Biology of the Cell (1997) 89, 259-273 259

o Elsevier, Paris

Review

Water transport across plant tissue: Role of water channels

Ernst Steudle
Lehrstuhl Pflanzendkologie, UniversiM Bayreuth, D-95440 Bayreuth, Germany

The contribution of water-filled, selective membrane pores (water channels) is integrated into a
general concept of water transport in plant tissue. The concept is based on the composite anatomi-
cal structure of tissues which results in a composite transport pattern. Three main pathways of
water flow have been distinguished, ie the apoplastic, symplastic and transcellular (vacuolar)
paths. Since the symplastic and transcellular components can not be distinguished experimentally,
these components are summarized as a cell-to-cell component. Water channel activity may control
the overall water flow across tissues provided that the contribution of the apoplastic component is
relatively low. The composite transport model has been applied to roots where most of the data are
available. Comparison of the hydraulic conductivity at the root cell and organ levels shows that,
depending on the species, there may be a dominating cell-to-cell or apoplastic water flow. Most
remarkably, there are differences in the hydraulic conductivity of roots which depend on the
nature of the force used to drive water flows (osmotic or hydrostatic pressure gradients). This is
predicted by the model. The composite transport model explains low reflection coefficients of
roots, the variability in root hydraulic resistance and differences between herbaceous and woody
species. It is demonstrated that there is also a composite transport of water at the membrane level
(water channel arrays vs bilayer arrays ). This results in low reflection coefficients of plasma mem-
branes for certain test solutes as derived for isolated internodes of Chara. The titration of water
channel activity in this alga with mercurials and its dependence on changes in temperature or
external concentration show that water channels do not exclusively transport water. Rather, they
are permeable to relatively big uncharged organic solutes. The result indicates that, at least for
Chara, the concept of an exclusive transport of water across water channels has to be questioned.

apoplastic transport / cell-to-cell transport / composite transport / hydraulic conductivity / reflection

coefficient / single-file transport/water channels

INTRODUCTION complicate tissue hydraulics which may be

In plants, water transport across tissues plays an
important role during many fundamental pro-
cesses. These include the uptake of water by roots
and extension growth. Water movement across tis-
sues is involved in the loading of phloem with
water from adjacent xylem which results in a circu-
lation flow of water in the plant. During all the pro-
cesses mentioned, there are interactions between
water and solutes (Steudle, 1989, 1994a; Meshcher-
yakov et al, 1992). The latter are compartmentalized
differently in protoplasts and the apoplast. Interac-
tions between both flows and compartments
described within the framework of irreversible
thermodynamics (Steudle, 1989, 1992, 1994a). The
major result is that, because of interactions, osmotic
properties of tissues may not be straightforwardly
derived from those of individual cells.
Despite the fact that water transport across tis-
sues is important, experimental techniques for
measuring the hydraulic conductivity of tissues are
not well developed. There has been some theoreti-
cal work on tissue water relations (Philip, 1958;
Molz and Ikenberry, 1974; Molz and Ferrier, 1982;
Steudle, 1989, 1992, 1994a, b), but in recent years
much more effort has been put into understanding

Water transport across plant tissue Steudle

260 Biology of the Cell (1997) 89, 259-273

xylem hydraulics (long distance transport of water;
Frensch and Steudle, 1989; Tyree and Sperry, 1989;
Steudle, 1995; Tyree, 1997) and water transport at
the cell level (short distance transport; Steudle,
1989, 1993, 1994a) rather than into the tissue or
organ level (medium distance transport). Difficul-
ties in measuring tissue water transport include a
lack of equipment for measuring water flow across
tissues and organs which may have a complicated
shape (such as a leaf) and small dimensions. Most
data are available for young (primary) roots, where
dimensions and shape are well defined, but only
little information is available for entire root systems
(Steudle et al, 1987; Radin and Matthews, 1989;
North and Nobel, 1991; Cruz et al, 1992; Nobel and
North, 1993; Riidinger et al, 1994; Steudle, 199413;
Steudle and Frensch, 1996; Steudle and Meshcher-
yakov, 1996; Steudle and Heydt, 1997). For the roof,
there is some difficulty in choosing an appropriate
reference for comparison. Sometimes fresh weight
has been used, but from a physiological and physi-
cal point of view, surface area would be much more
appropriate. Another difficulty arises from the fact
that data on hydraulic conductivity (such as for an
entire root system) would average out arrays of
quite different states of age and development. To
date, there is still some uncertainty about the con-
tribution of different root parts to the overall water
uptake (Kramer and Boyer, 1995). This uncertainty
is tied up with the fact that the water permeability
(hydraulic conductivity) of roots is quite variable
(Brewig, 1937; Brouwer, 1954; Weatherley, 1982;
Steudle, 1994b). This has an impact on the ability of
plants to supply the shoot with water, and is, there-
fore, of great importance. Although there have been
attempts to work out the reasons for the variable
root hydraulic conductance (eg Fiscus, 1975; Pas-
sioura, 1988), the factors that govern, adjust, or
even regulate it still remain unclear. Quantitative
models are missing.
In this review, I summarize some of the concepts
currently discussed to describe water relations of
plant tissue or, better, the transport of water across
tissues. Most of the work presented relates to roots,
the organs for which most data are available. Com-
parisons are made between the cell and the overall
tissue or organ level to assess the contribution of
different pathways to overall tissue transport. For
the cell (membrane) level there is a considerable
amount of transport data which indicates the exis-
tence of aquaporins. However, we have to state that
the concomitant molecular characterization of
transport proteins is lacking. Despite this difficulty,
I emphasize the putative role of aquaporins as
water channels. It is shown that in plant tissues,
overall water and solute transport may be
described in quantitative terms by a ‘composite
transport model’ which summarizes flows across
membranes and around cell protoplasts. The model
integrates hydraulic and osmotic processes. It
allows for interactions both between water and
solute flows and between different pathways. For
the root, it is shown that the model explains some
of the adaptive or regulatory functions of this organ
in response to external or internal parameters such
as drought or high transpiration. These functions
may also involve changes in the activity of water
channels.
THEORETICAL BASIS OF TISSUE
TRANSPORT: STEADY WATER FLOW
The conceptual or theoretical problem related to tis-
sue transport of water is that there are different
pathways along which water may move. Depend-
ing on the type of tissue and on its developmental
state, the relative contribution of pathways to over-
all water flow may differ. Schematically, the situa-
tion is shown in figure 1A. The three different path-
ways for water movement in plant tissue are: i) the
apoplast, ie the path around protoplasts. The apo-
plastic path includes water flow across cell walls
and intercellular spaces some of which may be
filled with water. Usually, the mean cross-sectional
area available for apoplastic water flow will only be
a few percent of the total cross-sectional area, but,
nevertheless, apoplastic water flow can be impor-
tant in plant tissue because of the high hydraulic

