Download A possible stress physiological role of abscisic acid

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Xylem transport of abscisic acid conjugates
A. Sauter et al.
Original ArticleBEES SGML
Plant, Cell and Environment (2002) 25, 223–228
A possible stress physiological role of abscisic acid
conjugates in root-to-shoot signalling
A. SAUTER,1 K.-J. DIETZ2 & W. HARTUNG1
1Julius-von-Sachs-Institut der Universität Würzburg, Lehrstuhl Botanik I, Würzburg, Germany and 2Lehrstuhl für
Stoffwechselphysiologie und Biochemie der Pflanzen, Universität Bielefeld, Universitätsstraße 25, D-33501 Bielefeld, Germany
ABSTRACT
Abscisic acid (ABA) conjugates, predominantly their glucose esters, have recently been shown to occur in the xylem
sap of different plants. Under stress conditions, their concentration can rise substantially to levels that are higher
than the concentration of free ABA. External ABA conjugates cannot penetrate apoplastic barriers in the root. They
have to be hydrolysed by apoplastic enzymes in the root
cortex. Liberated free ABA can then be redistributed to the
root symplast and dragged directly across the endodermis
to the stele. Endogenous ABA conjugates are formed in
the cytosol of root cells, transported symplastically to the
xylem parenchyma cells and released to the xylem vessels.
The mechanism of release is unknown; it may include the
action of ABC-transporters. Because of its extremely
hydrophilic properties, ABA-GE is translocated in the
xylem of the stem without any loss to the surrounding
parenchyma. After arrival in the leaf apoplast, transporters
for ABA-GE in the plasmalemma have to be postulated to
redistribute the conjugates to the mesophyll cells. Additionally, apoplastic esterases can cleave the conjugate and
release free ABA to the target cells and tissues. The activity
of these esterases is increased when barley plants are subjected to salt stress.
Key-words: ABA-GE; apoplast; leaf; stem; xylem transport.
Abbreviations: ABA, abscisic acid; ABAxyl, ABA in the
sylem sap; ABA-GE, abscisic acid glucose ester; ABAGExyl, abscisic acid glucose ester in the sylem; IWF,
intercellular washing fluid.
stantially high concentrations. In vacuoles they are trapped
because of their hydrophilic properties and withdrawn
from further metabolism. ABA glucose ester and other
non-hydrolysable unidentified conjugates were detected by
Kaiser, Weiler & Hartung (1985) in vacuoles of barley mesophyll cells.
Hormone conjugates, however, can also serve as longdistance transport forms in the xylem fluid. The major
transport form of cytokinins in the xylem is the zeatin riboside (Fußeder et al. 1992; Bano et al. 1993, 1994; Kamboj,
Blake & Baker 1998). Gibberellins are conjugated predominantly with glucose. They have been detected in the bleeding sap of trees by Dathe et al. (1982). Auxin conjugates
have never been reported to be translocated in the xylem.
Recently, much attention has been paid to ABA conjugates in the xylem sap of various plants. Munns & King
(1988) and Munns et al. (1993) reported that an unidentified
ABA conjugate, the ‘adduct’, is more important as a longdistance stress signal than free ABA. After arrival in the
leaf tissue, this complex form is believed to be physiologically more active than ABA. Bano et al. (1993, 1994) were
the first to identify ABA glucose ester (ABA-GE) in the
xylem sap of rice and sunflower plants. Other examples for
xylem-transported ABA conjugates are cited and discussed
below. Nothing is known about the origin of root-borne
ABA conjugates, their radial transport in roots to the xylem
elements, their transport in the xylem vessels of the stem, as
well as their fate in the leaf apoplast. Figure 1 presents a
schematic plant, numbering several factors that influence
transport and formation of ABA-GE. This article discusses
the present knowledge and open questions of this potentially important group of hormonal long-distance stress
signals.
INTRODUCTION
Plant hormone homeostasis is largely maintained by their
biosynthesis and metabolism. ABA can be degraded oxidatively to phaseic acid (PA) and dihydrophaseic acid (DPA)
and auxin to 3-methyleneoxindole. Gibberellins are converted to less active or inactive gibberellin metabolites. An
alternative mechanism of biotransformation of hormones is
their conjugation with sugars, amino acids and peptides.
