Plant Physiol. (1989) 89, 264-2680032-0889/89/89/0264/05/$01 .00/0

Received for publication April 19,1988and in revised form August 19, 1988

Water Transport Properties of Cortical Cells in Roots ofNitrogen- and Phosphorus-Deficient Cotton Seedlings1

John W. Radin*2 and Mark A. Matthews

Department of Viticulture and Enology, University of California, Davis, California 95616

ABSTRACT

Growth-limiting deficiencies of N or P substantially decreasethe hydraulic conductance of cotton (Gossypium hirsutum L.)roots. This shift could result from decreased hydraulic conductiv-ity of cells in the radial flow pathway. A pressure microprobe wasused to study water relations of cortical cells in roots of cottonseedlings stressed for N or P. During 10 days of seedling growthon a complete nutrient solution, root cell turgor was stable at 0.4to 0.5 megapascal, the volumetric elastic modulus increasedslowly from 6 to 10 megapascals, and the half-time for waterexchange increased from 10 to 15 seconds. In seedlings trans-ferred to N-free solution for 10 days, final values for each of thoseparameters were approximately doubled. Root cell hydraulic con-ductivity (cell Lp) was 1.4 x 10-7 meters per second per mega-pascal at the time of transfer. In the well-nourished controls, cellLp decreased over 10 days to 38% of the inifial value, but in theN-stressed plants it decreased much more sharply, reaching 6%of the initial value after 10 days. Transfer to solutions without Por with an intermediate level of N also decreased cell Lp. Thechanges in root cell Lp were consistent with nutrient effects onintact-root water relations demonstrated earlier. However, cell Lpwas about half that of the intact root, implying that substantialwater flow may follow an apoplastic pathway, bypassing thecortical cells from which these values were derived.

In recent years evidence has accumulated that nutrientstresses (N and P deficiencies in particular) decrease thehydraulic conductance ofintact plants or excised root systems(2, 9, 11-13, 16, 22). The ensuing change in plant waterrelations can limit leaf growth rates by increasing the waterdeficit of the expanding leaf blades (1 1, 12). A developmentalstudy showed that root conductance per unit length changedvery early in the progression of nutrient deficiency, beforethere were any effects on overall root system length or mor-

phology (12). The reasons for this change in root internalproperties have not been defined. Root conductance coulddecline from increased cell numbers or decreased cell Lp3 inthe pathway of water movement, or from structural changesin the root. Here we report the Lp and other water relations

' Supported in part by the 1986 Visiting Scientist Award from theAmerican Society of Agronomy to J. W. R.

2Permanent address: United States Department of Agriculture,Agricultural Research Service, Western Cotton Research Laboratory,Phoenix, AZ 85040.

3 Abbreviations: Lp, hydraulic conductivity; e, volumetric modulusof elasticity; t½, half-time for water exchange; 4w, water potential; *I',osmotic potential; I,, pressure potential; a, reflection coefficient; 7rw,effective external osmotic pressure.

properties of cells in the root cortex of nutrient-stressed cottonseedlings.

MATERIALS AND METHODS

Plant Growth

Seeds of cotton (Gossypium hirsutum L. cv Deltapine 70)were germinated in moist vermiculite for 3 d, and the seedlingswere then transferred to aerated liquid nutrient solution. Thefull nutrient solution was a modified half-strength Hoaglandsolution containing 5 mM N as nitrate and 0.5 mM P asphosphate (14). Nutrient deficiencies were established by sub-stituting chloride salts for the nitrate or phosphate salts (-Nand -P solutions, respectively). Plants were also grown on anintermediate-N solution containing 0.2 mm nitrate and 4.8mm chloride. Day/night growth conditions were as follows:temperature 30/21 ± 2°C; RH 60/90 ± 5%; 550 Umol.m-2.s-' PAR from cool-white fluorescent lamps; and 14-h day-length.The cotyledons began to unfold immediately after transfer

ofthe plants to nutrient solutions. Area ofthe larger cotyledonon each seedling was estimated as length x width x 0.86. Thiscoefficient, determined from numerous tracings ofcotyledonson paper ofknown weight per unit area, had a 95% confidenceinterval of ±0.01. Hourly expansion rates during daytime andat night were calculated by measuring areas at the beginningand end of the light periods over a 48-h interval (3-5 d aftertransfer). Growth was assumed to be exponential during theperiod between each pair of sequential measurements.

