American Journal of Botany 85(7): 897909. 1998.

INVITED SPECIAL PAPER

APPLICATIONS

OF THE COMPENSATING PRESSURE

THEORY OF WATER TRANSPORT1

MARTIN J. CANNY
Biology Department, Carleton University, 1125 Colonel By Drive, Ottawa, Canada K1S 5B6
Some predictions of the recently proposed theory of long-distance water transport in plants (the Compensating Pressure
Theory) have been verified experimentally in sunflower leaves. The xylem sap cavitates early in the day under quite small
water stress, and the compensating pressure P (applied as the tissue pressure of turgid cells) pushes water into embolized
vessels, refilling them during active transpiration. The water potential, as measured by the pressure chamber or psychrometer,
is not a measure of the pressure in the xylem, but (as predicted by the theory) a measure of the compensating pressure P.
As transpiration increases, P is increased to provide more rapid embolism repair. In many leaf petioles this increase in P is
achieved by the hydrolysis of starch in the starch sheath to soluble sugars. At night P falls as starch is reformed. A hypothesis
is proposed to explain these observations by pressure-driven reverse osmosis of water from the ground parenchyma of the
petiole. Similar processes occur in roots and are manifested as root pressure. The theory requires a pump to transfer water
from the soil into the root xylem. A mechanism is proposed by which this pump may function, in which the endodermis
acts as a one-way valve and a pressure-confining barrier. Rays and xylem parenchyma of wood act like the xylem parenchyma
of petioles and roots to repair embolisms in trees. The postulated root pump permits a re-appraisal of the work done by
evaporation during transpiration, leading to the proposal that in tall trees there is no hydrostatic gradient to be overcome in
lifting water. Some published observations are re-interpreted in terms of the theory: doubt is cast on the validity of measurements of hydraulic conductance of wood; vulnerability curves are found not to measure the cavitation threshold of water
in the xylem, but the osmotic pressure of the xylem parenchyma; if measures of xylem pressure and of hydraulic conductance
are both suspect, the accepted view of the hydraulic architecture of trees needs drastic revision; observations that xylem
feeding insects feed faster as the water potential becomes more negative are in accord with the theory; tyloses, which have
been shown to form in vessels especially vulnerable to cavitation, are seen as necessary for the maintenance of P, and to
conserve the supplementary refilling water. Far from being a metastable system on the edge of disaster, the water transport
system of the xylem is ultrastable: robust and self-sustaining in response to many kinds of stress.
Key words: embolism refilling; hydraulic architecture; hydrostatic gradient; pressure chamber; reverse osmosis; root
pressure; starch sheath; tissue pressure; transpiration; tyloses; ultrastability; water pump; xylem-feeding insects.

This is an invitation to an adventure of exploration, an

offer of a new way to look at plants, a new way to interpret old data, a new way to plan investigations. It is
my purpose to persuade you, not that the way is wholly
right, but that it connects previously unrelated facts and
quickly leads to unexplored territory. The argument is
interrupted at several points to suggest exploratory experiments to test some of the proposed ideas.
I must assume that you have read the original statement of the theory (Canny, 1995) where full details are
given of the reasons for presenting a new theory, and of
its scope and requirements as understood at that time. I
begin with a brief statement of its main points.

water it generates a pressure inside the box because the

cells are pressing against each other. The maximum available pressure is P, the osmotic pressure of the cell sap.
Some part of P is balanced by wall stretching, but some
also by mutual pressure of the cells (tissue pressure). For
each cell, wall and tissue pressure together make up the
turgor pressure. Through the organ, within this pressurized box, runs the xylem pipeline carrying water, and its
pressure is coupled to the tissue pressure surrounding it.
A first effect of pulling water through the xylem pipe is
to reduce some of the tissue pressure in the box. Call this
reduction the compensating pressure (P). The harder the
water is pulled, the more the tissue pressure is reduced
(i.e., P increases). Up to the limit of available P (,P )
the pressure in the pipeline is kept near 0 to 1 bar (100
kPa) absolute. The absolute pressure scale, on which atmospheric pressure is 11 bar (1100 kPa), will be used,
except in some published data. If the stretched water in
the pipeline breaks (to form an embolism), P provides
the force to push water out of static reservoirs and to
refill the embolized space. A major source of this tissue
pressure is the solute-rich phloem. A plant organ is able
to alter P both up and down as needed by osmoregulation
of P in the sap of some of the cells. An easy way to do
this is by interconversion of starch and sugar.

