant reduction in root respiration and reduced stomatal conductance to a greater extent in intact seedlings than in excised shoots. Apoplastic flow of water increased with the NaN3-induced decreases in Qv. Mercuric chloride (HgCl2) was also used to characterize the water flow responses and respiration of dogwood roots. Similarly to NaN3, 0.1 and 0.3 mM HgCl2 decreased root respiration rates and Qv. The lower, 0.05 mM HgCl2 treatment, reduced Qv, but had no significant effect on root oxygen uptake. The reduction of Qv in HgCl2-treated plants was only partly reversed by 50 mM mercaptoethanol. The mercurial inhibition of Qv suggested the presence of Hg-sensitive water channels in dogwood roots. The results indicate that root-absorbed NaN3 metabolically inhibited water channel activities in roots and in shoots and resulted in stomatal closure. It is suggested that the inhibition of respiration that occurs in plants stressed with environmental factors such as flooding, cold soils, and drought may be responsible for the closure of water channels in root cells and inhibition of root water flow.
Key words: Cornus stolonifera, water channels, sodium azide, mercuric chloride, root water flow.
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Introduction |
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Radial water transport in roots occurs simultaneously through the symplastic, transcellular and apoplastic pathways (Steudle and Frensch, 1996
; Steudle and Peterson, 1998). The apoplastic pathway is often considered to be of least hydraulic resistance. However, the fractional cross-sectional area of the apoplastic path is relatively small in many tissues. Extensive pressure probe studies with many cell types have shown that the hydraulic conductivity of cell membranes is high and probably only a small proportion of water flows via the apoplastic path (Tyerman et al., 1999). Hydraulic properties of these pathways are changed in response to endogenous and external signals as well as alterations in tissue anatomy (Zimmermann and Steudle, 1998).
There is growing evidence that water flow across intact higher plant membranes is predominantly through the water channel proteins (aquaporins). Under conditions in which the cell-to-cell pathway of water flow dominates, regulation of the activity of aquaporins could obviously have a major impact on the hydraulic properties of the tissue. Inhibition of water flow by mercurials in membrane vesicles (Maurel, 1997; Tyerman et al., 1999), individual root cells (Zhang and Tyerman, 1999) and whole root systems (Maggio and Joly, 1995; Carvajal et al., 1996; Tazawa et al., 1997; Wan and Zwiazek, 1999) points to the importance of aquaporins in the regulation of water flow through root systems. In whole plant experiments, HgCl2 has been used as channel blocker, but the inhibitory effect of HgCl2 on membrane water permeability can also be indirect via metabolic inhibition (Tyerman et al., 1999).
Regulation of water relations by plant metabolism has received little attention. Recent evidence pointing to phosphorylation as a likely factor required for the opening of water channels (Daniels et al., 1994; Maurel et al., 1995; Johansson et al., 1998) sheds new light on possible links between respiration and water relations. This process could be a common mechanism responsible for water flow inhibition in stressed plants. It has been noted frequently that flooding (Kozlowski and Pallardy, 1979), chilling (Wan and Zwiazek, 1999) and nutrient stresses (Radin and Ackerson, 1981; Radin and Eidenbock, 1984; Clarkson et al., 2000) can result in stomatal closure and reduced water uptake in the presence of water available to roots. However, stomatal closure has been often explained as a result of stress-induced synthesis of ethylene and (or) abscisic acid (Drew et al., 1979). An inhibition of water flow has also been observed in plants treated with respiration inhibitors (Pitman et al., 1981; Zhang and Tyerman, 1991). Sodium azide (NaN3), the cytochrome pathway inhibitor, has been often used in studies of metabolic inhibition. Drake showed that NaN3 could reduce the electric coupling between cells in oat coleoptiles (Drake, 1979). Depolarization of membrane potential and an increase in membrane resistance in response to NaN3 also led to a decreased hydraulic conductivity in cortical cells of wheat roots (Zhang and Tyerman, 1991). In the present experiment, NaN3 was used to examine the role of respiration in root water flow and stomatal conductance of red-osier dogwood (Cornus stolonifera Michx.). The hypothesis that an inhibition of root respiration would reduce the water flow rate of the cell-to-cell pathway and trigger leaf stomatal closure was studied. To examine the importance of root water flow in controlling stomatal conductance, the effects of NaN3 in intact seedlings and excised shoots were measured. To determine the extent to which mercury-sensitive water channels are involved in the control of root water flow, mercurial inhibition of root water flow was also examined using a pressure-flux approach. Red-osier dogwood is a deciduous, thicket-forming shrub native to North America and its ecological importance, fast growth and high stress resistance made it suitable for the present study.