Cell Size

Roots of seedlings were sectioned by hand with a razorblade approximately 5 cm from the tip, and the cross-sectionswere mounted on a microscope slide and stained with meth-ylene blue. Diameters of cortical cells were measured with anocular micrometer under a microscope. Longitudinal free-hand sections were treated similarly to derive cell lengths. Allmeasurements of cell size were made on the taproot. Datafrom numerous plants were combined because within-plantand between-plant variabilities were equal.

Turgor

Plants in nutrient solution were taken from the growthroom to the laboratory and incubated for 20 to 30 min toallow equilibration with their new environment (room tem-perature, dim light). Intact seedlings were removed from thenutrient solution and their roots were placed on filter paper

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NUTRIENT STRESS AND HYDRAULIC CONDUCTIVITY OF ROOT CELLS

moistened with the same solution. The roots were then cov-ered with another piece of moistened filter paper except for asegment about 1 cm in length located about 5 cm from thetip of the taproot. The entire assembly was supported on aflat platform mounted on a micromanipulator. The exposedsegment was aligned with the microcapillary tip ofthe pressureprobe, and the tip was inserted into the cortex of the root.Tip preparation and other procedures were as described byShackel et al. (17). Because measurements were being madeon interior cells, it was normally not possible to view the cellbeing penetrated. When a cell was penetrated, the pressurewas adjusted until the meniscus wasjust external to the surfaceof the root, and it was observed for stability (maintenance ofconstant position for 2 min). Readings from many penetratedcells were unstable, especially in -P roots. Pressure readingswere recorded only from those that exhibited stability, indi-cating the absence of leaks. The pressure was corrected forthe average displacement of the meniscus from the impaledcell surface, using Eq. 1 (after determination of e, see below).The magnitude of the correction varied with e from 0.1 to 0.4MPa. At least three independent measurements ofturgor wereobtained from cells exhibiting stable readings within the ex-posed 1-cm segment of each root and on up to 7 plants atany particular age. Readings were combined because within-plant and between-plant variabilities were equal.

Elastic Modulus

The volumetric elastic modulus was determined from therelationship

=V.A*p/AV (1

in which V is mean cell volume (5). Procedures were similarto those described earlier (7, 23). The cell was subjected to astep change in pressure of 0.01 to 0.07 MPa and the resultingchange in volume was noted. After a perturbation, volumechanged very rapidly for 1 to 2 s, then much more slowly.Returning the pressure to its original value directly after therapid phase ofthe response resulted in a return ofthe meniscusto approximately its original position, indicating that littlewater had been taken up or lost by the cell. Accordingly, therapid phase was taken to be due to the elastic properties ofthe cell wall. Correction for water transport during the per-turbation was deemed unnecessary because the readings wereobtained in a much shorter interval than the t½, 1 to 2 s versus10 to 30 s. Readings were repeated 5 to 8 times on each cell(at least 3 per root) and on up to six plants at any particularage. Readings were combined because within-plant and be-tween-plant variabilities were equal. Errors in estimation of ewere calculated by combining errors in the two componentsof Eq. 1, i.e. V and AIp/' V, each of which was determinedindependently.

Half-Time of Water Exchange

After a penetrated cell had displayed a stable turgor, thepressure was changed by 0.05 to 0.1 MPa. The meniscusmoved rapidly to a new position in the tip, and was held thereby manual adjustment of the pressure. The subsequent timecourse of change in pressure was recorded on a strip chartrecorder. The t½1, was determined graphically. Readings were

obtained from at least 2 (usually 3) positions within a rootand from up to five plants at any particular age. Readingswere combined because within-plant and between-plant var-iabilities were equal.

Hydraulic Conductivity

The Lp of cortical cells was calculated from the relationship

Lp = V.ln 2/A * tl/2 *(c - I,) (2)in which V = cell volume and A = cell surface area (23).These were calculated from mean cell diameters and lengthsassuming that the cells were cylindrical. Because measure-ments of turgor were made under conditions of very lowtranspirational water flux, the root *4', was assumed to be zeroand 'Pr was accordingly set equal to -Ip. Because p, << e,any errors in the approximation of I, had little influence oncalculated values of Lp. Errors in estimates of Lp were cal-culated by combining errors in the independently determinedcomponents of Eq. 2, i.e. V/A, t'v, e, and 'I'.

