Journal of Experimental Botany, Vol. 53, No. 366, pp. 27-32,
January 1, 2002
© 2002 Oxford University Press
Short Papers |
Abscisic acid in the xylem: where does it come from, where does it go to?
Julius-von-Sachs Institut für Biowissenschaften, Lehrstuhl Botanik I, Universität Würzburg, Julius-von-Sachs Platz 2, D-97082 Würzburg, Germany
Received 20 August 2001; Accepted 25 September 2001
Abstract
Abscisic acid is a hormonal stress signal that moves in the xylem from the root to the different parts of the shoot where it regulates transpirational water loss and leaf growth. The factors that modify the intensity of the ABA signal in the xylem are of particular interest because target cells recognize concentrations. ABAxyl, will be decreased as radial water flow through the roots is increased, assuming that radial ABA transport occurs in the symplast only. Such dilutions of the plant hormone concentration can be compensated in different ways, which help to keep the ABA-concentrations in the xylem constant: (i) apoplastic bypass flows of ABA, (ii) ABA flows between the stem parenchyma and the xylem during transport and (iii) the action of ß-D-glucosidases that release free ABA from its conjugates to the root cortex and the leaf apoplast. The significance of reflection coefficients (
ABA), permeability coefficients of membranes (PSABA) and apoplastic barriers for ABA is discussed.
Key words: Abscisic acid, roots, shoots, stress signal, xylem.
Introduction
The role and the physiological significance of abscisic acid (ABA) that is transported in the xylem sap from the roots to the shoots as a stress signal during early stress is well established. Its significance as a stress signal has been discussed recently in a number of review articles (Davies and Zhang, 1991
; Hartung et al., 1999; Sauter et al., 2001). These results strongly indicate that roots can sense several aspects of the soil water status. Stomatal behaviour and the development of the shoot can be regulated as a function of the strength of these signals.
Increased attention has been paid in the past to the factors that regulate the intensity of the hormonal signal in the xylem. Elegant and fundamental work of Michael Jackson's group (Else et al., 1994, 1995) has shown that large concentration changes of ABAxyl may also occur under unstressed conditions, when lateral water transport in the root to the xylem is altered. However, under field conditions such fluctuations have not often been observed (Tardieu et al., 1992). Mechanisms have, therefore, to be postulated that maintain an ABA homeostasis in the xylem under unstressed conditions.
The events occurring during the transport of ABA from the site of formation to the target cells are presented in the schematic diagrams of Figs 1, 2 and 3 and are discussed in the following paragraphs using those schemes.
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ABA in roots: where does it come from?
Abscisic acid in roots increases as a soil is drying and is derived to a significant extent from synthesis in the root tissues (Fig. 1A
). Both tissue types of the root, stele and cortex possess an equal capacity to synthesize ABA even at water losses of 50% and more. The largest accumulation is often observed in the root tips. This is very likely a result of the low vacuolization of the root tip cells with a high percentage of cytosol; that compartment where ABA is formed (Hartung et al., 1999).
A second internal source of ABAxyl originates in the leaves (Fig. 3A). Leaf synthesized ABA can be loaded to the phloem (Fig. 3B) and transported to the roots (Figs 1B, 2F, 3C). In the roots one part may be deposited in the tissue and another part recirculated to the xylem vessels (Figs 1C, 2G). Salt stress, phosphate deficiency and ammonium nutrition enhance the percentage of recirculated ABA (Jeschke et al., 1997a, b; Wolf et al., 1990; Peuke et al., 1994).
Both free ABA and ABA-glucose ester (ABA-GE) have been detected in the soil solution under a range of crop plants at concentrations up to 10 nM or 30 nM, respectively (Hartung et al., 1996; Sauter and Hartung, 2000). External free ABA can be taken up by the roots (Fig. 1D). It participates in maintaining an ABA equilibrium between roots and the external medium (Hartung et al., 1996). The uptake of external conjugated ABA is strongly dependent on the existence and properties of apoplastic barriers as discussed later in this article.
How does root ABA reach the xylem?
