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Physiologia Plantarum / Volume 114, Issue 3

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What are the driving forces for water lifting in the xylem conduit?

Ulrich Zimmermann , Heike Schneider … See all authors

First published: 05 April 2002

https://doi.org/10.1034/j.1399-3054.2002.1140301.x
Cited by: 29

Abstract
After Renner had shown convincingly in 1925 that the transpirational water loss
generates tensions larger than 0.1 MPa (i.e. negative pressures) in the xylem of cut leafy
twigs the Cohesion Theory proposed by Böhm, Askenasy, Dixon and Joly at the end of the
19th century was immediately accepted by plant physiologists. Introduction of the
pressure chamber technique by Scholander et al. in 1965 enforced the general belief that
tension is the only driving force for water lifting although substantial criticism regarding
the technique and/or the Cohesion Theory was published by several authors. As typical
for scientific disciplines, the advent of minimal‐ and non‐invasive techniques in the last
decade as well as the development of a new, reliable method for xylem sap sampling
have challenged this view. Today, xylem pressure gradients, potentials, ion
concentrations and volume flows as well as cell turgor pressure gradients can be
monitored online in intact transpiring higher plants, and within a given physiological
context by using the pressure probe technique and high‐resolution NMR imaging
techniques, respectively. Application of the pressure probe technique to transpiring
plants has shown that negative absolute pressures (down to − 0.6 MPa) and pressure
gradients can exist temporarily in the xylem conduit, but that the magnitude and
(occasionally) direction of gradients contrasts frequently the belief that tension is the only
driving force. This seems to be particularly the case for plants faced with problems of
height, drought, freezing and salinity as well as with cavitation of the tensile water.
Reviewing the current data base shows that other forces come into operation when
 exclusively tension fails to lift water against gravity due to environmental conditions.
Possible candidates are longitudinal cellular and xylem osmotic pressure gradients, axial
potential gradients in the vessels as well as gel‐ and gas bubble‐supported interfacial
gradients. The multiforce theory overcomes the problem of the Cohesion Theory that life
on earth depends on water being in a highly metastable state.

Introduction
Water plays diverse physical, structural and metabolic roles in higher plants, but most of the
water taken up by plants from the soil is transpired to the atmosphere. Plants recycle more
than half of the annual rainfall on land. The overall driving force for water lifting in plants is
ultimately the chemical potential difference of water between soil and atmosphere.
However, the mechanisms by which water rise against gravity occurs are still controversially
discussed, despite extensive research over more than 150 years (see, e.g. Passioura 1991,
Zimmermann et al. 1993a,1993b, 1994a, 1995, Canny 1995a, Milburn 1996, Shackel 1996,
Richter 1997, Tyree 1997, for a review, see Meinzer et al. 2001). The reason for this is the
extremely high structural and functional complexity of the plant system and conversely the
lack of appropriate techniques for direct measurements of the intricate force‐flow
relationships.

Since the work of Hales 1727, the xylem conduit of vascular plants has been recognized as
the prominent pathway for antigravitational water (and solute) ascent up to heights of over
100 m. It consists of abundant leaky, water‐conducting elements (tracheids and vessels)
interconnected with each other and hydraulically, osmotically and electrically linked with the
tissue. Therefore, even though the xylem conduit is by far the easiest compartment of the
apoplast to analyse quantitatively, effects of the tissue apoplast and symplast (including the
phloem) on the xylem water rise dynamics can not be ignored, neither experimentally nor
theoretically. They must equally be taken into account as transpiration effects when
analysing water rise. Non‐equilibrium thermodynamics allows to adequately describe the
multifarious coupling of forces/flows in highly integrated systems operating far from
equilibrium. Application of this approach to transpiring plants requires that the xylem and
tissue ‘water and solute relations’ parameters in the entire plant system must be known. The
relevant information cannot be obtained by measurements on excised roots or leaves
because excision disturbs the flow‐force interrelationships between the xylem and its
surrounding (due to breakdown of standing osmotic and hydrostatic pressure gradients in
the symplast and apoplast; Rygol et al. 1993). For the same reason the techniques used for
measurements in intact plants must be non‐invasive or at least minimal‐invasive.

