Journal of Experimental Botany, Vol. 51, No. 348, pp. 1255-1259,
July 2000
© 2000 Oxford University Press
Original papers |
Temperature effects on hydraulic conductance and water relations of Quercus robur L.
1 UA-PIAF, INRA, Site de Crouël, 63039 Clermont-Ferrand, France
2 INRA, Laboratoire d'Ecophysiologie Forestière, 54280 Champenoux, France
Received 1 November 1999; Accepted 8 March 2000
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Abstract |
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The effects of temperature on root and shoot hydraulic conductances (gshoot and groot) were investigated for Quercus robur L. saplings. In a first experiment, conductances were measured with a High Pressure Flow Meter on excised shoots and detopped root systems. The groot and gshoot increased considerably with temperature from 0–50 °C. Between 15 °C and 35 °C, gshoot and groot varied with water viscosity. In a second experiment, the impact of temperature-induced changes in groot on sapling transpiration (E) and leaf water potential (
leaf) was assessed. Intact plants were placed in a growth cabinet with constant air and variable soil temperatures. E increased linearly with soil temperature but leaf remained constant. As a consequence, a linear relationship was found between E and gplant. The results illustrate the significance of gplant for the stomatal control of transpiration and the significance of temperature for tree water transport. Key words: Water relations, temperature, hydraulic conductance, stomata, oak, Quercus robur L., Fagaceae.
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Introduction |
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In temperate woody species, stomata tend to close and leaf transpiration is reduced when soil water deficit increases (for a review see Hinckley and Braatne, 1994
). Consequently, leaf water deficit is controlled and xylem embolism is minimized (Jones and Sutherland, 1991; Cochard et al., 1996). The mechanism of stomatal closure is well documented (Hinckley and Braatne, 1994), but the mechanism by which stomata sense changes in soil dryness is not entirely understood. From a hydrodynamic point of view, a depletion in soil water content results in two kinds of constraints for the plant: one caused by a decrease in the soil water potential (soil) and one caused by a decrease in the hydraulic conductance of the soil–plant continuum (gplant). The first stress determines the leaf water potential (leaf) when transpiration is null, for instance at predawn (leaf equals soil approximately). The second stress develops only when a water flow (E) occurs in the soil–plant continuum. For a given E, gplant determines the drop in leaf below soil as:
 | (1) |
Many studies have demonstrated that stomata respond to changes in soil (Davies and Kozlowski, 1975; Bréda et al., 1993; Lu et al., 1995; Le Quéré et al., 1998). However, the possibility also exists that stomata could directly respond to changes in gplant (Whitehead, 1998). Indeed, for some species under soil drought conditions, a better correlation has been found between E and gplant rather than E and soil. This was the case for temperate oak species (Cochard et al., 1996; Bréda et al., 1993), spruce (Lu et al., 1996) and five tropical species (Meinzer et al., 1995). However, under soil drought conditions both soil and gplant are reduced, and it is then difficult to prove a direct response of stomata to a change in gplant.
The aim of this study was to assess a possible direct impact of gplant on stomatal function. An experiment was designed in which reversible changes in gplant could be operated while soil was kept constant. In a first experiment, the effects of temperature on root and shoot hydraulic conductances were measured. A direct method was used to assess gplant independent of E which was necessary to separate the effect of gplant on E. Then, in a second experiment, the temperature dependence of the root conductance (groot) was used to alter gplant. Stomatal closure following a chilling stress has been reported for many species (Ameglio et al., 1990; Fennell and Markhart, 1998; Bassirirad et al., 1993) and has usually been attributed to a decrease in groot. Therefore, well-watered potted saplings were exposed to a range of soil temperatures and plant transpiration rates and leaf water potentials were measured.
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Materials and methods |
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Experiments were conducted on 6–9-month-old oak saplings (Quercus robur L.). Acorns were germinated in water and transplanted into 5 dm3 plastic pots containing a natural soil from the Mondon forest, in the eastern part of France (soil texture was about 1:1 sand and loam). A slow releasing fertilizer (Nutricote T100) was added to the soil upon planting. Plants were grown at the INRA centre near Nancy (France) in a temperature-controlled greenhouse with daily maximum/minimum temperatures averaging 25/15 °C. Pots were automatically watered twice a day using deionized water.
Plants were used during June (experiment 1) and August 1998 (experiment 2), leaf area was c. 0.3 m2 and shoots were c. 1.3 m long.
