A potential role for xylemphloem interactions in the hydraulic architecture of trees: effects of...

Summary We investigated phloem–xylem interactions inAcer rubrum L. and Acer saccharum Marsh. Our experimentalmethod allowed us to determine xylem conductance of an in-tact branch by measuring the flow rate of water supplied at twodelivery pressures to the cut end of a small side branch. Wefound that removal of bark tissue (phloem girdling) upstreamof the point at which deionized water was delivered to thebranch resulted in a decrease (24% for A. rubrum and 15% forA. saccharum) in branch xylem hydraulic conductance. De-clines in hydraulic conductance with girdling were accompa-nied by a decrease in the osmotic concentration of xylem sap.The decrease in xylem sap concentration following phloemgirdling suggests that ion redistribution from the phloem wasresponsible for the observed decline in hydraulic conductance.When the same measurements were made on branches per-fused with KCl solution (~140 mOsm kg–1), phloem girdlinghad no effect on xylem hydraulic conductance. These resultssuggest a functional link between phloem and xylem hydraulicsystems that is mediated by changes in the ionic content of thecell sap.

Keywords: Acer rubrum, Acer saccharum, hydrogel, xylem sapion concentration.

Introduction

Forest tree photosynthesis occurs in a varied and dynamic can-opy environment. Much of this heterogeneity results from spa-tial and temporal variations in the effects of the trees them-selves on light penetration, wind movement of leaves andbranches, and vapor pressure deficits. Leaves employ a num-ber of physiological mechanisms (e.g., modulation of stomataaperture, xanthophyll cycle regulation), allowing them to re-spond to short term changes in irradiance or evaporative condi-tions in ways that tend to maximize photosynthesis. The effectof xylem sap ion concentrations on the hydraulic resistance ofthe supply pathway (Zimmermann 1978, van Ieperen et al.

2000, Zwieniecki et al. 2001) has led to the suggestion that therecirculation of ions between the phloem and xylem gives riseto short term changes in canopy-level hydraulic architecture(Zwieniecki et al. 2001). The existence of such a couplingmechanism might allow trees to enhance water delivery tobranches currently experiencing high rates of photosynthesis.Whether such active internal regulation occurs in trees re-mains to be demonstrated, although all of the component partsrequired for such regulation are known to exist. In this paper,we explore interactions between xylem and phloem, and theireffect on xylem water transport.

The xylem and phloem are the principal long-distance liq-uid transport pathways in plants. The xylem primarily trans-ports water and nutrients from the soil to the leaves, while thephloem transports photosynthate from sites of synthesis (e.g.,leaves) or storage (e.g., tubers) to regions of active growth. Inflowering plants, transport in the xylem takes place throughthe lumen of a series of axially connected cells, which arenon-living at maturity (Esau 1977). The driving force in thexylem is generated by the evaporation of water from leaves. Incontrast, the phloem is comprised of axially connected livingcells, in which mass flow results from gradients in turgor pres-sure generated primarily by the accumulation of sugars andpotassium phosphate (Milburn 1979). The two parallel path-ways are interconnected via parenchyma rays along the entirelength of the stem (Holl 1975, Esau 1977). The close connec-tion between xylem and phloem suggests a functional linkage(van Bel 1990). The phloem obtains water, ultimately, fromthe xylem, while the concentration of certain ions in the xy-lem, in particular K+, is influenced by recirculation from thephloem (Jeschke and Pate 1991, Pate and Jeschke 1995). Mod-els of long distance transport indicate that changes in xylempressure potentials have a marked effect on rates of carbohy-drate movement through the phloem (Boersma et al. 1991).However, the question of whether xylem transport can bemodified by the phloem has not been addressed.

