Review
Chemical root to shoot signaling
under drought
Daniel P. Schachtman1 and Jason Q.D. Goodger2
1
2
Donald Danforth Plant Science Center, 975N. Warson Rd, St. Louis, MO 63132, USA
School of Botany, The University of Melbourne, VIC 3010 Australia
Chemical signals are important for plant adaptation to
water stress. As soils become dry, root-sourced signals
are transported via the xylem to leaves and result in
reduced water loss and decreased leaf growth. The presence of chemical signals in xylem sap is accepted, but
the identity of these signals is controversial. Abscisic
acid (ABA), pH, cytokinins, a precursor of ethylene,
malate and other unidentified factors have all been
implicated in root to shoot signaling under drought. This
review describes current knowledge of, and advances in,
research on chemical signals that are sent from roots
under drought. The contribution of these different
potential signals is discussed within the context of their
role in stress signaling.
Chemical and hydraulic signaling under drought
stress
Numerous studies have shown that plant roots can sense
changes in abiotic factors such as soil water content [1,2],
soil bulk density or compaction [3], soil oxygen content [4]
and changes in the nutrient composition of soil (both
enrichment and depletion) [5]. Root sensing of water deficit
has been widely studied, and this review focuses on the
outcomes of the early stage of water-deficit sensing: the
transport through the xylem of chemical signals that ultimately reduce leaf transpiration and leaf growth. Chemical signals can be differentiated from hydraulic signals [6]
but both are important because they reduce stomatal
conductance and leaf growth under conditions of water
deficit. Chemical signals most probably dominate during
early stages of stress before hydraulic signals are produced
[7], and become less important under severe drought when
leaf water potential declines and leaves wilt. It is likely
that the hydraulic signals that may trigger the production
of the hormone abscisic acid (ABA) in leaves dominate as
plants become more water stressed [8]. This review focuses
on chemical signals because of their importance during the
early stages of plant response to water deficit, and because
their manipulation has applications in increasing water
use efficiency (WUE) in agriculture.
Agricultural practices involving chemical signals:
deficit irrigation and partial root-zone drying
Root to shoot signaling under conditions of both mild and
severe drought is an important area for research because of
its implications for agricultural production and the WUE of
plants. Fresh water supplies are predominantly used for
Corresponding author: Schachtman, D.P. ([email protected]).
agriculture, but this usage will need to be reduced in the
future as supplies become limited. Where irrigation can be
manipulated, researchers have experimented with, and
successfully implemented, both deficit irrigation and partial root-zone drying (PRD) [9,10]. Both of these drying
regimes reduce leaf transpiration and limit vegetative
growth, thereby increasing WUE, and have demonstrated
efficacy in both woody perennials [9] and herbaceous crop
plants [11,12] (Box 1). Although these treatments can
increase the WUE of certain crop species, knowledge of
the role of chemical signals sent from root to shoot during
such practices is still developing [13]. Some studies have
shown that chemical signals such as ABA are generated by
the reductions in soil water content and act on the leaves to
reduce transpiration and growth [14].
Where PRD and deficit irrigation have been used in
agriculture, the most success has come from applications to
tree crops and to vines (in viticulture) [9,10]. With horticultural crops, the management of individual plants is
more intensive and economic return is often linked to fruit
quality. In one study, the use of PRD or deficit irrigation in
viticulture increased WUE by about 40% while only
decreasing yield by 15% [10]. PRD improved the quality
of the grape berry by increasing the anthocyanin content
[10] and the quality of wine produced [1]. In tomato (Lycopersicon esculentum), PRD has been shown to increase crop
quality. For example, one PRD study found a 21% increase
in the Brix value of fruit (a measurement of the mass ratio
of dissolved sugar to water), and a 50% increase in WUE
with only a 15% decrease in yield [15]. A physiological
explanation for such a small reduction in yield has been
proposed on the basis that the fruit receives water and
minerals from the xylem early in development, but later,
more than 90% of the water supplying the fruit is transported via the phloem [15]. Particularly in arid climates,
the use of precision irrigation methods such as PRD and
deficit irrigation puts into practice the principles developed
from basic scientific studies on how root signals increase
WUE while maintaining crop quality and yields.
ABA is a key regulator of leaf stomatal conductance
The production of ABA in roots and its transport to the
leaves provides the plant with a mechanism for transmitting a chemical signal to report on the water status of the
soil. This system could have evolved specifically for this
purpose or the chemical signal could merely be a consequence of the increased production of ABA required to
maintain root growth under water deficit [16]. A dominant
1360-1385/$ – see front matter ß 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.tplants.2008.04.003 Available online 6 May 2008
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Review
Box 1. Partial root-zone drying and deficit irrigation in
plants
Partial root-zone drying (PRD) and deficit irrigation (DI) are
examples of the manipulation of root signals to enhance the water
use efficiency (WUE) of agriculture. PRD is an irrigation method
where half the root zone is allowed to dry while the other half is kept
wet. After a period of time, the irrigation is alternated so that the
previously dry root zone receives water and the previously watered
side is allowed to dry. DI is an irrigation method in which the
amount of water supplied is less than that required to achieve
maximum crop evapotranspiration. Both methods can reduce
transpiration and leaf growth while increasing WUE with only small
decreases in yield.