Experiment 1
The aim of the first experiment was to quantify the effects of temperature on root and shoot hydraulic conductances (groot and gshoot, mmol s-1 MPa-1 plant-1). Plants were brought to the laboratory and cut a few cm above soil level. Shoots and potted roots were immersed in an aerated tap water bath whose temperature could be adjusted between +1 °C and +50 °C. The gshoot and groot were measured with a High Pressure Flow Meter (HPFM, Tyree et al., 1993; Cochard et al., 1997). In short, the technique consists of measuring the water flow entering root or shoot systems when applying a series of water pressures between 0.1 and 0.5 MPa. Conductances are then derived from the flow/pressure relationships. Sample temperature was measure by a thermocouple either appressed against the bark (shoots) or inserted near the centre of the pot (roots). Bath temperature was first set to 20 °C then decreased to c. 2 °C in 5 °C steps. Bath temperature was then increased to 50 °C in 5 °C or 10 °C steps. For each target temperature, conductances were measured at least 30 min after the temperature had stabilized. Measurements were conducted on five root and three shoot systems.
Experiment 2
The second experiment aimed at assessing the impact of temperature-induced changes in groot on sapling transpiration (E, mmol s-1 plant-1) and leaf water potential (leaf, MPa). Intact potted plants were placed in a growth chamber where light (400 µmol m-2 s-1 at the top of the plant), air temperature (24 °C) and air vapour deficit (18 hPa) were maintained constant throughout the experiment. Pots were enclosed in an insulated box placed above the scale of an analytical balance (0.1 g resolution) inside the chamber. A copper coil, bypassing water from a thermostatted bath, refrigerated the air inside the box. Heat dissipation was effected by a little fan inside the box. The box was not touching the plant, the pot nor the balance in order to record plant transpiration accurately and continuously. Thermocouples were used to measure temperature of the soil, the air inside the box and of the air inside the chamber. Plants, watered to field capacity, were installed in the chamber with a target soil temperature set to 25 °C. After c. 12 h the soil was rewatered to field capacity. After a further 12 h, leaf water potentials were measured on three leaves with a pressure chamber. The same protocol was repeated on the same plant the following 5–6 d with different soil temperatures. The whole experiment was repeated for three plants. Soil temperature was adjusted between c. 7 °C and 40 °C in 10 °C steps following different pathways (increase then decrease or decrease then increase).
Whole plant hydraulic conductance (gplant, mmol s-1 MPa-1 plant-1) was computed as:
 | (2) |
soil has been analysed by Muromtsev (Muromtsev, 1981) and discussed by Kramer (Kramer, 1983). Because the soil was well-watered throughout the experiments, it can be concluded that temperature had virtually no effect on soil and that soil=0 MPa. |
Results |
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Results from experiment 1 are shown in Fig. 1
. Although the organs were perfused for several hours, the time-dependent changes in hydraulic conductance were negligible. When the temperature was decreased from 20 °C to 2 °C and returned to 20 °C after c. 4 h, only a 4.2% decrease in the hydraulic conductance was noticed. Because absolute values varied from plant to plant or between root and shoot (Fig. 1a), conductance values were divided, for each sample, by the conductance measured at 20 °C (Fig. 1b). Changes in organ temperature resulted in large variations in groot and gshoot. For example, from 20 °C to 2 °C, a c. 50% decrease in conductance was noticed. Between 15 °C and 35 °C, the variations in conductance could entirely be ascribed to variations in water viscosity (plain line in Fig. 1b; data from Lide, 1996). Below 15 °C, the decreases in groot and gshoot were c. 10% higher than the decrease in water fluidity. Above 35 °C, groot and, mostly, gshoot values increased much more than water fluidity.
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Results from experiment 2 are shown in Fig. 2
. Plant transpiration decreased linearly with decreasing soil temperature (Fig. 2a). From 40 °C to 7 °C, an 80% decrease in E was measured. However, leaf water potentials remained nearly constant (Fig. 2b). As a consequence, whole plant hydraulic conductance, gplant increased with soil temperature (Fig. 2c) and gplant was linearly correlated with E (not shown). Changes in water fluidity largely accounted for the variations in gplant (thick plain line in Fig. 2c).
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Discussion |
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The objective of this study was to assess the effect of plant hydraulic conductance (gplant) on plant transpiration (E). gplant was altered by changing the soil temperature and the impact on E was measured (experiment 2). However, the determination of gplant in such experiments is mathematically linked to E (see equation 2). It was therefore necessary to determine the dependence of gplant on temperature independently of E (experiment 1). This assumes that the HPFM technique correctly estimated groot and gshoot. Although this assumption may be questionable because, with the HPFM technique, positive pressures are applied which fill the intercellular spaces (Tyree et al., 1999
), there is evidence from the literature that this problem is minor and that the HPFM yields correct values (Yang and Grantz, 1996; Tsuda and Tyree, 1997). The comparison of the gplant values obtained during the two experiments of this study gives further credit to the HPFM technique. Indeed, the mean gplant derived from E and leaf was 0.24±0.03 SE (n=3) mmol s-1 MPa-1 at 20 °C, little different of the gplant value measured with the HPFM (0.236 mmol s-1 MPa-1 resulting from groot=0.38±0.12 SE (n=5) and gshoot=0.61±0.25 SE (n=3) mmol s-1 MPa-1). The two experiments were therefore relevant to distinguish the effects of changes in plant conductance on transpiration.
