Journal of Experimental Botany, Vol. 52, No. 362, pp. 1835-1846,
September 1, 2001
© 2001 Oxford University Press
Original Papers |
Hydraulic conductivity of rice roots
1 Lehrstuhl Pflanzenökologie, Universität Bayreuth, Universitätsstrasse 30, D-95440 Bayreuth, Germany
2 Faculty of Agriculture, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai-cho, Fuchu, 183-8509 Tokyo, Japan
3 International Rice Research Institute, DAPO 7777, Metro Manila, Philippines
Received 9 October 2000; Accepted 8 May 2001
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Abstract |
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A pressure chamber and a root pressure probe technique have been used to measure hydraulic conductivities of rice roots (root Lpr per m2 of root surface area). Young plants of two rice (Oryza sativa L.) varieties (an upland variety, cv. Azucena and a lowland variety, cv. IR64) were grown for 31–40 d in 12 h days with 500 µmol m-2 s-1 PAR and day/night temperatures of 27 °C and 22 °C. Root Lpr was measured under conditions of steady-state and transient water flow. Different growth conditions (hydroponic and aeroponic culture) did not cause visible differences in root anatomy in either variety. Values of root Lpr obtained from hydraulic (hydrostatic) and osmotic water flow were of the order of 10-8 m s-1 MPa-1 and were similar when using the different techniques. In comparison with other herbaceous species, rice roots tended to have a higher hydraulic resistance of the roots per unit root surface area. The data suggest that the low overall hydraulic conductivity of rice roots is caused by the existence of apoplastic barriers in the outer root parts (exodermis and sclerenchymatous (fibre) tissue) and by a strongly developed endodermis rather than by the existence of aerenchyma. According to the composite transport model of the root, the ability to adapt to higher transpirational demands from the shoot should be limited for rice because there were minimal changes in root Lpr depending on whether hydrostatic or osmotic forces were acting. It is concluded that this may be one of the reasons why rice suffers from water shortage in the shoot even in flooded fields.
Key words: Apoplastic barriers, composite transport model, hydraulic conductivity, pressure probe, root, rice, water relations.
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Introduction |
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It is well known that the hydraulic properties of roots vary with species and environmental conditions (Brewig, 1937
; Brouwer, 1954; Weatherley, 1982; Kramer and Boyer, 1995); these factors strongly influence root anatomy and morphology (Steudle and Peterson, 1998; Steudle, 2000a). Water uptake by roots can be regulated by physical and physiological processes (Steudle, 2000b, 2001). A composite transport model has been established to explain the variable permeability of roots to water (root hydraulic conductivity, Lpr) (Steudle and Frensch, 1996; Steudle and Peterson, 1998; Steudle, 2000b). In the model, three parallel pathways for water movement in the root cylinder are considered, i.e. the apoplastic, symplastic and transcellular pathways, the latter two representing the cell-to-cell path. In the presence of apoplastic barriers (Casparian bands, suberin lamellae), the amount of water that flows along the apoplast will be limited. On the other hand, water channel (aquaporin) activity in the plasma membranes of root cells affects the cell-to-cell component of radial water flow. Water uptake (root Lpr) usually represents the biggest resistance to the flow of liquid water in the plant. Its regulation could be the result of varying the contribution of each component. In addition, osmotic and hydrostatic pressures will cause different flow intensities through the apoplast, i.e. root Lpr depends on the nature of driving forces. Overall, the composite transport model provides both a coarse regulation of root Lpr (switching between the preferred path for water) that is purely physical in nature, and a fine regulation that is under metabolic control (water channel activity). The model allows for a rapid uptake of water from the soil, when the demand from the shoot is large (high tensions in root xylem; Steudle, 2001). On the other hand, when the soil is dry, the hydraulic resistance of the root will be great and may limit water losses into the dry soil. Hence, the model would explain the variability in root hydraulic conductivity in terms of useful adaptive mechanisms that provide regulation of water uptake.
Even for rice crops in paddy fields, where supply from the wet soil should be no problem, water shortage has been reported (Ishihara and Saito, 1987; Jiang et al., 1988; Hirasawa et al., 1992, 1996). Rice roots have developed apoplastic barriers such as an endo- and exodermis with Casparian bands and layers of cortical sclerenchyma with exceptionally thick, lignified walls (Morita and Abe, 1999). These may contribute to the observed problems with water uptake in this important crop. Data about root hydraulics are required to understand mechanisms of water uptake by rice roots, and to assess the extent to which root properties limit crop water use.
In this paper, basic studies on the ability of rice roots to take up water are reported and it is shown that there is little or no flexibility of Lpr in response to environmental conditions that bring about marked changes in maize (Zimmermann and Steudle, 1998; Freundl et al., 2000). Neither were there significant differences in the behaviour or the anatomy of a paddy and an upland variety. Transport properties were examined with osmotic and hydrostatic driving forces or steady-state and transient water flows, using pressure chambers and root pressure probes (Steudle, 1993). The results show that the hydraulic conductivity of rice roots is relatively low (compared with other herbaceous species) and that it does not adapt to any significant extent to the changing environmental conditions employed.