Strides in this direction have been achieved recently by the introduction of the xylem
pressure probe (Balling and Zimmermann 1990), NMR imaging techniques (Kuchenbrod
et al. 1996, Rokitta et al. 1999) and by advanced electron microscopy. These techniques
fulfil the above‐mentioned criteria for studying short‐ and long‐distance water relations in
intact plants. In addition, their spatial and temporal resolution is high enough to study short‐
term and diurnal changes of water relations parameters on the single vessel/cell level — a
prerequisite for the evaluation of the mechanism of water ascent.

This review is to demonstrate that application of these techniques to higher plants and tall
trees indeed warrants a critical assessment of the current ‘water ascent’ theory and the
methods used for its verification so far.

Tension‐driven water ascent

Modern textbooks interpret the ascent of water in the xylem in terms of the Cohesion
Theory. Loss of water by transpiration sets up a tension that is transmitted to the xylem, and
from there, down continuous columns of water to the roots. This implies that the tension
gradient between the root and leaf xylem is the only driving force for water extraction from
the soil to replenish the loss. The weakness of this theory is that tensions of at least 3 MPa
are required to lift water to the foliage of a 100‐m‐high tree. Supporters of this theory
overlook that tension is not only needed to overcome the gravitational force and hydraulic
resistance in the xylem of the trunk and the branches of a tree, but also to lift water in the
root xylem from 10‐m‐ to 30‐m‐deep ground water to the surface.

Water under tensions larger than 0.1 MPa (corresponding to negative pressures) is in a
metastable state like superheated water. Such states are generally short‐lived. Therefore,
the pivotal question of the extent to which the water columns break during transpiration (by
cavitation and/or entry of air) has been much debated. The cohesive forces between water
molecules are high enough to withstand tensions of 2 MPa or in excess (see Zimmermann
et al. 1993a,1993b, 1994a, 1995 for an overview). Even though this is consistent with
equilibrium thermodynamics, the relevant parameter for the cavitation threshold is the
adhesion of the water molecules to the xylem walls, i.e. the wettability of the inner surface of
the vessels (Laschimke 1989, Wagner et al. 2000). Vessel walls are much less wettable than
usually believed because of the hydrophobicity of incrusting lignin and other features (see
below). Infiltration of leaves with benzene and other organic solvents showed that the
apoplast is quite hydrophobic (Scott 1966). Similarly, rise kinetics of benzene in the xylem of
dry twigs of trees and resurrection plants were equal to, or even faster, than water rise
kinetics (Schneider et al. 1999, Wagner et al. 2000). The hydrophobicity of xylem walls is
totally ignored by the Cohesion Theory even though it reduces the cavitation threshold
considerably (Smith 1994). Various model experiments have shown that the frequency of
cavitation increased beyond a tension of 0.2 MPa and that tensions of about 1 MPa can be
sustained only for a fraction of a second, even when the surface is hydrophilic (for an
overview see Zimmermann et al. 1993a, 1993b, 1994a).

However, the evidence that encouraged the general acceptance of the Cohesion Theory was
the claim of Scholander et al. (1965) that measurements of the balancing gas pressure
required to force sap through the protruding cut end of an excised leaf in a pressure
chamber are good estimates of the original xylem tension of the intact plant. The balancing
pressure values ranged (species‐dependent) from 0.1 MPa up to 17 MPa. From the
beginning there were many controversial discussions about what the pressure chamber in
fact measured (reviewed in Meinzer et al. 2001). What has been especially glossed over is
that reference model experiments to calibrate the chamber have never been performed.
Exploration of the pressure chamber by simultaneous pressure probe readings on the
single‐vessel level demonstrated that the transmission of the chamber pressure to the
xylem is attenuated in transpiring plants (Melcher et al. 1998). Excess pressure is required
for compression of the air‐filled spaces and to overcome — among other things (see below)
— elastic forces and the osmotic pressure of the tissue. Therefore, the balancing pressure
can only be equated with the xylem tension before cutting when osmotic pressure effects
can be neglected and leaves are taken from well hydrated, non‐transpiring plants (or from
transpiring plants when the transpirational water loss is immediately compensated by root
pressurization). Recent measurements with an NMR‐compatible pressure chamber also
corroborate the view that a substantial part of the balancing pressure is used for lateral
water shifting in the excised leaf of a transpiring plant (Zimmermann et al. 2000). Spin
density‐ and T1‐weighted images were taken of the petioles of excised, stiff leaves of a well‐
hydrated liana and subjected to pressures of up to 0.5 MPa. The leaves were placed either
completely within the chamber or with the cut end protruding through the seal of the
chamber lid. In both leaf arrangements the spin density (= water concentration) did not
change significantly, whereas the T1‐weighted signal increased markedly with increasing
pressure (see Fig. 2 in Zimmermann et al. 2000). The change in T1 can only be explained by
a shift of water within the leaf petiole from large water‐filled to small water‐ or air‐filled
compartments. Such effects are, of course, expected to be more pronounced in leaves that
are less stiff and less hydrated.
 Figure 2