These conjugated forms are usually physiologically inactive
and deposited in plant vacuoles where they can reach subCorrespondence: W. Hartung. Fax: + 49 931 888 6158;
e-mail: [email protected]
© 2002 Blackwell Science Ltd
CONJUGATED ABA IN TRANSPORT FLUIDS
Over the last decade ABA conjugates have been analysed
in the xylem sap of various plants (Table 1). Bano et al.
(1993) first reported a rise in concentration of conjugated
ABA in the xylem sap of non-irrigated sunflower and rice.
After rewatering the concentration of free and bound ABA
decreased again. The conjugates of the major ABA metabolites PA and DPA were also present in sunflower xylem
sap.
Salt stress has also been shown to increase ABA-GExyl in
barley and maize plants (Dietz et al. 2000; Sauter, unpub223
224 A. Sauter et al.
C leaf
cc
st
tr
1
B stem
phloem xylem
A root
palisade
parenchyma
2
stoma
2
ABA-GE
ABA
ß-D-glucosidase
ABC-transporter ?
xylem
phloem
1
1
2
4
3
exodermis
rhizodermis
cortex
5
endodermis
xylem
pericycle
Figure 1. A schematic presentation of the origin, the transport and the fate of ABA-GE in a vegetative plant. The arrows indicate the flows
of ABA-GE (red) and free ABA (blue) in roots (a), stems (b) and leaves (c). The numbering refers to the text. Extracellular enzyme activity
is coloured light green, the putative transporter of the xylem parenchyma plasma membrane light blue. The cell wall (grey), the thickenings
of the endodermis and the Casparian band of the exo- and endodermis are yellow. In the leaf (c) a schematic vascular bundle, the crosssectioned palisade parenchyma cells and a stoma are presented. The colouring is as in (a). cc, companion cell; st, sieve tube; tr, tracheid.
Table 1. Content of free and bound ABA in xylem sap of different plants coping with various stress conditions
Species
Rice
a
Sunflowerb
Barleyc
Maized
Anastatica hierochunticae
Maizef
Betula pendulag
Treatment
Free ABA
(nM)
Well watered
Drought-stressed
Rewatered
Well watered
Drought-stressed 24 h
Rewatered 2–3 h
Control
50 mM NaCl
100 mM NaCl
Control
100 mM NaCl
Control
250 mM NaCl +40 mM CaCl2
Control
Single-rooted plants
Control
Dry
7·2
92
52
10
252
32
1·8
2·2
3·8
2·8
5·5
3·7
42·9
30·9
4·1
31
829
±
±
±
±
±
±
±
±
±
±
±
1
3
12
0·6
7·5
0·5
0·6
0·3
0·2
0·5
0·4
±
±
±
±
6·1
0·4
17
267
Bound ABA
(nM)
73
499
87
120
546
145
0·3
0·3
0·9
1·5
2·5
0·2
33·9
0·4
1·0
15
263
±
±
±
±
±
±
±
±
±
±
±
7·5
75
5·7
0·6
104
2·2
0·1
0·2
0·2
0·3
0·2
±
±
±
±
0·1
0·2
16
63
Ratio ABA : ABA-conjugate
0·1
0·2
0·6
0·1
0·5
0·2
5·8
7·3
4·4
1·8
2·2
16·1
1·3
77
4
2·1
3·2
a
Bano et al. 1993; bBano et al. 1994; cDietz et al. 2000; dSauter, unpublished results; eHartung & Jeschke (1999); fJeschke et al. 1997b; gFort
et al. 1998
© 2002 Blackwell Science Ltd, Plant, Cell and Environment, 25, 223–228
Xylem transport of abscisic acid conjugates 225
Xylem
Table 2. Concentration of ABA and ABA-
Phloem
Treatment
Free ABA
(nM)
Bound ABA
(nM)
Free ABA
(nM)
Bound ABA
(nM)
Control
Low P
180 ± 40
1100 ± 800
1·4 ± 0·3
4·4 ± 0·3
1800 ± 100
8300 ± 2300
90 ± 30
160 ± 30
lished results). A substantial rise of ABA-GExyl was
observed by Grimmer (1993; cited by Hartung & Jeschke
1999) in the winter annual desert plant Anastatica hiërochuntica that had been treated with a mixture of NaCl and
CaCl2 in similar concentrations to those that have been
found in the solution of the soils of the original desert habitat. Here the ratio of free ABA : conjugated ABA
decreased from 16·1 : 1 in control plants to 1·3 : 1 in saltstressed plants.