Outstanding questions
Is the source of ABA that results in stomatal closure under drought
coming from the roots or the leaves?
How much variation in root to shoot signaling and xylem sap
composition is there within a species?
How does the nutrient status of a plant interact with chemical
signaling during water stress?
In which region of the root and in which particular root cells is ABA
synthesized?
What are the different forms of cytokinins that are transported in
xylem sap, and what roles do they play in root to shoot signaling?
What causes changes in pH in sap under drought and why do pH
changes appear inconsistent between certain species?
role for ABA in root to shoot signaling under drought and in
the control of stomatal conductance was demonstrated in
early reports [17]. Several groups have also used a bioassay
approach to show that ABA that is fed to leaves decreases
transpiration [18,19]. It is also well known that ABA has a
direct effect on guard cell closure [20]. However, the ABA
that acts on guard cells may not originate entirely in the
roots. Recent reports suggest that the ABA that acts on
guard cells could be produced in the leaves of some species,
such as tomato and sunflower [21–23]. In tobacco (Nicotiana plumbaginifolia), grafting experiments showed that
ABA came from the roots under conditions of drought [24].
ABA is synthesized in both roots [25] and leaves, but not
much is known about the precise location of this synthesis
in roots, which may influence how plants perceive and
monitor soil water content. ABA content in roots is well
correlated with both soil moisture and the relative water
content of roots in many plant species [26,27]. Some reports
suggest that ABA is synthesized in root tips [28], but
synthesis has been assessed mainly by measuring ABA
content rather than synthetic activity, so conclusions
related to the site of synthesis need to be re-examined
more carefully. One study using detached roots of pea
(Pisum sativum) and Asiatic dayflower (Commelina communis) found that ABA synthesis occurred somewhere
between the root tip and a point 3 cm distal to the tip
[29]. Recent studies have tried to locate enzymes that are
involved in ABA biosynthesis, including aldehyde oxidase,
which catalyzes the final steps in ABA biosynthesis; however, these studies have focused on ABA production under
differing nitrogen nutrition rather than drought stress
[30]. More work will be required to clarify exactly where
the ABA is produced in roots under drought stress.
Although the role of ABA in controlling stomatal conductance is strongly supported by many experiments
and experimental approaches [25], there may be other
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substances in the sap that act in concert with ABA to
control drought-induced stomatal closure. For example,
recent findings have suggested an interaction between
jasmonic acid and ABA in plants under drought stress
[31]. In addition, the dominant role of ABA as a root to
shoot signal has been challenged by experiments showing
that the ABA concentrations of xylem sap from droughtstressed plants were much lower than the concentrations
of exogenous ABA required to close stomata in detached
leaves [32]. It may be that the use of exogenous hormones
in bioassays may exclude important components of xylem
sap that act synergistically with ABA in planta, thus
accounting for the higher levels of exogenous ABA that
are required to reduce transpiration. Grafting experiments
have also been used to determine the source of ABA in
drought-induced stomatal closure. Some of these experiments suggest that leaf-sourced ABA is important for
stomatal closure [22], but the influence of ABA precursors
that might be transported from roots to leaves was not
measured, and therefore the role of roots in chemical
signaling was not completely resolved [25]. Other studies
show that production of ABA in the rootstock has a strong
influence on and is negatively correlated with stomatal
conductance [33]. Overall, ABA is a dominate signal in
controlling growth and transpiration, but other factors
could also be important. The importance and role of
root-sourced ABA is still controversial, but some of the
conflicting findings may be due to differences in the intensity of stress imposed and the time-course of the development of water deficit.
Involvement of pH in signaling
Changes in the pH of xylem sap commonly observed under
drought stress can be an important component of root to
shoot signaling and may act synergistically with ABA. In
many plant species (e.g. sunflower [Helianthus annuus]
[34], Phaseolus coccineus [35] and C. communis [36]), xylem
sap pH becomes more alkaline when plants are water
stressed and this leads to enhanced stomatal closure
and even reduced growth. The potential effects of pH have
been outlined previously [37] and include: i) changes in
ABA metabolism resulting in increased leaf ABA concentration; ii) direct effects on leaf water status that could
alter guard cell turgor or sensitivity to leaf ABA concentrations; iii) direct effects on ion fluxes through the guard
cell plasma membrane; and iv) altered distribution of ABA
in the leaf, specifically an increase the concentration of
ABA in the apoplast outside of the guard cells (Figure 1). It
is this change in apoplast pH that probably has the greatest role in signaling.