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Demonstration of acid mucopolysaccharides within the xylem sap of the Chaco
tree A. fraxinifolium (A‐C) and the Hawaiian mangrove Rhizophora mangle (D) by
Alcian blue staining (bars = 50 µm). Large amounts of mucilage‐dye complexes
are found in xylem extracts after subjecting woody branch pieces to a
compression‐decompression cycle (A; see also Fig. 3B) and in vessels after dye
rise (B: cross‐section;C, D: longitudinal sections).

Other current methods used for the determination of ‘xylem pressures’ such as Passioura's
root pressurization technique and psychrometry are as indirect as the pressure chamber,
and have also never been tested for their reliability in measuring xylem tension by adequate
model experiments. At the present state of the art the calibrated xylem pressure probe is
the only tool that gives direct access to the pressure of single xylem vessels. The impaled
vessel can be identified by dye injection into the probed lumen via the pressure probe and
by subsequent examination of cross‐sections above the impalement site (Balling and
Zimmermann 1990, Benkert et al. 1991, Zimmermann et al. 1993a, 2001a). Probing of
vessels of various herbaceous plants as well as leaf petioles of lianas and tall trees
demonstrated that negative pressures and axial gradients exist in transpiring plants under
some circumstances as predicted by the Cohesion Theory. Consistent with the theory,
increased light intensity and temperature as well as decreased relative humidity result in a
(temporary) decrease of the xylem pressure towards more negative values (see below).

As revealed by concomitant probe measurements and flow‐weighted NMR imaging, in well

hydrated plants increases in tension are reflected in corresponding increases of xylem
volume flow and flow velocity (Wistuba et al. 2000), whereas in plants subjected to severe
drought the relationship between both quantities is inverse. High‐resolution flow‐weighted
NMR imaging of both xylem and phloem provided cogent evidence that (in contrast to the
xylem volume flow and flow velocity) the phloem flow velocity did not change; rather, the
volume flow in the phloem increased during darkness (Rokitta et al. 1999). Apparently,
excess xylem water is recycled during the dark period due to opening of sieve pores and,
thus, increasing the phloem conducting area.

The correlation between xylem pressure and flow velocity is in favour of the Cohesion
Theory. Consistent with this theory are also the tensions measured in small plants (potato,
tobacco, maize, wheat, etc.) and in up to 10‐m‐tall lianas (see below). At high transpiration
rates, absolute negative pressures down to − 0.4 MPa were recorded before cavitation
occurred. These pressures equal those measured by Renner (1925) with the leafy twig‐
vacuum pump method and in model experiments. Pressures of − 0.5 to − 0.6 MPa could only
be recorded in plants which were severed from the roots or drought‐stressed for several
days (Zimmermann et al. 1994a), even though the pressure probe is capable of reading
down to much more negative values (Thürmer et al. 1999).

However, the operating xylem tensions in tall trees were frequently much lower than
expected from tension‐driven water ascent. For example, probe measurements in the
midrib of well hydrated leaves at a height of 35 m on a tropical tree (Anacardium excelsum)
yielded only maximum tensions of 0.2 MPa during the rainy season (by probe as well as
chamber measurements; see above). Similar values were measured at the same site and
time on A. excelsum seedlings growing beneath the tree (Zimmermann et al. 1994a). In a
liana, concomitant probing at different heights revealed diurnally changing tension gradients
(Benkert et al. 1995, Thürmer et al. 1999). Their magnitude was consistent with the
assumption of tension‐driven sap ascent (Fig. 1). However, gradients were occasionally
smaller than predicted by the Cohesion Theory (see arrows in Fig. 1) or even oppositely
directed (Benkert et al. 1995). Transpiration‐induced changes at the plant apex were not
transmitted instantaneously to the leaves at ground level (Fig. 1). These and other results
contradicting the Cohesion Theory have been reported in the literature, notably, also before
the introduction of the pressure chamber.