Xylem ABA concentrations are strongly affected by changes of radial water flows in the roots caused by transpiration (Else et al., 1994, 1995). When ABA is transported in the symplast exclusively, efflux from the xylem parenchyma cells across the plasma membrane to the apoplast and the xylem vessels is a rate-limiting step (Fig. 1E). Lateral water flows caused by transpiration will dilute the ABAxyl dramatically and changes in stomatal opening as a result of light-induced stomatal oscillations will cause huge concentration changes of ABAxyl under unstressed conditions.
Freundl et al. have shown that an apoplastic bypass flow of ABA across the endodermis is possible (Fig. 1F) (Freundl et al., 1998), participating in an ABAxyl homeostasis. They have determined the reflection coefficient of ABA for maize and sunflower roots under different conditions. When ABA=1, all ABA molecules are reflected at the endodermis. They are forced to enter the symplast. Table 1 shows that ABA is always below 1 indicating that substantial amounts of ABA can be dragged with the water across the endodermis directly into the xylem, buffering ABA fluctuations caused by increased transpirational water transport. An ABAxyl homeostasis has been observed in field-grown plants subjected to abrupt changes of evaporative demand (Tardieu et al., 1992).
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The exodermis: an apoplastic barrier that retards ABA loss
Most of the roots growing in a well-aerated soil form a Casparian band in the hypodermis—the exodermis. Only roots of a few species, predominantly legumes, lack an exodermis (Perumalla et al., 1990). It has been demonstrated (Freundl et al., 2000; Hose et al., 2001, 2002) that efflux of ABA from the apoplast to the surrounding medium or rhizosphere can be retarded significantly when Casparian bands are present. Thus a high apoplastic ABA concentration can build up in the cortex. Redistribution to the symplast (Fig. 1G) can enforce the hydraulic conductance of roots (Hose et al., 2000). So, under transpiring conditions more ABA can be dragged with the enhanced water flow directly into the xylem (Fig. 1F, H).
The velocity of ABA loss to the rhizosphere depends strongly on the permeability coefficients of root cortex membranes for ABA. Root membranes of maize and runner bean exhibit the lowest permeability coefficients for ABA known (Table 2). ABA loss directly from the symplast to the apoplast is up to 4000 times lower than from mesophyll cells, phloem elements and stem parenchyma cells.
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The contribution of conjugated ABA to ABAxyl
ABAxyl may also originate from ABA-glucose ester (ABA-GE) taken up by the roots into the cortex apoplast. Sauter and Hartung have shown that, besides free ABA, ABA-GE can also be present in the soil solution, often at higher concentrations than free ABA (Fig. 1I) (Sauter and Hartung, 2000). Both the exodermis and the endodermis are perfect barriers for ABA-GE. Sauter et al. concluded from a series of transport experiments with ABA-GE that the ABA-GE=1 (Sauter et al., 2002). When Casparian bands are not formed in the hypodermis (hydroponic culture, root systems of legumes, seminal root of barley) external ABA-GE can be dragged with the water into the root cortex. ß-D-glucosidases have been shown to be present in the root cortex of maize. They can release free ABA from the conjugate which again can be dragged directly to the xylem (Fig. 1K).
Abscisic acid: where does it go? The significance of the stem
Very little is known about the fate of ABA during its transport in the xylem through the stem. Studies of Jeschke and co-workers (Jeschke and Hartung, 2000) have shown that ABAxyl becomes significantly lower when ABA transport is diverted to leaves (Fig. 2A). Sauter and Hartung perfused bean internodes with ABA and ABA-GE in the concentrations that occur in the xylem under natural conditions (Sauter and Hartung, 2002). They demonstrated that free ABA can be fed into the xylem from stem parenchyma when ABAxyl is low (Fig. 2B), when ABA in the stem parenchyma is high and when pHxyl increases (as shown by Wilkinson and Davies, 1997, for stressed plants). On the other hand ABAxyl can also be redistributed to the stem parenchyma, especially when ABAxyl is high (Fig. 2C). Perfusion of an ABA free buffer through stems resulted in an ABA flow of 1.1 pmol m-2 s-1. This flow rate can be used to estimate the permeability coefficient of the stem parenchyma plasma membranes for undisocciated ABAH (assumptions that are necessary to perform this calculation are given in the legend of Table 2). It was found to be the highest PABAH of all cell types, indicating that ABA redistribution between stem parenchyma and the xylem is the fastest within an intact plant, contributing significantly to ABA homeostasis in the xylem.