Xylem vessels are formed from dead cells, and it has been

Tree Physiology 24, 911–917© 2004 Heron Publishing—Victoria, Canada

A potential role for xylem–phloem interactions in the hydraulicarchitecture of trees: effects of phloem girdling on xylem hydraulicconductance

MACIEJ A. ZWIENIECKI,1,2 PETER J. MELCHER,1,3 TAYLOR S. FEILD1,4 and N. MICHELEHOLBROOK1

1 Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA2 Corresponding author ([email protected])3 Present address: Department of Biology, Ithaca College, Ithaca, NY 14853, USA4 Present address: Department of Botany, University of Toronto, Toronto, ON M5S 3B2, Canada

Received, August 20, 2003; accepted January 18, 2004; published online June 1, 2004

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assumed that their hydraulic capacity remains constant withthe only variation being a change to a non-functional (i.e.,embolized) state resulting from cavitation (Sperry and Tyree1988). This binary view conflicts with reported changes in xy-lem hydraulic conductance in response to changes in ion con-centration of the liquid flowing through the vessels (Zimmer-mann 1978, van Ieperen et al. 2000, Zwieniecki et al. 2001).Changes in xylem flow rate that result from changes in theionic concentration of the perfusing solution are both revers-ible and repeatable and occur in all major groups of plants(ferns, conifers, angiosperms) and growth forms (herbaceousand woody), although the magnitude of the response varies(Zwieniecki et al. 2001). A mechanistic analysis of this phe-nomenon in Laurus nobilis L. demonstrates that xylem con-ductance is related to ion concentration in the xylem sap andthat the effect involves the swelling or deswelling of hy-drogels (most likely pectins) in inter-vessel pit membranes(Zwieniecki et al. 2001). The existence of ion-mediated chan-ges in xylem conductance leads to the possibility that livingxylem parenchyma cells actively modify xylem hydraulicproperties by altering the ion concentration in the xylem sap.

Ion concentration in the xylem sap is determined by twoprocesses, namely, uptake by roots and recycling from thephloem (Pate and Jeschke 1995). Sap concentrations varytemporally, with the concentration of some ions being inver-sely proportional to flow rate, some showing no relation toflow rate and some varying in proportion to flow rate (Schurr1998). Potassium ions (K+) appear to follow the latter pattern,suggesting that the dilution effect of the transpirational fluxcan be overridden by physiological processes (Schurr andSchulze 1995). While investigating methods to estimate invivo changes in branch hydraulic conductance (Zwieniecki etal. 2000), we observed that phloem girdling decreased xylemconductance in several woody species (unpublished data). Atthe time, we had no explanation for this observation. However,the demonstration of ion-mediated changes in xylem hydrau-lic properties (Zwieniecki et al. 2001) provides a possiblemechanism to explain this effect. Specifically, cessation ofphloem transport could decrease lateral ion transport into thexylem. The resulting decrease in xylem sap ion concentrationcould, in turn, cause a decrease in xylem conductance. In thisstudy, we test whether mechanical injury to the phloem resultsin a decrease of xylem hydraulic conductance and determine ifthis effect can be overcome by providing ions to the xylem.

Traditional approaches to the determination of xylem hy-draulic conductance require that branch segments be excisedfrom the plant, thus precluding an assessment of phloem–xy-lem interactions. Studies based on root pressurization allowwork on intact plants (Passioura and Munns 1984, Schurr andSchulze 1995), however, the ability to discern changes in xy-lem hydraulic conductance may be obscured by the non-vas-cular resistances in both roots and leaves (Tyree and Ewers1991). Here, we report an investigation of xylem–phloem in-teractions by measuring xylem sap flow in an intact branchduring the supply of water at two delivery pressures to the cutend of a side branch.

Methods

Plant material and study site

Studies were performed on mature trees of Acer rubrum L. andAcer saccharum Marsh., during June and July 2000 at the Har-vard Forest (Petersham, MA). Both trees were open- grown.South-facing branches, 6 to 10 m above the ground, were ac-cessed from scaffolding. Measurements were made on a totalof 43 branches.