As ABA is a weak acid it may become protonated or
deprotonated in the pH range found in the apoplast of
leaves. This was clearly shown in the early 1980s in
experiments on mesophyll protoplasts that documented
high rates of ABA uptake at acidic pH and almost no
uptake at the more alkaline pH of 7.5 [38]. In certain plant
species, the pH of the leaf apoplast increases as the soil
dries because of the delivery of xylem sap that is of a more
alkaline pH. The ABA that arrives from roots via the xylem
will remain deprotonated under the more alkaline conditions and will not be taken up passively by mesophyll
Review
cells. The result is that less ABA is transported into the
mesophyll cells and a build-up of ABA in the apoplast leads
to enhanced stomatal closure. Under well-watered conditions, when the apoplast is more acidic, ABA would
passively enter the symplast, and apoplastic concentrations would not increase as rapidly as they do under
water stress. Therefore, the effect of pH is indirect in that it
leads to the accumulation of ABA in the apoplast and
enhances the effect of ABA on guard cells [35].
This mechanistic explanation is both attractive and
intuitive. Nevertheless, the explanation sets up another
hypothesis that ABA receptors are on the plasma membrane rather than inside the guard cells. Recently, three
ABA receptors have been found [39–41]. Two of these ABA
receptors reside inside the cell but a third was found on the
cell surface [39]. Therefore, plant cells could sense both
extracellular and intracellular ABA concentrations. Under
conditions of drought, the increased stomatal closure that
occurs because of the increased pH of sap suggests that
extracellular ABA is sensed by guard cells via receptors on
the plasma membrane.
Several studies have shown that pH does not act alone
on guard cells or in controlling leaf growth. For example,
the use of tomato [42] and barley (Hordeum vulgare) [43]
mutants that are deficient in ABA biosynthesis showed
that ABA was necessary for both stomatal closure and the
inhibition of leaf growth. In the tomato mutant flacca,
transpiration increased as the pH of artificial sap
increased, suggesting that ABA is also necessary to prevent stomatal opening and water loss. In the barley mutant
Az34, ABA was necessary for pH to act as a signal under
conditions of drought stress [43]. Many studies that show a
role for pH in stomatal closure have used tomato as a model
system. It is important to point out, however, that there
may be differences in response to ABA and pH between
species and perhaps even between genotypes within the
same species. One study compared C. communis and Arabidopsis thaliana and found that the increased pH of
external solutions led to a 27% increase in stomatal opening in C. communis but had no effect on A. thaliana [44].
Both species, however, responded similarly in the presence
of ABA and only changes in the kinetics of response were
observed. In soybean (Glycine max) [45], xylem sap pH did
not change in response to mild drought and was not
correlated with decreased stomatal conductance during
the initial stages of drought. The xylem sap of soybean
did, however, become more alkaline during extended
drought, but this alkalization occurred well after a
measured decrease in stomatal conductance.
The response of xylem sap pH to drought stress does not
appear to be consistent in all species or even in different
experiments using the same species. One study showed
that the sap pH of sunflower and C. communis did not
change significantly as soil dried, whereas the xylem sap
pH of tomato did increase as soil dried [46]. In maize (Zea
mays) grown using ammonium as the nitrogen source,
there was no change in sap pH during early [7] or even
during later stages of drought (L. Ernst and D.P. Schachtman, unpublished). Other experiments using maize have
been conducted in the field and have found that the sap pH
of drought-stressed plants growing on a loam soil was more
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Vol.13 No.6
alkaline as the period of drought lengthened [47]. Such
inconsistencies may be explained by the fact that solute
concentrations within the xylem sap vary with flow rate in
intact plants [48,49]. The sap solute concentrations and
delivery rates that best represent those of xylem sap flow in
intact plants are most accurately determined when sap is
collected at rates equivalent to whole-plant transpiration.
Therefore the rate of whole plant transpiration must be
determined prior to detopping plants to harvest sap. External pressure must be applied to roots so that sap exudes at
the flow rate of whole plant transpiration, a fact often
overlooked by experiments in which only xylem sap is
collected [49].
The mechanism of pH change might involve nitrate
availability. As soils dry, nutrient availability is reduced
because of physiochemical changes. Under conditions of
reduced nitrate availability, nitrate reductase activity
shifts to roots, causing changes in the pH of sap [50].
Changes in the activity of nitrate reductase that are caused
by drought conditions lead to changes in organic acid
production, which alter sap pH. In particular, malate
concentration increases in xylem sap under drought,
resulting in sap that is less acidic than that in well-watered
conditions when more nitrate is loaded into the xylem.