ABA-GE was also present in the xylem sap of maize
plants that were supplied by their seminal roots only
(Jeschke et al. 1997a). These plants suffer from drought
stress in the leaves although the roots have been watered
sufficiently. Single-rooted plants transported ABA-GE in a
higher concentration and the ratio of free ABA : conjugated ABA was reduced from 77 : 1 in control plants to 4 : 1.
Fort et al. (1998) investigated seedlings of Betula pendula
cultivated in a split root system. As the soil of both compartments started to dry ABA-GExyl increased as well as
free ABA.
Jeschke et al. (1997a) have investigated both xylem and
phloem sap of phosphate-deficient Ricinus communis L.
(Table 2). Under these condition xylem sap concentration
of ABA-GE rose 3·1-fold. Phloem sap concentration of
control plants was higher by a factor of 64 in comparison
with the xylem, the ABA-GE concentration in the phloem
of phosphorus-deficient plants was enhanced 1·8-fold. From
these data it was concluded that leaves may also be a source
for ABA-GExyl (Fig. 1c).
Conjugated ABA in the xylem was also increased in castor beans when plants were supplied with N by foliar application only (Hartung, Peuke & Davies 1999). Ammonium
spraying proved to be more effective than nitrate spraying
(Peuke & Hartung unpublished results).
It can be concluded from this compilation that ABA
conjugates in the xylem are widely or even ubiquitously distributed among plants and that their fraction of the total
ABA pool consisting of bound and free ABA frequently
increases under stressful growth conditions.
NATURE OF THE ABA CONJUGATE
Munns et al. (1993) postulated that root-borne ABA might
be travelling in the xylem in a complexed form (the
‘adduct’) and that this compound exhibits a stronger inhibitory activity on stomatal conductance than free ABA.
Under conditions of storage this substance changed from a
low molecular weight precursor into a highly polymerized
© 2002 Blackwell Science Ltd, Plant, Cell and Environment, 25, 223–238
GE in stem base xylem sap and phloem sap
of Ricinus communis L. grown under control
and phosphorus deficient conditions (after
Jeschke et al. 1997b)
compound. However, the exact chemical structure of this
substance remains unknown.
Hansen & Dörffling (1999) investigated the content of
conjugated ABA in the xylem sap of drought-stressed sunflower plants by high-performance liquid chromqtography.
They detected five conjugates in the xylem sap of wellwatered plants. The sap of drought-stressed plants contained six ABA conjugates. Some conjugates were alkaline
stable and could only be cleaved by the enzyme β-glucosidase. Thus the enzymatic test characterized these ABA conjugates as ABA glucose esters with β-glucosidic linkages.
Baier, Gimmler & Hartung (1990) have shown that the
permeability coefficient of guard cell membranes of Valerianella locusta is extremely low for ABA-GE (PABA-GE ∼
10−8 ms−1). Bearing in mind that the basic permeability of
the guard cell plasmalemma seems to be higher than that of
the mesophyll and the root cortex by a factor of 10 and 100,
respectively (Baier et al. 1990; Daeter, Slovik & Hartung
1993) biomembranes can be regarded as impermeable for
ABA-GE. Therefore, the question arises by which mechanism the ABA-GE that is synthesized in the cytosol of the
root cortex, is released to the stelar apoplast and the xylem.
During xylem transport in the stem no loss to the surrounding tissues is to be expected as may happen in the case of
free ABA. Having arrived in the leaf two mechanisms could
be involved in the avoidance of extremely high apoplastic
concentrations of ABA-GE. First, the transporters for
ABA-GE, located in the mesophyll plasmalemma could
redistribute the conjugates to the mesophyll and second,
apoplastic glucosidases could cleave the physiologically
inactive conjugates and release free ABA to their targets,
the stomata or the growing cells of young leaves.