Fig 1. Pathwaysfor the movement of water and solutesacross plant tissue. A. Schematic view of a tissue of thickness8 b
representedby four ceils arranged in series. i) The apoplasticpath is aroundthe protoplasts; ii) the symplasticpath is me-
diated by plasmodesmatawhich bridge the cell wallsso that a cytoplasmic continuumis formed. Duringthe passagealong
the apoplastic and symplastic pathways no membraneshave to be crossed; iii) the transcellularpath is only important for
water (which has a very high membranepermeability and may be affected by the activity of water channels),but not for
solutes such as nutrient ions. Along the transcellular path, two plasma membraneshave to be crossed per cell layer.
B. Radialuptake of water acrossthe root cylinder. Here, apoplasticbarriers occur in the endo-and exodermisduring root
development(Casparianbands),which tend to interrupt the water flow across the apoplast. Note that the symplastic and
transcellular water flow can not be separated experimentallyand should be summarizedas a cell-to-cellcomponent of
water flow. It should also be noted that there is a rapid exchangeof water betweenthe cell-to-celland apoplastic pathways
so that local water flow equilibriumbetweenprotoplasts and adjacentapoplastwill be achieved.

Water transport across plant tissue Steudle

Biology of the Cell (1997) 89, 259-273 261

B
exodermis cortex
I
rlMzoderqis

(cl

(a)
(b)