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Materials and methods |
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Plant material
Seeds of rice (Oryza sativa L.: upland cultivar Azucena and lowland cultivar IR64) were germinated in the light in the climatic chamber used for plant growth (see below) on tissue soaked with tap water for 5–6 d. During this time, seedlings developed roots of up to 20 mm long and shoots of up to 35 mm tall (1st leaf emergence). The seedlings were transferred to a hydroponic culture system consisting of boxes of nutrient solution (10 l), which accommodated 24 seedlings per box. The nutrient solution contained 0.09 mM (NH4)2SO4, 0.05 mM KH2PO4, 0.05 mM KNO3, 0.03 mM K2SO4, 0.06 mM Ca(NO3)2, 0.07 mM MgSO4, 0.11 mM Fe-EDTA, 4.6 µM H3BO3, 1.8 µM MnSO4, 0.3 µM ZnSO4, 0.3 µM CuSO4 (pH=5.5–6.0). After 2–4 d, aeration of the nutrient solution began. Nutrient solution was completely renewed every 7 d with solution adjusted to chamber temperature. Half the seedlings were transferred to an aeroponic culture system. Concentration of nutrient solution for the aeroponic system was 2-fold greater than that used for hydroponics. Using two plastic discs with slits, seedlings were fixed on top of a round polyvinyl chloride box (diameter: 0.45 m; depth 0.6 m). Roots protruded into the box through the slits. At the bottom of the box, there was an air humidifier, which continuously produced mist (Defensor, Barth&Stoecklein, Garching, Germany). Both culture systems were placed in a climatic chamber (day/night rhythm: 12/12 h; 27/22 °C, light intensity: 500 µmol m-2 s-1). Plants used in experiments were grown for 31–40 d including the time for germination. When used, root systems of young plants of IR64 from hydroponic culture were 265–515 mm long. The overall shoot length was 325–445 mm (8th–11th leaf emergence). Plants grown in aeroponic culture had root system and shoot lengths of 320–630 mm and 290–410 mm, respectively (7th–8th leaf emergence). Young plants of Azucena grown in hydroponics developed 385–610 mm of root systems and 485–570 mm of shoots (8th–11th leaf emergence). For the plants grown in aeroponics, length of root systems and shoots was 390–720 mm and 340–440 mm, respectively (7th–8th leaf emergence). Overall, Azucena (i.e. the upland variety) grew somewhat faster in both hydroponics and aeroponics than IR64 (the lowland rice variety). Diameters of adventitious roots from hydroponics and aeroponics for IR64 were up to 1.1 mm and 0.9 mm, respectively. Those for Azucena were up to 1.3 mm and 1.1 mm, respectively. Diameters of stele from hydroponics and aeroponics for IR64 were up to 190 µm and 135 µm, respectively. Those for Azucena were up to 280 µm and 260 µm, respectively.
Root anatomy and surface area of root system
Freehand cross-sections were prepared from adventitious roots. Cross-sections were made at different distances from the root tip (10, 20, 40, 60, 80, 100, 150, 200, 250 mm). They were stained for 1.5 h with Sudan Red 7B at room temperature (Brundrett et al., 1991). Sections were viewed under an optical microscope (DIALUX 22 EB, Leitz, Germany). For photographs, Kodak Elite 64 ASA film was used.
Surface areas of root systems were determined using a video camera and an image analysing software (Skye Instruments, Llandrindod Wells, UK). For better contrast, roots were stained with toluidine blue O (0.03% w/v). Surface areas of root systems were calculated from projected areas of roots that were assumed to be cylindrical in shape. The system was calibrated using metal wires of known length and diameter. For IR64, surface areas of root systems from hydroponics and aeroponics ranged between (1.1–3.5)x10-2 m2 and (1.7–5.4)x10-2 m2, respectively. Those for Azucena were (2.2–2.7)x10-2 m2 and (1.2–2.6)x10-2 m2, respectively.
Measurement of root exudation in the absence of hydrostatic pressure gradients (osmotic exudation)
Before starting these measurements, shoots were cut off using razor blades at distances of 40–70 mm from the base. All tillers except the main stem were closed using clamps. With the aid of a syringe, xylem sap exuding from the main stem was collected at the cut surface. It was collected in Eppendorf tubes and weighed (Fig. 1A). In the absence of hydrostatic pressure gradients, differences in osmotic pressure (
in MPa) between the medium (RTxC°) and xylem sap (RTxCi) drove the water uptake by the root, i.e.:
 | (1) |
sr denotes the reflection coefficient of solutes, which was determined from experiments with the root pressure probe described below. To calculate root Lpr, a value of sr=0.4 was used (see below). Osmotic concentration of the medium and of the xylem sap was measured using a freezing-point depression osmometer (Osmomat 030; Gonotec, Berlin, Germany). The osmotic pressure of nutrient solution was 0.0075 MPa.
