Tree Physiology 24, 911–917
© 2004 Heron Publishing—Victoria, Canada
A potential role for xylem–phloem interactions in the hydraulic
architecture of trees: effects of phloem girdling on xylem hydraulic
conductance
MACIEJ A. ZWIENIECKI,1,2 PETER J. MELCHER,1,3 TAYLOR S. FEILD1,4 and N. MICHELE
HOLBROOK1
1
Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA
2
Corresponding author ([email protected])
3
Present address: Department of Biology, Ithaca College, Ithaca, NY 14853, USA
4
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
Summary We investigated phloem–xylem interactions in
Acer rubrum L. and Acer saccharum Marsh. Our experimental
method allowed us to determine xylem conductance of an intact branch by measuring the flow rate of water supplied at two
delivery pressures to the cut end of a small side branch. We
found that removal of bark tissue (phloem girdling) upstream
of the point at which deionized water was delivered to the
branch resulted in a decrease (24% for A. rubrum and 15% for
A. saccharum) in branch xylem hydraulic conductance. Declines in hydraulic conductance with girdling were accompanied by a decrease in the osmotic concentration of xylem sap.
The decrease in xylem sap concentration following phloem
girdling suggests that ion redistribution from the phloem was
responsible for the observed decline in hydraulic conductance.
When the same measurements were made on branches perfused with KCl solution (~140 mOsm kg –1), phloem girdling
had no effect on xylem hydraulic conductance. These results
suggest a functional link between phloem and xylem hydraulic
systems that is mediated by changes in the ionic content of the
cell sap.
Keywords: Acer rubrum, Acer saccharum, hydrogel, xylem sap
ion concentration.
Introduction
Forest tree photosynthesis occurs in a varied and dynamic canopy environment. Much of this heterogeneity results from spatial and temporal variations in the effects of the trees themselves on light penetration, wind movement of leaves and
branches, and vapor pressure deficits. Leaves employ a number of physiological mechanisms (e.g., modulation of stomata
aperture, xanthophyll cycle regulation), allowing them to respond to short term changes in irradiance or evaporative conditions in ways that tend to maximize photosynthesis. The effect
of xylem sap ion concentrations on the hydraulic resistance of
the supply pathway (Zimmermann 1978, van Ieperen et al.
2000, Zwieniecki et al. 2001) has led to the suggestion that the
recirculation of ions between the phloem and xylem gives rise
to short term changes in canopy-level hydraulic architecture
(Zwieniecki et al. 2001). The existence of such a coupling
mechanism might allow trees to enhance water delivery to
branches currently experiencing high rates of photosynthesis.
Whether such active internal regulation occurs in trees remains to be demonstrated, although all of the component parts
required for such regulation are known to exist. In this paper,
we explore interactions between xylem and phloem, and their
effect on xylem water transport.
The xylem and phloem are the principal long-distance liquid transport pathways in plants. The xylem primarily transports water and nutrients from the soil to the leaves, while the
phloem transports photosynthate from sites of synthesis (e.g.,
leaves) or storage (e.g., tubers) to regions of active growth. In
flowering plants, transport in the xylem takes place through
the lumen of a series of axially connected cells, which are
non-living at maturity (Esau 1977). The driving force in the
xylem is generated by the evaporation of water from leaves. In
contrast, the phloem is comprised of axially connected living
cells, in which mass flow results from gradients in turgor pressure generated primarily by the accumulation of sugars and
potassium phosphate (Milburn 1979). The two parallel pathways are interconnected via parenchyma rays along the entire
length of the stem (Holl 1975, Esau 1977). The close connection between xylem and phloem suggests a functional linkage
(van Bel 1990). The phloem obtains water, ultimately, from
the xylem, while the concentration of certain ions in the xylem, in particular K+, is influenced by recirculation from the
phloem (Jeschke and Pate 1991, Pate and Jeschke 1995). Models of long distance transport indicate that changes in xylem
pressure potentials have a marked effect on rates of carbohydrate movement through the phloem (Boersma et al. 1991).
However, the question of whether xylem transport can be
modified by the phloem has not been addressed.
Xylem vessels are formed from dead cells, and it has been
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ZWIENIECKI, MELCHER, FEILD AND HOLBROOK
assumed that their hydraulic capacity remains constant with
the only variation being a change to a non-functional (i.e.,
embolized) state resulting from cavitation (Sperry and Tyree
1988). This binary view conflicts with reported changes in xylem hydraulic conductance in response to changes in ion concentration of the liquid flowing through the vessels (Zimmermann 1978, van Ieperen et al. 2000, Zwieniecki et al. 2001).