Y rian
plasmodesmata

111111) ( a ) amplastic path

- + ( b ) symplastic path
cell-to-cell path
- + ( c ) transcellular path
l

Water transport across plant tissue Steudle

262
conductivity of cell wall material (Zhu and Steudle,
1991); ii) the symplastic path mediated by plasmo-
desmata. This path involves water movement
within the cytoplasmic continuum. Like the apo-
plastic path, no membranes have to be crossed
along the symplastic path. There is some uncer-
tainty about the hydraulic resistance of plasmodes-
mata, because the actual cross-sectional area avail-
able for transport within the pores is not really
known (Lucas ef al, 1993); iii) the third path, the
transcellular path which includes the flow of water
across membranes. Water channel activity, if
present, affects the transcellular path only. Along
the transcellular path, the plasma membrane rather
than the tonoplast is considered to be the major
hydraulic resistance (eg Kiyosawa and Tazawa,
1977). Thus, for each cell layer, only two mem-
branes have to be considered. The contribution of
the walls between adjacent cells will be negligible.
Usually, the cross-sectional area available for trans-
cellular flow is high (some 90% of the entire cross
section). The transcellular component is something
significant for water transport. Since the permeabil-
ity of membranes to water is larger than that to ions
by five to six orders of magnitude, transcellular
flow is much more important for water than for
ions. For the latter, transcellular flow will usually
be negligible.
To date, the transcellular (transmembrane) com-
ponent of flow can not be separated experimentally
from the symplastic component. Hence, we have to
combine both components as ‘cell-to-cell’ or
‘protoplastic’ flow. Although the term ‘cell-to-cell
is firmly entrenched in the literature, the term
‘protoplastic’ would, perhaps, be more adequate
because the apoplast is also part of the cell (Mel-
chior and Steudle, in preparation).
As shown in figure 1, we have, in a tissue, two
parallel components through which water may
flow. Hydraulic conductances of parallel pathways
are additive for each cell layer. Hydraulic resis-
tances (the inverse of conductances) of each layer
will add to the overall hydraulic resistance. This is
analogous to the situation in electrical networks
with resistors arranged in parallel and in series
(Ohm’s and Kirchhoff’s laws). For a planar tissue of
a given thickness L, which contains &Ax cell layers
of thickness dx, we have a tissue hydraulic conduc-
tivity Lp, of (Steudle, 1992, 1994a; Steudle and
Frensch, 1996):
yccLp/2 + xcwLp,, 11+ SF (I- qyJ1
LP, = (1)
l/b e when the tissue does not shrink or swell. This is
Equation (1) is valid during steady flow and in
the presence of both purely hydrostatic and
Water transport across plant tissue
Biology of the Cell (1997) 89, 259273
osmotic pressure gradients. The symbols “/ccand */cw
denote the average relative cross-sectional areas
available for water transport along the apoplastic
and protoplastic pathways (‘Y,~ + “/cw= 1) and Lp
and Lp,, the hydraulic conductivities of cell mem-
branes and of the apoplast, respectively. The
switching factor (SF) in equation (1) accounts for
the fact that the hydraulic conductivity of a tissue
will be different depending on whether a hydro-
static or osmotic gradient is acting across or within
a tissue. This is so because, in the apoplast, there
are no membrane barriers, and reflection coeffi-
cients (6,) should be close to zero for solutes. In
the presence of a hydrostatic gradient, the flow
across the tissue at a given pressure gradient will
be maximal and SF = 0. In the presence of a purely
osmotic gradient, there will be no apoplastic water
flow if the reflection coefficient of the wall material
Ocw= 0. Hence, we may conclude that, depending
on the nature of the driving force, there should be
some variability in the intensity by which different
pathways are used by water, which then results in
different overall hydraulic resistances. The situa-
tion may be further complicated by the fact that the
absolute value of Lp, may depend on the nature
of the flows (osmotic vs hydrostatic) or on the abso-
lute value of water flow (Mel&or and Steudle, in
preparation).
In equation (1), the cell-to-cell component (ie cell
Lp) would include water channels, if present.
According to the activity of water channels, tissue
Lp, may vary. However, it is clear that the contribu-
tion of water channels will depend on the relation
between apoplastic and cell-to-cell flow and it is
important to know which component will domi-
nate under certain conditions. This simple fact is
often neglected when the role of water channels
during tissue transport is discussed (Chrispeels and
Maurel, 1994; Maurel, 1997; Schaffner, 1997). Before
accepting a dominant role of water channels, it has
to be shown that the contributions of other compo-
nents are really negligible. For example, in plant
roots, the relative contribution of pathways will
largely depend on whether or not there are apo-
plastic barriers (Casparian bands, suberin lamellae)
which interrupt the flow around protoplasts and
reduce the apoplastic component.
TRANSIENT WATER
FLOW ACROSS TISSUES
Equation (1) describes the situation of a steady flow
of water across a tissue at constant water content, ie
realized during steady state root exudation or dur-
ing steady transpiration from leaves. Transient
water flows, on the other hand, occur during the
Steudle
Biology of the Cell (1997) 89, 259-273
shrinking or swelling of tissues. They are brought
about by changes in the ambient water potential.
From a physiological point of view, the time con-
stant of the shrinking or swelling of a tissue is
important during water stress or osmoregulation of
plants. During transient responses, changes in
water potential will propagate across a tissue from
layer to layer, and the rate at which this occurs will
depend on the factors already discussed above
(hydraulic conductances of pathways, geometrical
factors, nature of driving forces, etc; eqn (1)). How-
ever, in addition, the storage capacities of the com-
partments involved play a role (protoplasts, C,;
apoplast, C,,). It can be shown that for a homoge-
nous tissue, the kinetics of shrinking or swelling
will be, mathematically, of a diffusion type,
although the processes are by no means diffusional
in nature. What is happening during shrinking and
swelling is a displacement of bulk water resulting
in changes in turgor and osmotic pressure of proto-
plasts and in water potential of the tissue. The rate
at which changes in water content and of flows
occur can be characterized by a ‘diffusivity’ (D,)
which has the same units as a diffusion coefficient
(m2 s-1). Again, if we assume that tissue protoplasts
behave like nearly perfect osmometers (reflection
coefficient, os s 1) the diffusivity can be expressed
as (Steudle, 1989, 1992, 1994a; Steudle and Frensch,
1996):
Lp/2 act Ax2 + Lp,, acwAx 11 + SF (l-o,,)}
Df =
cc + =cw
(2)
acwAx act Ax P,Ax
+-DC,+-----• -a
vcw vc 2 of driving forces which causes a switching between
Here acw and act are the cross-sectional areas
available for the cell-to-cell and apoplastic path (see
fig 1A). The first term on the right side of this equa-
tion represents changes due to water flow. It can be
seen that D, increases with increasing conductances
of the cell-to-cell (Lp/2a,,) and apoplastic
(Lp,w/a,,/Ax) pathways. The ability of cells to
store water reduces the rate (storage capacity of
cells, C,, and of apoplast, C,, in the denominator).
When osmotic solutes act as a driving force, the
propagation of changes of water potential and tur-
gor across a tissue will also depend on the move-
ment of the solutes within the tissue (eg by diffu-
sion along the apoplast or from cell to cell across
membranes). The second term on the right side of
equation (2) denotes the contribution of passive
solute flow along the apoplastic path: this is con-
trolled by the geometry of the path and by the dif-
fusion coefficient of solutes (D,). Along the proto-