STATEMENT
A plant organ is like a mass of osmometers (cells)
confined in a box (epidermis, bark). When supplied with
1 Manuscript received 17 September 1997; revision accepted 5 March
1998.
Symbol convention: Italic symbols are used for primary measured
quantities, plain text symbols for derived quantities.
The author thanks Margaret McCully and Steve Vogel for helpful
discussions and criticism of the manuscript, Adam Baker for making
the plate, and the Natural Sciences and Engineering Research Council
of Canada for an operating grant.

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Figs. 14. Figs. 12. Preparations of a strand of xylem in the petiole of a sunflower leaf, frozen intact during active transpiration, and viewed
(still frozen) in the cryo-scanning electron microscope. 1. Living cells are grey, containing white lines of solute crystals in a matrix of black ice.
Some of the vessels contain black ice and were filled with sap when frozen, others contain gas and were embolized when frozen. Bar 5 100 mm.
2. View inside an embolized vessel in a preparation like that in Fig. 1. The vessel was refilling with drops of water entering through pits from
adjacent parenchyma cells. Bar 5 10 mm. Figs. 34. Starch sheaths in the petiole of a hollyhock leaf. Transverse sections of petioles of adjacent
leaves harvested on a day of bright sunshine. Iodine stain. 3. At 0645. 4. At 1930. Bars 5 100 mm.

DIRECT OBSERVATIONS OF EMBOLISMS

DeductionConsideration of the phenomena and experimental techniques of plant water relations from the
viewpoint of the theory led me to propose that what is
referred to as the water potential (C) of the organ was in
fact a measure (as far as the limit near P) of the compensating pressure P, and that this was the quantity measured by the customary techniques (the pressure chamber
and the psychrometer). Beyond the limit P 5 P, C is
manifested as tension in the xylem water, as in the cohesion theory. In Fig. 12 of Canny (1995) this argument
is traced in detail following the changes in water content
and pressure in various parts of a transpiring leaf when
it is cut off, and after its equilibration with gas pressure
in a Scholander chamber. Because no one had ever followed the changes in water content of xylem conduits
following excision of an organ, and because I had at hand

the means to do this, an experimental investigation was

carried out to test the predictions of Fig. 12 of Canny
(1995).
Experiment 1. Changes on leaf excisionThe instantaneous content of the xylem conduits in a plant organ
can be ascertained by snap freezing the organ, planing it
flat in the desired section with a cryo-microtome, and
studying the planed face, still frozen, in the cryo-scanning electron microscope (CSEM) (Fig. 1). The tracheary
elements are easily distinguished from surrounding parenchyma by their solute-poor sap (appearing black) and
their thickened walls. Any tracheary element that is embolized shows empty space (also black, but often filled
with debris formed during the planing).
The percentages of embolized vessels were determined
by this technique in petioles and midribs of sunflower

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OF A THEORY OF WATER TRANSPORT