Figure 1

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Simultaneous measurements of diurnal changes in xylem pressure on the liana
Tetrastigma voinierianum at heights of 1 m (solid line), 5 m (dashed line) and 9.5 m
(dotted line) by using the xylem pressure probe. Note that the pressure gradient
between 1 m and 5 m decreased considerably after exposure of part of the leaves
to light. Redrawn from Thürmer et al. (1999).

Tall plants have apparently developed additional strategies for lifting water against gravity
because they are faced with much more severe problems than ‘laboratory‐sized’ plants due
to their height, in addition to drought, freezing and salinity.

Impact of interfacial water streaming on cavitated

vessels
Various methods have rendered convincing evidence that a large proportion of the xylem
conduits of higher plants and tall trees are cavitated at times of peak transpiration (Tyree
et al. 1986, McCully et al. 1998, Melcher et al. 2001, for a review, see Meinzer et al. 2001).
The pressure in cavitated vessels assumes positive, subatmospheric values. The vessels are
not necessarily deemed to have become completely filled with gas. Many vessels apparently
contain only tiny gas bubbles because they still show conductance as indicated by NMR
measurements. Refilling of such vessels occurs usually very rapidly when transpiration
progressively decreases, whereas refilling of completely embolized vessels needs — if it
occurs at all — much more time. Such vessels have a high resistance. Complete embolism of
vessels is apparently recorded by measurements of the so‐called vulnerability curves
(Sperry et al. 1988, Sperry and Tyree 1990, Cochard et al. 1992, Alder et al. 1997, for a
review see Meinzer et al. 2001). Thus, it is not surprising that ‘cavitation thresholds’ of about
2 MPa are measured by this method.

At the beginning of the last century it has been recognized that gas bubbles create
antigravitational water movement. However, the corresponding driving force remained
mysterious at that time. Today, it is clear that surface tension gradients established by
gradients in temperature, surface‐active substances or electrolytes at fluid/gas or
hydrophilic/hydrophobic interfaces drive an interfacial flow against gravity. In a capillary, this
so‐called Marangoni streaming is associated with an oppositely directed flow in the bulk
solution. Consequently, if water is withdrawn at the upper end of a vessel by evaporation, a
net mass flow against gravity is generated (Zimmermann et al. 1993b). Theory shows that
the flow rates are consistent with the flow data obtained experimentally. Therefore, the
formation of gas bubbles in vessels may not necessarily be a catastrophic event for trees
provided that the vessel walls remain wetted. Even though there is an enormous bulk of
literature supporting the ‘Marangoni streaming’ hypothesis (Zimmermann et al. 1993b,
Schneider et al. 2000b, Wagner et al. 2000), the contribution of interfacial forces to water
ascent can only be elucidated unambiguously when high‐resolution NMR techniques
become available to resolve flow and gas bubbles on the single‐vessel level.

Implications of gel‐like compounds for water rise

The question of how mangroves extract water from sea water (osmotic pressure about 2.5
MPa) is analogous to the question of how trees lift water to great heights, but requires work
against an osmotic, not a gravitational force. Measurements of xylem tensions of 3–7 MPa
by means of the pressure chamber apparently solved the problem (Scholander et al. 1966,
Scholander 1968, Zimmermann et al. 1994b), although on rainy days tensions of only about
0.1 MPa were recorded with leaves of the same tree (Zimmermann et al. 1994b). In contrast
to the pressure chamber, the xylem pressure probe and the leafy‐twig/vacuum method of
Renner (1925) yielded only positive subatmospheric or slightly negative pressure values
(Scholander et al. 1962, Zimmermann et al. 1994b). Maximum tensions were about 0.2
MPa, suggesting that other forces besides tension operate in the xylem of plants subjected
to extreme salinity.