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Measurement of root exudation in the presence of hydrostatic pressure gradients
Plants used for measuring osmotic water flow were also employed to measure hydraulic conductivity of root systems in the presence of hydrostatic pressure gradients. During these measurements, roots were enclosed into a steel chamber to apply pneumatic pressure to the root medium (Fig. 1A
). The base was tightly sealed using silicone seals which were prepared with a hole which had a diameter already adjusted to that of the base of main stem. The seal was cut longitudinally. For the fine adjustment of the seal, flexible rubber material (Terostat, Germany) was used, which was placed in the two halves of the seal. The pressure in the chamber was raised in steps of 0.03–0.05 MPa up to 0.35 MPa above atmospheric. Exuded xylem sap was collected as described above and weighed. For a given applied gas pressure (Pgas in MPa), the volume exuded from the root system (V in m3) was plotted against time. The slopes of these relations were calculated and referred to unit surface area. This yielded the volume flow, JVr in m3 m-2 s-1. There was no axial water flow across the aerenchyma, because this was interrupted by the seal. Since there is a connection between vascular bundles of tillers with those of the main stem (Hanada, 1993), it was assumed that roots from tillers transport water to the main stem and that there is no difference in the resistance to water transport among roots from main stem and tillers. A possible effect of roots emerged from tillers has been tested for in experiments where plants were grown without tillers in hydroponics. In hydrostatic experiments, the hydraulic conductivity of root systems (Lpr in m s-1 MPa-1) was similar in both cases. Root Lpr was calculated from the slopes of JVr against driving forces (Pgas+sr) according to the following relation:
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sr is the root reflection coefficient for nutrient salts in the xylem which was estimated to be sr=0.4. This value was the upper limit of the reflection coefficient found for NaCl which was assumed to be similar to that of the salts in the xylem solution according to earlier results for maize (Steudle and Peterson, 1998). The effect of the osmotic term was not very pronounced in the range of higher values of Pgas. Measured values of were used to calculate the overall driving force in Equation (1). Alternatively, Lpr was determined from plots of JVr against Pgas. Slopes of the plots were non-linear in the range of low forces, i.e. root Lpr depended on the magnitude of water flow as found for other species (Fiscus, 1975; Rüdinger et al., 1994). Lpr was determined from the linear part of pressure/flow curves (high pressure gradients, Pgas), where the osmotic component of the driving force was small due to dilution effects.
Root pressure probe measurements
Root pressure probe measurements were carried out as described previously (Steudle et al., 1987; Steudle and Frensch, 1989). Using a cylindrical silicone seal which was prepared from liquid silicone material (Xantopren; Bayer, Leverkusen, Germany), excised end segments of individual roots (root tips) were tightly connected to a root pressure probe (Fig. 1B). Segments had lengths of 125–235 mm and diameters of 0.7–1.2 mm for Azucena or 0.5–0.9 mm for IR64. Inner diameters of seals were adapted to diameters of individual root segments and adjusted by a screw. Seals were water-tight even at pressures of several bars, but did not interrupt water flow in the xylem. After each measurement, the proper function of seals was tested by cutting off the root at the seal and controlling the decrease in root presssure and the increase in hydraulic conductivity. When root xylem remained open, root pressure dropped to zero and there was a dramatic decrease in half-time after the cut (increase of hydraulic conductance). Otherwise, the experiment was discarded which happened with about one-third of the roots used. Root segments fixed to the probe were bathed in aerated nutrient solution (the same composition as that used for growth in hydroponic culture) which circulated along the roots to avoid problems with external unstirred layers. The circulation rate was high so that the medium around a root was exchanged within a fraction of a second. Root pressures (Pr in MPa) were measured with a pressure transducer and recorded. Usually, it took over 5 h to establish stable root pressures. Hydrostatic and osmotic relaxations were performed by either changing the xylem pressure (moving the metal rod in the probe) or the osmotic pressure of the medium. Transient responses in pressure were followed which allowed Lpr to be calculated from rate constants, krw, or half-times of pressure relaxations (T 1/2w) according to the following relation (Steudle et al., 1987):
 | (3) |
Pr/Vs (in MPa m-3) is the elastic coefficient of the measuring system; Vs denotes the water volume of the system, and Ar is the surface area of the root. The ratio of Pr/Vs was measured by inducing step changes in the volume by moving the metal rod in the probe and recording the resulting changes in root pressure (Pr). Root surface area was calculated from its length and diameter. Test solutions used in osmotic experiments were prepared by adding NaCl or ethanol to tap water. Osmotic pressure of added solutes ranged between 0.12 and 0.25 MPa (50 and 100 mOsmol kg-1) and 0.23 and 0.63 MPa (92 and 250 mOsmol kg-1), respectively. These concentrations were not toxic to the roots as shown by a constant root pressure. Root pressure is sensitive to toxic substances (e.g. heavy metals) which affect the active pumping of nutrients to the root xylem. Responses of root pressure to changes of osmotic pressure of the medium were biphasic. There was a rapid water phase (water efflux or influx) followed by a slower solute phase (water dragged by solute diffusion). From the solute phase the permeability coefficient for given solutes (Psr in m s-1) was calculated:
 | (4) |
sr) were calculated from (Steudle et al., 1987):
 | (5) |
is the change in osmotic pressure of medium and tmin the time required to reach the minimum.
