Tree Physiology 21, 765–770
© 2001 Heron Publishing—Victoria, Canada
Stomatal and leaf growth responses to partial drying of root tips in
willow
L. LIU,1 A. J. S. McDONALD,2,5 I. STADENBERG3 and W. J. DAVIES4
1
Department of Plant Breeding and Genetics, International Rice Research Institute, P.O. Box 933, 1099 Manila, Philippines
2
Department of Plant and Soil Science, University of Aberdeen, Cruickshank Bldg, St. Machar Drive, Aberdeen AB24 3UU, U.K.
3
Department of Production Ecology, Swedish University of Agricultural Sciences, P.O. Box 7042, Uppsala, Sweden
4
Biological Sciences Department, Institute of Environmental and Natural Sciences, Lancaster University, Bailrigg, Lancaster LA1 4YQ, U.K.
5
Author to whom correspondence should be addressed
Received July 21, 1999
Summary Root tips of intact willow (Salix dasyclados
Wimm., Clone 81-090) plants were partially dried by exposure
to ambient greenhouse air and then kept in water-vapor-saturated air for up to 3 days. The drying treatment increased
abscisic acid (ABA) concentrations in both the roots tips subjected to drying and in the xylem sap, while it reduced leaf stomatal conductance and leaf extension rate. Despite the decrease in stomatal conductance, leaf water potentials were unaffected by the root drying treatment, indicating that the
treatment reduced hydraulic conductivity between roots and
foliage. After roots subjected to drying were returned to a nutrient solution or excised, ABA concentrations in the remaining
roots and in the xylem sap, stomatal conductance of mature
leaves and extension rate of unfolding leaves all returned to
values observed in control plants. The 4-fold increase in xylem
sap ABA concentration following the root drying treatment
was not solely the result of reduced sap flow, and thus may be
considered a potential cause, not merely a consequence, of the
observed reduction in stomatal conductance.
Keywords: abscisic acid, leaf extension rate, root drying,
stomatal conductance, willow.
Introduction
Several studies have indicated a likely role of root-sourced
chemical signals in the regulation of stomatal conductance
(e.g., Zhang and Davies 1987, 1989a, 1989b, Neales et al.
1989, Gowing et al. 1990, Khalil and Grace 1993, Masia et al.
1994) and leaf growth (e.g., Passioura 1988, Saab and Sharp
1989, Davies et al. 1990, Saab et al. 1990, Zhang and Davies
1990a, 1990b, Munns and Sharp 1993, Dodd and Davies
1994, Cramer et al. 1998) in response to soil drying. In many
instances, the dynamics of xylem sap abscisic acid (ABA)
concentration are related to changes in stomatal conductance.
It has been assumed that this is a causal relationship because
ABA is known to induce stomatal closure (see reviews by
Davies and Zhang 1991, McDonald and Davies 1996). Studies
with herbaceous species suggest that root-produced ABA, not
a hydraulic signal, is the major regulator of stomatal responses
to partial root drying. It is unclear, however, whether this is
also true of woody species (cf. Saliendra et al. 1995, Fuchs and
Livingston 1996). Consistent with the possible role of a hydraulic signal is evidence that leaf water status modulates
stomatal sensitivity to ABA (Tardieu and Davies 1993,
Tardieu et al. 1993).
Recently, we showed that ABA is synthesized in excised,
water-stressed leaves and roots of willow (Salix dasyclados
Wimm.) and that an exogenous supply of ABA fed to well-watered willow leaves causes partial stomatal closure (Liu 1998,
Liu et al. 2001). We therefore postulated that roots subjected to
drying produce ABA at an increased rate, thereby increasing
xylem sap ABA concentration, which in turn reduces stomatal
conductance. This hypothesis does not, however, preclude the
possibility that hydraulic signals (cf. Saliendra et al. 1995,
Fuchs and Livingston 1996) or changes in the compartmentation of leaf ABA in response to changes in xylem sap pH
(Wilkinson and Davies 1997, Wilkinson et al. 1998, Hartung
et al. 1998) mediate changes in stomatal conductance in response to root drying. Because ABA can inhibit leaf extension
growth in willow, we postulated that root-produced ABA has a
role in the inhibition of leaf extension in response to root drying. Here, we report on simultaneous changes in root and xylem sap ABA concentrations and in stomatal and leaf-growth
responses to root drying and rehydration in intact willow
plants.