plastic path (third term on the right side of
Water transport across plant tissue
263
equation (2)), the permeability of cell membranes to
the solutes present in the system will be important
(P,). However, this is usually negligible. Of course,
there may be some active solute movement in the
tissue (eg nutrient uptake into root protoplasts; sup-
ply of sink tissue with assimilates by the phloem;
Meshcheryakov et al, 1992). This is not integrated
into equation (2). In the presence of active solute
flow, there will usually be no analytical expression
for D,. Rather, swelling or shrinking characteristics
would have to be solved numerically (Steudle,
1992).
As already discussed with respect to steady
flows, equation (2) predicts differences in the kinet-
ics depending on whether there are osmotic or
hydrostatic gradients acting to cause the flow.
Experimental results indicate that the hydraulic
conductivity of the wall path (Lp,,) can also vary
which may be related to changes in water content
of the porous walls or other factors (Steudle and
Frensch, 1996; Melchior and Steudle, in prepara-
tion). With respect to an adjustment or even regula-
tion of water flow in plants, this is of particular
interest (see below).
There is good experimental evidence for the
validity of equations (1) and (2). Equation (1) sim-
ply extends the catenary hypothesis of water flow
in plants (van den Honert, 1948) which is usually
used for whole plants, to tissue and cell dimen-
sions. The validity of equation (2) has been checked
in experiments with various tissues (eg Molz et d,
1973; Molz and Boyer, 1978; Steudle and Boyer,
1985; Westgate and Steudle, 1985; Zhu and Steudle,
1991). Both equations indicate some variability in
water flow across tissues depending on the nature
pathways. This is different from the idea of con-
stant hydraulic resistors underlying the catenary
hypothesis.
EFFECTS OF WATER CHANNEL
ACTIVITY ON TISSUE TRANSPORT
Water channel activity during tissue transport
affects the cell-to-cell rather than the apoplastic pas-
sage of water. Water channel activity may be con-
trolled by metabolism (eg by a phosphorylation of
aquaporins; Johansson et al, 1996) or may be trig-
gered by environmental factors (Steudle and Henz-
ler, 1995). For example, in pea it has been found
that water shortage increases the expression of
water channels (Guerrero et al, 1990). In corn roots,
high salinity reduces the permeability to water of
both root cells and (to a lesser extent) whole roots
(Azaizeh and Steudle, 1991; Azaizeh et al, 1992).
Recently, Carvajal et al (1996) have shown that
depriving wheat plants of nutrients also decreased
Steudle
264
root Lp,, apparently by affecting the activity of
water channels. These findings are in line with the
observation that blocking roots with mercurials
reduced root Lp, reversibly (Maggio and Joly,
1995). At the level of an individual, intact plant cell,
the effects have been documented in great detail
with Chavu (Wayne and Tazawa, 1990; Henzler and
Steudle, 1995; Tazawa et al, 1996; Schlitz and Tyer-
man, 1997). In these experiments, water channel
activity has been titrated with mercurials (mercuric
chloride or p-chloromercuriphenylsulfonic acid).
Similarly, high external concentrations of permeat-
ing solutes have been employed to affect the open
or closed state of channels (Steudle and Henzler,
1995). Higher plant cells have been used as well in
these latter studies which have been performed
using the cell pressure probe (Steudle, 1993). The
results demonstrated that water and small
uncharged test solutes used different pathways
across the plasma membrane, as postulated for suf-
ficiently narrow pores selective for water. How-
ever, the quantitative treatment of interactions
between water and solute flows also showed that
there was some slippage of the small uncharged
test molecules across water channels (see below).
To date, there are no experiments with intact plant
tissue which actually demonstrate this. One would
need to measure cell Lp in the presence and
absence of functioning water channels as well as
the overall tissue hydraulic conductivity (eg root
Lp,), and quantitatively compare the results.
Changes in the expression of water channel pro-
teins in the membranes of cells would have to be
demonstrated as well. These experiments are
underway.
VARlABlLlTY OF TISSUE HYDRAULICS
From the discussion presented so far, it is clear that
there may be different reasons for the variability in
tissue water transport which has often been docu-
mented, namely, for roots (Brewig, 1937; Brouwer,
1954; Weatherley, 1982; Passioura, 1988; Steudle,
1989, 1994a, b; Steudle and Frensch, 1996). It may
be related either to changes in the apoplastic or cell-
to-cell components of water flow. This has to be
kept in mind when discussing possible effects of
water channels on overall transport properties of
tissues. Since the apoplast may dominate transport
under certain conditions, no firm conclusion can be
drawn about the physiological role of water chan-
nels just by demonstrating their existence in the
membranes of tissue cells. Transport studies are
required to separate the apoplastic component from
that due to water channels. To date, this is largely
missing (Maurel, 1997; Schgffner, 1997). In tissues
such as the root, transport studies have to be com-
Water transport across plant tissue
Biology of the Cell (1997) 89, 259-273
bined with careful studies of anatomy (Melchior
and Steudle, 1993; Peterson and Steudle, 1993;
Peterson et a2,1993; Steudle et al, 1993; Frensch et al,
1996). For example, the formation of suberin lamel-
lae may reduce water flow across the cell-to-cell
path during root development, but this may be
compensated for by the retention of passage cells in
both the exo- and endodermis (Peterson and
Enstone, 1996). It has been speculated that passage
cells have a higher density of water channels and
thus a higher permeability to water than typical
cortex cells (SchHffner, 1997). 0~ the other hand,
the formation of apoplastic transport barriers in the
endo- and exodermis may change the ratio of cell-
to-cell to apoplastic transport. Hence, physiological
studies on the role of water channels have to
include both the apoplastic and membrane compo-
nents.
ROOT HYDRAULICS:
CELL VS ORGAN LEVEL
Roots have been the plant part most intensively
studied, both at the cell and organ levels (Steudle
and Jeschke, 1983; Steudle et a&1987; Zhu and Steu-
dle, 1991). In these organs, comparisons of the rela-
tive importance of the cell-to-cell and apoplastic
pathways are possible. The reason that many data
are available for roots is that measurements are
fairly simple to obtain at the tissue level using ordi-
nary root exudation, pressure-exudation or the root
pressure probe, and at the cell level with the cell
pressure probe. The root pressure probe also per-
mits the measurement of the solute permeability of
roots (eg for nutrient salts) or interactions between
water and solute transport which are expressed by
root reflection coefficients (a,>. Thus, complete sets
of transport coefficients may be obtained at the cell
and root levels. As for the cell level, the quantifica-
tion of interactions between water and solutes pro-
vides a deeper insight into root osmotic properties.
These are tightly linked with the question of path-
ways.
Tables I and II summarize available data on root
cell Lp and overall root Lp, for both herbaceous
and woody species. To date, data for the mem-
brane level are only available for herbaceous
plants. The comparison shows that in some cases,
there may be a consistency with a cell-to-cell
model (barley, bean, wheat) independent of the
force applied. In others, there is a dominating apo-
plastic water flow when hydrostatic gradients are
applied. The prediction made in equation (2)
seems to hold that in the presence of osmotic
forces, the cellular path is preferred. The data
show that differences caused by a variation of
forces are most dramatic for woody species which
Steudle
Biology of the Cell (1997) 89, 259-273 265