Changes in xylem flow rate that result from changes in the
ionic concentration of the perfusing solution are both reversible and repeatable and occur in all major groups of plants
(ferns, conifers, angiosperms) and growth forms (herbaceous
and woody), although the magnitude of the response varies
(Zwieniecki et al. 2001). A mechanistic analysis of this phenomenon in Laurus nobilis L. demonstrates that xylem conductance is related to ion concentration in the xylem sap and
that the effect involves the swelling or deswelling of hydrogels (most likely pectins) in inter-vessel pit membranes
(Zwieniecki et al. 2001). The existence of ion-mediated changes in xylem conductance leads to the possibility that living
xylem parenchyma cells actively modify xylem hydraulic
properties by altering the ion concentration in the xylem sap.
Ion concentration in the xylem sap is determined by two
processes, namely, uptake by roots and recycling from the
phloem (Pate and Jeschke 1995). Sap concentrations vary
temporally, with the concentration of some ions being inversely proportional to flow rate, some showing no relation to
flow rate and some varying in proportion to flow rate (Schurr
1998). Potassium ions (K+) appear to follow the latter pattern,
suggesting that the dilution effect of the transpirational flux
can be overridden by physiological processes (Schurr and
Schulze 1995). While investigating methods to estimate in
vivo changes in branch hydraulic conductance (Zwieniecki et
al. 2000), we observed that phloem girdling decreased xylem
conductance in several woody species (unpublished data). At
the time, we had no explanation for this observation. However,
the demonstration of ion-mediated changes in xylem hydraulic properties (Zwieniecki et al. 2001) provides a possible
mechanism to explain this effect. Specifically, cessation of
phloem transport could decrease lateral ion transport into the
xylem. The resulting decrease in xylem sap ion concentration
could, in turn, cause a decrease in xylem conductance. In this
study, we test whether mechanical injury to the phloem results
in a decrease of xylem hydraulic conductance and determine if
this effect can be overcome by providing ions to the xylem.
Traditional approaches to the determination of xylem hydraulic conductance require that branch segments be excised
from the plant, thus precluding an assessment of phloem–xylem interactions. Studies based on root pressurization allow
work on intact plants (Passioura and Munns 1984, Schurr and
Schulze 1995), however, the ability to discern changes in xylem hydraulic conductance may be obscured by the non-vascular resistances in both roots and leaves (Tyree and Ewers
1991). Here, we report an investigation of xylem–phloem interactions by measuring xylem sap flow in an intact branch
during the supply of water at two delivery pressures to the cut
end of a side branch.
Methods
Plant material and study site
Studies were performed on mature trees of Acer rubrum L. and
Acer saccharum Marsh., during June and July 2000 at the Harvard Forest (Petersham, MA). Both trees were open- grown.
South-facing branches, 6 to 10 m above the ground, were accessed from scaffolding. Measurements were made on a total
of 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 method
described in Zwieniecki et al. (2000). The approach was to
measure the steady state flow rate of deionized water or solution into a side branch while the main branch remained attached to the tree (Figure 1). Measurements were made at two
delivery pressures, allowing the hydraulic conductance to be
determined without explicit knowledge of the total driving
force. Measurements were made under steady state conditions,
justifying the use of a linear relationship between flow rate and
driving gradient:
Q1 /L = Pdelivery1 + Pplant
(1)
Q2 /L = Pdelivery2 + Pplant
(2)
where Q1 and Q2 are the flow rates into the petiole for two delivery pressures, Pdelivery1 and Pdelivery2, L is the conductance, and
Pplant is the hydrostatic pressure within the xylem. If we assume
that Pplant remains constant during the measurement cycle, then
the conductance (L) can be calculated as:
Figure 1. Diagram of the method used to measure in situ hydraulic
conductance.
TREE PHYSIOLOGY VOLUME 24, 2004
XYLEM–PHLOEM INTERACTIONS AND THE HYDRAULIC ARCHITECTURE OF TREES
L=
Q2 − Q1
Pdelivery2 − Pdelivery1
(3)
Flow rate was determined according to methods described
in Zwieniecki et al. (2000). The instrument consisted of two
air tanks connected to one of a set of interchangeable pressurized plastic solution reservoirs. The interchangeable reservoirs
allowed us to switch easily between solutions. Water flowed
from the pressurized reservoirs through a calibrated, polyetheretherketone (PEEK) capillary tube and was delivered to
the side branch via a low resistance tube (Figure 1). The pressure drop across the capillary tube was measured by two
pressure transducers (Omega PX236-100 Series, Omega Engineering, Stanford, CT). The relationship between the pressure
drop and the flow rate (and thus the conductance of the PEEK
tube) was previously determined empirically by directing the
outflow onto an analytic balance (± 0.01 mg). The minimum
resolution of the two-point flow meter (approximately ± 3.5 ×
10 –6 g s –1) was set by the accuracy of the differential pressure
measurement (± 3.5 kPa) and the conductance of the calibrated
tube (1.04 mg s–1 MPa –1).