leaves, frozen intact on the plant, and at intervals after

cutting leaves off the plant (Canny, 1997a). The answer
to the original question, that there was no significant
movement of water into or out of the vessels on cutting
except for a limited, slow efflux during an hour or so in
the middle of the day, was overshadowed by the unexpected observations on the intact plants. As anticipated,
the percentage of embolized vessels rose from a low value in the morning to a maximum of 40% around noon.
But then the percentage declined again throughout the
time of peak transpiration in the early afternoon, and
reached near zero by 1600. Refilling of embolized vessels
has been recognized as a fact, but believed to occur only
at night or in rainy weather when transpiration has ceased
and tension in the xylem has become a positive pressure.
Its occurrence during active transpiration, implying a
pressure in the xylem at that time above 0.02 bar (20
kPa) absolute (the vapor pressure of water), is so directly
opposed to the operation of the cohesion theory that it
was necessary to design a second experiment to verify or
disprove it.
Experiment 2. Vessel contents during transpiration
Note that this measure of percentage embolized vessels
is a direct measure of both water stress and tension in
the vessels. When you pull on something and it breaks,
the extent of breaking is a measure of the pull. Here it
measures both the evaporative stress and the transmission
of this stress through tension in the water in the vessels,
the greater the tension, the more the breaks. Moreover
the measure is an integrated one for the whole organ
because it is based on the state (water content or gas) of
all the individual vessels in the petiole.
The percentages of embolized vessels were measured
as before in petioles of sunflower leaves (Canny, 1997b),
but this time all leaves were frozen while still attached
to the plant, and concurrent measurements were made of
irradiance, leaf temperature, transpiration rate, and leaf
water potential (using a pressure chamber). The plants
were large, the days were longer, and additional water
stress was imposed by withholding water from the pots
during the day. Embolisms occurred earlier in the day
(by 0900), but again were reduced during the day, and
reached a minimum (4%) at 1500, which was the time
of peak transpiration and most negative water potential
(highest balance pressure). Again embolized vessels were
being refilled with water during vigorous transpiration.
The images of the vessels revealed this refilling process
at work: water being extruded through pits into empty
vessels from the neighboring cells, and vessels at all
stages of partial filling (Fig. 2). X-ray microanalysis of
the entering liquid showed that it contained no significant
concentrations of solutes, eliminating the osmotic pressure of the xylem sap as a possible filling force. The vigor
of the refilling process increased as transpiration increased, keeping ahead of the increasing evaporative demand. Comparison of the time courses of percentage embolized vessels with those of balance pressure in the pressure chamber showed that the balance pressure was not
a measure of water stress, and was certainly not a measure of tension in the vessels. Just the opposite. When
the balance pressure was low, the tension was greatest,
as shown by high or rising percentage embolisms. When

899

the balance pressure was at its maximum, the tension was

lowest because the embolisms fell to a minimum. What
the balance pressure was strongly correlated with was
what I have called the vigor of the refilling process, the
rate of reduction of embolisms. As explained above, the
force driving the refilling process is part of the tissue
pressure of the cells surrounding the xylem, in fact the
compensating pressure P. Thus the second experiment
demonstrated practically the theoretical prediction in
Canny (1995) that the chamber balance pressure is a measure of the compensating pressure.
Hypothesis of vessel refillingGiven these new facts
it is easy to construct a hypothesis to explain refilling.
Just as a small overpressure in the pressure chamber forces water by reverse osmosis out of parenchyma cells and
into the vessels, so in the intact leaf the tissue pressure
in the petiole pushes a small constant influx of water into
all the vessels. This influx is an insignificant part of the
main transpiration flux through the vessels and depends
upon the magnitude of P and the hydraulic conductivity
of the cell membranes (Lp). When the water cavitates in
a vessel, it is replaced by gas, and the forward flow stops.
The influx continues, the vessel refills over a short period
(minutes), and forward flow through it resumes. The time
to refill is proportional to the vessel radius, and small
vessels both fill and empty faster than large ones. Herein
lies a major value of a population of small vessels in a
block of xylem. They spend little time out of action and
provide continuity of transpiration until the liquid contents are restored in large vessels. The source of water in
the petiole to supply the influx for the whole days transpiration is the mass of ground parenchyma cells, and the
amount of water consumed in this repair function could
be roughly estimated by the amount of petiole shrinkage
during the day. I will refer to this constant minor influx
for embolism repair as the supplementary water.
The regulation of increasing P in response to increased
transpiration could be provided by changes in the osmotic
pressure of a small population of petiole cells. The main
mass of water-supplying parenchyma needs to stay at its
customary osmotic pressure so that water is still forced
out of them. The starch sheath cells were suggested (Canny, 1997b) as the source of the necessary extra pressure.
Starch in the sheath cells would be converted into sugars
with increasing water stress. This is easily demonstrated
experimentally. On days of rapid transpiration there is
extensive disappearance of petiole starch by the afternoon
(Figs. 34). The starch polymer reforms overnight and
the pressure provided by the starch sheath drops. This is
a necessary stage of the process, because it allows the
water storages of the ground parenchyma to be recharged
by water coming from the roots during the night. Thus
the petiole acts as a water pump on a 24-h cycle, squeezing water out of parenchyma cells into the vessels during
the day at whatever rate is necessary to refill them, and
refilling the parenchyma cells at night via the vessels
from the supply below, ready for the next days repairs.
A prediction of this hypothesis is the existence of a
flow of xylem water from roots into the shoot at night
with zero transpiration. The water-deficient reservoirs
would act as sinks for water, exert a small tension on the
sap of the tracheary elements, and draw a slow flow of