Table 1. Root hydraulic conductivity (Lpi), solute permeability (P,,), and reflection coefficients &I of roots of herbaceous
species as determined with the root pressure probe and other techniques. Where available, hydraulic conductivities of root
cell membranes (cell Lp) are added for comparison. It can be seen that, because of the high cell Lp, there are no differ-
ences between osmotic and hydraulic water flow (Lp,) in barley and Phaseolus coccineus. For maize and Phaseolus vul-
garis, there are large differences. The findings are explained by the composite transport model of the root (see text and
fig 21. Values of root Go, are significantly lower than unity for solutes for which cell membranes exhibit a cr, of virtually unity.

Species Root Lp, .1Oa Root permeability, Root reflection Techniques Ref
(r-n s-1 MPa-1) P,, 109 (rn s-1)
l coefficient,
Hydraulic Osmotic OS,(1)

Hordeum 0.3-4.3 0.3-4.3 mannitol: Cell and root

distichon, Cell Lp: pressure probe a
primary root 12

Triticum - 0.5-5.5 Cell pressure probe

aestivum, Cell Lp: and stop flow b,c
primary root 12

Zea mays, 1-46 0.1-5 sucrose: 3.0 mannitol: 0.4-0.7 Cell and root
primary root Cell Lp: NaCI: 6-14 sucrose: 0.54 pressure probe
24 NaCI: 0.5-0.6
KCI: 0.53

Zea mays, 21 2.2 nutrients: 0.85 Stop-flow technique h, i

root system and osmotic flow

Allium cepa, 14 0.02- NaNO,: 0.7 KCI, mannitol, NaNO,; Root pressure
primary root 2 to 0.35-0.88 probe
NH,NO, J-I

Phaseolus 2-8 3-7 mannitol: 0.15 mannitol: 0.68

coccineus, Cell Lp: NaCI: 0.21 NaCI: 0.59
primary root 30-470 KCI: 0.7-0.9 KCI: o-43-0.54

Phaseolus 30 0.56 nutrients: 1.3 nutrients: 0.98 Pressure chamber

vulgaris, and osmotic flow
root system h, m

Agave desert;, - Constant flow

Ferocactus mode
acanthodes, l-50 n
Opuntia ficus-
indica,
root systems

a Steudle and Jeschke, 1983; b Jones et al, 1983; c Jones et al, 1988; d Steudle et al. 1987; e Steudle and Frensch 1989;
f Zhu and Steudle, 1991; g Peterson et al, 1993; h Newman, 1973; i Miller, 1985; i Melchior and Steudle, 1993; k Melchior
and Steudle, (1995); 1Steudle and Brinckmann 1989; m Fiscus, 1986; n Nobel and North, 1993.

also show reduced permeability for both water COMPOSITE TRANSPORT ACROSS
and solutes. This is theoretically predicted (see ROOTS
below). The small overall reflection coefficients
found for both types of species are not compatible The data given in table I are consistent with the the-
with the simple osmometer model of the root. ory outlined above when some assumptions are
However, they are in accordance with the compos- made about switching between transport modes or
ite transport model of water which is based on changes of Lp,,. The corresponding model has
irreversible thermodynamics and on the composite been termed ‘composite transport model of the
anatomical structure of roots (Steudle et aI, 1993; root’. It may apply to tissues in general (fig 2). The
Steudle 1994a, b; Steudle and Frensch, 1996; Steu- model stresses the fact that in a root, we have par-
dle and Peterson, 1997). allel pathways of quite different selectivity (Steudle

Water transport across plant tissue Steudle

266 Biology of the Cell (1997) 89, 259-273

Table II. Root hydraulic conductivity (Lp,), solute permeability (P,,], and reflection coefficients (~~sr)of some woody species
as determined with the root pressure probe and other techniques, It can be seen that, on average, the hydraulic conductiv-
ity of tree roots is substantially smaller than that of roots of herbs (table II. Differences between osmotic and hydraulic root
Lp, (osmotic and hydraulic water flow) are large. Root reflection coefficients of tree roots are smaller by a factor of two
than those of herbs. Permeability coefficients of tree roots are much smaller than those of herbs. Usually they are not mea-
surable mm) with the root pressure probe.

Species Root Lp, 010s Root permeability, Root reflection Techniques Ref.
Im s-1 MPa-1) P,, .I 09 (rn s-1) coefficient,
Hydraulic Osmotic OS,(II
Picea abies, 6.4 0.017 nm Na, SO,, K,SO,,
root system Ca(NO,),:
0.18-0.28

Quercus 0.5-4.8 0.003- nm mannitol: 0.19-0.43 Root pressure a to c

robur, 0.062 NaCI: 0.17-0.31 probe
root system KCI: 0.12-0.35

Fagus 0.35-l .6 0.022- nm mannitol: 0.29-0.82

sylvatica, 0.11 KCI: 0.22-0.55
root system NaCI: 0.32-0.64

Pinus taeda, 20 (young - Pressure chamber d

root system roots);
7.6 (old roots)

a Rtidinger et a/, 1994; Steudleand Meshcheryakov, 1996; c Steudleand Heydt, 1997; * Sandset a/, 1982.

Compodto tfan8poft model of root

0A

Fig 2. Compositetransport modelof root. The osmotic barrier of the root is made up by two parallel pathways,the cell-to-
cell and apoplastic path (fig 1). Sincethe cell-to-cellpath has a high selectivity for solutesLos= 11,water will be driven into
the root osmotically so that a root pressure builds up. This, in turn, will cause a back-flow of water along the apoplast,
since Casparianbandsare not completelytight. In the apopfast,the selectivity will be small(a, = 0). Hence, there will be a
circulation flow of water as long as the osmotic pressuredifference is maintained.This reduces the overall root nssr to a
value of a,, < 1 (asfound). Other propertiesof the compositetransport modelare discussedin the text.