When the effects of a nitrate reductase inhibitor (sodium
tungstate) were tested [51], the inhibitor was found to
prevent the alkalization of the sap in tomato under drought
conditions. Similarly, the addition of nitrate to tomato
under water-stress conditions enhanced the alkalization
of the xylem sap [46]. A synergistic effect of xylem nitrate
and ABA on stomatal conductance in detached leaves of C.
communis has also been shown [46]. Moreover, the results
of work on maize suggest that, under some circumstances
where neither compound is as effective alone, a combination of ABA and nitrate is required to elicit an effect on
shoot physiology [52].
The effects of changes in the internal pH of the guard
cells have been very well characterized [20]. Less is known
about the effects of apoplastic changes in pH on guard cells,
but one study [53] showed that stomatal opening is inhibited by acidification and that the plasma membrane potential is depolarized (which would facilitate the opening of
outward-rectifying potassium channels) when the apoplast
is acidified. More studies are needed to clarify the effects of
changes in external pH on guard cells when the internal
pH is held constant. If extracellular alkalinization
also leads to an increased intracellular pH, it could be
an important part of the signaling process for stomatal
closure.
Conjugates of ABA as potential signals
Although ABA seems to play a dominant role in root to
shoot signaling under drought, it also seems likely, on the
basis of several studies, that other substances are also
involved. ABA is present in xylem sap in conjugated forms,
such as abscisic acid-glucose ester (ABA-GE). It has been
suggested that a conjugated form of ABA could serve as a
transported form of the hormone and, moreover, as a stress
signal [32,54]. As many as six ABA conjugates have been
found in xylem sap from well-watered and water-stressed
sunflower [55], and a correlation was found in one study
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Trends in Plant Science Vol.13 No.6
Figure 1. Changes in xylem sap composition under drought. Drought causes the alkalinization of xylem sap pH in certain plant species. (a) Well-watered plant with
apoplastic pH 6.0. (b) Plant under drought conditions with apoplastic pH 7.0. In plants in which xylem sap pH increases when the soil becomes dry, ABA-induced stomatal
closure is enhanced. This is thought to be due to increased apoplastic concentrations of ABA. Further changes in xylem sap composition under drought are also responsible
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between increased ABA-GE concentrations and drought
[56]. The importance of conjugated forms of ABA in
drought responses and the mechanisms of hydrolysis
[57] of such forms of ABA in the apoplast are, however,
still poorly understood. A next step in establishing the
importance of conjugated forms of ABA might be to genetically vary the hydrolysis of ABA conjugates. To do this, it
will be essential to identify the genes encoding the apoplastic b-glucosidases that are responsible for hydrolysis
before subsequent manipulation of these enzymes can
proceed.
Cytokinins as signals
Cytokinins could also be an important signal traveling
from roots to the shoots. Root-produced cytokinins are
clearly involved in responses to nutrient deprivation [5]
and, as they are produced mainly in roots, could be important in drought responses [58]. Despite this, there have
been few reports that provide information on the cytokinin
content of xylem sap and how that content changes under
drought conditions. In grapevines, a 50% reduction in
zeatin (Z) and zeatin riboside (ZR) was found in plants
that had been subjected to PRD [59]. In a more recent study
in which Z, ZR and zeatin nucleotide (ZN) were measured,
PRD of tomato reduced the ZN content of the xylem sap,
but the magnitude of that change and the contribution of
ZN to the total cytokinin content were not shown [60]. In at
least two studies on sunflower, xylem sap, combined Z and
ZR and combined isopentenyladenine and isopentenyladenosine concentrations in xylem sap decreased under
drought-stressed conditions [61]. It is possible that the
ABA:cytokinin ratios in xylem sap are important for stress
signaling [55]. The effects of cytokinins are also supported
by a study showing that transpiration was higher in transgenic plants that overexpressed the isopentenyltransferase, causing the plants to produce more cytokinins after a
heat shock treatment [62]. Although recent data show
decreased cytokinin concentrations in the xylem under
drought stress, it is still not clear that all plant species
respond in the same way to cytokinin at the concentrations
found in the leaf and guard cells [63].
Strong conclusions about cytokinin content are premature because the complexity of the cytokinin profiles has
not been fully explored [64]. In a recent study on maize [65],
we found a decrease in Z and ZR concentrations in xylem
sap coming from roots of drought stressed plants as compared to well watered controls. Surprisingly, we also found
high concentrations of the aromatic cytokinin 6-benzylaminopurine (BAP) in maize xylem sap, the concentration of
which increased significantly as a result of water stress
[65]. With the availability of increasingly sensitive mass
spectrometry methods, it should be possible to explore
comprehensively the changes in concentrations of many
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Vol.13 No.6
of the cytokinins, and to identify those that play a role in
root to shoot signaling.