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restoring water from the roots. The tension on the sap

might be sufficient to embolize tracheary elements, so
that a low percentage of embolisms would persist far into
the night.
The time scale of all these events depends critically on
the value of Lp for the petiole parenchyma cells, and this
has not yet been measured. The maximum rate of vessel
emptying at greatest water stress in Experiment 1 was ;4
min. Some sample calculations are done in Appendix 1
using likely values for Lp and P, which show that a 5%
shrinkage in diameter of the petiole would provide a
days supply of supplementary water. The necessary supplementary water is ;1% of the transpiration water. This
does not seem unreasonable, and could easily be tested.
Experiments: Investigate changes in xylem content after excision
in other plants and organs. Repeat the measurements of percentage
embolized vessels during transpiration with as many other plants
as possible. Measure Lp of parenchyma cells adjacent to vessels.
Look for the distribution of water channels in xylem parenchyma
cells. Measure organ shrinkage and compare with the required volume of supplementary water. Look for changes in starch morning
and evening in relation to transpiration rate (store tissues in 50%
ethanol, cut hand sections, stain with I2/KI). Look for the signals
that pass between the starch/sugar equilibrium and the rate of transpiration. Leave a xylem pressure probe inside a vessel after observing a cavitation, and time the refilling process. Look for the
restoring current of water at night with zero transpiration, and for
the slow disappearance of embolisms during the night.

Shift of emphasisThese observations and the induced hypothesis of refilling vessels change somewhat
my view of how the compensating pressure theory works.
In the original formulation (Canny, 1995) the main focus
was on raising the pressure in the vessels to stop the
water threads breaking. Now a major effect of the compensating pressure appears also to be the provision of the
steady influx of supplementary water to the vessels from
a water reservoir, refilling embolized vessels fairly quickly when the threads do break. This view of the xylem
parenchyma, as providing a constant low-level supplement to the transpiration stream, stimulates useful insights into the operation of a number of other regions of
the plant, some of which will be briefly discusssed.
ROOTS, ROOT EXUDATIONS, AND
ROOT PRESSURE
There is good evidence that a process similar to that
found in the leaves is operating also in roots. McCully,
Huang, and Ling (1998) followed changes of embolisms
in the vessels of transpiring corn roots, frozen intact in
the field. The technique used was the same cryo-scanning
microscopy of the fully hydrated tissues and assessment
of the contents of the individual vessels. Early in the day
no root vessels were embolized. Embolisms appeared at
sunrise, increased to a plateau (;75%) during the middle
of the day, and fell during the afternoon or evening during active transpiration, to reach zero again by dusk. In
embolized vessels at all times water could be seen entering through the pits in the vessel walls from the adjacent
parenchyma and from branch roots (Fig. 2). Again, a reverse osmosis of water squeezed from the xylem parenchyma by the tissue pressure confined within the mechanical barrier of the endodermis seems a likely expla-