Measurement of branch hydraulic conductance

In situ measurements of the hydraulic conductance (g MPa–1

s–1) of freely transpiring branches were made by the methoddescribed in Zwieniecki et al. (2000). The approach was tomeasure the steady state flow rate of deionized water or solu-tion into a side branch while the main branch remained at-tached to the tree (Figure 1). Measurements were made at twodelivery pressures, allowing the hydraulic conductance to bedetermined without explicit knowledge of the total drivingforce. Measurements were made under steady state conditions,justifying the use of a linear relationship between flow rate anddriving gradient:

Q1 /L P P= +delivery1 plant (1)

Q2 /L P P= +delivery2 plant (2)

where Q1 and Q2 are the flow rates into the petiole for two de-livery pressures, Pdelivery1 and Pdelivery2, L is the conductance, andPplant is the hydrostatic pressure within the xylem. If we assumethat Pplant remains constant during the measurement cycle, thenthe conductance (L) can be calculated as:

912 ZWIENIECKI, MELCHER, FEILD AND HOLBROOK

TREE PHYSIOLOGY VOLUME 24, 2004

Figure 1. Diagram of the method used to measure in situ hydraulicconductance.

LQ Q

P P= −

−2 1

delivery2 delivery1

(3)

Flow rate was determined according to methods describedin Zwieniecki et al. (2000). The instrument consisted of twoair tanks connected to one of a set of interchangeable pressur-ized plastic solution reservoirs. The interchangeable reservoirsallowed us to switch easily between solutions. Water flowedfrom the pressurized reservoirs through a calibrated, poly-etheretherketone (PEEK) capillary tube and was delivered tothe side branch via a low resistance tube (Figure 1). The pres-sure drop across the capillary tube was measured by twopressure transducers (Omega PX236-100 Series, Omega Engi-neering, Stanford, CT). The relationship between the pressuredrop and the flow rate (and thus the conductance of the PEEKtube) was previously determined empirically by directing theoutflow onto an analytic balance (± 0.01 mg). The minimumresolution of the two-point flow meter (approximately ± 3.5 ×10–6 g s–1) was set by the accuracy of the differential pressuremeasurement (± 3.5 kPa) and the conductance of the calibratedtube (1.04 mg s–1 MPa–1).

Measurements began with removal of the side branch underwater to prevent air from entering the xylem. The cut surfacewas subsequently shaved with a razor blade and the branch im-mediately attached to the two-point flow meter (Figure 1). Theflow rate into the branch was determined using first the low-pressure tank, followed by the high-pressure tank. This wasrepeated at 1-min intervals (Figure 2A). Delivery pressures

(measured by transducer 2) were typically ~0.05 MPa and~0.01 MPa for the high and low-pressure inputs, respectively.The time course of pressure changes after switching betweensupply tanks showed that a relatively constant delivery pres-sure (and thus flow rate) was achieved rapidly (Figure 2B). Ingeneral, consecutive measurements showed a slight change inthe delivery pressure; however, the calculated conductivitywas fairly stable after the first few minutes (Figure 2C).

Pushing water into the end of a cut side branch measures theimpedance of a network of hydraulic elements (branch, stemand transpiring leaves). This precludes determination of theexact water flow pathways that were measured (Zwieniecki etal. 2000), but it allows us to assess changes in hydraulic con-ductance in response to our treatments. After 20 min, brancheswere girdled ~20 cm proximal to the point at which thetwo-point flow meter was attached. A 1-cm strip of the barkwas removed with a dull razor blade, without damaging thexylem. The girdled region was covered with vacuum greaseand Parafilm (American National Can, Minasha, WI) to pre-vent water loss.