RADIAL TRANSPORT OF ABA GLUCOSE
ESTER IN ROOTS
ABA glucose esters in the xylem can originate from external or internal sources. The soil solution under different
crops contains ABA-GE in concentrations up to 35 nM.
Sauter & Hartung (2000) have shown that external ABAGE is not transported laterally to the stele in significant
amounts even when roots lack an exodermis such as roots
from hydroponically cultivated maize seedlings (Fig. 1a, 2).
When lateral water flow in the root systems was increased
by applying vacuum to the mesocotyl of decapitated seedlings in the presence of 100 nM ABA-GE in the external
medium, its concentration in the xylem decreased. Simultaneously, however, ABAxyl increased, suggesting cleavage
226 A. Sauter et al.
Tissue
Table 3. ABA-GE content of isolated
Medium
Treatment
Cortex
(pmol g−1 FG−1)
Stele
(pmol g−1 FG−1)
Cortex
(pmol m−2)
Stele
(pmol m−2)
1
2
3
7·8 ± 3·1
6·5 ± 3·7
16·7 ± 7·2
15·6 ± 3·7
27·7 ± 8·8
47·0 ± 13·8
0·4 ± 0·2
0·4 ± 0·2
0·8 ± 0·3
1·0 ± 0·3
2·1 ± 0·9
4·3 ± 1·5
of the conjugate by an apoplastic esterase in the cortex (Fig.
1a, 1). Indeed the intracellular washing fluid of maize roots
contained a β-glucosidase which could be inhibited by
ABA-GE.
The same type of experiment was performed with root
systems of aeroponically cultivated maize seedlings. Free
ABA did not increase in the xylem sap. It was concluded
that the Casparian bands formed in the hypodermis of
aeroponically cultivated maize plants (Freundl, Steudle &
Hartung 1998; 2000) prevent the uptake and radial transport of ABA-GE in roots (Fig. 1a, 3).
These results show that for the extremely hydrophilic
ABA-GE both the endodermis and the exodermis are perfect transport barriers. Applying the flux equation of radial
ABA-flow in roots (Freundl et al. 1998) the reflection coefficient σ of ABA-GE for maize roots is 1·0. Therefore ABAGE formed in the cytosol of cortical cells must be translocated symplastically to the stele (Fig. 1a, 4).
Having arrived in the xylem parenchyma cells ABA-GE
must be released across the plasma membrane to the stelar
apoplast. Stelar tissues of maize release ABA-GE with
rates that can be three to five times higher than from cortical tissues (Table 3). Efflux of ABA-GE from isolated stelar tissues of maize is particularly high under conditions
when ABA degradation is inhibited. In experiments with
intact plants, salt stress (100 nM) stimulated ABA-GEefflux to the xylem three-fold.
The mechanism of the membrane transport of ABA-GE
remains unknown. Sauter & Hartung (2000) speculated
that transmembrane transport of ABA conjugates could be
mediated by ABC-transporters (Fig. 1a, 5). Sidler et al.
(1998) provided evidence that an AtPGP1 transporter is
localized in the plasmalemma of Arabidopsis thaliana seedlings in both root and shoot and perhaps involved in hormone-regulated developmental processes. According to
preliminary data of Enrico Martinoia (Neuchatel, CH, personal communication) membrane transport of another hormone conjugate, the indolyl-acetyl-aspartate, seems to be
mediated by an ABC-transporter.