Materials and methods
Preparation of plant material
Cuttings (~20 cm long) from 1-year-old stems of willow (Salix
dasyclados Wimm., Clone 81-090) were planted in a 2:1 (v/v)
peat:sand mixture in 2-l pots in a greenhouse. Additional illumination insured a minimum daylength of 12 h at a photosynthetic photon flux density (PPFD) of not less than 250 µmol
m –2 s –1 at the shoot apex. Diurnal temperature ranged from 22
to 30 °C. Relative humidity ranged from 30 to 45%.
The base of each pot was perforated with 50, 0.5-cm-diame-
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LIU, MCDONALD, STADENBERG AND DAVIES
ter holes. Pots were flushed with nutrient solution (Ericsson
1981) and then positioned above a container of nutrient solution, with the base of the pot 2–3 cm above the solution surface. Shoots began sprouting within about a week, and all but
two were removed as they sprouted. Three weeks after planting, roots appeared through the holes in the base of the pots,
and extended into the nutrient solution below. During the following 2 weeks, the nutrient solution in each container was
changed, initially, every 2 days and then daily. Plants that
showed poor shoot or root growth were discarded. Of the remaining plants, a few were harvested to determine the proportion of total root biomass external to the pot.
Root drying treatment
When the portion of root biomass outside the pot accounted
for 30 to 50% of total root biomass, the root drying treatment
was applied by laying the plant pots on the greenhouse bench
with the outgrowing roots exposed to ambient air for 15 min.
The pots were then placed in containers lined with wet tissue
to prevent further root desiccation, while preventing the roots
from making contact with liquid water. Twenty-four hours after the drying treatment, roots external to the plant pots were:
(1) retained in the humid environment for an additional 2 days;
(2) returned to nutrient solution; or (3) excised. Control plants
remained throughout with roots immersed in nutrient solution.
Roots external to the plant pots were excised from one group
of control plants.
Sampling and harvesting
For 3 days after the drying event, measurements of stomatal
conductance, leaf water potential and leaf length were made
on plants from all treatments. Additional plants were harvested for ABA analysis of leaf, root and xylem sap and for
root water content of outgrowing roots.
Leaf extension
Rates of leaf extension were calculated from successive length
measurements (± 0.5 mm) on leaves of similar size (one leaf
per plant).
Leaf water potential
Leaf water potential of the second or third fully extended leaf
from the shoot apex was measured in a custom-built pressure
chamber. The chamber pressure (compressed air) was increased at a rate of about 0.01 MPa s –1. The resolution of the
pressure meter was 0.001 MPa.
Stomatal conductance
Stomatal conductance to water vapor was measured with a leaf
porometer (AP4 Porometer, Delta-T Devices, Cambridge,
U.K.) on the first or second fully extended leaf from the shoot
apex. Artificial illumination was used as necessary to insure a
PPFD incident on the leaf to be measured of at least 350 µmol
m –2 s –1 for 10 min before measurement. Each measurement
took about 1 min and the number of measurements on any occasion was kept to a minimum to avoid build-up of CO2 respired by the operator. A directional fan further limited local
accumulation of CO2 while measurements were being made.
The porometer chamber was attached to one side of the midrib
halfway along the leaf and evaporative loss was measured
from the lower leaf surface. In all experiments, measurements
were made on one leaf from each of five randomly selected
plants per treatment. Successive measurements were made on
plants from different treatments.
Sampling of plant material for ABA analysis
Leaves selected for stomatal conductance measurements were
subsequently harvested for ABA analysis. Immediately after
the porometer measurement, the leaf was excised and one half
of the blade excluding the midrib was removed, frozen in liquid nitrogen, wrapped in aluminum foil to prevent
photodegradation of ABA, and stored at –20 °C.
Abscisic acid was measured in root sections that were harvested within 10 min of leaf harvesting. Measurements were
made on samples of approximately 10 root tips, each 3–5 cm
in length. Sample fresh weight (leaf or root material) was
about 150 mg. Root pieces were frozen in liquid N, foil
wrapped and stored at –20 °C.
Collection of xylem sap for ABA analysis
Xylem sap was collected for ABA analysis immediately after
leaf and root samples had been taken. Shoots of plants to be
sampled were excised 10–15 cm above the soil surface. Five
cm of bark was peeled from the upper end of the stump to reduce contamination of extruded xylem sap by phloem exudate.