Sap analysis

Xylem sap samples were collected from each branch follow-ing the conclusion of the in vivo hydraulic measurements.Branches were excised from the tree 20 cm proximal to thepoint of attachment of the two-point flow meter and all leavesimmediately removed to stop transpiration. Sap was collectedfrom the distal end of the branch (downstream from the wa-ter/solution delivery point). The bark was removed from the

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XYLEM–PHLOEM INTERACTIONS AND THE HYDRAULIC ARCHITECTURE OF TREES 913

Figure 2. Example of results from asingle control run. (A) Time trace ofsimultaneous output from two pres-sure transducers used to determineflow rate. Upstream pressure (trans-ducer 1) was switched automaticallyat 1-min intervals between the highand low pressure tanks. (B) Magnifi-cation of the portion of time trace(A), steady state pressures werereached within 20 s after a pressurechange. (C) Estimates of conductance(Lp) were calculated from the aboverun. Gray areas represent final cut ofthe branch from the tree.

cut end of the branch and the xylem surface was shaved cleanwith a razor blade. This surface was rinsed with deionized wa-ter and dried with clean tissue. Parafilm was wrapped tightlyaround the branch end and a plastic tube was attached to thebranch through which suction was applied using a hand-heldvacuum pump. Liquid was released from the xylem intothe plastic tubing by repeatedly cutting the basal end of thebranch, a procedure that allows for the consecutive removal ofvessel end walls. The sap samples were rapidly transferred toglass microcapillary tubes and sealed with Parafilm. We col-lected about 10 to 25 µl of sap from each branch. In addition,sap was collected from 14 branches that were not used in thehydraulic conductance measurements.

Osmolarity of sap (mOsm kg–1) was determined by measur-ing the total osmotic potential of the sap with isopiestic psych-rometers according to methods outlined in (Boyer 1995).Samples were held at a constant temperature until the out-put stabilized (~1 h). Thermocouple outputs were amplifiedthrough a custom-built multiplexed nanovolt amplifier (BC-MPNV 100; Burns Consulting, Altadena, CA) and recordedby a computer.

Effect of ion concentration on xylem hydraulic conductance

The effect of ion concentration on xylem hydraulic conduc-tance was determined on branch segments collected from thesame trees as used in the in vivo measurements. Flow ratesthrough 12-cm-long branch segments were measured by di-recting the outflow onto an analytical balance (± 0.1 mg).Solutions were supplied at a constant delivery pressureof 0.03 MPa. For each segment, flow was determined for140 mOsm kg–1 KCl solution and subsequently for deionizedwater (n = 8 for A. saccharum, n = 6 for A. rubrum). One-year-old branch segments were used in this study. The flowenhancement that occurred in the presence of KCl was calcu-lated as a percentage of that for water after returning from KClto deionized water.

Results

Our experimental approach was to compare the effect ofphloem girdling on in situ measurements of branch hydraulicconductance when side branches were supplied with eitherdeionized water or KCl solution. We used a high KCl concen-tration (140 mOsm kg–1) to saturate any ionic response of xy-lem hydraulic conductance. A non-girdled treatment, in whichbranch hydraulic conductance was measured by perfusing thebranch with deionized water, served as a control. In situ mea-surements of branch hydraulic conductance typically showedsome variability during the first 5 to 10 min, after which thereadings stabilized. After 20 min of water perfusion, branchhydraulic conductance was nearly constant in A. saccharum,but continued to show a small decrease in A. rubrum (Figure 3;control). Phloem girdling upstream of the point where waterwas supplied to the branch resulted in a significant decrease inthe measured branch hydraulic conductance compared to thenon-girdled control (Figure 3; Table 1). The response to gir-dling was detected within 10 min. The mean reduction inhydraulic conductance relative to non-girdled control bran-

ches was 24.1% for A. rubrum and 15.4% for A. saccharum.When branches were perfused with ~140 mOsm kg–1 KCl, gir-dling did not significantly alter branch conductance (Figure 3).However, there was a significant difference between girdledbranches measured with deionized water and girdled branchesmeasured with KCl (Figure 3). These results indicate that sup-plying KCl solution to the xylem prevented the reduction inbranch hydraulic conductance otherwise caused by girdling.