Water transport across plant tissue Steudle

Biology of the Cell (1997) 89, 259-273
et al, 1993; Steudle 1994a, b; Steudle and Frensch,
1996). Pathways contribute to the overall osr value
according to their conductance. Hence, measured
osr values can be substantially smaller than unity at
a reasonable overall Lp, and low solute permeabil-
ity (I’,,), as found experimentally. The composite
transport model explains other important features
of roots such as: i) the variability of root hydraulic
conductivity; ii) the low reflection coefficients of
roots; and iii) differences between woody and her-
baceous species.
The variability in Lp, is explained by the fact that
at low hydrostatic gradients, flow is largely osmotic
and from cell to cell, which causes a high resistance
and a back-flow of water within the root (circula-
tion flows; fig 2). As hydrostatic gradients increase,
the situation changes and there will be no back-
flow which, in turn, will increase the overall Lp,. In
terms of the model, increases can be brought about
by differences in the relative importance of path-
ways, but water channel activity may be triggered
as well. Thus, within the model, the flexibility of
the system is just a consequence of the root struc-
ture which is also the reason for the low overall ossr.
It is important to note that the model allows for a
low asr in the presence of a low solute permeability
(root P,J. So, roots are not leaky, despite low root
crsr. Nutrient ions, once taken up by active pro-
cesses, do not leak back into the medium.
POSSIBLE ROLE OF WATER CHANNELS
DURING COMPOSITE TRANSPORT
It is clear that wherever apoplastic water flow domi-
nates in plant tissue, the regulatory function of
water channels could only be small. This should
usually be the case for tissues lacking apoplastic
barriers (Casparian bands). Results show that this
would also be the case in roots under conditions of
high transpiration, provided that apoplastic bar-
riers do not completely interrupt water flow at the
exo- and endodermis. It may be speculated that as
roots age and suberin lamellae develop, Casparian
bands become more impermeable to water. Under
these conditions, the cell-to-cell movement should
become important, namely, in passage cells of the
endodermis and exodermis (Peterson and Enstone,
1996). It appears that the regulation of water flow
across roots occurs in a hierarchical way. In parts of
roots lacking an apoplastic barrier or allowing for
some apoplastic bypass in the endodermis, there
would be a ‘course regulation’ dictated by structu-
ral features and a sharing of flows according to the
demand of the plant (Steudle et al, 1993; Steudle,
1994b; Steudle and Peterson, 1997). This situation
would apply to well-watered transpiring plants
which have a demand of water from the shoot.
Water transport across plant tissue
267
However, under conditions of water shortage and
low rates of transpiration, the apoplastic by-pass in
the root would not be effective and the cell-to-cell
component would dominate. Under these condi-
tions, water channels may provide a ‘fine
regulation’ of water flow which is under metabolic
control. In mature roots, the fine regulation may be
performed by passage cells in the endo- and exo-
dermis.
THE FUNCTIONING
OF WATER CHANNELS
In both animal and plant physiology, the idea that
water transport across the plasma membrane is
mediated largely by water-filled pores or channels
has a long history (Paganelli and Solomon, 1957;
Ray, 1960; Dainty, 1963; House, 1974; Levitt, 1974;
Stein, 1986; Finkelstein, 1987). In the literature, the
term ‘water channel’ is used for narrow pores
which selectively allow for the passage of water,
regardless of their chemical nature. Traditional
models of water channels have been based on the
fact that water and certain test solutes use different
pathways (as indicated from inhibition experi-
ments) and from experiments in which interactions
between water and solute flows have been meas-
ured. In the latter experiments, the reflection coeffi-
cient was used as a quantitative measure of selec-
tivity or of interactions between water and solutes.
Interactions only occur if water and solutes use a
common path, ie a pore (Dainty and Ginzburg,
1964a, b; Steudle and Tyerman, 1983). There are, in
fact, three basic mechanisms or models for the
movement of water across membranes (fig 3). In
the first model, the membrane has no pores at all to
facilitate water transport (fig 3A). In this case, water
would have to dissolve at the surface of the bilayer
and would then move across purely by some type
of diffusion (solubility-diffusion mechanism).
Water and solutes crossing the membrane would
not ‘see’ each other during their passage. Hence,
they would not interact. Of course, there would
also be no interaction if water and solutes move
separately across different selective pores or other
porters (fig 3B), and this latter mechanism may not
be easy to distinguish from the former. In these
cases, solute flow would only affect the passage of
water by changing the osmotic gradient across the
membrane, ie by changing the force driving the
water. In the absence of a common path for water
and solutes (fig 3A, B), irreversible thermodynamics
predicts a reflection coefficient which is given by:
o-=1-
b
psvs.
-.
Lp RT (3)
Steudle
268 Biology of the Cell (1997) 89, 259-273

Fig 3. Interactions between water and solutes during their passage across membranes. A, 6. Water and solutes move
independently of each other by diffusion either across the lipid bilayer (solubilitydiffusion mechanism) or across different
selective pores (eqn (3)). C. A wide pore is sketched which permits water and solutes to pass each other in the pore. This
results in some frictional interaction between flows which can be expressed in terms of the reflection coefficient (solvent
drag; eqn (4)). D. Single-file pores are indicated which allow the passage of water and solutes, but no passing of molecules
within the pore. This results in a tight stochiometric coupling between water and solutes (eqn (5)).

V, is the molar volume of the solute. The measured
value of oS for a given solute may be compared
with that calculated from the measured permeabil-
ity coefficient (I’,) and the water permeability
(hydraulic conductivity, Lp). When equation (3) is
satisfied, this proves that there is no interaction
between water and solute flow. In an alternative
model (fig 3C), there are relatively wide pores in
the membrane which allow the simultaneous pas-
sage of both water and solutes. Pore diameters are