Besides free ABA, conjugated ABA (predominantly ABA-GE) is also transported in the xylem. Because of its hydrophilic properties this molecule is, different from free ABA, transported without any losses or enrichments through the stem (Fig. 2D). The significance of ABA-GE as a stress signal is discussed in detail by Sauter et al. (Sauter et al., 2002).
Abscisic acid: where does it go? The significance of the leaves
Biosynthesis of ABA in plant leaves is increased only when leaf turgor approaches zero. Stomatal closure, however, occurs as the soil starts drying when 
leaf is still unaffected. It is therefore suggested that ABA import via the xylem is necessary to regulate leaf conductance under conditions of mild stress (Fig. 3D).
ABAxyl imported into the leaf tissue does not always accumulate there. ABA will be degraded rapidly after having acted on the stomata, especially under phosphate deficiency. Consequently, ABA is not deposited in the leaves despite an increased import of ABA via the xylem.
After its arrival in the leaf apoplast ABA may be redistributed to the leaf tissues (Figs 2E, 3E), in particular to alkaline compartments according to the anion trap concept (Slovik et al., 1995). The velocity of the redistribution again depends strongly on the permeability coefficients of the plasma membranes of the different cell types. It is highest in the case of the plasma membranes of the sieve tubes and the guard cells (Fig. 3F) (Table 2). Epidermal cells are also effective cells for ABA deposition, first because in many leaves they occupy a large percentage of the leaf volume and, second, because ABA transporters support ABA accumulation there (Daeter and Hartung, 1995; Dietz and Hartung, 1996).
Wilkinson et al. observed an alkalization of the xylem sap in plants growing in drying soil (Wilkinson et al., 1998). An alkalization of less than 1 pH unit is enough to close stomata significantly without extra ABA (Wilkinson and Davies, 1997). The authors have shown that under these conditions ABA redistribution to the leaf tissues is strongly reduced. Thus the intensity of the ABA signal is not weakened during its transport in the leaf apoplast to the guard cells.
ABA glucose ester in the leaf apoplast
Sauter et al. have pointed out that ABA-GE can only play a role as a hormonal stress signal when ABA is released from the extremely hydrophilic and physiologically inactive conjugate (Sauter et al., 2002). The different ratios of free ABA/conjugated ABA in xylem sap (4–7) and apoplastic washing fluids from barley leaves (22–32) permit the conclusion that fluids of the leaf apoplast contain glucosidases that may release the free hormone from the conjugate (Fig. 3G). Their activity increased 7-fold when plants were salt-stressed (Sauter et al., 2002), contributing to an increase of the concentration of free ABA in stressed barley leaves. Holbrook et al. performed experiments with grafted plants constructed from the ABA-deficient tomato mutants sitiens and flacca and their near isogenic wild-type parent (Holbrook et al., 2002). They concluded that stomata of stressed plants respond to ABA that is made in situ rather than transported from the root to the leaves. ABA-GE is a good candidate to act as a root-to-shoot signal that releases free ABA to the target cells in situ (Sauter et al., 2002).
Conclusion
Abscisic acid fluxes in the xylem can be regulated by several factors on their way from the roots to the target cells in the shoot. These factors include anatomical, physiological and biochemical features in the tissues of roots, stems and leaves. More research is required about the link between a change of soil conditions and the generation of the ABA signal, the putative transporters that may release ABA-glucose ester from the xylem parenchyma to the xylem vessels and the apoplastic glucosidases that liberate ABA from its conjugate at the site of action.
Acknowledgments
We are grateful to Deutsche Forschungsgemeinschaft [Ha 963/11–1; Graduiertenkolleg, SFB 251; (WH)] for generous financial support. The expert technical assistance of B Dierich (Lehrstuhl Botanik I, Universität Würzburg) and of Burkhard Stumpf (Lehrstuhl für Pflanzenökologie) Universität Bayreuth, is gratefully acknowledged.
Notes
1 To whom correspondence should be addressed. Fax: +49 931 888 6158. E-mail: Hartung{at}botanik.uni\|[hyphen]\|wuerzburg.de 
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