Measurements began with removal of the side branch under
water to prevent air from entering the xylem. The cut surface
was subsequently shaved with a razor blade and the branch immediately attached to the two-point flow meter (Figure 1). The
flow rate into the branch was determined using first the lowpressure tank, followed by the high-pressure tank. This was
repeated at 1-min intervals (Figure 2A). Delivery pressures
913
(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 between
supply tanks showed that a relatively constant delivery pressure (and thus flow rate) was achieved rapidly (Figure 2B). In
general, consecutive measurements showed a slight change in
the delivery pressure; however, the calculated conductivity
was fairly stable after the first few minutes (Figure 2C).
Pushing water into the end of a cut side branch measures the
impedance of a network of hydraulic elements (branch, stem
and transpiring leaves). This precludes determination of the
exact water flow pathways that were measured (Zwieniecki et
al. 2000), but it allows us to assess changes in hydraulic conductance in response to our treatments. After 20 min, branches
were girdled ~20 cm proximal to the point at which the
two-point flow meter was attached. A 1-cm strip of the bark
was removed with a dull razor blade, without damaging the
xylem. The girdled region was covered with vacuum grease
and Parafilm (American National Can, Minasha, WI) to prevent water loss.
Sap analysis
Xylem sap samples were collected from each branch following the conclusion of the in vivo hydraulic measurements.
Branches were excised from the tree 20 cm proximal to the
point of attachment of the two-point flow meter and all leaves
immediately removed to stop transpiration. Sap was collected
from the distal end of the branch (downstream from the water/solution delivery point). The bark was removed from the
Figure 2. Example of results from a
single control run. (A) Time trace of
simultaneous output from two pressure transducers used to determine
flow rate. Upstream pressure (transducer 1) was switched automatically
at 1-min intervals between the high
and low pressure tanks. (B) Magnification of the portion of time trace
(A), steady state pressures were
reached within 20 s after a pressure
change. (C) Estimates of conductance
(L p) were calculated from the above
run. Gray areas represent final cut of
the branch from the tree.
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ZWIENIECKI, MELCHER, FEILD AND HOLBROOK
cut end of the branch and the xylem surface was shaved clean
with a razor blade. This surface was rinsed with deionized water and dried with clean tissue. Parafilm was wrapped tightly
around the branch end and a plastic tube was attached to the
branch through which suction was applied using a hand-held
vacuum pump. Liquid was released from the xylem into
the plastic tubing by repeatedly cutting the basal end of the
branch, a procedure that allows for the consecutive removal of
vessel end walls. The sap samples were rapidly transferred to
glass microcapillary tubes and sealed with Parafilm. We collected about 10 to 25 µl of sap from each branch. In addition,
sap was collected from 14 branches that were not used in the
hydraulic conductance measurements.
Osmolarity of sap (mOsm kg –1) was determined by measuring the total osmotic potential of the sap with isopiestic psychrometers according to methods outlined in (Boyer 1995).
Samples were held at a constant temperature until the output stabilized (~1 h). Thermocouple outputs were amplified
through a custom-built multiplexed nanovolt amplifier (BCMPNV 100; Burns Consulting, Altadena, CA) and recorded
by a computer.
Effect of ion concentration on xylem hydraulic conductance
The effect of ion concentration on xylem hydraulic conductance was determined on branch segments collected from the
same trees as used in the in vivo measurements. Flow rates
through 12-cm-long branch segments were measured by directing the outflow onto an analytical balance (± 0.1 mg).
Solutions were supplied at a constant delivery pressure
of 0.03 MPa. For each segment, flow was determined for
140 mOsm kg –1 KCl solution and subsequently for deionized
water (n = 8 for A. saccharum, n = 6 for A. rubrum). Oneyear-old branch segments were used in this study. The flow
enhancement that occurred in the presence of KCl was calculated as a percentage of that for water after returning from KCl
to deionized water.
ches was 24.1% for A. rubrum and 15.4% for A. saccharum.