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nation. This is a manifestation of the well-known but inadequately explained phenomenon of root pressure. A
possible source of the pressure, though not an explanation
of the pressure-driven xylem flux of water, was identified
in Canny (1995) as the tissue pressure generated by phloem and parenchyma cells confined within the stele. The
additional hypothesis of the reverse osmosis of cellular
water into the vessels, which refills embolisms, is a step
towards explaining the water flux observed in excised
roots. We shall return to this question presently.
Recent work has shown that there are at least two other
exudations produced by roots, which may be generated
by tissue-pressure-driven reverse osmosis, but operating
in the cortex, not the stele. The first of these to be published was the finding of liquid water (with varying concentrations of solutes) in some of the intercellular spaces
of the root cortex (Canny and Huang, 1993). The intercellular solutions were found at all times of the day, and
in all ages of root, and were present even at times of
considerable water stress. Such accumulations of solution
outside cells have been observed by us constantly since,
in many hundreds of root samples examined with the
CSEM (e.g., McCully, 1994) and come to be regarded as
a normal component of root tissues. More recently, much
larger accumulations of liquid water were recorded, filling some of the large aerenchyma spaces in corn roots
(Van der Weele, Canny, and McCully, 1996; Watt et al.,
1996).
The second kind of expressed water is that found exuding from field-grown corn roots at night (McCully,
1995). Convex drops of water were seen (again frozen
preparations in the CSEM) on the epidermis and root
hairs and filling much of the space between soil particles
in the early morning. By midday the liquid had gone, and
the rootsoil interface contained only air among the plant
tissues and the soil particles. Without attempting to formulate detailed mechanisms for these two kinds of exudation, it is tempting to couple them with the supplementary water as examples of pressure-driven reverse osmosis from root cells. But if cortical cells may be considered as confined and under pressure, the epidermal
cells are certainly not so, and the source of pressure for
them is less clear (but see below).
Hypothesis of the root water pumpThe logic deriving from the compensating pressure theory demands that
there must be a water pump in roots. The reasons for this
are several. First, with the pressure in the xylem conduits
not far from zero bar absolute, a pump is needed to take
water from the soil where the water potential may be
several bars negative, and transfer it to the conduits. With
the simpler cohesion theory no such pump was necessary,
and none was looked for. Pressures in the xylem were
believed to be far enough negative to extract water from
even quite dry soils. Without this comfortable simplicity,
some role for the living cells of the root in extracting
water from the soil is required.
Second, the compensating pressure theory requires a
supply of supplementary water to refill embolisms in the
roots. In the stem and leaves this is stored locally, used
during transpiration, and recharged at night from below.
But in roots, though the cortex may act as a temporary
store, the ultimate source of the supplementary water for

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the whole plant is outside in the soil, and a pump is

needed to transfer the water to the empty vessels.
Third, though the compensating pressure theory explains the origin of the pressure in root pressure, in order
to provide also the flow of xylem sap up through an excised root, which constitutes the root-pressure-driven exudation from the cut stump, there must be a one-way flux
of water from outside the root to the xylem conduits, i.e.,
a pump.
Fourth, the maintenance of the not-far-negative pressure in the xylem by the compensating pressure requires
valves at the top and bottom of the conduits, so that the
compensating pressure is not dissipated while water flows
through them (Canny, 1995). As explained in that paper,
the flows through the two valves must be independent of
pressure in the conduits. Taken with the first three points,
this implies that the bottom gateway must be more than
a valveit must be a pump.
None of these root processes can be separate from the
main activity of roots, the provision of the major flux of
transpiration water to supply evaporation from the leaves.
The pump required in the four above points must have
all the properties consistent with the known attributes of
the transpiration stream in roots. It must have the capacity
to deliver water at the measured rates. It may respond to
increased demand by increasing throughput (Passioura,
1988), but at the same time (point 4) it must be independent of pressure in the conduits. It would be an added
bonus if it were slowed down by low temperatures (since
many plants wilt when their root systems are cooled), or
if it could explain Rygol et al.s (1993) observation of
increased solute concentrations in the inner cortical cells
of transpiring roots, which dispersed in 20 min after transpiration stopped, or the finding of Schneider, Zhu, and
Zimmermann (1997) that transpiration induces a change
in root radial reflection coefficients. How is it possible to
construct a pump with all these properties from the
known hardware of cell membranes, osmotic vacuoles,
cell walls, and plasmodesmata?
I propose the broad outlines of a hypothetical water
pump that satisfies these criteria. The pump is constructed
from the whole mass of the endodermis and the tissues
it contains. One function of the endodermis is to act as
the mechanical barrier that confines pressure within it.
The output of the pump is the reverse-osmotic flux from
stele parenchyma to the xylem conduits driven by the
tissue pressure in the stele (Canny, 1995). The energy
driving the pump is the difference in osmotic energy of
the cells inside the stele relative to that in the cells of the
cortex (see quantities and gradients measured by McCully, 1994). This energy is converted into a pressure to
drive the reverse osmosis by the turgor pressure of the
phloem and parenchyma cells of the stele (Canny, 1995).
It is likely that the osmotic energy in roots is based, not
on carbon compounds as in the stem and leaves, but on
mineral ions, which are available close by in the soil.
The input of the pump is a flux of water through the
endodermis from the cortical cells, and via them from the
soil. The endodermis acts also as a one-way valve that
allows the influx of water to the stele and prevents the
efflux of water from the stele. This valve is the essential
and novel element of the pump and deserves more detailed attention.