Cutting experiments
Information on the development of xylem vessels was obtained from cutting experiments. Roots attached to the root pressure probe were successively excised from the tip step by step using a razor brade. Substantial drops in Pr were observed when mature xylem was cut and xylem sap leaked out into the medium.
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Results |
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Root anatomy: development of adventitious roots
There were no visible differences in the development of endodermis, exodermis and aerenchyma between the two varieties and growth conditions. Therefore, photographs taken from cross-sections of adventitious roots are only shown for IR64 (the lowland variety) in Fig. 2
. Aerenchyma was completely developed at the distance of 150 mm from the tip (Fig. 2A). At a distance of 40 mm from tips, roots developed a secondary endodermis, with suberin depositions on inner cell walls at the endodermis (Sudan Red staining; Fig. 2B). Passage cells were not stained. Tertiary development (cell wall thickening on suberin lamellae) of the endodermis was observed at a distance of 100 mm from the tip. The exodermis, which is a hypodermis with Casparian bands, developed at distances of 40 mm from the tip and suberin depositions were detected. With the plants used (age: 31–40 d) tertiary wall thickening in the exodermis was never seen. Highly lignified sclerenchyma tissue was found below the exodermis. At a distance of 20–40 mm from the root tip, cortical cells started to collapse and aerenchyma developed.
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Steady-state hydraulic experiments
At a given Pgas, exuded volumes, V, increased linearly with time as shown in Fig. 3A. In Fig. 3B, water flows are plotted against both the gas pressure applied to the root systems (Pgas) and the overall driving force P=Pgas+sr. The slope was found to become steeper as Pgas or JVr increased. This means that Lpr was low at low P or flow rates and increased with increasing driving force to reach a maximum value usually at pressure differences of 0.05–0.15 MPa. It can be seen that at high water flow, slopes were similar, because xylem sap was strongly diluted, and the osmotic term did not contribute much to the overall driving force in this range. Maximum Lpr values are reported in this paper. Mean Lpr values (±SD) of Azucena grown in hydroponics and aeroponics were (6.3±3.1)x10-8 m s-1 MPa-1 and (7.4±4.2)x10-8 m s-1 MPa-1, respectively (Table 1). Those of IR64 were (5.6±2.7)x10-8 m s-1 MPa-1 and (4.0±1.9)x10-8 m s-1 MPa-1, respectively. Only for IR64 grown in aeroponics Lpr were values significantly smaller than those of Azucena grown in aeroponics (t-test; 
=0.05).
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Osmotic exudation experiments
Osmotic exudation rate was measured at an external osmotic concentration of 0.0075 MPa. Osmotic Lpr was calculated from the osmotic exudation rate per unit surface area of root system (Ar) divided by the reflection coefficient (sr=0.4) and the osmotic pressure difference between xylem sap and medium. Osmotic Lpr of roots of Azucena grown in hydroponics and aeroponics were (5.5±3.7)x10-8 m s-1 MPa-1 and (2.8±1.5)x10-8m s-1 MPa-1, respectively (Table 1). Those of IR64 were (4.2±2.5)x10-8 m s-1 MPa-1 and (3.6±1.3)x10-8m s-1 MPa-1, respectively. Only for Azucena grown in hydroponics, were osmotic Lpr values significantly bigger than those of IR64 grown in aeroponics. Except for Azucena grown in aeroponics, the values of osmotic and hydrostatic Lpr were similar. It can be seen from Table 1 that except for Azucena grown in aeroponic culture, ratios between hydrostatic and osmotic Lpr were not significantly different from unity, although mean values were greater than unity in all cases.
Root pressure probe measurements
5-12 h after root segments were connected to a root pressure probe, steady root pressures were established. Values varied between 0.07 and 0.40 MPa. Hydrostatic Lpr was calculated from pressure relaxation curves that resulted from induced water flow (see Materials and methods; Fig. 4A). The values for hydroponic plants of Azucena and IR64 were (4.7±1.0)x10-8 m s-1 MPa-1 and (5.0±2.5)x10-8 m s-1 MPa-1, respectively (Table 2). Those for aeroponic plants were (3.1±1.3)x10-8 m s-1 MPa-1 and (2.3±1.1)x10-8m s-1 MPa-1, respectively. From the water phase of biphasic osmotic relaxations, osmotic Lpr was calculated (Fig. 4B). For hydroponic plants of Azucena and IR64, osmotic Lpr were (4.0–3.8)x10-8 m s-1 MPa-1 and (9.2–10.3)x10-8 m s-1 MPa-1, respectively. Those of aeroponic plants were (2.0–5.4)x10-8 m s-1 MPa-1 and (2.1–2.9)x10-8 m s-1 MPa-1, respectively. The conclusion from the Lpr values given in Table 2 is that osmotic and hydrostatic values obtained in root pressure probe experiments were statistically not different except for osmotic Lpr for IR64 grown in hydroponics. They were almost identical to the values obtained during steady-state experiments except for osmotic Lpr for IR64 grown in hydroponics (Table 1). The result differed markedly from results obtained earlier with maize. For this species, hydrostatic Lpr was much bigger than the osmotic (Table 2).