According to the ‘Plumb‐Bridgman theory’ (Plumb and Bridgman 1972) antigravitational

water rise is conceivable at low tension gradients or even at constant tension if a gradient in
water activity of appropriate magnitude exists in the vessel (Benkert et al. 1995, Thürmer
et al. 1999). Gradients in water activity can be envisaged if the xylem is segmented into
osmotically active compartments or if the vessels contain filamentary gel‐like chains
attached to the walls (Plumb and Bridgman 1972). Candidates for gel‐like structures are
(surface‐active) acid mucopolysaccharides (Zimmermann et al. 1994b, 2001b). There is a
bulk of evidence that symplastic and apoplastic mucilages play an important role in water
storage, especially when plants are subjected to frost, drought or salinity (Watt et al. 1993,
1994, Zimmermann et al. 1994b, 2001b, McCully 1999, see also below). Indeed, mangroves
and tall trees rooting in saline groundwater (e.g. trees of the central Chaco in Paraguay
which can reach heights of up to 25 m) show a conspicuous abundance of
mucopolysaccharides in the xylem vessels (Fig. 2; see also Zimmermann et al. 1994b,
2001b). Clear‐cut evidence for this was obtained by pressurization of woody branch pieces
of these species (4 MPa) followed by instantaneous decompression. The sudden pressure
release resulted in bubble formation in the vessels, expelling the xylem sap from the vessels
without contamination with cell sap or cell damage (Schill et al. 1996). Alcian blue staining of
the collected liquid or immediate refilling of the emptied vessels with Alcian blue solutions
showed large amounts of mucopolysaccharides in the extract and less material left in the
vessels (Fig. 2; see also Zimmermann et al. 2001b).

Central to the implications of xylem mucosubstances for water ascent is the demonstration
of concentration gradients. At present, an unambiguous analysis of xylem sap cannot be
performed (see below). However, dynamic gradients can be expected because of the
concentrating effect by evaporative separation of water.

Slime‐like films of surface‐active mucopolysaccharides are apparently also important for

‘conditioning’ the xylem elements in order to keep continuous water films up to the foliage
when vessels are (partly) filled with air and/or vapour (see above). Spin echo 1H NMR cross‐
sectional images of branches of a 25‐m‐tall Chaco tree(Astronium fraxinifolium) with contact
to ground water at20 m depth showed that only a minor part of the vessels was completely
filled with water, whereas the majority apparently contained large amounts of gas
(Zimmermann et al. 2001b). Despite this, the leaves containing huge amounts of
mucopolysaccharides were fully turgescent (unpublished data). The fact that the xylem of
branches is supplied continuously or in regular intervals with mucopolysaccharides residing
in nearby cells and in the tissue apoplast supports this view. Acid polysaccharides also may
reverse transpiration, i.e. cause water uptake from the atmosphere through the stomata to
the xylem. This additional mechanism is suggested by water uptake of excised weakly
hydrated leaves of Chaco trees in a humid atmosphere (Zimmermann et al. 2001b).

Retrospectively, the outlined mechanism of hydrogel‐mediated water transport obviously

revives the Imbibition Theory postulated by Sachs (1887). In this context it is interesting to
note that mucosubstances have also been detected recently in the xylem of willow branches
during autumn and winter — but in lower concentrations than in mangroves or Chaco trees
(unpublished data), suggesting that mucosubstances may protect xylem sap against freezing
and/or support water ascent in spring. It is obvious that more data are needed (particularly
on trunks) in order to explore in detail the contribution of hydrogels to ‘xylem conditioning’
for water lifting.

Finally, obviously a considerable excess pressure in the Scholander chamber experiment is

required to squeeze water out of a hydrogel‐containing xylem. This circumstance renders
the interpretation of balancing pressure values in terms of xylem tension obsolete. For
mucilage‐containing species one can expect again only in the case of well‐hydrated leaves
that small pressures are needed to cause water to appear at the cut end of the pressurized
leaf. The presence of mucosubstances in the xylem and in the tissue explains quite readily
the variance of the balancing pressure data found for mangroves and Chaco trees
(Zimmermann et al. 1994b, 2001b).