Other chemical signals
Chemical and protein-based factors other than ABA, cytokinins or pH could also be involved in root to shoot signaling. Although it has now been established clearly that
xylem sap from many plant species contains proteins
[66,67], the presence of peptides in xylem sap has only
recently been demonstrated [68]. The addition of xylem sap
from tomato induced rapid alkalinization in a tomato cellsuspension bioassay within minutes. This approach has
been used previously to identify peptides. In an experiment
using maize suspension cells, alkalinization was induced
by maize xylem sap, but the activity could not be purified or
abolished with proteases [65]. MicroRNAs have also been
implicated as potential signal molecules that move systemically [69], and recent work on Arabidopsis found that
drought treatment induced the synthesis of a specific
microRNA: miR-169 g [70]. The functional significance of
peptides, microRNAs and proteins in the xylem sap
remains largely unknown, but peptides have been shown
to play important signaling roles in plants and have also
been shown to move systemically via the phloem [71,72].
Many compounds, including hormones, inorganic ions,
amino acids, sugars and organic acids have been identified
in xylem sap [7,34], but among the organic acids found in
abundance in the xylem sap, only malate has been implicated in the control of stomatal closure [73]. Stomatal
opening in ash (Fraxinus excelsior) leaves could be prevented when these leaves were supplied with 0.5–3 mM
malate. Similarly, elevated extracellular concentrations of
malate have also been shown to close stomates in Vicia
faba [74]. Further work is needed to establish the role of
malate in root to shoot signaling.
Ethylene could be another important factor under
drought conditions. It is known that a precursor of ethylene, 1-aminocyclopropane-1-carboxylic acid (ACC), moves
in the xylem from root to shoots [75]. Under drought stress,
ACC transported in the xylem sap might result in the
measured increase of ethylene evolution in leaves [76]. A
role for ethylene under drought was demonstrated by the
use of an ACC oxidase (ACO) antisense in tomato. In these
antisense plants, ethylene evolution was much lower than
normal under both well-watered and drought conditions.
Under soil-drying conditions, the stomatal response in the
ACO antisense plants was the same as wild type, but a
decrease in leaf growth was measured in wild type but not
the ACO antisense plants in response to soil drying [76]. In
maize, ethylene evolution in leaves could not be correlated
with reductions in leaf elongation under drought [77]. This
study also showed that ABA does not play a role in reducing leaf elongation in maize [77]. This suggests that
for reduced transpiration and inhibition of leaf growth. These changes include increases in malate and ACC (1-aminocyclopropane-1-carboxylate) concentrations, decreases
in flow rates, and reductions in the concentrations of cytokinins, zeatin and zeatin riboside. After guard cells perceive ABA, changes in potassium (K+) and anion (A ) fluxes
result in stomatal closure. (c) Stomatal closure under drought. The affects of ABA on guard cells under drought suggest the importance of a plasma-membrane-bound
receptor, such as the recently identified GCR2 (G-PROTEIN COUPLED RECEPTOR2), but the importance of intracellular receptors, such as CHLH (the H subunit of the
magnesium protoporphyrin-IX chelatase that is localized in the chloroplast), cannot be ruled out. Other unknown and yet-to-be-identified plasma membrane receptors
could also be important in transducing the increased ABA concentrations in the apoplast that cause stomatal closure. After guard cells perceive ABA, the efflux of potassium
(K+) and anions (A ) leads to stomatal closure. SLAC, slow anion channel; RAC, rapid anion channel.
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ethylene may play a role in decreased leaf growth in one
plant species and that ACC may be one component of longdistance root-sourced signals under drought.
Conclusions
The production of root-sourced chemical signals under
conditions of water deficit has been associated with
reduced transpiration and/or leaf growth. However, the
identity and relative contribution to signaling of these rootsourced chemicals remains controversial. This controversy
may be due to differing responses between species, the
different intensities of stress treatments applied, the time
at which samples were collected during the imposition of
drought, and/or the different methods used for xylem sap
extraction [43]. Until recently [65], few studies have provided comprehensive information on the composition of
xylem sap. Such comprehensive analyses will clarify the
contribution of different chemicals to root to shoot signaling, and the complexity of constituents and their interactions. As we increase our knowledge of the precise
identity and biosynthesis of the primary chemical signals
that are produced by roots, it will become feasible to alter
plant sensitivity to soil water deficit. This will provide new
molecular breeding strategies for tailoring crops to maintain or even increase yields under specific water stress
conditions, such as intermittent and terminal drought.
Acknowledgements
DPS was supported in part by NSF-Plant Genome #0211842. JQDG is the
recipient of an Australian Research Council Post-doctoral Fellowship
(Inductry linkage project #LP0775362)
References
1 Davies, W.J. et al. (2002) Stomatal control by chemical signalling and
the exploitation of this mechanism to increase water use efficiency in
agriculture. New Phytol. 153, 449–460
2 Wilkinson, S. and Davies, W.J. (2002) ABA-based chemical signalling:
the co-ordination of responses to stress in plants. Plant Cell Environ.