The peeled stem was secured in the lid of a custom-built pressure chamber. The root system was then placed in the chamber
and the lid sealed with the stump protruding (about 2 cm) from
the lid. Silicone tubing was attached to the protruding stem to
collect extruded sap. The pressure in the chamber was increased at approximately 0.02 MPa s –1 to a final value of
0.2 MPa. A sample of at least 100 µl (typically 150–200 µl)
was collected with a capillary pipette from the tubing reservoir
and transferred to a 200-µl tube. During collection of sap,
which took less than 10 min, the collection tube was wrapped
in aluminum foil to prevent sample evaporation and photodegradation of ABA. After collection, the sample tubes were
cooled in liquid N, wrapped in aluminum foil and stored at –20
°C.
Radioimmunoassay (RIA) for ABA
Before analysis, root and leaf samples were freeze-dried.
Dried samples of 60 mg were ground in 10-ml polyethylene
tubes and 1.5 ml of sterile deionized water was added to each
tube. The tubes were placed in a rack on a shaker for 8–10 h at
4 °C in darkness. After extraction, tubes were stored at –20 °C.
For analysis, the samples were thawed at room temperature in
the dark, and a 50-µl aliquot of the supernatant or xylem sap
transferred to a 2-ml tube for radioimmunoassay determination of ABA concentration, as described by Quarrie et al.
(1988). The monoclonal antibody, MAC252, was supplied by
Steve Quarrie (John Innes Centre, Norwich, U.K.). A contamination test was run to confirm the appropriateness of using
aqueous extracts of root and leaf samples for ABA analysis.
TREE PHYSIOLOGY VOLUME 21, 2001
ROOT DRYING IN WILLOW
767
Root water content
Outgrowing roots were weighed fresh, oven-dried at 70 °C for
48 h and reweighed and their original water content determined by difference.
Statistics
Treatment effects were assessed by analysis of variance (Microsoft Excel Version 5.0, single-factor ANOVA). The significance of treatment effects was assessed at P = 0.05.
Results
Root water content and leaf water potential
Three hours after the root drying treatment, root water content
was significantly lower (P = 0.05) than in well-watered controls (Figure 1), and the difference persisted throughout the
3-day measurement period. Within one day of rewatering,
there was no longer a significant effect (P = 0.05) of the root
drying treatment on root water content. Leaf water potentials
did not differ significantly (P = 0.05) among treatments on any
measurement occasion (Figure 2).
Stomatal conductance and leaf extension
Three hours after treatment, stomatal conductance and leaf extension rate were 30–40% lower in plants subjected to the root
drying treatment compared with well-watered controls (Figures 3 and 4). These differences persisted throughout the 3-day
measurement period so long as roots external to the plant pots
were not rewatered. However, when roots exposed to the drying treatment were rewatered after an interval of 24 h, both
stomatal conductance of mature leaves and extension rate of
young leaves measured one day later did not differ significantly (P = 0.05) from those of well-watered controls. Excising roots external to the pot, i.e., those subjected to drying,
Figure 1. Time course of root water content (% of fresh weight) in response to a root drying treatment and subsequent rewatering. At time
t = 0, part of the root system of a number of plants was exposed to a
drying event (䊏). Other plants served as controls (䉬). At time t = 24 h,
roots subjected to drying were either rewatered (䊊) or held in water-vapor-saturated air. Bars indicate ± SE; shaded bars denote hours
of darkness; and n = 5.
Figure 2. Time course of leaf water potential (MPa) in response to a
root drying treatment and subsequent perturbations. At time t = 0, part
of the root system of a number of plants was exposed to a drying event
(䊏). Other plants served as controls (䉬). At time t = 24 h, roots that
had experienced drying were either rewatered (䊊), excised (䊐) or
held in water-vapor-saturated air. At time t = 24 h, part of the root system was also excised from some of the control plants (䉫). Inset: the
time course of leaf water potential during the first 6 h following the
root drying treatment. Bars indicate ± SE; shaded bars denote hours of
darkness; and n = 5.
had the same effect as rewatering. In well-watered controls, removing roots external to the pot, i.e., those immersed in nutrient solution, had no effect on stomatal conductance or leaf
Figure 3. Time course of stomatal conductance (% of control) in response to a root drying treatment and subsequent perturbations. At
time t = 0, part of the root system of a number of plants was exposed to
a drying event (䊏). Other plants served as controls (䉬). At time t =
24 h, roots that had experienced drying were either rewatered (䊊), excised (䊐) or held in water-vapor-saturated air. At time t = 24 h, part of
the root system was excised from some of the well-watered controls
(䉫). Bars indicate ± SE; shaded bars denote hours of darkness; and n
= 5.