Water transport across plant tissue Steudle

Biology of the Cell (1997189, 259-273
large enough so that water and solutes may pass
each other within the pore. When this is possible,
water and solutes could exert some friction on each
other, ie the water flow will drag solutes on its way
across (‘solvent drag’) or vice versa. In an osmotic
cell, solute and water flows will be opposite and,
therefore, the frictional drag will result in a reduc-
tion of reflection coefficients. In the presence of a
solvent drag. the reflection coefficient (a,) can be
expressed by (eg Katchalsky and Curran, 1965):
q=l-.-.-K v, -- %v?d
Lp RT RTfiw (4)
Here, ‘d’ is the membrane thickness. The term
f,, represents the frictional coefficient between
solute and water in the membrane pore. High fric-
tional interaction is expressed by a high value of
fw % is the water content of the membrane. It is
verified from equation (4) that for an ideally
semipermeable membrane, we have a, = 1. Under
these conditions, the solute permeability (I’,) is
zero and there is also no interaction between
solutes and water in the membrane (the frictional
coefficient, f,, = 0). On the other hand, when Lp,
I’,, and os are measured and it holds that a, < 1
-P,V,/LpRT, this indicates a coupling or a fric-
tional interaction between water and solutes and,
hence, pores which are used in common by water
and solutes (despite some problems with unstirred
layer effects which may cause an underestimation
of os of rapidly permeating solutes; Dainty, 1963;
Steudle and Tyerman, 1983; Henzler and Steudle,
1995; Hertel and Steudle, 1997). Also, in the pres-
ence of pores, there should be large differences
between the diffusional (measured using isotopic
water) and bulk flow (occurring as a result of
osmotic and hydrostatic gradients). With increas-
ing pore diameter, differences between the diffu-
sional (I’,) and osmotic (I’,) water permeability
should increase (eg House, 1974; Finkelstein, 1987;
Steudle and Henzler, 1995).
As pores become smaller and only allow the pas-
sage of individual water and solute molecules one
by one across the pore, the picture changes some-
what. In this case, we have a single-file transport of
water and solutes, and there will be a stochiometric
coupling between water and solutes (fig 3D). Each
solute which moves across will drag along all the
water molecules aligned in the pore. Under these
conditions we get (Steudle and Henzler, 1995; Her-
tel and Steudle, 1997):
a,=l-(Nw~w+vs)~s
Lp RT (5)
Water transport across plant tissue
269
where N, is the number of water molecules in the
pore. Again, the reflection coefficient will be
smaller than expected from equation (3).
When pores only allow the passage of individual
water molecules and completely exclude solutes,
the picture changes again. In this case, where there
is a single-file or no-pass transport of water, reflec-
tion coefficients of the pores should become unity.
In the past few years, methods have been worked
out to determine the reflection coefficient of water
channels (Henzler and Steudle, 1995; Steudle and
Henzler, 1995). The results indicate that reflection
coefficients are substantially smaller than unity.
Theory shows that, in the presence of channels
through which water moves in a single file, the
ratio between the osmotic water permeability (PJ
derived from the hydraulic conductivity (Lp) and
the diffusional water permeability (I’& measured in
an experiment with isotopic water, will directly
yield the number of water molecules within a pore
(Levitt, 1974).
For the Chara internode it has been shown that
when water channels were titrated with the channel
blocker HgCl,, water channel reflection coefficients
were not unity for small organic solutes (alcohols,
ketones, amides, etc), although most of the solutes
were not moving across the channels (Henzler and
Steudle, 1995). In the experiments, complete sets of
Lp, I’, and a, were measured showing that upon
channel closure, Lp was reduced by 75% at con-
stant P,. Reflection coefficients were strongly
reduced. This indicated a composite transport of
water and solutes across the membrane whereby
water channel and bilayer arrays contributed differ-
ently to the overall transport coefficients. Since the
reflection coefficients of water channels were sub-
stantially smaller than unity, the results indicated a
slippage of solutes across the water channels which
dragged along substantial amounts of water result-
ing in a low overall reflection coefficient. Thus, at
least for Chara, the results show that water channels
are not selective. For the rather lipophilic and elon-
gate solute ethanol and the rather polar and globu-
lar (bulky) solute dimethylformamide, it has been
estimated that water channels were only less
permeable than water by a factor of 40 or 80,
respectively. The fact that heavy water (HDO)
showed an increased reflection coefficient and a
decreased permeability in the presence of the inhib-
itor provided further evidence for the validity of
the model. So, pores were not ideally selective for
water and allowed substantial slippage of solutes.
Even the rather bulky dimethylformamide moved
across to some extent.
For Chru, external concentration affected trans-
port (Lp, P, os) in the same way as did the inhibi-
tion ,with the channel blocker HgCl,. This is consis-
Steudle
270
tent with the old observation that with these cells,
membrane dehydration causes a reduction of Lp
and os at constant P, (Dainty and Ginzburg, 1964a,
b; Kiyosawa and Tazawa, 1977; Steudle and Tyer-
man, 1983). It has been concluded that both mem-
brane dehydration and mercury treatment may
cause a similar and reversible collapse of water
channel proteins.
Further evidence for composite membrane trans-
port and for the idea of a slippage of solutes across
water channels in Chara came from measurements
of the temperature dependence of complete sets of
Lp, P, and a, which have been recently obtained for
the first time (Hertel and Steudle, 1997). The data
confirmed the low Qio values and activation ener-
gies for water transport (Lp) found by other
authors (Dainty and Ginzburg, 1964a,b; Wayne and
Tazawa, 1990) which are in line with the idea that
water moving across the plasma membrane faces
an environment similar to that in bulk water. So, at
least for Chara, the water within the pores is not
highly ordered (such as in ice), which would tend
to increase the temperature dependence. However,
higher Qlo values were found for the cell mem-
branes of higher plants (Tomos et al, 1981). For
Charu, Qlo values increased when water channels
were blocked by the treatment with mercurials, ie
when water was forced to move across the bilayer
(Wayne and Tazawa, 1990). The comparison of the
temperature dependence of Lp with that of a, and
P, showed that there was a considerable slippage of
the test solutes used (low molecular mass alcohols).
Again, the changes in the absolute values of reflec-
tion coefficients were most interesting. It was con-
cluded that the low cell as was caused by consider-
able amounts of water being dragged along with
the solutes in the pores. Most interestingly the tem-
perature dependence of the reflection coefficient of
heavy water was opposite to that found for the
other solutes. This indicated that within the pores,
the mechanisms of hydraulic and diffusional water
movement were different (Hertel and Steudle,
1997).
From the work with the small uncharged test
solutes done with Chara internodes, we have to
conclude that water channels are by no means as
selective as it was thought (Chrispeels and Maurel,
1994; Maurel, 1997; Schaffner, 1997). It appears that
the effective diameter is considerably larger than
that of a water molecule. These findings do not nec-