25, 195–210
3 Masle, J. and Farquhar, G.D. (1988) Effects of soil strength on the
relation of water-use efficiency and growth to carbon isotope
discrimination in wheat seedlings. Plant Physiol. 86, 32–38
4 Drew, M.C. et al. (1990) Regulation of K+ uptake and transport to
the xylem in barley roots; K+ distribution determined by electron
probe X-ray microanalysis of frozen-hydrated cells. J. Exp. Bot. 41,
815–825
5 Schachtman, D.P. and Shin, R. (2007) Nutrient sensing and signaling:
NPKS. Annu. Rev. Plant Biol. 58, 47–69
6 Gollan, T. et al. (1986) Soil water status affects the stomatal
conductance of fully turgid wheat and sunflower leaves. Aust. J.
Plant Physiol. 13, 459–464
7 Goodger, J.Q.D. et al. (2005) Relationships between xylem sap
constituents and leaf conductance of well-watered and waterstressed maize across three xylem sap sampling techniques. J. Exp.
Bot. 56, 2389–2400
8 Christmann, A. et al. (2007) A hydraulic signal in root-to-shoot
signalling of water shortage. Plant J. 52, 167–174
9 Fereres, E. and Soriano, M.A. (2007) Deficit irrigation for reducing
agricultural water use. J. Exp. Bot. 58, 147–159
10 dos Santos, T.P. et al. (2003) Partial rootzone drying: effects on growth
and fruit quality of field-grown grapevines (Vitis vinifera). Funct. Plant
Biol. 30, 663–671
11 Kang, S. et al. (1998) Water use efficiency of controlled
alternate irrigation on root-divided maize plants. Agric. Water
Manag. 38, 69–76
12 Tang, L.S. et al. (2005) Physiological and yield responses of cotton
under partial rootzone irrigation. Field Crops Res. 94, 214–223
286
Trends in Plant Science Vol.13 No.6
13 Dodd, I.C. (2007) Soil moisture heterogeneity during deficit irrigation
alters root-to-shoot signaling of abscisic acid. Funct. Plant Biol. 34,
439–448
14 Dry, P.R. and Loveys, B.R. (1999) Grapevine shoot growth and
stomatal conductance are reduced when part of the root system is
dried. Vitis 38, 151–156
15 Davies, W.J. et al. (2000) Regulation of leaf and fruit growth in plants
growing in drying soil: exploitation of the plants’ chemical signaling
system and hydraulic architecture to increase the efficiency of water
use in agriculture. J. Exp. Bot. 51, 1617–1626
16 Sharp, R.E. et al. (1994) Confirmation that abscisic-acid accumulation
is required for maize primary root elongation at low water potentials.
J. Exp. Bot. 45, 1743–1751
17 Davies, W.J. and Zhang, J. (1991) Root signals and the regulation of
growth and development of plants in drying soil. Annu. Rev. Plant
Physiol. Mol. Biol. 42, 55–76
18 Munns, R. (1992) A leaf elongation assay detects an unknown growth
inhibitor in xylem sap from wheat and barley. Aust. J. Plant Physiol.
19, 127–135
19 Zhang, J. and Davies, W.J. (1991) Antitranspirant activity in xylem sap
of maize plants. J. Exp. Bot. 42, 317–321
20 Schroeder, J.I. et al. (2001) Guard cell signal transduction. Annu. Rev.
Plant Physiol. Mol. Biol. 52, 627–658
21 Fambrini, M. et al. (1995) Characterization of a wilty sunflower
(Helianthus annuus L.) mutant III. Phenotypic interaction in
reciprocal grafts from wilty mutant and wild-type plants. J. Exp.
Bot. 286, 525–530
22 Holbrook, N.M. et al. (2002) Stomatal control in tomato with ABAdeficient roots: response of grafted plants to soil drying. J. Exp. Bot. 53,
1503–1514
23 Jones, H.G. et al. (1987) Growth and water relations of wilty mutants of
tomato (Lycopersicon esculentum Mill.). J. Exp. Bot. 38, 1848–1856
24 Borel, C. et al. (2001) Does engineering abscisic acid biosynthesis in
Nicotiana plumbaginifolia modify stomatal response to drought? Plant
Cell Environ. 24, 477–489
25 Thompson, A.J. et al. (2007) Regulation and manipulation of ABA
biosynthesis in roots. Plant Cell Environ. 30, 67–78
26 Zhang, J. and Davies, W.J. (1989) Abscisic acid produced in
dehydrating roots may enable the plant to measure the water status
of the soil. Plant Cell Environ. 12, 73–81
27 Liang, Z. et al. (1997) How do roots control xylem sap ABA
concentration in response to soil drying. Plant Cell Physiol. 38, 10–16
28 Zhang, J. and Tardieu, F. (1996) Relative contribution of apices and
mature tissues to ABA synthesis in droughted maize root systems.