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Materials and methods |
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Experimental conditions
Six-month-old dogwood seedlings grown in styrofoam containers filled with a peat:sand mixture (1:1, v:v) were transferred to aerated solution culture. The roots were gently washed free of soil in cold tap water and the seedlings were transferred to half-strength modified Hoagland's solution (Epstein, 1972
) in 20 l containers. Six containers, each with 20 seedlings, were placed in a growth room set to a 16 h photoperiod with photosynthetic photon flux of 300 µmol m-2 s-1, 22/18 °C (day/night) temperatures, and a constant relative humidity of approximately 65%. The seedlings were grown in solution culture for about 8 weeks and the solution was replaced every 2 weeks. The containers were periodically rotated on the experimental bench to eliminate possible location effects on the seedlings.
Measurements of Qv
The steady-state flow rate (Qv) was measured following the hydrostatic pressure method (Rüdinger et al., 1994; Wan and Zwiazek, 1999). A glass tube of 250 ml capacity containing full-strength Hoagland's solution was inserted into a pressure chamber (PMS Instruments, Corvallis, Oregon). The solution was kept continuously stirred during the measurements with a magnetic stirrer. For the measurements, stem was severed above the collar region and the roots sealed in the pressure chamber. The entire root system was immersed in the solution with the debarked part of the stem protruding through a rubber gasket secured to the lid of the pressure chamber. Chamber pressure was gradually increased to 0.3 MPa and held constant during the measurements. The protruding stem was fitted to a graduated pipette by a short piece of rubber tubing and the water expressed through the stem was collected into the pipette. Root Qv of the whole root system was monitored over time by recording the volume of sap every 5 min and the results were expressed in µl min-1 root system-1.
Measurements of Qv in response to NaN3 and HgCl2
Qv was measured in root systems treated with 0.5 mM and 1 mM NaN3. Roots from five plants, each plant from a different growth container, were selected at random and measured for each treatment. Qv of each root system was recorded for at least 45 min under constant pressure of 0.3 MPa. Then the pressure was released and an appropriate amount of concentrated NaN3 solution was injected into the root medium to achieve the desired concentration before pressurizing the roots again to 0.3 MPa. Qv was also measured for five control root systems where NaN3 was replaced with distilled water. The flow was monitored for 2 h following the injection of NaN3. Mean Qv values obtained over 45 min before the application of NaN3 were used to normalize the data for each root system.
The above procedure was also followed to measure root Qv in response to 0.05, 0.1 and 0.3 mM HgCl2. When a stable Qv was reached, an appropriate amount of HgCl2 stock solution was injected into the root medium to achieve the desired concentration. When a new steady-state was observed following the injection of HgCl2, 2-mercaptoethanol (ME) was injected into the root medium for a final concentration of 50 mM. Qv was monitored for 30 min before the injection of HgCl2, 100 min after the injection of HgCl2 and then another 100 min after adding ME. Root systems serving as controls were also measured at the same time with distilled water added in place of HgCl2. Mean Qv values obtained over the 30 min period before injecting HgCl2 were used to normalize the data for each root system.