RESULTS

Blade Expansion

Expansion of the cotyledonary blades was markedly af-fected by the nutrient regime on which the plants were grown.With full nutrients, expansion proceeded rapidly, with slightslowing of growth after about 6 d (Fig. 1). On a nutrientsolution either without N or without P, growth began to slowalmost immediately after transfer; for the two treatments, thedifference in blade area from the control was significant (P =0.05) by 3 and 4 d after transfer, respectively. Growth on anintermediate level of N was less affected than in -N or -Ptreatments. Essentially all of the growth differences aroseduring the daytime, with no consistent effects on relative leaf

25, Full Nutrients

E 20 <,/'MO-

6 0 4 6a TaIntermediate N

0. 10s00

0

'( 5

010 2 4 6 8 10

Days after TransferFigure 1. Growth of cotyledons of cotton seedlings after transfer tonutrient solution. Only the larger of the two cotyledons of eachseedling was measured. Results are means ± SE of six plants.

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Plant Physiol. Vol. 89, 1989

expansion rates at night (data not shown). In this respect theseedlings responded to nutrients as reported earlier (11, 12).

Cell Size

Cell sizes were determined 5 cm from the tip of the taproot4, 5, and 8 d after transfer to nutrient solution. In each case

the distributions ofboth diameters and lengths were Gaussian,allowing the use of parametric statistics to assess differences.Diameters were not significantly different over either treat-ment or age, with a mean ± SE of 55 ± 0.6 ,um (n = 468).Cell lengths tended to increase slightly with age, but againdifferences were small. The mean length was 151 ± 3 um (n= 720). The volume of a cylindrical cell of these dimensionsis 359 ± 8 pL, and this value was used in subsequent calcu-lations. At all times of sampling, the root systems fromdifferent treatments were visually indistinguishable (length,diameter, color, etc., except that nutrient deprivation be-gan to inhibit branching after 7 to 10 d); nor were con-

sistent differences noted in the sections examined under themicroscope.

Turgor and Elastic Modulus

Calculation of Lp requires knowledge of cell volume andsurface area, I,. (here assumed equivalent to Ip), c, and t½.These data were measured over the entire period of growthfor only the control and the -N treatments. In both cases

turgor increased during development, but much more so in-N roots than in the controls. In the stressed roots turgormore than doubled from the initial value of0.4 MPa, whereasin the controls it increased only to 0.5 MPa over 10 d (Fig.2A). Differences in turgor due to N stress were apparent byapproximately 4 d after transfer (Fig. 2A).The modulus of elasticity also was increased in cells of N-

stressed roots. In the controls, it increased very slowly from6.2 MPa at d 0 to 9.9 MPa 10 d later (Fig. 2B). In the -Nroot cells, however, e increased more rapidly and to a muchgreater extent, reaching a value above 20 MPa after 9 d. Thetiming of increases in e approximately coincided with that forincreases in turgor. In both cases, effects ofN stress were notfirmly established until 4 d after transfer, although there mayhave been small differences before that time (Fig. 2, A andB).

Half-Time for Water Exchange

The t½, followed a very different pattern from that of turgoror e. In the controls, t½1, gradually increased from 10 s to about15 s with age (Fig. 2C). In the -N root cells, though, the t½1,increased very rapidly upon transfer to -N nutrient solution,reaching its maximum value of 30 s after only 2 to 3 d. Thislarge differential between treatments was then maintainedthroughout the remainder of the period over which it wasmonitored. The rapid development of large differences in t-1,clearly occurred when differences in turgor, e, and even leafgrowth rate, were small (Figs. 1; 2, A and B).

Hydraulic Conductivity

The Lp of cortical cells was calculated from the data ofFigure 2, and trends were determined by regression. At the

RADIN AND MATTHEWS

00

I-

a

o

cb

2

On

0.8

0.4

U I .

21

14

0

40

I-

201

l I

0 2 4 6 8 10

Days after Transfer

Figure 2. Water relations characteristics of root cortical cells ofcotton seedlings after transfer to nutrient solution. A, Turgor; B,modulus of elasticity; C, half-time for water exchange. Results areshown as means ± SE. Symbols in all panels as in panel A.