Plant Cell Physiol. 37, 598–605
29 Zhang, J. and Davies, W.J. (1987) Increased synthesis of ABA in
partially dehydrated root tips and ABA transport from roots to
leaves. J. Exp. Bot. 38, 2015–2023
30 Katalin Barabás, N. et al. (2000) Distribution of the Mo-enzymes
aldehyde oxidase, xanthine dehydrogenase and nitrate reductase in
maize (Zea mays L.) nodal roots as affected by nitrogen and salinity.
Plant Sci. 155, 49–58
31 Mahouachi, J. et al. (2007) Hormonal changes in papaya seedlings
subjected to progressive water stress and re-watering. Plant Growth
Regul. 53, 43–51
32 Munns, R. and King, R.W. (1988) Abscisic acid is not the only stomatal
inhibitor in the transpiration stream of wheat plants. Plant Physiol. 88,
703–708
33 Soar, C.J. et al. (2006) Scion photosynthesis and leaf gas exchange in
Vitis vinifera L. cv. Shiraz: Mediation of rootstock effects via xylem sap
ABA. Aust. J. Grape Wine Res. 12, 82–96
34 Gollan, T. et al. (1992) Stomatal response to drying soil in relation to
changes in the xylem sap composition of Helianthus annus. I. The
concentration of cations, anions, amino acids in, and pH of, the xylem
sap. Plant Cell Environ. 15, 551–559
35 Hartung, W. et al. (1998) Factors that regulate abscisic acid
concentrations at the primary site of action at the guard cell.
J. Exp. Bot. 49, 361–367
36 Wilkinson, S. and Davies, W.J. (1997) Xylem sap pH increase: a
drought signal received at the apoplastic face of the guard cell that
involves the suppression of saturable abscisic acid uptake by the
epidermal symplast. Plant Physiol. 113, 559–573
37 Wilkinson, S. (1999) pH as a stress signal. Plant Growth Regul. 29, 87–99
Review
38 Kaiser, W.M. and Hartung, W. (1981) Uptake and release of abscisic
acid by isolated photoautotrophic mesophyll cells, depending on pH
gradients. Plant Physiol. 68, 202–206
39 Liu, X. et al. (2007) A G protein-coupled receptor is a plasma membrane
receptor for the plant hormone abscisic acid. Science 315, 1712–1716
40 Razem, F.A. et al. (2006) The RNA-binding protein FCA is an abscisic
acid receptor. Nature 439, 290–294
41 Shen, Y.Y. et al. (2006) The Mg-chelatase H subunit is an abscisic acid
receptor. Nature 443, 823–826
42 Wilkinson, S. et al. (1998) Effects of xylem pH on transpiration from
wild-type and flacca tomato leaves. A vital role for abscisic acid in
preventing excessive water loss even from well-watered plants. Plant
Physiol. 117, 703–709
43 Bacon, M.A. et al. (1998) pH-regulated leaf cell expansion in droughted
plants is abscisic acid dependent. Plant Physiol. 118, 1507–1515
44 Prokic, L. et al. (2006) Species-dependent changes in stomatal
sensitivity to abscisic acid mediated by external pH. J. Exp. Bot. 57,
675–683
45 Liu, F.L. et al. (2003) Hydraulic and chemical signals in the control of
leaf expansion and stomatal conductance in soybean exposed to
drought stress. Funct. Plant Biol. 30, 65–73
46 Jia, W. and Davies, W.J. (2007) Modification of leaf apoplast pH in
relation to stomatal sensitivity to root-sourced abscisic acid signals.
Plant Physiol. 143, 68–77
47 Bahrun, A. et al. (2002) Drought-induced changes in xylem pH, ionic
composition, and ABA concentration act as early signals in field-grown
maize (Zea mays L.). J. Exp. Bot. 53, 251–263
48 Else, M.A. et al. (1994) Concentrations of abscisic acid and other solutes
in xylem sap from root systems of tomato and castor-oil plants are
distorted by wounding and variable sap flow rates. J. Exp. Bot. 45, 317–
323
49 Jackson, M.B. (1997) Hormones from roots as signals for the shoots of
stressed plants. Trends Plant Sci. 2, 22–28
50 Liu, F.L. et al. (2005) A review of drought adaptation in crop plants:
changes in vegetative and reproductive physiology induced by ABAbased chemical signals. Aust. J. Agric. Res. 56, 1245–1252
51 Wilkinson, S. (2004) Water use efficiency and chemical signalling. In
Water Use Efficiency in Plant Biology (Bacon, M.A., ed.), pp. 75–112,
Blackwell Publishing Ltd
52 Wilkinson, S. (2007) Nitrate signalling to stomata and growing leaves:
interactions with soil drying, ABA, and xylem sap pH in maize. J. Exp.