Root respiration in response to NaN3 and HgCl2
Root respiration was measured as oxygen uptake using a Clark-type electrode (Yellow Springs Instruments, Yellow Springs, OH). Respiration rates of each root system were determined once, just before the measurements of Qv in the pressure chamber. The root system was placed in an air-tight cylinder containing Hoagland's solution that was kept continuously stirred with a stirrer bar during measurements. Oxygen uptake was monitored for 25 min by recording data every 5 min and the roots were placed for 2 h in 0.5 mM NaN3, 1 mM NaN3, 0.05 mM HgCl2, 0.1 mM HgCl2 or 0.3 mM HgCl2. Control seedlings remained for 2 h in Hoagland's solution. Five root systems per treatment were used. Respiration rate was the slope of regression of oxygen uptake over time expressed in mg min-1. Respiration rate recorded before treatment was used to normalize the data for each root system.
Measurements of gs
Stomatal conductance (gs) of leaves was measured in whole plants and excised shoots treated with NaN3. The measurements were carried out with a steady-state porometer (Li-Cor, Lincoln, NE) in the same growth chamber where the seedlings were grown. During the measurements, root systems of the seedlings were maintained in aerated full-strength Hoagland's solution. The second fully developed leaf was marked and used for measurements over time. After the first measurement, NaN3 was added to the nutrient solution to a concentration of 1 mM. There were five seedlings assigned for NaN3 treatment and five for control group.
A second experiment was conducted to verify the effect of NaN3 on gs of excised shoots following the same procedure. Shoots were severed by a sharp cut at the lower part of the stems under water. The root medium was also kept aerated during the treatment with 1 mM NaN3. There were five excised shoots measured in the NaN3 treatment and five control shoots. The possible changes in gs over time in both the experiments were explored by using Student t-test.
Determination of apoplastic flow
Fluorescent tracer dye, trisodium 3-hydroxy-5,8,10-pyrenetrisulphonate (PTS), was used to quantify the apoplastic flux in response to application of NaN3 (Hanson et al., 1985). PTS was added to Hoagland's solution to reach the concentration of 0.02% and the roots were immersed in this solution and pressurized to 0.3 MPa for Qv measurements. NaN3 treatment (1 mM) was applied in a pair-wise manner, such that the response of a single treated root system was compared to an untreated control. Using this system, six root systems were measured for NaN3 treatment and for control.
Qv of each root system was recorded for 1 h under constant pressure of 0.3 MPa and then NaN3 stock solution was injected into the root medium to achieve 1 mM NaN3. Distilled water was injected in place of NaN3 for the root systems serving as controls. After the application of NaN3, Qv was monitored for 2 h. Qv values obtained before the application of NaN3 were used to normalize the data for each root system.
For PTS concentration determinations, xylem sap was collected at the end of first hour before NaN3 application, at the end of first hour after NaN3 application and at the end of second hour after NaN3 application. PTS concentrations in the xylem sap and root medium were determined with a luminescence spectrometer (LS 50B, Perkin Elmer Ltd., UK) using excitation wavelength of 410 nm and emission wavelength of 515 with a slit width of 10 nm. Proportion of apoplastic flow was calculated as the ratio of PTS concentration of xylem sap to that of bathing solution.
The possible increase in PTS concentration in the xylem sap due to the decreased flow through the cell-to-cell pathway as a result of NaN3 treatment was estimated with the data on exudation of xylem sap by keeping the apoplastic water flow constant. For the purpose, the data of xylem sap in volume units obtained over 1 h prior to NaN3 treatment (V0), the PTS concentration of the xylem sap (C0) and the decreased amounts of xylem sap in volume units (
V) over the first or the second hour after NaN3 treatment were used. The PTS concentration of the xylem sap after NaN3 treatment (C) was calculated from the following equation:
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Results |
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Qv in response to NaN3 and HgCl2
Pressure-induced Qv in NaN3-treated root systems declined rapidly, while Qv in the untreated root systems remained constant throughout the measurement period (Fig. 1a
). The decline in Qv was more pronounced in 1 mM than in 0.5 mM concentration. Two hours after injection of NaN3, Qv decreased to about 35% of the pretreatment flow rate in 0.5 mM concentration and about 50% in 1 mM concentration (Fig. 1a).