901

The operation of the valve depends on the distinction

between pressure flow and diffusion. Flow is driven by
differences in pressure; diffusion is driven by differences
in concentration (activity). The valve takes advantage of
the fact that at a septum with holes in it the two processes
respond differently to changes in the size of the holes. In
qualitative terms: smaller holes restrict pressure flow
much more strongly than they restrict diffusion. By making the holes small enough it is possible to change the
septum into a valve that permits diffusion while preventing pressure flow. With high concentration on the
outside of the septum, diffusive influx can build up a
positive pressure in the space inside the septum, and yet
this pressure cannot drive significant flow back through
the holes. For a quantitative statement see Appendix 2.
The principle has been shown to operate in the gaseous
phase in leaves of water lilies by Dacey (1981). There
the septum pores are ;1-mm-wide spaces between the
mesophyll cells of young, developing, floating leaves,
which are small enough to generate gas pressures inside
the leaves when there are differences in gaseous composition or temperature between inside and out. This
pressure drives a flow of gas down through the petioles
of the young leaves, along the rhizomes and back out
through the stomata of older leaves. In the endodermis
the pump would operate in the liquid phase (water), and
the critical pores are the plasmodesmata through the inner
tangential wall between endodermis and pericycle. In order to confine the diffusion to these critical pores, alternative apoplastic paths for flow or diffusion through the
cell walls are blocked by thickenings, suberized lamellae
and the Casparian strip. In short, the endodermis, with its
known structures, acts as a valve to allow diffusive water
influx to the stele and to prevent pressure-driven efflux
from the stele.
The driving force of the pump, the difference in water
concentration between the cells of the cortex and those
of the stele, is maintained in two ways. First, the solutes
of the cortical and stelar cells are confined within vacuoles and cannot easily diffuse through the plasmodesmata
to equalize their concentrations (and hence the concentration of water). The water flux is from cell to cell, from
vacuole to vacuole in the cortex and stele, but, at the
endodermal septum where the one-way valve operates,
through the symplast only (Fig. 5). Second, as water is
withdrawn from the roots through the xylem by transpiration, the water concentration within the stelar vacuoles
falls. The gradient of water concentration from cortex to
stele becomes steeper, and the diffusive flux increases.
The pressure within the stele is higher than the pressure
in the cortex, but never high enough to prevent the inward diffusion of water because it is relieved by the flux
of transpiration and supplementary water to the xylem
outlet, which the pressure drives. As we know from the
behavior of leaves in the pressure chamber, quite small
overpressures are sufficient to express water from cells.
An assessment of some of the quantitative requirements
of the valve is attempted in Appendix 2. The reader must
judge whether they accord with acceptable limits. The
operation of the valve depends on the balance between
pore size and viscosity. For water the pore size is impossibly small. But if the viscosity of the watery protoplasm in the pores is as high as 20 Pas, the pore size is

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Fig. 5. Diagram of the features of a root required for the operation of the water pump. The thickened cell walls of the endodermis and the
central xylem vessel are shown black; cytoplasm, pink; vacuoles and the sap of the central xylem vessel, blue. The solute concentration in the
vacuoles increases progressively from the cortex (u, v), through the endodermis (w), the pericycle (x), and the xylem parenchyma (y). In other
words, the water concentration in these vacuoles decreases along this path. The plasmodesmata between the endodermis and the pericycle constitute
the one-way valve that permits the inward diffusion of water (red arrows) down a concentration gradient of water, but restrict the outward (pressuredriven) flow of water. Pressure builds up in the stele, and drives water from the stelar cells into the vessel (black arrows). For details see Appendix
3 and text.

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in the range accepted for the gaps in the annulus around