When branches were perfused with ~140 mOsm kg –1 KCl, girdling did not significantly alter branch conductance (Figure 3).
However, there was a significant difference between girdled
branches measured with deionized water and girdled branches
measured with KCl (Figure 3). These results indicate that supplying KCl solution to the xylem prevented the reduction in
branch hydraulic conductance otherwise caused by girdling.
The osmolarities of xylem sap collected from intact branches and non-girdled branches perfused with deionized water
(control) were almost identical, indicating that supplying deionized water to the branch resulted in little dilution of the xylem sap (Figure 4). There was a trend for the osmolarity of the
sap of girdled branches to be lower than that in either intact or
non-girdled branches. However, these differences were not statistically significant (Figure 4). Branches perfused with KCl
solution had osmolarities similar to the supplied KCl solution,
which was significantly different from the osmolarities of
branches in other treatments.
We examined the effect of ions on the hydraulic conductance of the xylem using excised branch segments. In both
A. rubrum and A. saccharum, flow rates increased significantly
when the perfusing solution was switched from deionized water to a 140 mOsm kg –1 KCl solution (Figure 5). The magnitude of the increase varied among branch segments, ranging
from 15 to 57%, with a mean of 38%, for A. rubrum and from 8
to 29%, with a mean of 24%, for A. saccharum. Switching
from 140 mOsm kg –1 KCl back to deionized water returned the
flow rate to its initial value. The response was rapid, with stable flow rates occurring within several seconds of switching
between solutions. Because the driving force for water movement was constant, the observed changes in flow rate represent
changes in branch hydraulic conductance. The magnitudes of
these changes were similar to those observed in the in situ studies of branch conductance.
Results
Our experimental approach was to compare the effect of
phloem girdling on in situ measurements of branch hydraulic
conductance when side branches were supplied with either
deionized water or KCl solution. We used a high KCl concentration (140 mOsm kg –1) to saturate any ionic response of xylem hydraulic conductance. A non-girdled treatment, in which
branch hydraulic conductance was measured by perfusing the
branch with deionized water, served as a control. In situ measurements of branch hydraulic conductance typically showed
some variability during the first 5 to 10 min, after which the
readings stabilized. After 20 min of water perfusion, branch
hydraulic 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 water
was supplied to the branch resulted in a significant decrease in
the measured branch hydraulic conductance compared to the
non-girdled control (Figure 3; Table 1). The response to girdling was detected within 10 min. The mean reduction in
hydraulic conductance relative to non-girdled control bran-
Figure 3. Percent change in xylem hydraulic conductance (mean ±
SD) between 20 and 30 min after the start of conductance measurements. Girdling took place after 20 min of water/solution supply. Upper and lowercase letters indicate significant differences between
treatment means (ANOVA, performed separately for each species).
TREE PHYSIOLOGY VOLUME 24, 2004
XYLEM–PHLOEM INTERACTIONS AND THE HYDRAULIC ARCHITECTURE OF TREES
915
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 samples
collected from: non-treated branches, control branches (no girdling/H2O), branches treated with girdling/H2O, and samples of water supplied to
the branch. The KCl treatment was excluded from the analysis of xylem sap concentrations as it overshadowed differences between the above
effects.
Description
Effects
d.f.
A. saccharum
Xylem conductance
Treatment
Within
2
25
A rubrum
Xylem conductance
Treatment
Within
2
11
A. saccharum
Sap concentration
Effect
Within
3
20
237.29
84.48
2.81
0.0658
A rubrum
Sap concentration
Effect
Within
3
25
305.15
98.32
3.10
0.0447
Discussion
Decreases in the ionic concentration of the xylem sap are
thought to reduce xylem conductance because of the swelling
of hydrogels in bordered pit membranes (Zwieniecki et al.
2001). Thus, the decrease in hydraulic conductance of girdled
branches compared to non-girdled controls could reflect a decrease in xylem ion concentration caused by reduced ion transport between phloem and xylem. Addition of high concentrations of KCl eliminated the effects of girdling on xylem hydraulic conductance, suggesting that girdling affects xylem
sap ion concentration. Supporting this interpretation, the decrease in hydraulic conductance observed in the girdled branches was associated with a decline in the ion concentration of
the xylem sap.
Although our data are consistent with the hypothesis that
phloem girdling reduces xylem hydraulic conductance by affecting ion recycling from phloem to xylem, it is possible that
a more generalized wound response to girdling is involved.