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Similarly to NaN3, a decline in Qv occurred in HgCl2-treated roots (Fig. 1b
). The decline was within 10 min after injection of 0.1 mM and 0.3 mM HgCl2, while it took approximately 50 min to make an appreciable decrease in Qv for 0.05 mM HgCl2 (Fig. 1b). In the lower concentrations of HgCl2, Qv decreased after 2 h by 46–52% of the corresponding pretreatment flow rates. At the same time, 0.3 mM HgCl2 reduced Qv by approximately 67% of the pretreatment rate (Fig. 1b).
The inhibition of Qv by 0.3 mM HgCl2 was only partly reversed by ME. Within 10 min after injection of ME into the bathing solution, Qv increased by about 8% (Fig. 1b). In the lower concentrations, no appreciable increase in Qv was observed, but the declining Qv trend stopped within 20 min after the application of ME and Qv remained stable during the remaining measurement time (Fig. 1b).
Root respiration in response to NaN3 and HgCl2
NaN3 treatment significantly reduced respiration rates of the root systems (Fig. 2). Two hours following injection of 0.5 mM and 1 mM NaN3, a decline in oxygen root uptake was reduced by about 35% and 42%, respectively (Fig. 2). Oxygen uptake rates in untreated root systems remained unchanged over the measurement period.
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Two hour treatment with 0.1 mM or 0.3 mM HgCl2 also drastically reduced oxygen uptake rates in roots. However, the 0.05 mM HgCl2 treatment had no significant effect on root respiration rates (Fig. 2
).
Stomatal conductance, gs
NaN3 treatment significantly reduced gs in intact plants (Fig. 3a). After 4 h of 1 mM NaN3 treatment, gs in seedlings decreased to about 60% of the untreated control level (Fig. 3a). The decrease of gs was statistically significant in NaN3-treated intact seedlings within 1 h of treatment.
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In excised shoots, 1 mM NaN3 treatment also reduced gs, compared to control shoots and the decrease was statistically significant after 2 and 3 h following the treatment (Fig. 3b
). However, the inhibition of gs was more pronounced in treated intact seedlings compared to treated excised shoots.
Apoplastic flow in response to NaN3
Pressure-induced Qv decreased rapidly in root systems treated with 1 mM NaN3, reaching 40% of the pretreatment level after 2 h of treatment (Fig. 4a). Parallel measurements of untreated root systems did not show a significant change in Qv over time (Fig. 4a).
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Mean PTS concentration in xylem sap was about 1% of that in the root incubation medium before injecting 1 mM NaN3 (Fig. 4b
). It increased to about 4% during the first hour after NaN3 treatment and to about 11% during the second hour. No appreciable change in PTS concentration in xylem sap of untreated root systems was observed over the measurement period of 3 h. The increased PTS ratio following NaN3 treatment was the result of the decreased water transport through the cell-to-cell pathway and the increased apoplastic water transport. These estimates using equation (1) showed that the decreased water transport in NaN3-treated root systems could account for 1.7% and 2.1% PTS concentration after 1 h and 2 h of treatment, respectively. Therefore, the increased apoplastic ratio as a result of NaN3 treatment was mostly due to the increased water flow through the apoplastic pathway.