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As shown in Fig. 4B
and C, apparent water flow reached zero after some time. The osmotic pressure of the medium was then changed and apparent water flow changed its direction according to the influx or efflux of solutes, which increased or decreased the osmotic pressure in the xylem. From rate constants of solute phases, permeability coefficients of the two solutes were determined (Psr in m s-1). Psr values of ethanol and NaCl for both cultivars were similar (). In contrast to the water permeability, there were significant decreases of solute permeabilities of NaCl in roots of IR64 grown in aeroponics as compared with hydroponics. The value of 0.3–0.4 of the reflection coefficient (sr) for NaCl was significantly greater than that of ethanol (sr=0.1), but treatment (hydroponics versus aeroponics) did not affect the absolute values of reflection coefficients. When comparing the rice data of Psr and sr with those for maize, it can be seen that in most cases, Psr for rice grown in aeroponics was smaller for rice than for maize. Since the values used for Vx were probably upper limits, Psr values calculated according to Equation (4) are probably upper limits, and the differences could have been even bigger. At the same time, sr values of rice were smaller by a factor of two than those of maize.
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Cutting experiments
At the ends of root pressure probe measurements, cutting experiments were performed. Pr dropped to near zero after 40 mm of segments were cut (Fig. 5A). After each cut, hydrostatic pressure relaxations were performed. At a distance of 70 mm from tip, T 1/2w was decreased to about 10% of the original value for the intact segment (Fig. 5B). Hence, the hydraulic resistance of severed roots remaining at the seal was much less than that of intact root segments. This proved that during the experiments, the radial water flow across the roots rather than a resistance created at the base during sealing was measured (see above).
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Discussion |
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As far as is known, the first detailed set of data of the hydraulic properties of rice roots is presented in this paper. Different varieties (lowland and upland) have been used which were grown under different conditions (hydroponic and aeroponic culture). Experience with other species (see reviews by Steudle and Peterson, 1998
; Steudle 2000a, b, 2001) has shown that hydrostatic and osmotic driving forces would change the relative contributions of water flow via the apoplastic and cell-to-cell pathways, resulting in substantial changes in the hydraulic conductivity of roots (Lpr). Conditions of either steady (pressure chamber) and transient (root pressure probe) water flow were also employed. In parallel with the measurements of root Lpr, the structure of roots was examined to see if this was different for the two varieties and if it varied when they were grown under different conditions.
The root anatomy, revealed by freehand cross-sections, did not differ for the two cultivars or for roots grown in hydro- and aeroponics. Hence it is not surprising that absolute values of root Lpr were similar in the lowland (IR64) and upland (Azucena) varieties. The use of different driving forces did not cause significant changes of root Lpr. In contrast to other species, there was no or little switching in root Lpr. In maize, differences were as large as up to an order of magnitude (Frensch and Steudle, 1989; Steudle and Frensch, 1989; Zimmermann and Steudle, 1998; Steudle and Peterson, 1998). In maize, the hydrostatic root Lpr was similar to that of the Lp of individual root cells. It was concluded that most of the water was flowing in the apoplast around protoplasts under these conditions, even in the exo- and endodermis of young roots. On the other hand, osmotic water flow was from cell to cell, and this probably explained the lower root Lpr and higher hydraulic resistance under these conditions. For tree roots, differences between hydraulic and osmotic flow were even larger (Steudle and Heydt, 1997). In rice, one may tend to attribute the similarity between osmotic and hydraulic Lpr to the existence of an exodermis and fibre tissue (sclerenchyma) in the outer parts of the roots which were present during all treatments and in both varieties. However, this conclusion should be made cautiously, because the walls of the endodermis appeared to be quite suberized and heavily lignified and may impede water flow along the apoplastic path.