FATE OF ABA GLUCOSE ESTER IN
THE STEM
Free ABA that is translocated over long distances in the
xylem through stems may be redistributed to the surrounding parenchyma, especially when the xylem sap is acid (Fig.
cortical and stelar tissue segments after preincubation of intact root segments for 24 h
with (1) 5 nM ABA, (2) 50 nM ABA and (3)
50 nM ABA plus tetcyclacis. The tissue
ABA-GE concentrations were determined
immediately after preloading, the medium
was analysed after preloaded segments were
kept for 120 min in a hormone-free medium
(after Sauter & Hartung 2000)
1b, 2). This could result in a significant ABA loss during
xylem transport. Indeed, Jokhan, Harink & Jackson (1999)
and Jeschke & Hartung (2000) were able to show that during transport in the stem the ABA signal can be weakened
significantly. The ABA-GE-molecule, however, because of
its physico-chemical properties must be expected to stay in
the xylem unchanged until its arrival in the leaves, as long
as there is no glucose esterase activity in the xylem sap
(Fig. 1b, 1). Indeed, xylem saps, both from stressed and
unstressed plants were absolutely free of any enzymatic
activity that could release ABA from its glucose esters. Sauter and Hartung (unpublished results) have perfused 10 cm
lengths of isolated second internode segments of Phaseolus
coccineus with buffers that contain ABA-GE, in concentrations that might be expected under stress conditions, by
application of vacuum to the apical cut surface. ABA-GE
passes the bean internodes unchanged without being taken
up by the stem tissues (Fig. 1b, 1). ABA-GE proved to be
perfectly suited for efficient long-distance transport.
FATE OF ABA GLUCOSE ESTER IN
THE LEAF
As discussed above ABA-GE can only play a role as a hormonal stress signal when ABA is released from the physiologically inactive conjugate by apoplastic enzymes (Fig. 1c,
1,2).
The action of enzymes that cleave hormone conjugates
in the leaf apoplast becomes evident by comparing the
ratios of free ABA : conjugated ABA in the xylem sap (4–
7) of barley and intracellular washing fluids of barley leaves
(22–32; Table 4). Intercellular washing fluids (IWF) are
Table 4. Eleven-day-old barley seedlings were grown at varying
salt concentrations. Xylem sap of excised roots as wells an
intercellular washing fluid of the primary leaves were analysed for
free and bound ABA (after Sauter & Hartung 2000)
ABA-GE (nM)
Ratio of ABA :
ABA-GE
NaCl (mM)
Xylem sap
IWF
Xylem sap
IWF
0
50
100
0·32 ± 0·09
0·50 ± 0·26
1·31 ± 0·30
0·07 ± 0·01
0·09 ± 0·02
0·16 ± 0·03
5·8
7·3
4·4
22·3
32·7
29·4
© 2002 Blackwell Science Ltd, Plant, Cell and Environment, 25, 223–228
Xylem transport of abscisic acid conjugates 227
PERSPECTIVES AND CONCLUDING
REMARKS
1·0
0·9
This review shows that ABA conjugates must be discussed
as important and effective hormonal stress signals that
intensify the ABA long-distance signal. The following problems should be investigated in the future: (1) the chemical
structure of all ABA conjugates of the xylem sap needs to
be elucidated; (2) the transport of ABA conjugates across
root and mesophyll plasma membranes should be investigated under control and stress conditions, including a possible involvement of ABC-transporters; and (3) apoplastic
β-glucosidases that hydrolyse ABA-glucose esters need to
be purified and characterized.
Extinction (405 nm)
0·8
0·7
0·6
0·5
0·4
0·3
0·2
0·1
0·0
3
4
5
6
7
8
9
10
pH
Figure 2. Isoelectric focusing of extracellular β-glucosidases of
barley primary leaves. Intercellular washing fluid (IWF) was
prepared as described previously (Dietz et al. 2000). The protein of
300 µL IWF protein was separated by isoelectric focusing in
immobilized pH gradients (Immobilin strips 3–10, Pharmacia,
Uppsala, Sweden). The strips were cut in sections and the activity
was determined using the substrate p-nitrophenol-β-Dglucopyranoside. The data represent means of three replicates
±SD.
ACKNOWLEDGMENTS
We are grateful to Deutsche Forschungsgemenchaft (SFB
261, TP A3) for financial support and W. J. Davies
(Lancaster) and Dr E. Hose for their interest and
stimulating discussions and to Miss B. Dierich for technical
help.
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Received 1 March 2001; received in revised form 6 June 2001;
accepted for publication 6 June 2001
© 2002 Blackwell Science Ltd, Plant, Cell and Environment, 25, 223–228