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Discussion |
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It was demonstrated that the metabolic inhibitor NaN3 brought about a rapid and substantial reduction in root water flow rates in red-osier dogwood seedlings. The pattern and extent of decline due to NaN3 was similar to that observed in response to HgCl2 (Fig. 1
). The inhibitory effect of NaN3 or HgCl2 on root water transport was probably due to their inhibition of root hydraulic conductivity rather than by changes in the osmotic pressure gradient between the xylem and the surrounding medium. It has been previously demonstrated that applied hydrostatic pressure dominates over osmotic pressure gradient in pressurized excised root systems (Maggio and Joly, 1995; Quintero et al., 1999). Therefore, it was assumed that the osmotic component of the driving force in these pressure-induced experiments was negligible. In this study, the reduction in root water flow rates by NaN3 or HgCl2 was probably due to the inhibition of water transport across water channels (aquaporins). The presence of water channel proteins in the plasma membrane and the tonoplast allows a plant to regulate its water flow through the cell-to-cell pathway (Chrispeels et al., 1997). A number of aquaporins are sensitive to HgCl2 (Preston et al., 1992; Maurel et al., 1993). Inhibition by mercurials of water flow through most aquaporins (Maurel, 1997; Tyerman et al., 1999) suggests that mercury-sensitive aquaporins in the tonoplast and/or the plasma membranes play a major role in water transport through the root system. The reduction in Qv in response to HgCl2 as observed in the present study is consistent with several other studies (Maggio and Joly, 1995; Carvajal et al., 1996; Tazawa et al., 1997; Wan and Zwiazek, 1999) and suggests the presence of mercury-sensitive aquaporins in dogwood roots. In tomato roots, 0.5 mM HgCl2 caused a 57% decrease in the hydraulic water conductivity with no significant changes in the K+ concentration of the xylem sap (Maggio and Joly, 1995).
The inhibition of Qv in dogwood roots by HgCl2 was only partly reversed by ME (Fig. 1b). A partial recovery of HgCl2-induced inhibition of hydraulic conductivity was also reported for wheat root cells (Zhang and Tyerman, 1999). In their study no effects of HgCl2 on the hydraulic conductivity of metabolically depressed cells were noticed and this was interpreted that HgCl2 might reduce the hydraulic conductivity by general metabolic inhibition rather than by a direct blockade of water channels (Zhang and Tyerman, 1999).
A reduction in hydraulic conductivity has been reported for NaN3-treated cortical cells in wheat roots and interpreted as an effect on plasmodesmata and plasma membrane (Zhang and Tyerman, 1991). Pitman et al. recorded a significant inhibition of exudation in maize and barley roots in the presence of a metabolic inhibitor, carbonyl cyanide m-chlorophenyl hydrazone, and suggested that the inhibition was due to the blocking of water transport pathway at the plasmodesmata (Pitman et al., 1981).
One conspicuous effect of low oxygen concentration is rapid depolarization of the plasma membrane (Buwalda et al., 1988). Depolarization of membrane as a result of hypoxia or anoxia is similar to the effects of metabolic inhibitors like NaN3 (Drake, 1979). Inhibition of electrogenic pumps can be partly responsible for the depolarization of membranes. There is a strong correlation between inhibition of electrogenic pumps and an increase in membrane resistance (Blatt, 1987). NaN3 can induce a rapid increase in membrane resistance (Drake, 1979) resulting in a decreased root water flux across the membrane.
In this study, oxygen uptake of NaN3-treated roots as well as of those exposed to higher HgCl2 concentrations was significantly reduced (Fig. 2). NaN3 is an effective inhibitor of electron transport and oxidative phosphorylation. In barley roots, NaN3 induced a decline in cytoplasmic ATP concentration and depolarization of membranes over a period of several min (Reid et al., 1985). HgCl2 can act as metabolic inhibitor and inhibit respiration rates in sensitive cells (Jardim et al., 1993; Tyerman et al., 1999).
It is conceivable that in this experiment the decline in Qv of roots treated with NaN3 and higher concentrations HgCl2 might be partly due to the inhibitory effects of cell hydraulic conductivity mediated through the decreased respiration rates. Although in the present and previous (Wan and Zwiazek, 1999) studies, metabolic inhibition was not observed at the low concentrations of HgCl2 that were effective in reducing root water flow, it is conceivable that the mercury-induced closure of water channels in higher HgCl2 concentrations was partly due to its effect on phosphorylation.