the desmotubule (Terry and Robards, 1987).
It may seem paradoxical that a process transmitting
such large volumes of water as the transpiration stream
of a tree should depend at a critical step on diffusive
transfer. The traditional understanding of diffusion is that
it is a slow process, which indeed it is over distances
greater than a few tens of micrometres. But diffusion over
short distances is very rapid. The limiting distance in the
model is the length of the endodermal plasmodesmata. In
Appendix 3 a calculation is made from some simple assumptions, which shows that the model is not hopelessly
inadequate. It is sufficiently promising to stimulate the
collection of some real data about the two determining
variables, the radius and number of the pores in the endodermal plasmosdesmata and the gradients of water
concentration between cortex and stele.
Hypodermal pumpThe same structures that block
the apoplast and confine diffusive transfer to the symplast
are found at the outer boundary of the root cortex in the
hypodermis. That too could be the site of a valve and
pump. The hypodermal pump could be responsible for
the elevated tissue pressure in the cortex to drive the exudations into the intercellular spaces. The whole root,
cortex plus stele, would then be a two-stage pump with
the pressure rising in two steps. Note that this kind of
pump can be made to work in either direction by reversing the gradient of water concentration. The hypodermal
pump might be reversed at night by solute uptake into
the epidermis reversing the water gradient between cortex
and epidermis, and so drive the outward water flux observed into the soil.
Experiments: Work with branch roots of plants transpiring at different rates during the day, and at night guttating with positive
xylem pressures. Measure exclusion limits of endodermal/hypodermal plasmodesmata. Look for gradients of solute and water activities in vacuoles of inner cortex/stele and outer cortex/epidermis
with the CSEM. Measure the effects of low temperatures on rates
of refilling (percentage embolisms). Look at the distribution of
water channels (aquaporins) in the critical boundaries: hypodermis/
cortex; endodermis/pericycle; xylem parenchyma/vessel. Test
whether damage to the endodermis by herbivory or rot affects the
pump.

STEMS, TREES, STATIC AND MOVING WATER,

AND THE HYDROSTATIC GRADIENT
So far, the experiments on embolisms and supplementary water have been done on petioles and roots, but the
same processes are at work in stems and the trunks of
trees. In trees the source of static water is water-filled
fibers and tracheary elements of small diameter, or the
elastic tissues of the inner bark. Static water in trees is
much more voluminous and can supply transpiration as
well as the supplementary water (Waring, Whitehead, and
Jarvis, 1979). The source of pressure is the ray and paratracheal parenchyma, and again the pressure is regulated
to provide higher pressures during rapid transpiration by
the conversion of starch to sugar. Again, the pressure is
relaxed at night when starch reforms. Determinations of
the osmotic pressure of ray cells of wood are few, and I
have found none published for different times of day.

903

Kny (1909) measured osmotic pressures of ray cells of

Salix, Populus, and Aesculus, and recorded some very
high values. The contact cells of Aesculus in early spring
had osmotic pressures of 45 bar (4.5 MPa), and in late
summer, 50 bar (5.0 MPa). Ursprung and Blum (1916)
record 35 bar (3.5 MPa) for the wood rays of Fagus.
Pressures generated by such cells could drive large volumes of water from the static stores of the wood.
Experiments. Take cores from the outer xylem of trees at different
times of day, and different rates of evapotranspiration, and assess
the starch content by iodine staining; express the sap and measure
its refractive index or freezing point. Measure P for ray and paratracheal parenchyma by modern methods on a similar program.

The supplementary water is a more abundant and general manifestation of the water postulated (and rather deviously demonstrated) by Munch (1930) to arise from the
phloem. For Munch it was the superfluous water from
the translocated sugar solution, left over after the sugar
had been used in a sink. This water would be returned
to the plant body and the source by transfer to the xylem.
Milburn (1996) has revived the idea and proposed that
this released water helps to repair embolisms.
The phloem was recognized as a likely source of pressure (Canny, 1995). A fairly direct measure of the tissue
pressure that exists in the phloem, and which could drive
some of the reverse osmosis, was made by Buttery and
Boatman (1966) in the bark of rubber trees. Manometers
inserted into the bark were readily sealed into the pool
of exuding latex and gave reproducible measures of the
pressure driving the latex out of the laticifers. They record pressures in the range 19 to 113 bar (10.9 to 11.3
MPa) morning and evening. The high values at dawn fell
by ;4 bar (0.4 MPa) at times of high evaporative demand. This fall is a direct measure of the compensating
pressure P.
Experiments. Revive and exploit this system to investigate the behavior of P.