TREE PHYSIOLOGY ONLINE at http://heronpublishing.com
768
LIU, MCDONALD, STADENBERG AND DAVIES
well-watered controls. The concentration of ABA in xylem
sap (Figure 6) increased significantly (P = 0.05) within 3 h of
the root drying treatment, compared with that of well-watered
controls, and the difference was maintained throughout the
3-day measurement period. Within one day of rewatering or
removal of the roots subjected to drying, ABA concentration
in the xylem sap was not significantly different (P = 0.05) from
that of well-watered controls. The concentration of ABA in
leaves (Figure 7) did not differ (P = 0.05) among treatments on
any measurement occasion.
Discussion
Root ABA concentration increased significantly within 3 h of
the root drying treatment and remained high so long as treated
roots were not rewatered (Figure 5). Rewatering resulted in a
rapid decrease in root ABA concentration to the value of
The 15-min root drying treatment caused a measurable reduction in water content of roots external to the plant pot (Figure 1) and substantial decreases in stomatal conductance and
leaf extension rate (Figures 3 and 4, respectively). Although
stomatal conductance decreased, leaf water potentials approximated those found in control plants (Figure 2). This indicates
that hydraulic conductivity between the upper (wet) part of the
root system and the leaves must have decreased in response to
the root drying treatment.
The decrease in hydraulic conductivity is likely to have been
due to a change in the large resistance to radial water movement in the root rather than in the smaller resistances to axial
transport in roots and stems (cf. Steudle and Peterson 1998). In
woody species, the radial apoplastic bypass to water transport
has a much higher conductivity than the parallel cell-to-cell
pathway and is generally found to increase with increasing
transpiration rates (cf. Steudle and Frensch 1996, Steudle and
Peterson 1998, Steudle 2000 and references therein), possibly
because of an increase in the effective cross-sectional area.
Decreased stomatal conductance (and transpiration rate) fol-
Figure 5. Time course of root ABA concentration (nmol gdw –1) in response to a root drying treatment and subsequent perturbations. At
time t = 0, part of the root system of a number of plants was exposed to
a drying event (䊏). Other plants served as controls (䉬). At time t =
24 h, roots subjected to drying were either rewatered (䊊) or held in
water-vapor-saturated air. Bars indicate ± SE; shaded bars denote
hours of darkness; and n = 5.
Figure 6. Time course of xylem ABA concentration (% of control) in
response to a root drying treatment and subsequent perturbations. At
time t = 0, part of the root system of a number of plants was exposed to
a drying event (䊏). Other plants served as controls (䉬). At time t =
24 h, roots subjected to drying were either rewatered (䊊), excised (䊐)
or held in water-vapor-saturated air. At time t = 24 h, part of the root
system was excised from some of the well-watered controls (䉫). Bars
indicate ± SE; shaded bars denote hours of darkness; and n = 5.
Figure 4. Time course of leaf extension (% of control) in response to a
root drying treatment and subsequent perturbations. At time t = 0, part
of the root system of a number of plants was exposed to a drying event
(䊏). Other plants served as controls (䉬). At time t = 24, roots subjected to drying were either rewatered (䊊), excised (䊐) or held in water-vapor-saturated air. At time t = 24 h, part of the root system was
excised from some of the well-watered controls (䉫). Bars indicate ±
SE; shaded bars denote hours of darkness; and n = 5.
extension rate (P = 0.05).
ABA concentration
TREE PHYSIOLOGY VOLUME 21, 2001
ROOT DRYING IN WILLOW
Figure 7. Time course of leaf ABA concentration (nmol gdw –1) in response to a root drying treatment and subsequent perturbations. At
time t = 0, part of the root system of a number of plants was exposed to
a drying event (䊏). Other plants served as controls (䉬). At time t =
24 h, roots subjected to drying were either rewatered (䊊), excised (䊐)
or held in water-vapor-saturated air. At time t = 24 h, part of the root
system was excised from some of the well-watered controls (䉫). Bars
indicate ± SE; shaded bars denote hours of darkness; and n = 5.
lowing the root drying treatment (Figure 3) may, therefore,
have lowered the hydraulic conductivity in the apoplast,
thereby preventing leaf water potential from recovering to pretreatment values. If so, the change in hydraulic conductivity
would have been the result, not the cause, of the observed
changes in stomatal conductance and transpiration rate.