Evidence for osmotic water lifting

Xylem segments in which ions and other osmotically active solutes are separated by solute–
reflecting barriers provide an alternative way of constraining the required activity gradient of
water. In order to exert an osmotic pressure the reflection coefficient σ, i.e. the coupling
coefficient between solute and water flow, of the solutes must be larger than zero. A
maximum osmotic driving force (equivalent to that predicted by the Van't Hoff equation) is
expected when the barriers consist of solute‐impermeable membranes (σ = 1). Roots of
mangroves, but also of non‐transpiring maize plants exhibit reflection coefficients close to
zero when subjected to various salt regimes (Zimmermann et al. 1994b, Schneider et al.
1997a,1997b), thus minimizing the problem to extract water from a saline environment (see
above). The reflection coefficients of xylem solutes are not known. Taking the hydrophobicity
of the xylem wall, the membranes of the adjacent living cells and other factors into account
it seems reasonable to assume that σ is of the order of 0.5 or less.
Analyses of expressed xylem sap samples have shown that the concentrations of ions and
low‐molecular weight nonelectrolytes are generally rather low (around 40 mOsmol or less).
However, the possibilities of dilution artifacts and solute contamination effects are
presumably not negligible because of the rapid water exchange times between the vessels
and the accessory cells (15–60 s). Xylem sap collected from maize leaves with an oil‐filled
xylem pressure probe (after pressurization of the roots) yielded values for ions similar to
expressed xylem sap, but sugars which were present in the leaf exudate were not found
(Lohaus et al. 2000). At variance with these results are the much higher values for the
osmotic pressure provided by X‐ray analysis of elements in the veins of bulk‐frozen leaves of
sunflower in the scanning electron microscope (Canny 1995b). The reasons for these
discrepancies are not known.

Promising progress may come from combining the xylem pressure probe with solute‐
selective microelectrodes allowing ‘online’ measurements in the vessels of intact transpiring
plants (Schneider et al. 2000a). Indeed, using a K+‐sensitive xylem pressure probe in the
root xylem of maize shows that the activity (concentration) of this ion is as low as suggested
by the analysis of expressed sap (unpublished data).

These findings seem to rule out water lifting by osmotic pressure gradients within the
vessels. However, there is a bulk of evidence that this mechanism plays a very important
role in deciduous trees during spring. The most reliable tool for xylem sap analysis of trunks
and branches of tall trees is the compression/decompression method (see above and Fig. 3;
Schill et al. 1996, Zimmermann et al. 2001b) because water is extracted from the vessels in
a few seconds thus avoiding dilution with cell water. With this method it was demonstrated
for trunk and branch pieces of birch and maple (taken at heights of up to 22 m) that large
axial osmotic pressure gradients temporarily developed during bud burst (Fig. 3; see also
Schill et al. 1996, Schneider et al. 2000a). The maximum value of xylem sap osmotic
pressure was found to be about 0.6 MPa (corresponding to an effective osmotic pressure of
about 0.3, if σ = 0.5; Schneider et al. 2000a). This value is high enough (particularly if root
pressures of about 0.1 MPa are additionally taken into account) to drive water up to large
heights in the absence of transpiration.
 Figure 3

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Seasonal xylem sap osmolality of birch branches taken from trees at a height of
approximately 5 m (A). Sap samples were extracted by application of the
compression/decompression technique schematically depicted in (B). It is obvious
that xylem osmolality was quite low and (within the limits of accuracy) constant
along the branch when samples were collected during autumn (28.09.99, ▪) and
winter (28.01.00, •) time. Osmolality increased considerably and height‐
dependent gradients developed during spring before bud break (19.03.00, ▴
12.04.00, ▾ 13.04.00, ♦). Note that gas bubble‐supported sap ejection from the
vessels (B; enlarged area) occurs in a few seconds, thus being much faster than
the water exchange time of the accessory cells (approximately 15 s). See also
Schneider et al. (2000a).

In contrast to trees of moderate climate, osmotic water lifting seems to be an all‐year‐round

mechanism of water ascent in tropical trees. This is suggested by measurements of the
physiological activity of accessory cells (Braun 1983, 1984) and is consistent with the low
tensions found by both the xylem pressure probe and the pressure chamber in A. excelsum
at a height of 35 m (Zimmermann et al. 1994a).

Due to the hydraulic coupling of xylem and tissue cells, longitudinal cellular osmotic
pressure gradients must also be considered as a driving force for water ascent. From its first
introduction, the Cohesion Theory was recognized as having no dependence on living cells.
Support for this view arrived from the demonstration of Strasburger (1891) that tall trees
and vines ‘continued to transpire’ for considerable time periods after addition of water‐
soluble poisons to the transpiration stream. Strasburger's interpretation based only on the
observation how long it took the leaves to wilt. However, since the uptake rates were very
low and transpiration not measured this experiment may be completely misinterpreted.