It has been shown that water transport through some aquaporins is regulated through phosphorylation (Daniels et al., 1994; Maurel et al., 1995; Johansson et al., 1998). The plasma membrane aquaporin PM28A in spinach leaves, for example, is a major phosphoprotein (Johansson et al., 1996) and its water permeability is reduced upon dephosphorylation (Johansson et al., 1998). Reduced phosphorylation of root cell aquaporins caused by metabolic inhibitors might offer an explanation of the decreased Qv under the metabolic inhibition of NaN3 or HgCl2 observed in this study and those of other authors (Zhang and Tyerman, 1999; Tyerman et al., 1999).
In this study, when NaN3 was supplied to plants through the roots, a significant decline in gs occurred within 1 h (Fig. 3). A loss of shoot hydration due to reduced water flow might have conceivably triggered stomatal closure. This early decline in gs is consistent with the reduction in Qv of NaN3-treated root systems (Fig. 1a). It is plausible that, similar to HgCl2 (Wan and Zwiazek, 1999), NaN3 inhibited the water channel activities in roots resulting in a decreased Qv, which, in turn, decreased gs. However, in contrast to HgCl2, excised shoots treated with NaN3 also showed significant decrease in gs suggesting that NaN3 triggered a similar reaction in the shoots to that observed in the roots. Since the level of gs inhibition was quite large in rooted plants, it is suggested that root hydraulic conductivity plays a significant role in regulating stomatal conductance, a process also observed in plants with roots exposed to HgCl2 (Wan and Zwiazek, 1999) and low temperature (Wan et al., 1999).
In the present study, PTS concentration in xylem sap expressed from control roots was about 1% of that in the root medium (Fig. 4b). This estimate of apoplastic flux is comparable to other studies that used fluorescent tracer dyes (Hanson et al., 1985; Moon et al., 1986; Skinner and Radin, 1994; Wan and Zwiazek, 1999) and suggests that only a small fraction of water was transported through the apoplastic pathway. The concentration of PTS in the xylem sap following NaN3 treatment increased gradually to about 11% within the 2 h measurement period resulting in the increase in the apoplastic to cell-to-cell water flow ratio. The extent to which the increased PTS ratio was due to the decreased water transport through cell-to-cell pathway was calculated. This estimate showed that the decreased water transport in NaN3-treated root systems could account for only 2% PTS concentration after 2 h of treatment. In fact, the apoplastic water flow rate increased following NaN3 treatment, possibly due to decrease in the apoplastic resistance. Radin and Matthews suggested that a low root reflection coefficient could be associated with a substantial apoplastic flux of water through a bypass (Radin and Matthews, 1989). Hanson et al. reported an increased apoplastic bypass in roots of red pine when experimentally measured under oxygen deprivation and suggested that the increase in apoplastic flux under anaerobic conditions resulted from an increase in the water potential difference across the apoplastic pathway (Hanson et al., 1985).
The results presented in this paper point to the presence of water channels in roots of red-osier dogwood seedlings which are sensitive to both HgCl2 and NaN3. Both inhibitors rapidly and severely decreased cell-to-cell or (and) symplastic root water flow. It is suggested that the inhibition of oxidative phosphorylation by sodium azide and other metabolic inhibitors including environmental stresses such as low soil temperature, flooding and nutrient stress may be a common mechanism responsible for the closure of water channels and reduction of water flow to shoots.
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Acknowledgments |
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We gratefully acknowledge funding in the form of a research grant from the Natural Sciences and Engineering Research Council of Canada to JJZ and a research fellowship award from the World Bank to MK to support this study. We thank Xianchong Wan for his help in setting the experiments.
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Notes |
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1 To whom correspondence should be addressed. Fax: +1 780 492 1767. E-mail: janusz.zwiazek{at}ualberta.ca
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