0

l-

I-

xa-

I-

Q

J1

1.5

1.0

0.5

0

0 2 4 6 8 10

Days after TransferFigure 3. Hydraulic conductivities of cotton root cells. Regressionequations are as follows: full nutrients, Y = 1.30 - 0.08X (r = 0.72*);-N, Y = 0.75 - 0.29 In (X + 0.1) (r = 0.96**). * and ** indicatesignificance at P = 0.05 and 0.01, respectively.

time of transfer to nutrient solutions, Lp was 1.4 x 10-' ms-'. MPa-'. In both well-nourished and -N root cells, the Lpdeclined with plant age, but much more rapidly in the lattercase (Fig. 3). The trend lines indicate that 10 d after transfer,the Lp had decreased by 62% in the controls and by 94% inthe -N roots. As little as 2 d of N deprivation caused more

than a twofold difference between the estimated values of Lpfor the two treatments (Fig. 3). Thus, there were large devel-opmental changes in Lp in both cases, but N deficiency

A

Full Nutrients

0 I-~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~

I,t-e-t;+/a+ Af-?

\ ~~~Full Nutrients

I~~~ ~\

. ~ ~ -

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NUTRIENT STRESS AND HYDRAULIC CONDUCTIVITY OF ROOT CELLS

Table I. Water Relations Characteristics of Root Cortical Cells ofCotton Seedlings 4 D After Transfer to Nutrient Solution

Results are means ± SE of 6 to 17 measurements.Treatment Turgor e tw Lp X 107

MPa MPa s m.s1'.MPa-'Full nutrients 0.41 ± 0.07 6.6 ± 0.7 11 ± 2 1.19 ± 0.25Intermediate N 0.44 ± 0.03 5.9 ± 0.7 22 ± 3 0.67 ± 0.12-P 0.47 ± 0.03 7.3 ± 0.7 29 ± 4 0.45 ± 0.08-N 0.63 ± 0.04 12.1 ± 1.5 33 ± 5 0.22 ± 0.04

Table II. Comparison of Hydraulic Properties of Cortical Cells toThose of Intact Root SystemsThe cellular data are from Table I and the intact root data are

recalculated in the appropriate units from Radin and Eidenbock (12).Lp x 107

SourceFull nutrients -P

m.s'1 .MPa-1Cortical cells 1.19 0.45Intact roots 2.3 1.0

accelerated their appearance. This pattern is very similar tothe time courses reported earlier for intact-root conductivityin fully nourished and -P plants (12).

Similar data on cellular water relations were collected forother nutrient-stress treatments, but only at 4 d after transfer.In these experiments, the lowest cell Lp was seen in the -Ntreatment, followed in increasing order by the -P, interme-diate-N, and control treatments (Table I). The effects of stresstreatments on cell Lp were all significant (P = 0.05). Notably,the magnitude of these changes closely paralleled the degreeof growth limitation by nutrient stress (Fig. 1).

DISCUSSION

Intact-plant and excised-root experiments revealed earlierthat nutrient stress decreases root hydraulic conductivity (11-13). Effects of nutrient stress on root cell Lp reported heremay provide a basis for this shift. The alteration of corticalcell Lp, and the recent observation that nutrient effects onxylem anatomy are minor (13) both indicate that stress-induced limiting resistances occur in the radial rather thanthe axial component of the water pathway. This conclusionis consistent with the concept that radial resistance dominatesthe overall resistance of the root (25).

Earlier work (12) also revealed an age dependency fornutrient stress effects upon root conductivity. The conductiv-ity of excised roots and intact plants decreased as seedlingsdeveloped, but more so in -P plants than in well-nourishedcontrols. Similarly, in cortical cells, nutrient deficiency exag-gerated the rate ofchange ofLp but did not otherwise modifydevelopmental patterns. Thus, nutrient effects on Lp mayoccur partially via some effect on root development. Thesecomparisons among treatments are independent of the age ofindividual cells, as root extension rates were not different andall measurements were at a fixed distance from the apex.Developmental changes have previously been reported in bothcell e (20, 21) and Lp (20).