Bot. 58, 1705–1716
53 Roelfsema, M.R. and Prins, H.B. (1998) The membrane potential of
Arabidopsis thaliana guard cells; depolarizations induced by
apoplastic acidification. Planta 205, 100–112
54 Munns, R. and Sharp, R.E. (1993) Involvement of abscisic acid in
controlling plant growth in soils of low water potential. Aust. J.
Plant Physiol. 20, 425–437
55 Hansen, H. and Dorffling, K. (1999) Changes of free and conjugated
abscisic acid and phaseic acid in xylem sap of drought-stressed
sunflower plants. J. Exp. Bot. 50, 1599–1605
56 Sauter, A. et al. (2002) A possible stress physiological role of abscisic acid
conjugates in root-to-shoot signalling. Plant Cell Environ. 25, 223–228
57 Dietz, K.J. et al. (2000) Extracellular beta-glucosidase activity in barley
involved in the hydrolysis of ABA glucose conjugate in leaves. J. Exp.
Bot. 51, 937–944
Trends in Plant Science
Vol.13 No.6
58 Sakakibara, H. (2006) Cytokinins: activity, biosynthesis, and
translocation. Annu. Rev. Plant Biol. 57, 431–449
59 Stoll, M. et al. (2000) Hormonal changes induced by partial rootzone
drying of irrigated grapevine. J. Exp. Bot. 51, 1627–1634
60 Kudoyarova, G. et al. (2007) Effect of partial rootzone drying on the
concentration of zeatin-type cytokinins in tomato (Solanum
lycopersicum L.) xylem sap and leaves. J. Exp. Bot. 2, 161–168
61 Hansen, H. and Dörffling, K. (2003) Root-derived trans-zeatin riboside
and abscisic acid in drought-stressed and rewatered sunflower plants:
interaction in the control of leaf diffusive resistance? Funct. Plant Biol.
30, 365–375
62 Teplova, I. et al. (2000) Response of tobacco plants transformed
with the ipt gene to elevated temperature. Russ. J. Plant Physiol.
47, 367–369
63 Dodd, I.C. (2003) Hormonal interactions and stomatal responses.
J. Plant Growth Regul. 22, 32–46
64 Davies, W.J. et al. (2005) Long-distance ABA signaling and its relation
to other signaling pathways in the detection of the soil drying and the
mediation of the plant’s response to drought. J. Plant Growth Regul. 24,
285–295
65 Alvarez, S. et al. (2008) Metabolomic and proteomic changes in the
xylem sap of maize under drought. Plant Cell Environ. 31, 325–340
66 Alvarez, S. et al. (2006) Characterization of the maize xylem sap
proteome. J. Proteome Res. 5, 963–972
67 Kehr, J. et al. (2005) Analysis of xylem sap proteins from Brassica
napus. BMC Plant Biol. 5, 11
68 Neumann, P.M. (2007) Evidence for long-distance xylem transport of
signal peptide activity from tomato roots. J. Exp. Bot. 58, 2217–2223
69 Sunkar, R. et al. (2007) Small RNAs as big players in plant abiotic
stress responses and nutrient deprivation. Trends Plant Sci. 12, 301–
309
70 Zhao, B. et al. (2007) Identification of drought-induced microRNAs in
rice. Biochem. Biophys. Res. Commun. 354, 585–590
71 Lindsey, K. et al. (2002) Peptides: new signalling molecules in plants.
Trends Plant Sci. 7, 78–83
72 Ryan, C.A. et al. (2002) Polypeptide hormones. Plant Cell 14 (Suppl),
S251–S264
73 Patonnier, M.P. et al. (1999) Drought-induced increase in xylem malate
and mannitol concentrations and closure of Fraxinus excelsior L.
stomata. J. Exp. Bot. 50, 1223–1229
74 Hedrich, R. et al. (1994) Malate-sensitive anion channels enable guardcells to sense changes in the ambient CO2 concentration. Plant J. 6,
741–748
75 Else, M.A. and Jackson, M.B. (1998) Transport of 1aminocyclopropane-1-carboxylic acid (ACC) in the transpiration
stream of tomato (Lycopersicon esculentum) in relation to foliar
ethylene production and petiole epinasty. Aust. J. Plant Physiol. 25,
453–458
76 Sobeih, W.Y. et al. (2004) Long-distance signals regulating stomatal
conductance and leaf growth in tomato (Lycopersicon esculentum)
plants subjected to partial root-zone drying. J. Exp. Bot. 55, 2353–2363
77 Voisin, A.S. et al. (2006) Are ABA, ethylene or their interaction
involved in the response of leaf growth to soil water deficit? An
analysis using naturally occurring variation or genetic
transformation of ABA production in maize. Plant Cell Environ. 29,
1829–1840
287