Our results do not preclude the possibility of root-sourced
hydraulic signals or changes in xylem pH in the rapid control
of stomatal aperture. However, our data are consistent with a
contribution from root-sourced ABA in the overall regulation
of stomatal conductance in response to root drying. This argument is consistent with the 10-fold increase in root ABA concentration (Figure 5) in response to the root drying treatment,
which was followed by a fourfold increase in xylem sap ABA
concentration (Figure 6). The large increases in root and xylem sap ABA concentration cannot be explained solely by the
concentrating effects of a 50% reduction in stomatal conductance (Figure 3) and hence sap flow velocity. Increased xylem
sap ABA concentration must, therefore, be considered as a potential cause of the observed decrease in stomatal conductance.
There is evidence that ABA can increase hydraulic conductivity in the cell-to-cell pathway of roots, perhaps by affecting
water channels in the membrane (cf. Steudle 2000). If an
ABA-induced transcellular response occurred in our experiment, its importance to the overall hydraulic conductivity of
the root would depend on the extent to which the apoplastic
pathway dominates. However, the net response to root drying
was an apparent decrease in overall hydraulic conductivity,
consistent with the overriding contribution of variable hydraulic conductivity in the apoplast of root cells in woody species
at all but the lowest transpiration rates (cf. Steudle 2000).
769
Full recovery of stomatal conductance following rewatering
or excision of drying roots (Figure 3) without any significant
change in leaf water potential (Figure 2) indicates that hydraulic conductivity must have increased between the remaining
part of the root system and the shoot. An indirect increase in
hydraulic conductivity might be expected following increased
stomatal conductance (Figure 3) and transpiration rate (cf.
Steudle and Frensch 1996, Steudle and Peterson 1998, Steudle
2000 and references therein). This would be consistent with
the observation that rewatering or root excision causes removal of an ABA source (Figure 5) and decreased xylem ABA
concentration (Figure 6). Excision of roots external to the
plant pot had no effect on xylem ABA concentration or
stomatal conductance in control plants (Figures 6 and 3, respectively).
The root drying treatment had no significant effect on leaf
ABA concentration (Figure 7). Consistent with this finding,
Jeschke et al. (1997) observed rapid degradation of imported
leaf ABA in Ricinus communis L. Likewise, Jia et al. (1996)
and Zhang et al. (1997) found that the bulk of ABA transported
in the xylem was rapidly metabolized in the leaves of
Commelina communis L. and Zea mays L. They concluded
that shoot physiology was affected by ABA delivered in the
xylem sap without measurable change in bulk leaf ABA concentration. Similarity among treatments in bulk leaf ABA concentrations does not necessarily preclude local differences in
ABA concentration (cf. Zhang and Davies 1987) caused, for
example, by pH-dependent shifts in the partitioning of ABA
between the apoplast and cytosol (Wilkinson and Davies 1997,
Hartung et al. 1998, Wilkinson et al. 1998).
Decreases in leaf extension rate in response to root drying
(Figure 4) followed the increases in root and xylem ABA concentrations (Figures 5 and 6, respectively). Because leaf extension rate has been shown to decrease in leaves fed with ABA in
the xylem stream (e.g., Dodd and Davies 1994, Cramer et al.
1998), we conclude that increased xylem ABA concentration
may have caused the observed reduction in leaf extension rate
in willow plants subjected to the root drying treatment. Removal of the ABA source by rewatering or excision of roots
subjected to drying resulted in recovery of leaf extension rates
in the young leaves to values found in control plants. The dynamics of leaf extension thus appear to have followed those of
ABA concentration in the xylem.
In conclusion, root-sourced ABA increased in response to a
root drying treatment in intact willow plants. An associated increase in xylem sap ABA was associated with decreases in
stomatal conductance and leaf extension rate, without significant perturbation in leaf water potential. The reduction in
stomatal conductance without a significant change in leaf water potential implies that the root drying treatment decreased
hydraulic conductivity between roots and leaves. This is consistent with the known effect of transpiration rate on hydraulic
conductivity in roots of woody species, and is consistent with
the view that decreased hydraulic conductivity was the result,
not the cause, of decreased stomatal conductance following
the root drying treatment. The reported dynamics of ABA concentrations in the root and xylem in response to root drying are
TREE PHYSIOLOGY ONLINE at http://heronpublishing.com
770
LIU, MCDONALD, STADENBERG AND DAVIES
consistent with a role for ABA as an inhibitor of stomatal
opening and leaf extension (Liu 1998, Liu et al. 2001).
Acknowledgments
The authors thank the technical staff at The Swedish University of
Agricultural Sciences, and at the Universities of Aberdeen and Lancaster for support with the experimental work. The research was
funded by The Swedish National Board for Industrial and Technical
Development.
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