In some species, e is dependent upon turgor (18, 19, 23,

24). Such a dependency might account for the changes in e ofnutrient-stressed cotton root cells, as turgor more than dou-bled over 10 d of N withdrawal, and changes in turgor and ewere almost simultaneous (Fig. 2). Measurements with artifi-cially lowered turgor (by displacement of the meniscus) didnot reveal any differences in e (not shown); however, varia-bility of e was such that only large effects could have beendemonstrated. N stress also increased e of leaf cells of cotton(15) and wheat (8).

In addition to e, Lp may also be turgor-dependent (21, 23).In cotton root cells this explanation for nutrient effects isdiscounted, because Lp decreased substantially in nutrient-deficient root cells before any changes in turgor were meas-urable (Figs. 2 and 3). It is important to note that componentsof Lp were determined with hydrostatic gradients, yet flowthrough roots normally is driven by both hydrostatic andosmotic gradients. However, Tyerman and Steudle (24)showed that cell Lp determined with a pressure probe was thesame whether flow was osmotically or hydrostatically driven.Therefore, the conclusions from our studies may be inde-pendent of the experimental methods.Comparisons of hydraulic properties of cells with those of

intact roots can often support deductions about pathways ofwater flow (1, 7, 18, 19, 25). Table II presents comparisonsbetween hydraulic conductivities of cells and of intact rootsof cotton. The intact-root conductivities were generated ear-lier by pressure-flux methods and were validated against intacttranspiring plants (12). In both the control and the -P treat-ment, the intact-root conductivity was about twice the Lp ofindividual cells. These data provide no support for cell-to-cell(vacuolar) flow of water, in which case each cortical cell inthe pathway acts as a resistor in series (1, 25). In cotton rootswith approximately five cell layers outside the stele, the cell-to-cell model predicts a root conductivity about 10% of cellLp. Evidence from barley (18) and wheat (7) roots did supporta cell-to-cell pathway, but a reevaluation led Jones et al. (6)to assign the pathway a minor role in wheat. A cell-to-cellpathway was also discounted in maize roots (19).The criteria that preclude existence of a vacuolar pathway

also preclude operation of a significant symplastic pathway(i.e. through plasmodesmata). Relaxation of cells after a per-turbation could occur by water movement through either theplasmalemma or the plasmodesmata. Thus, the cell Lp com-bines the conductivity to water of both sites.The alternative to vacuolar or symplastic flow is an apo-

plastic pathway (1, 25). In this model, water flow is usuallyenvisioned to bypass cortical cells, with the Casparian stripforcing water to enter the symplast at the endodermis. Aswater enters and exits the symplast, it must cross two mem-branes, and the maximum root Lp therefore is half that ofindividual cells (25). Our data are inconsistent with this modelas well (Table II), although the discrepancy is smaller thanwith the other models above. However, this comparison maybe flawed because Lp was determined at only one site alongthe length of the root, and it was not determined specificallyon the endodermal cells.A third possibility is that a large portion of the radial water

flow bypasses cell membranes entirely. As a test of this hy-pothesis, root reflection coefficients and effective externalosmotic pressures were calculated from earlier data (12) ac-

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RADIN AND MATTHEWS

cording to Fiscus (3). Values of a were 0.90 and 0.76 forcontrol and -P roots, respectively, and values of ir0 were

0.247 and 0.138 MPa for the same roots. Both these param-eters are consistent with increased shunting of water aroundcell membranes with nutrient stress. The values of a representmore or less the limits of the normal range cited in theliterature for roots (see "Discussion" in 19). Even when rootshave a low a, cortical 'sleeves' from those roots retain a veryhigh a, showing that the loss of semipermeability is not a

property of the cells per se (19). This evidence implies that a

low a for roots may be associated with some apoplastic fluxof water through a bypass, and that such a pathway mayoccur rather frequently. Hanson et al. (4) reported a dominantapoplastic bypass in roots of red pine during 02 deprivation.Possible locations for a bypass include sites of lateral rootemergence, where the Casparian strip is discontinuous (10).

Finally, we note that decreases in root conductivity (12)and root cell Lp (Fig. 2) are among the earliest plant responsesto nutrient stress, preceding even the changes in leafexpansionrate. Earlier studies (1 1, 12) strongly imply that root hydraulicconductivity is a primary limitation to leaf expansion innutrient-stressed seedlings. Presuming that properties of rootcell membranes contribute to the stress-induced changes, thenthese studies have specified a site to search for the initialmetabolic events leading to stress injury.