The osmolarities of xylem sap collected from intact bran-ches and non-girdled branches perfused with deionized water(control) were almost identical, indicating that supplying de-ionized water to the branch resulted in little dilution of the xy-lem sap (Figure 4). There was a trend for the osmolarity of thesap of girdled branches to be lower than that in either intact ornon-girdled branches. However, these differences were not sta-tistically significant (Figure 4). Branches perfused with KClsolution had osmolarities similar to the supplied KCl solution,which was significantly different from the osmolarities ofbranches in other treatments.

We examined the effect of ions on the hydraulic conduc-tance of the xylem using excised branch segments. In bothA. rubrum and A. saccharum, flow rates increased significantlywhen the perfusing solution was switched from deionized wa-ter to a 140 mOsm kg–1 KCl solution (Figure 5). The magni-tude of the increase varied among branch segments, rangingfrom 15 to 57%, with a mean of 38%, for A. rubrum and from 8to 29%, with a mean of 24%, for A. saccharum. Switchingfrom 140 mOsm kg–1 KCl back to deionized water returned theflow rate to its initial value. The response was rapid, with sta-ble flow rates occurring within several seconds of switchingbetween solutions. Because the driving force for water move-ment was constant, the observed changes in flow rate representchanges in branch hydraulic conductance. The magnitudes ofthese changes were similar to those observed in the in situ stud-ies of branch conductance.



Figure 3. Percent change in xylem hydraulic conductance (mean ±SD) between 20 and 30 min after the start of conductance measure-ments. Girdling took place after 20 min of water/solution supply. Up-per and lowercase letters indicate significant differences betweentreatment means (ANOVA, performed separately for each species).

Discussion

Decreases in the ionic concentration of the xylem sap arethought to reduce xylem conductance because of the swellingof hydrogels in bordered pit membranes (Zwieniecki et al.2001). Thus, the decrease in hydraulic conductance of girdledbranches compared to non-girdled controls could reflect a de-crease in xylem ion concentration caused by reduced ion trans-port between phloem and xylem. Addition of high concentra-tions of KCl eliminated the effects of girdling on xylem hy-draulic conductance, suggesting that girdling affects xylemsap ion concentration. Supporting this interpretation, the de-crease in hydraulic conductance observed in the girdled bran-ches was associated with a decline in the ion concentration ofthe xylem sap.

Although our data are consistent with the hypothesis thatphloem girdling reduces xylem hydraulic conductance by af-fecting ion recycling from phloem to xylem, it is possible thata more generalized wound response to girdling is involved.

Pathogens are known to induce the production of vascular gels(Van der Molen et al. 1983), and mechanical injury results inthe occlusion of vessels by pectin-like polysaccharides (Zim-mermann 1983). An increase in hydrogel production in re-sponse to girdling could decrease hydraulic conductance byphysically obstructing flow through the xylem. However, thisrequires an explanation of how the addition of KCl negated theeffect of girdling on hydraulic conductance. One possibility isthat supplying KCl to the xylem prevents a wound response togirdling. Alternatively, the high concentration of ions in theperfusing solution should cause shrinkage of any hydrogels.Thus perfusing with KCl solution should minimize the effectof any wound-induced gels on hydraulic conductance (Fig-ure 6). At present, we cannot distinguish between a reductionin phloem-to-xylem ion recycling and a wound response as the



Figure 4. Xylem sap osmolarity (mean ± SD). Upper and lowercaseletters indicate significant differences between treatment means (AN-OVA, performed separately for each species). The KCl treatment wasexcluded from the analysis.

Figure 5. Time course of water flow through branch segments of (A)A. rubrum and (B) A. saccharum at a constant pressure. Increases andreductions in flow were associated with changes between deionizedwater to 140 mOsm kg–1 KCl solution.