Temperature greatly affected root and shoot hydraulic conductances of Quercus robur. In the literature, changes in groot with temperature have been attributed to changes in membrane fluidity and permeability (Améglio et al., 1990; Carvajal et al., 1996), or changes in water viscosity (Lopez and Nobel, 1991; Hertel and Steudle, 1997). Water viscosity was mostly responsible for the variation of groot in this study. However, for temperature below 15 °C and above 35 °C, groot varied more than water viscosity itself. This would suggest that a modification of membrane fluidity might have occurred at such temperatures.
As far as is known, direct temperature effects on whole shoots hydraulic conductance have not yet been reported. Temperature effects were as large in shoots as in roots are were also mostly related to water viscosity. The drastic increase in gshoot at high temperatures were irreversible (data not shown) and might have been caused by membrane degradations in the leaf blade.
Direct measurements of the temperature effects on hydraulic conductances were relevant to whole plant response to temperature, as shown by the second experiment. Changes in gplant were also explained by changes in water viscosity, as expected from the dependence of gplant and groot on temperature (Fig. 1
).
Results from the second experiment also validated the hypotheses that, in Quercus, stomata can close in response to the sole decrease in groot and gplant, without the need for a decrease in soil. Plant transpiration responded linearly to temperature-induced changes in gplant. Under drought soil conditions, a linear relationship has also been found between gplant and E in Quercus (Cochard et al., 1996). Other evidence for a coupling between gplant and E can be found in the literature. For instance, Sperry and Pockman demonstrated that, in Betula, stomata were closing when shoot hydraulic conductance was reduced by xylem embolism (Sperry and Pockman, 1993). Using partial defoliation, Meinzer and Grantz have also shown a co-ordination between stomatal and hydraulic conductances in sugarcane (Meinzer and Grantz, 1990). Altogether, these experiments demonstrate that stomata can respond to changes in gplant, independently of the way gplant is altered (temperature, drought, xylem embolism or defoliation). The significance of gplant for the understanding of tree water relations has probably been underestimated, especially on studies dealing with stomatal regulation. The results also raise the issue of the mechanism by which stomata could sense changes in gplant. It has been proposed that a possible effect of gplant is on ABA production in sugarcane (Meinzer and Grantz, 1991). ABA may also have triggered stomatal closure in our experiment because there is evidence for an increase in ABA production in freeze-stressed trees (Bertrand et al., 1994, 1997). However, in Quercus robur, Triboulot et al. (Triboulot et al., 1996) and Fort et al. (Fort et al., 1997) found no evidence for an increase in xylem sap [ABA] when gplant was reduced by drought, so for this species ABA might not be produced in response to a cooling stress as well. Another hypothesis is that E might have been regulated by an hydraulic signal, i.e. by leaf. The constancy of the bulk leaf water potential is an argument against a direct effect of leaf on gs. leaf was nearly constant in this experiment, but, as gplant varied, xylem must have changed. The possibility exists that changes in xylem in the leaf blade may trigger the release of ABA in the leaves (Whitehead, 1998). Indeed, Tardieu and Davies developed a model for stomatal response to soil drought that combines hydraulic and chemical signals (Tardieu and Davies, 1993). The possibility also exists that a drop in gplant may induce a transient drop leaf which would promote a stomatal closure. Direct measurements in the leaf xylem and the leaf mesophyll with the pressure probe technique (Tomos and Leigh, 1999) may validate these hypotheses.
These data also illustrate the significance of temperature for plant water relations. Wood temperature can fluctuate considerably within a day or from day to day under field conditions. For instance, these fluctuations reached 20 °C in beech branches measured in eastern France during the 1997 growing season (personal observations). Root and soil temperatures were more buffered. Little attention has been paid to the impact of such temperatures on plant hydraulic conductances. However, when the temperature increases from 15 °C to 35 °C, gshoot doubles (Fig. 1). The impact on gplant is lower and depends on the ratio between groot and gshoot. The impact on tree transpiration is less predictable because air vapour pressure deficit also changes with temperature, but is certainly not negligible and should be considered.
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Notes |
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3 To whom correspondence should be addressed. Fax: +33 4 73 62 44 54. E-mail: cochard{at}clermont.inra.fr
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