There was some variability between half-times of water exchange which were between 5 and 240 s during both osmotic and hydrostatic experiments. Although this was somewhat longer than for other species, relaxations were, on average, still rather fast, considering the structure of the roots with the exodermis, sclerenchyma, aerenchyma, and endodermis as potential barriers to water flow. The hydraulic resistance of the aerenchyma may be regarded as low. According to the osmotic experiments, water may flow along the rims of living cells in the strands connecting the stele with the outer root at a rate which was similar to that found during the hydrostatic experiments. During hydrostatic relaxations, changes in water potential (pressure) were produced in the xylem. Only small water volumes are transferred during these experiments. Because air has a high compressibility, the aerenchyma has a rather high potential storage capacity for water and should, therefore, dampen the propagation of changes in pressure in the experiments with the root pressure probe without any significant filling of the lacunae of aerenchyma. Hence, it is considered that the Lpr measured during these experiments largely reflects that of the endodermis/stele rather than of the rest of the root. On the other hand, the root Lpr measured during steady-state (pressure chamber) experiments included both the hydraulic resistance of the outer parts and of the stele. Since both values were similar, it may be concluded that the hydraulic resistance located in the endodermis/stele was substantial. For a definite decision of the relative contribution of outer and inner parts of roots, however, a more detailed separate measurement of the two hydraulic resistances in series would be required. Separation may be achieved by micro surgery or by puncturing the outer parts of the roots (Peterson and Steudle, 1993; Peterson et al., 1993; Steudle et al., 1993). However, this is technically difficult, as is the puncturing of individual root cells with the cell pressure probe to work out the cell-to-cell component of water flow. Cells are small and their walls fairly rigid.
From a comparison with other species it was found that absolute values of root Lpr of rice were similar in some cases but were substantially smaller than those of other herbaceous roots. For example, for roots of bean (Phaseolus coccineus) and barley, root Lpr was the same order as found here for rice (Steudle and Brinckmann, 1989; Steudle and Jeschke, 1983). For others such as onion, bean, and corn, Lpr of roots from hydroponics was substantially greater than found here for rice. However, when comparing the osmotic root Lpr of some of the other species with that of rice, values were similar. For corn roots grown in aeroponics, values were also similar (Table 2). Under these conditions, corn roots develop an exodermis which reduces Lpr by a factor of nearly four (Zimmermann and Steudle, 1998). So, overall the hydraulic conductivity of rice roots grown under comparable conditions appears to be substantially smaller than that of other herbs. Hydrostatic root Lpr would be comparable to that of young tree roots such as spruce, oak, beech or pine (for data, see reviews by Steudle and Peterson, 1998; Steudle and Heydt, 1997).
It should be remembered that these data were gathered from chamber-grown young plants with high root zone aeration. For field-grown rice, root Lpr may be even smaller than the values obtained in this study. It is known that under anaerobic conditions (such as in paddy fields), the radial loss of oxygen across rice roots is substantially decreased (Colmer et al., 1998). This may be due to changes in the structure of the outer part of the root, perhaps, due to a thickening of the fibre tissue. Under these conditions, root Lpr may also decrease; if it does there may be problems for water uptake. So, rice roots growing in stagnant anaerobic substrates would need a rather tight outer boundary to prevent oxygen losses, but this may result in a reduced capability to take up water even from a wet environment. Of course, this problem would only occur for paddy and deepwater rice. For upland rice growing in soils with high oxygen contents, an additional outer barrier may serve no purpose and be a liability for water relations of the shoot. The authors argue that the relatively low values of root Lpr of rice are due to the anatomical structure of these roots, namely, the existence of efficient apoplastic barriers (endodermis, exodermis and lignified sclerenchyma; Morita and Abe, 1999; Clark and Harris, 1981).
Although differences were not significant, there was a tendency for the pressure-driven water flow to be larger than the osmotic. This trend is in line with the finding that there was a substantial flow of NaCl across the apoplastic barriers. However, the solute permeability (Psr) measured in rice was smaller than in maize lacking an exodermis. It was larger than or similar to the salt permeability of species which have a dominating cell-to-cell flow of water (Steudle and Brinckmann, 1989). For rice, an apoplastic bypass flow of NaCl has been reported by Flowers and co-workers (Yeo et al., 1987; Yadav et al., 1996; Garcia et al., 1997). These authors showed that NaCl as well as the apoplastic tracer PTS were dragged apoplastically into the root xylem along with the transpiration stream. The permeability studies with NaCl performed in this paper are in line with these observations, although Psr may be less than in corn. In rice, the permeability of NaCl was similar to that of ethanol which should move rapidly because it also crosses cell membranes.
Experiments of the type shown in this paper need to be done on field-grown plants to verify that low values of root Lpr are of wider significance. Usually, roots from the field are more intensely suberized than those from hydroponics or aeroponics (Stasovsky and Peterson, 1993). If this is true for rice, hydraulic conductivities of plants from the field may be even smaller than those reported here.