Table 1. Analysis of variance (ANOVA) tables for branch conductance and xylem sap ion concentration. Treatments for branch conductance are:no girdling/H2O (control), girdling/H2O, girdling/KCl. Treatments for isopiestic measurements of xylem sap ion concentration include samplescollected from: non-treated branches, control branches (no girdling/H2O), branches treated with girdling/H2O, and samples of water supplied tothe branch. The KCl treatment was excluded from the analysis of xylem sap concentrations as it overshadowed differences between the aboveeffects.

Description Effects d.f. MS F P

A. saccharum Treatment 2 0.0617 17.15 0.00002Xylem conductance Within 25 0.0036

A rubrum Treatment 2 0.0874 19.9 0.00015Xylem conductance Within 11 0.00437

A. saccharum Effect 3 237.29 2.81 0.0658Sap concentration Within 20 84.48

A rubrum Effect 3 305.15 3.10 0.0447Sap concentration Within 25 98.32

mechanism by which phloem girdling leads to changes in xy-lem conductance. Moreover, it is possible that both mecha-nisms contribute to the observed response to girdling and xy-lem sap ionic content.

The classical view that the dead xylem vessels allow for pas-sive transport of water between roots and shoots must be modi-fied to recognize that ions can rapidly alter xylem hydraulicconductance (Zwieniecki et al. 2001). Both of the species ex-amined here exhibited ion-mediated changes in xylem hydrau-lic conductance. Ion mediated enhancement of xylem conduc-tance reached values as high as 57%, similar to earlier observa-tions with A. saccharum (Zimmermann 1978). The magnitudeof the response suggests a functional link between xylem con-ductance and phloem mediated by the active exchange ofions from phloem to xylem via living parenchyma cells (Pate1975).

To our knowledge, this is the first study demonstrating thatphloem can influence the hydraulic performance of xylem on

time scales of minutes to hours. It is known that girdling canhave a dwarfing effect on plant and leaf size (Fumuro 1998);however, there is no direct evidence that the effect is mediatedby changes in water transport capacity. Girdling has been re-ported to affect the water status of vines, leading to a decreasein stomatal conductance and a drop in transpiration up to 50%(Williams et al. 2000). However, it was not determined wheth-er these effects were caused by a change in xylem hydrauliccapacity.

It is debatable whether short-term changes in xylem hydrau-lic resistance of the magnitude we observed are of biologicalsignificance. Xylem is only one component of the total resis-tance to water transport in plants, and the ability to alter flowrates via changes in xylem resistance depends on the relativecontribution of the xylem to the total resistance. Althoughstomata are the dominant resistance encountered as waterflows from soil to atmosphere (Jones 1992), their ability tocontrol flow rates may be constrained by their role in main-



Figure 6. A schematic outline of theproposed mechanisms underlyingphloem–xylem interactions in the de-termination of xylem hydraulic con-ductance. The upper panel indicates anongirdled branch, supplied with de-ionized water (thick arrow). The mid-dle panel shows an experimentally gir-dled branch supplied with deionizedwater, while the lower panel shows agirdled branch supplied with 140 mMKCl solution. Specific interactions oreffects are noted on the figure. Ques-tion marks indicate potential interac-tions.

taining a favorable leaf water status (Turner 1974, Tardieu andDavies 1993, Tardieu and Simonneau 1998). As in an electri-cal circuit with a voltage regulating component, the phloem–xylem system cannot be analyzed as a passive network. Whenleaves are operating at a constant water potential, as is fre-quently observed under conditions favorable to rapid transpi-ration, the flow rate through individual branches is propor-tional to branch relative xylem resistance. Thus, ion-mediatedchanges in xylem resistance may play an important role in re-distributing water flow to leaves within a complex network ofbranches subject to short-term changes in local conditions.Xylem–phloem interactions that couple rates of phloem ex-port with increased xylem conductivity are likely to have theirgreatest impact on plants with large complex canopies inwhich large changes in local conditions for photosynthesis oc-cur throughout the day.

Acknowledgments

This work was supported by grants from the Andrew W. Mellon Foun-dation, NSF IBN-0078155 and USDA NRICGP 9800878.

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