ACKNOWLEDGMENTS

We thank M. Anderson and M. Eidenbock for technical help, M.Serpe, Dr. K. A. Shackel, and Dr. T. C. Hsiao for helpful cooperationand discussions, and Drs. J. B. Passioura, E. Steudle, and J. S. Boyerfor critical reviews of the manuscript.

LITERATURE CITED

1. Briggs GE (1967) Movement of Water in Plants. F. A. Davis,Philadelphia, pp 91-105

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3. Fiscus EL (1977) Determination of hydraulic and osmotic prop-erties of soybean root systems. Plant Physiol 59: 1013-1020

4. Hanson PJ, Sucoff EI, Markhart AH III (1985) Quantifyingapoplastic flux through red pine root systems using trisodium,3-hydroxy-5,8,10-pyrenetrisulfonate. Plant Physiol 77: 21-24

5. Husken D, Steudle E, Zimmermann U (1978) Pressure probetechnique for measuring water relations of cells in higherplants. Plant Physiol 61: 158-163

6. Jones H, Leigh RA, Wyn Jones RG, Tomos AD (1988) Theintegration of whole-root and cellular hydraulic conductivitiesin cereal roots. Planta 174: 1-7

7. Jones H, Tomos AD, Leigh RA, Wyn Jones RG (1983) Water-relation parameters of epidermal and cortical cells in theprimary root of Triticum aestivum L. Planta 158: 230-236

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9. Passioura JB, Tanner CB (1985) Oscillations in apparent hy-draulic conductance of cotton plants. Aust J Plant Physiol 12:455-461

10. Peterson CA, Emanuel ME, Humphreys GB (1981) Pathway ofmovement of apoplastic fluorescent dye tracers through theendodermis at the site of secondary root formation in corn(Zea mays) and broad bean (Viciafaba). Can J Bot 59: 618-625

11. Radin JW, Boyer JS (1982) Control ofleafexpansion by nitrogennutrition in sunflower plants. Role of hydraulic conductivityand turgor. Plant Physiol 69: 771-775

12. Radin JW, Eidenbock MP (1984) Hydraulic conductance as afactor limiting leaf expansion of phosphorus-deficient cottonplants. Plant Physiol 75: 372-377

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14. Radin JW, Hendrix DL (1988) The apoplastic pool of abscisicacid in cotton leaves in relation to stomatal closure. Planta174:180-186

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16. Safir GR, Boyer JS, Gerdemann JW (1972) Nutrient status andmycorrhizal enhancement ofwater transport in soybean. PlantPhysiol 43: 700-703

17. Shackel KA, Matthews MA, Morrison JC (1987) Dynamicrelation between expansion and cellular turgor in growinggrape (Vitis vinifera L.) leaves. Plant Physiol 84: 1166-1171

18. Steudle E, Jeschke WD (1983) Water transport in barley roots.Measurements of root pressure and hydraulic conductivity ofroots in parallel with turgor and hydraulic conductivity of rootcells. Planta 158: 237-248

19. Steudle E, Oren R, Schulze ED (1987) Water transport in maizeroots. Measurement of hydraulic conductivity, solute permea-bility, and of reflection coefficients of excised roots using theroot pressure probe. Plant Physiol 84: 1220-1232

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21. Steudle E, Zimmermann U, Luttge U (1977) Effect of turgorpressure and cell size on the wall elasticity of plant cells. PlantPhysiol 59: 285-289

22. Syvertsen JP, Graham JH (1985) Hydraulic conductivity ofroots, mineral nutrition, and leaf gas exchange of citrus root-stocks. J Am Soc Hortic Sci 110: 865-869

23. Tomos AD, Steudle E, Zimmermann U, SchulzeED (1981) Waterrelations of leaf epidermal cells of Tradescantia virginiana.Plant Physiol 68: 1135-1143

24. Tyerman SD, Steudle E (1982) Comparison between osmoticand hydrostatic water flows in a higher plant cell: determina-tion of hydraulic conductivities and reflection coefficients inisolated epidermis of Tradescantia virginiana. Aust J PlantPhysiol 9: 461-479

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