In conclusion, the results show that, compared with other herbaceous species, rice roots offer a rather high hydraulic resistance to water flow. Concomitantly, the apoplastic solute (NaCl) permeability is reduced. The data indicate that effects are caused by the existence of substantial apoplastic transport barriers. Values of root Lpr were the same when water was driven by either hydrostatic or osmotic forces and this implies that rice plants may not be able to meet higher transpirational demands from the shoot. The salient features of the structure of roots need to be clearly understood in relation to their effects on the low hydraulic conductivity. Without such knowledge much effort in breeding rice varieties that can well grow under conditions of reduced water supply in upland areas may be wasted. The results suggest that apoplastic barriers in the peripheral layers (exodermis/sclerenchyma) and in the endodermis are of great functional significance. It may be worthwhile to screen for genotypes with less developed apoplastic barriers or with barriers exhibiting a different chemical composition (Schreiber et al., 1999; Zimmermann et al., 2000). This approach is not discouraged by the lack of any readily observable differences in structure or root Lpr in the two contrasting varieties used here. Perhaps an alternative approach would be to manipulate the cell-to-cell pathway so as to increase its conductivity. Current opinion suggests that this conductivity is strongly dependent on the density or activity of water channels (aquaporins) in the plasma membranes of root cells (Tyerman et al., 1999; Kjellbom et al., 1999). Genes that encode for plasma membrane aquaporins have been cloned and rice can be routinely transformed. It remains to be seen how much scope there can be for increasing the expression of membrane proteins which are, in wild-type plants, very abundant.
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We thank Professor DT Clarkson, IACR-Long Ashton Research Station, University of Bristol, UK, and Dr TD Colmer, Faculty of Agriculture, University of Western Australia, Perth, for their critical reading and discussion of the manuscript, and Drs T Henzler and HM Zimmermann (Lehrstuhl Pflanzenökologie, University of Bayreuth) for their collaboration. The excellent technical assistance of Burkhard Stumpf (Lehrstuhl Pflanzenökologie, University of Bayreuth) is gratefully acknowledged.
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To whom correspondence should be addressed. Fax: +49 921 552564. E-mail: ernst.steudle{at}uni\|[hyphen]\|bayreuth.de
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|---|
Brewig A. 1937. Permeabilitätsänderungen der Wurzelgerwebe, die vom Spross beeinflusst werden. Zeitschrift für Botanik 31, 481–540.
Brouwer R. 1954. The regulation influence of transpiration and suction tension on the water and salt uptake by roots of intact Vicia faba plants. Acta Botanica Neerlandica 3, 264–312.[Web of Science]
Brundrett MC, Kendrick B, Peterson CA. 1991. Efficient lipid staining in plant material with Sudan red 7B or Fluorol yellow 088 in polyethylene glycol-glycerol. Biotechnology and Histochemistry 66, 111–116.
Clark LH, Harris WH. 1981. Observations on the root anatomy of rice (Oryza sativa L.). American Journal of Botany 68, 154–161.
Colmer TD, Gibberd MR, Wiengweera A, Tinh TK. 1998. The barrier to radial oxygen loss from roots of rice (Oryza sativa L.) is induced by growth in stagnant solution. Journal of Experimental Botany 49, 1431–1436.
Fiscus E. 1975. The interaction between osmotic- and pressure-induced water flow in plant roots. Plant Physiology 55, 917–922.
Fiscus EL. 1986. Diurnal changes in volume and solute transport coefficients of Phaseolus roots. Plant Physiology 80, 752–759.
Frensch J, Steudle E. 1989. Axial and radial hydraulic resistance to roots of maize. Plant Physiology 91, 719–726.
Freundl E, Steudle E, Hartung W. 2000. Apoplastic transport of abscisic acid through roots of maize: effect of the exodermis. Planta 210, 222–231.[Web of Science][Medline]
Garcia A, Rizzo CA, Ud-Din J, Bartos SL, Senadhira D, Flowers TJ, Yeo AR. 1997. Sodium and potassium transport to the xylem are inherited independently in rice, and the mechanism of sodium–potassium selectivity differs between rice and wheat. Plant, Cell and Environment 20, 1167–1174.
Hanada K. 1993. Tillers. In: Matsuo T, Hoshikawa K, eds. Science of the rice plant, Vol. 1. Morphology. Tokyo: Food and Agriculture Policy Research Center, 222–258.
Hirasawa T, Tenmyo N, Suyuki M, Ishihara K. 1996. Mechanism on occurrence of white head of rice plants at heading stage under high temperature, low humidity and high wind velocity conditions: factors increasing stem resistance to water flow at the panicle base. Japanese Journal of Crop Science 65, (Extra issue 2) 129–130.
Hirasawa T, Tsuchida M, Ishihara K. 1992. Relationship between resistance to water transport and exudation rate and the effect of the resistance on the midday depression of stomatal aperture in rice plants. Japanese Journal of Crop Science 61, 145–152.
Ishihara K, Saito K. 1987. Diurnal course of photosynthesis, transpiration and diffusive conductance in the single-leaf of rice plants grown in the paddy field under submerged condition. Japanese Journal of Crop Science 56, 8–17.
Jiang CZ, Hirasawa T, Ishihara K. 1988. Physiological and ecological characteristics of high yielding varieties in rice plants. II. Leaf photosynthetic rate. Japanese Journal of Crop Science 57, 139–145.
Kjellbom P, Larsson C, Johansson I, Karlsson M, Johanson U. 1999. Aquaporins and water homeostasis in plants. Trends in Plant Science 4, 308–314.[Web of Science][Medline]
Kramer PJ, Boyer JS. 1995. Water relations of plants and soil. Orlando: Academic Press.