Figure 4. Xylem sap osmolarity (mean ± SD). Upper and lowercase
letters indicate significant differences between treatment means (ANOVA, performed separately for each species). The KCl treatment was
excluded from the analysis.
MS
F
P
0.0617
0.0036
17.15
0.00002
0.0874
0.00437
19.9
0.00015
Pathogens are known to induce the production of vascular gels
(Van der Molen et al. 1983), and mechanical injury results in
the occlusion of vessels by pectin-like polysaccharides (Zimmermann 1983). An increase in hydrogel production in response to girdling could decrease hydraulic conductance by
physically obstructing flow through the xylem. However, this
requires an explanation of how the addition of KCl negated the
effect of girdling on hydraulic conductance. One possibility is
that supplying KCl to the xylem prevents a wound response to
girdling. Alternatively, the high concentration of ions in the
perfusing solution should cause shrinkage of any hydrogels.
Thus perfusing with KCl solution should minimize the effect
of any wound-induced gels on hydraulic conductance (Figure 6). At present, we cannot distinguish between a reduction
in phloem-to-xylem ion recycling and a wound response as the
Figure 5. Time course of water flow through branch segments of (A)
A. rubrum and (B) A. saccharum at a constant pressure. Increases and
reductions in flow were associated with changes between deionized
water to 140 mOsm kg –1 KCl solution.
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ZWIENIECKI, MELCHER, FEILD AND HOLBROOK
Figure 6. A schematic outline of the
proposed mechanisms underlying
phloem–xylem interactions in the determination of xylem hydraulic conductance. The upper panel indicates a
nongirdled branch, supplied with deionized water (thick arrow). The middle panel shows an experimentally girdled branch supplied with deionized
water, while the lower panel shows a
girdled branch supplied with 140 mM
KCl solution. Specific interactions or
effects are noted on the figure. Question marks indicate potential interactions.
mechanism by which phloem girdling leads to changes in xylem conductance. Moreover, it is possible that both mechanisms contribute to the observed response to girdling and xylem sap ionic content.
The classical view that the dead xylem vessels allow for passive transport of water between roots and shoots must be modified to recognize that ions can rapidly alter xylem hydraulic
conductance (Zwieniecki et al. 2001). Both of the species examined here exhibited ion-mediated changes in xylem hydraulic conductance. Ion mediated enhancement of xylem conductance reached values as high as 57%, similar to earlier observations with A. saccharum (Zimmermann 1978). The magnitude
of the response suggests a functional link between xylem conductance and phloem mediated by the active exchange of
ions from phloem to xylem via living parenchyma cells (Pate
1975).
To our knowledge, this is the first study demonstrating that
phloem can influence the hydraulic performance of xylem on
time scales of minutes to hours. It is known that girdling can
have a dwarfing effect on plant and leaf size (Fumuro 1998);
however, there is no direct evidence that the effect is mediated
by changes in water transport capacity. Girdling has been reported to affect the water status of vines, leading to a decrease
in stomatal conductance and a drop in transpiration up to 50%
(Williams et al. 2000). However, it was not determined whether these effects were caused by a change in xylem hydraulic
capacity.
It is debatable whether short-term changes in xylem hydraulic resistance of the magnitude we observed are of biological
significance. Xylem is only one component of the total resistance to water transport in plants, and the ability to alter flow
rates via changes in xylem resistance depends on the relative
contribution of the xylem to the total resistance. Although
stomata are the dominant resistance encountered as water
flows from soil to atmosphere (Jones 1992), their ability to
control flow rates may be constrained by their role in main-
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XYLEM–PHLOEM INTERACTIONS AND THE HYDRAULIC ARCHITECTURE OF TREES
taining a favorable leaf water status (Turner 1974, Tardieu and
Davies 1993, Tardieu and Simonneau 1998). As in an electrical circuit with a voltage regulating component, the phloem–
xylem system cannot be analyzed as a passive network. When
leaves are operating at a constant water potential, as is frequently observed under conditions favorable to rapid transpiration, the flow rate through individual branches is proportional to branch relative xylem resistance. Thus, ion-mediated
changes in xylem resistance may play an important role in redistributing water flow to leaves within a complex network of
branches subject to short-term changes in local conditions.
Xylem–phloem interactions that couple rates of phloem export with increased xylem conductivity are likely to have their
greatest impact on plants with large complex canopies in
which large changes in local conditions for photosynthesis occur throughout the day.
Acknowledgments
This work was supported by grants from the Andrew W. Mellon Foundation, NSF IBN-0078155 and USDA NRICGP 9800878.
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