Concomitant probe measurements of xylem and turgor pressure at different heights in

‘laboratory‐sized’ and resurrection plants (see below) as well as studies of water ascent in tall
lianas against, with and in the absence of gravity revealed that diurnal changes in absolute
xylem pressure were accompanied by corresponding changes in turgor pressure of the
tissue cells (Fig. 4; see also Schneider et al. 1997b, 1999; Thürmer et al. 1999, Wistuba et al.
2000).

Figure 4

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Part of a simultaneous recording of xylem pressure (Px) and cortex cell turgor
 pressure (P) in an intact root of a 14‐day‐old‐hydroculture maize plant by using
the xylem and turgor pressure probe. In contrast to the xylem pressure probe
(which is always filled with water for long‐term measurements), the turgor
pressure probe is filled with silicon oil resulting in the formation of a cell sap/oil
meniscus upon puncturing of the cell (inset; arrow in the enlarged area). During
measurements the meniscus is kept at a constant position close to the root
surface by means of appropriate displacement of the metal rod. Note that the
decrease as well as the ‘overshoot’ in xylem pressure upon an increase in light
intensity from 5 µmol m−2 s−1 to 1200 µmol m−2 s−1 (downwardly directed arrow)
are accompanied by similar changes in turgor pressure, indicating the tight
hydraulic coupling of both compartments.

In upright lianas, probing has shown that the apical cells do not become fully turgid during
the night even when the roots are well watered. Their osmotic pressure is unbalanced and
the resulting longitudinal gradients in cellular osmotic pressure represent, besides
transpiration‐induced tension, an additional driving force for water ascent against gravity
(Wistuba et al. 2000). Such gradients may also be responsible for the occasional occurrence
of reverse xylem pressure gradients in these ‘understory’ plants (see above) because the
direction of these gradients depends strongly on the site of light incidence.

These and other findings demonstrate that the water in the cells and the tissue apoplast
provides a ‘buffer’ to be fed into the transpiration stream when the demand is high, thus
delaying the development of tension as well as the transmission of local tension changes
down the vessels (see above). The assumption that unbalanced cellular osmotic pressure is
an important driving force is also in accordance with the finding that xylem pressure
remains negative even when transpiration is stopped completely by a water‐impermeable
layer on the leaves (Zimmermann and Balling 1989). It is also consistent with the
observation that the disappearance of tiny gas bubbles in cavitated vessels and the re‐
occurrence of negative pressures always coincides with an increase in turgor pressure.

Involvement of electric driving forces in water rise

Non‐equilibrium thermodynamics predicts that electric driving forces can contribute to
water lifting. Physicists have also shown that the gravitational term of 100‐m‐tall trees can
be compensated by the energy of an electric double‐layer capacitor formed by a thin film of
ions on the negatively charged inner surface of the vessels (Amin 1982). It is obvious that a
film of acid mucosubstances as discussed above would enhance such a mechanism. Despite
the interesting features of this model, little effort has been spent in exploring electric‐
hydraulic coupling phenomena in tall trees. Recent integration of a microelectrode into a
xylem pressure probe and application of this xylem pressure‐potential probe to ‘laboratory‐
sized’ plants has provided some insight into this subject matter (Wegner and Zimmermann
1998, Wegner et al. 1999). Light‐ and osmotically induced xylem (and turgor) pressure
changes (and oscillations) were accompanied with corresponding changes in the trans‐root
potential (i.e. the potential difference between a xylem vessel and the external medium)
(Fig. 5; see also Wegner and Zimmermann 1998, Schneider et al. 2000a). Interestingly, the
response of the trans‐root potential was always faster than the response of the xylem
pressure upon illumination (Wegner and Zimmermann 1998). Maize plants that were
temporarily deprived of any N‐source additionally exhibited a close electrical coupling
between the xylem and the accessory cells (Wegner et al. 1999). From measurements with a
xylem pressure‐potential probe on detached shoots of tobacco there is also first evidence
for light‐dependent longitudinal potential gradients within the xylem conduit (Schneider
et al. 2000a and unpublished data). Thus, further exploration of water lifting using this novel
probe might lead to a better understanding of the electrical basis of xylem transport.