Melchior W. Steudle E. 1993. Water transport in onion (Allium cepa L.) roots. Changes of axial and radial hydraulic conductivities during root development. Plant Physiology 101, 1305–1315.[Abstract]
Morita S, Abe J. 1999. Perspective of root research. Japanese Journal of Crop Science 68, 453–462.
Newman EI. 1973. Permeability to water of five herbaceous species. New Phytologist 72, 547–555.
Peterson CA, Murrmann M, Steudle E. 1993. Location of major barriers to water and ion movement in young roots of Zea mays L. Planta 190, 127–136.
Peterson CA, Steudle E. 1993. Lateral hydraulic conductivity of early metaxylem vessels in Zea mays L. roots. Planta 189, 288–297.
Rüdinger M, Hallgren SW, Steudle E, Schulze ED. 1994. Hydraulic and osmotic properties of spruce roots. Journal of Experimental Botany 45, 1413–1425.
Schreiber L, Hartmann K, Skrabs M, Zeier J. 1999. Apoplastic barriers in roots: chemical composition of endodermal and hypodermal cell walls. Journal of Experimental Botany 50, 1267–1280.
Stasovsky E, Peterson CA. 1993. Effects of drought and subsequent rehydration on the structure, vitality and permeability of Allium cepa adventitious roots. Canadian Journal of Botany 58, 577–588.
Steudle E. 1993. Pressure probe techniques: basic principles and application to studies of water and solute relations at the cell, tissue, and organ level. In: Smith JAC, Griffith H, eds. Water deficits: plant responses from cell to community. Oxford: Bios Scientific Publications, 5–36.
Steudle E. 2000a. Water uptake by roots: effects of water deficit. Journal of Experimental Botany 51, Special Issue, 1531–1542.
Steudle E. 2000b. Water uptake by roots: an integration of views. Plant and Soil 226, 45–56.[Web of Science]
Steudle E. 2001. The cohesion–tension mechanism and the acquisition of water by plant roots. Annual Review of Plant Physiology and Plant Molecular Biology 52, 847–875.[Web of Science][Medline]
Steudle E, Brinckmann E. 1989. The osmometer model of the root: water and solute relations of roots of Phaseolus coccineus. Botanica Acta 102, 85–95.
Steudle E, Frensch J. 1989. Osmotic responses of maize roots. Planta 177, 281–295.
Steudle E, Frensch J. 1996. Water transport in plants: role of the apoplast. Plant and Soil 187, 67–79.
Steudle E, Heydt H. 1997. Water transport across tree roots. In: Rennenberg H, Eschrich W, Zeigler H, eds. Trees—contribution to modern tree physiology. Leiden: Backhuys Publishers, 239–255.
Steudle E, Jeschke WD. 1983. Water transport in barley roots. Measurements of root pressure and hydraulic conductivity of roots in parallel with turgor and hydraulic conductivity of root cells. Planta 158, 237–248.
Steudle E, Murrmann M, Peterson CA. 1993. Transport of water and solutes across maize roots modified by puncturing the endodermis. Further evidence for the composite transport model of the root. Plant Physiology 103, 335–349.[Abstract]
Steudle E, Oren R, Schulze ED. 1987. Water transport in maize roots. Measurement of hydraulic conductivity, solute permeability and of reflection coefficients of excised roots using the root pressure probe. Plant Physiology 84, 1220–1232.
Steudle E, Peterson CA. 1998. How does water get through roots? Journal of Experimental Botany 49, 775–788.
Tyerman SD, Bohnert HJ, Maurel C, Steudle E, Smith JAC. 1999. Plant aquaporins: their molecular biology, biophysics and significance for plant water relations. Journal of Experimental Botany 50, 1055–1071.[Abstract]
Weatherley PE. 1982. Water uptake and flow into roots. In: Lange OL, Nobel PS, Osmond CB, Zeigler H, eds. Encyclopedia of plant physiology, Vol. 12B. Berlin: Springer Verlag, 79–109.
Yadav R, Flowers TJ, Yeo AR. 1996. The involvement of the transpirational bypass flow in sodium uptake by high- and low-sodium-transporting lines of rice developed through intravarietal selection. Plant, Cell and Environment 19, 329–336.
Yeo AR, Yeo ME, Flowers TJ. 1987. The contribution of an apoplastic pathway to sodium uptake by rice roots in saline conditions. Journal of Experimental Botany 38, 1141–1153.
Zimmermann HM, Hartmann KD, Schreiber L, Steudle E. 2000. Chemical composition of apoplastic transport barriers in relation to radial hydraulic conductivity of maize roots of maize (Zea mays L.). Planta 210, 302–311.[Web of Science][Medline]
Zimmermann HM, Steudle E. 1998. Apoplastic transport across young maize roots: effect of the exodermis. Planta 206, 7–19.
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