essarily disagree with those of Maurel et al (1993)
who used ions and glycerol to test for the selectiv-
ity of aquaporins which were expressed in Xenoptis
oocytes. Ions should behave quite differently from
uncharged solutes. The permeability of glycerol of
the plasma membrane of Chara is also low (see
below).
Water transport across plant tissue
Biology of the Cell (1997) 89, 259-273
To some extent, the results obtained for the Chara
internode are at variance with older results from
red blood cells (for a discussion and references, see
Stein, 1986). These suggested that the frictional
component was zero and that water and solutes
such as urea moved independently across the mem-
brane. However, there were considerable technical
difficulties in these experiments, namely, to work
out the correct values of reflection coefficients
(Levitt and Mlekoday, 1983). These difficulties do not
occur with Churu, and, therefore, the data obtained
with this alga are reliable. So, we are left with the
finding that the values of reflection coefficients are
too low be explained in terrns of a membrane con-
sisting of a bilayer with a certain permeability for
water and solutes and of different channels or port-
ers which exclusively transport either water or
solutes. Hence, we have to conclude that the water
channels also allow for a certain passage of solute
which drags along a considerable amount of water.
At least for Chara, water channels can not be per-
fectly selective. It should be noted that, in the Chara
internode ‘small solutes’ such as urea or glycerol do
not really pass the membrane. They have a rather
low permeability coefficient and a reflection coeffi-
cient which is close to unity. The problem of the
discrepancy between measured and calculated
reflection coefficients occurs for solutes such as low
molecular mass monohydric alcohols, formamide,
dimethylformamide, or the like, which, in part,
should also pass across the bilayer. So, simple
models have to be extended. Perhaps, the reason
for discrepancy is that the molecules which show
the discrepancy fit into the mouth of water chan-
nels and are, therefore, permeating (Hertel and
Steudle, 1997). If true, the examination of transport
coefficients in dependence on the molecular struc-
ture of test solutes could be a tool, to get more
information about the molecular structure of water
channels.
The results from the work with the intact cells of
Chara are consistent with those obtained from Xeno-
pus oocytes (Maurel et al, 1993) in that the effect of
mercurials was selective to water and did not affect
solute transport. However, simultaneous measure-
ments of reflection coefficients and water flows
(Lp) were not possible with the oocytes. This would
have been necessary to get a deeper insight into the
selectivity of water channels and into interactions
between water and solutes as they pass across the
pores. Using solutes of different molecular size,
polarity, etc, should allow characterization of the
path for water and solutes across the channels. For
example, it would be interesting to see whether or
not branched molecules such as iso-propanol or
tert-butanol have a significantly higher 6, value
compared with elongated molecules (n-propanol,
Steudle
Biology of the Cell (1997) 89, 259273
n-butanol), although their solubilities in the bilayer
should be similar. This was found for Chara. It sug-
gested that branched molecules cause a stronger
drag on the water in the channels although their
passage across the pores should be sterically hin-
dered (Hertel and Steudle, 1997).
WORK WITH ROOT CELLS
Preliminary results with root cortex cells showed
that mercurials act similarly on their transport
properties as they do with Chum. Cell Lp and us
values of cortical cells were reduced at constant P,
(as for Chara). However, there were difficulties in
interpreting the results because of unstirred layer
effects, especially when measuring cells sitting
deep in the tissue (Henzler and Steudle, unpub-
lished results). Overall changes in root Lp, and root
osr were also similar to those found with the alga.
In some cases, negative root a,, values have been
measured for corn roots in the presence of the
blocker HgCl, (as for Chara). So, in principle, the
results obtained for corn roots suggest that there is
a similar trend as for Charu, both at the cell and tis-
sue level, but more data are necessary to evaluate
the selectivity of water channels of corn root mem-
branes. Measurements have to be made along the
developing root as well as in cells of different
depths. It is possible that the expression of water
channels varies during development (ie along
roots), and this may be affected by the growth con-
ditions as well. Also, the development of the exo-
and endodermis (Casparian bands, suberin lamel-
lae) may be paralleled by the expression of water
channels. All these open questions are presently
investigated using cell and root pressure probes.
The results should answer the question of how
changes at the membrane level result in changes at
the overall tissue or organ level under different
conditions. Transgenic plants in which the density
of water channels in the plasma membrane
changed are included in these studies.
CONCLUSIONS
The quantitative assessment of water transport
across plant tissue shows how the different path-
ways existing in tissues contribute to the overall
flow. Depending on the conditions, contributions
can be quite variable which results in a variability
of tissue hydraulic conductivity. The phenomenon
has been known for a long time, but has not yet
been explained satisfactorily. The composite trans-
port model explains the findings. Water channel
activity contributes to the overall water flow, and
the regulation of water channel activity may be
used by plants to adjust water flow. This should be
Water transport across plant tissue
271
most obvious in roots where the cell-to-cell compo-
nent dominates, In roots, an additional variability is
brought about by the existence of apoplastic bar-
riers in the endo- and exodermis (Casparian bands,
suberin lamellae). The composite anatomical struc-
ture of the root results in a composite transport of
water, which is useful for the plant. Any analysis of
tissue water and of the regulation of water flow has
to separate its components, ie the apoplastic from
the cell-to-cell component. Firm conclusions about
the role of water channels in plant tissues can be
only drawn when the components have been separ-
ated. At the membrane level, there is also a com-
posite transport of water (bilayer, water channels,
etc). Models show how the selectivity of water
channels affects the overall transport properties of
membranes, namely, the reflection coefficient. At
least for the Chru internode, it has been shown that
water channels are by no means ideally selective
and that rather big uncharged organic solute mole-
cules may pass the pores. If there are aquaporins in
the membranes of these cells, they should allow
some kind of a single-file transport of water and
solutes. At least to some extent, this would explain
low reflection coefficients. If the slippage of solutes
is a general phenomenon in cell membranes, this
will have consequences for the ongoing discussion
about the function of water channels in plants.
ACKNOWLEDGMENTS
I thank Dr Carol A Peterson, Department of Biology, Uni-
versity of Waterloo, Ontario, Canada, for reading the
manuscript. This work was supported from the Deutsche
Forschungsgemeinschaft, Schwerpunktprogramm 717:
‘Apoplast’.
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Received 11 July 1997; accepted 18 September 1997
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