Figure 5

Open in figure viewer PowerPoint

Simultaneous probe recordings of pressure oscillations (Px) and of the trans‐root
potential (TRP) in the root xylem of a 9‐day‐old hydroculture wheat plant using
the xylem pressure‐potential probe (Wegner and Zimmermann 1998, Schneider
et al. 2000a). After vessel probing (*) light intensity was increased from 10 to 250
µmol m−2 s−1 (→) resulting in an initial drop of the xylem pressure and of the
trans‐root potential. Thereafter, pronounced oscillations of both parameters
occurred. With time the amplitude of the oscillations decreased accompanied by
a shift of the mean value of the two parameters to values before illumination.
 Redrawn from Wegner and Zimmermann (1998).

Resurrection plants: an example for multiforce

operation
Several features of water lifting partly reviewed above are apparently emphasized in
Myrothamnus flabellifolia. This fascinating resurrection plant can reach heights of up to about
1 m. Refilling of the empty vessels upon water supply transforms the lifeless‐looking woody
shrub into a living and functioning plant within a day. Several lines of evidence have shown
that the inner surface of the vessels and tracheids is extremely hydrophobic due to an up to
80‐nm‐thick lipid lining and to lipid inclusions in the intervessel pits (Schneider et al. 1999,
Wagner et al. 2000). The lipids apparently prevent drying of the tissues beyond tolerable
levels. Axial water ascent occurs in M. flabellifolia initially only in a very few neighbouring
conducting elements. 1H NMR imaging demonstrated that refilling of the other conducting
elements and of the (lipid body‐containing) tissue cells was mainly achieved by radial water
extraction from the initial conducting elements (Schneider et al. 2000a, Wagner et al. 2000,
Zimmermann et al. 2001c). Several forces such as root pressure, capillary forces and
interfacial streaming as well as osmotic and turgor pressure of the tissue cells were
identified as being involved in this process (Schneider et al. 2000b, Wagner et al. 2000).
Radial water spreading is apparently important for the successive disintegration of the lipid
lining under formation of lipid bodies, thus facilitating further axial water lifting.
Concomitantly with radial refilling of the tissue, leaves expanded and transpired. Tension‐
driven water lifting, however, became only effective when refilling of the xylem elements
was completed. There has also been some evidence that the lipid bodies in the xylem sap of
rehydrated plants may additionally generate interfacial streaming (Schneider et al. 2000b,
Wagner et al. 2000). At times of peak transpiration, xylem pressure did not drop below − 0.3
MPa. However, cavitation usually occurred at much lower tensions as expected in the light of
the hydrophobicity of the surface of the xylem elements (Schneider et al. 1999).

M. flabellifolia can apparently be considered as an extreme case of a more general

phenomenon (see comment by Canny 2000), because lipid bodies were also found recently
in the xylem sap of willow, birch and poplar during autumn (unpublished data). They seem
to be also permanently present in water‐conducting xylem elements of Chaco trees
(particularly in Bulnesia sarmientoi; Zimmermann et al. 2001b). This subject matter certainly
deserves further exploration.

Concluding remarks
The purpose of this review article was to convey the message that multiple physical
strategies exist for water lifting against gravity. Tension is one important driving force, but
others must obviously come into operation when higher plants and trees are faced with
cavitation, height, frost, drought and/or salt stress. This view contrasts the current dogma,
but is in accordance with the old literature and with recent work published by several
laboratories. The beauty of the multiforce theory is its implication that life on earth does not
depend on water being in a highly metastable state. ‘Beauty is the splendor of truth’ wrote
the English economist Schumacher.

We hope that drawing attention to experimental and theoretical evidence, being heretofore
ignored or not available, will assist plant physiologists to reconsider fictitious assumptions
about water lifting. Scientific dogmas tend to develop when established techniques are
applied indiscriminately. This tendency also includes the introduction of new parameters
lacking a thermodynamically sound formulation; for instance, the term ‘water potential’
ignores flux coupling.

The scope of some new techniques, briefly outlined in the review, opens an integrated
understanding of water ascent in intact transpiring higher plants and tall trees. Yet, further
incisive new experimental and theoretical approaches are needed to arrive at a detailed
description of water ascent at the molecular, cellular and tissue level.

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