The hydrostatic gradientOnce the possibility is admitted of a water pump in roots, which might deliver
water into the xylem conduits against a pressure of several bars, it becomes possible to think in a new way about
the movement of water up trees. Since the first mention
of this question it has been a commonplace that the water
must be lifted up the tree against the force of gravity, that
1 bar (0.1 MPa) of tension must be applied to lift the
water through each 10 m, or 10 bar (1 MPa) for the tallest
(100 m) trees. I find no mention of the fact that the water
is already up the tree, that the tree is in fact a standing
tank of static water surrounding a few conduits in which
water moves. The static water, contained in living cells,
fibers, intercellular spaces, and the smallest conduits,
must be a continuum, even if it contains islands of dry
material and gas. Isolated regions of static water cannot
persist. So the continuum of static water has a weight,
and the force exerted by this weight is proportional to
the height. A standing tank of water with a pipe running
up it from bottom to top has a gradient of positive pressure increasing downwards, not a tension in the pipe increasing upwards. Everywhere the pressure in the pipe
equals the pressure in the tank. To suck water from the
top of the pipe requires no more force than to suck water

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through it when it is lying horizontal. The hydrostatic

gradient is irrelevant to the flow through the pipe.
The tree differs from the tank and pipe in two respects.
(1) The bottom of the xylem pipe is not open and continuous with the static water. (2) The bottom of the tree,
both the static water and the xylem pipe, ramifies into
narrowing branches (the roots), which are buried under
another weight (the soil). Because of (1), a pump is necessary to move water from the soil into the pipe against
the positive pressure, and this is where the energy is expended to lift the water up the tree. The pump described
above, with an output pressure of 10 bar (1 MPa) (Appendix 2), would transfer water into the conduits at the
base of the tallest trees. Because of (2), the pressure in
the root conduits will be less than at the bottom of the
tank, but how much less is not easily assessed.
Experiments. It should not be difficult to distinguish a gradient of
increasing pressure from top to bottom, from a gradient of increasing tension from bottom to top. At each level the living cells must
be in balance with the prevailing pressure. Measure osmotic/turgor
pressure of xylem/phloem parenchyma at different heights. Buttery
and Boatman (1966), in the experiments already mentioned, found
a gradient in their measured tissue pressures decreasing upwards
at about the rate of the gravity gradient.

VULNERABILITY CURVES
As explained in Canny (1995) the results of almost all
experiments are interpretable equally by the cohesion theory and the compensating pressure theory. As an example
of alternative explanation I take the experiments of Pockman, Sperry, and OLeary (1995) who tried to show that
the pressure chamber did indeed measure tension in the
xylem by inducing known amounts of water stress in
branches. They compared the effects of the centrifugal
stress generated by spinning branches with two other
stress treatments, drying in air and external air pressure
applied around the branch. They measured the effects of
these stresses by estimating the hydraulic conductances
of the branches. Their argument is that the hydraulic conductance gives a measure of the cavitations produced in
the conduits by the stresses. The stresses of centrifugation
and drying act by moving or extracting water, and air
pressure acts by forcing air into the conduits through
pores in pit membranes. The results are displayed in the
form of vulnerability curves, plots of the percentage
loss of conductance against the stress (Fig. 6). The three
stresses are measured as pressures in MPa, centrifugal
stress calculated from the angular velocity, drying stress
measured by the pressure chamber on leaves taken from
the branches, and pressure stress by the air pressure applied in a jacket around the branch.
To understand the procedure it is necessary to consult
an earlier paper (Sperry and Saliendra, 1994) describing
the apparatus (Fig. 7). Air pressure was applied in a jacket around the body of the branch, while one end was
connected to a reservoir supplying solution for the conductance measurement under small pressure determined
by the elevation of the reservoir. Note the air vent, which
allowed escape of bubbles driven through the branch by
the air pressure, and the notches that admitted air to the
branch. An initial flow measurement was made with an
air pressure of 11 bar (1100 kPa) . The pressure was

Fig. 6. Figure and legend reproduced by permission of the editors

of Nature from Fig. 1 of Pockman, Speery, and OLeary (1995). Decrease in hydraulic conductivity (kh) in xylem against xylem pressure
(Cpx) generated by centrifuging (filled symbols) and air-drying (open
symbols) stems of a Populus fremontii, b, Salix gooddingii, c, Acer
negundo and d, Abies lasiocarpa. Centrifuge data only are shown for
Juniperus monosperma (d). Decrease of kh from air injection of xylem
(ac, open circles) is shown against the negative of the injection pressure for comparison.

raised to the desired level (up to 40 bar [4 MPa]), held

for 10 min, depressurized to 11 bar (1100 kPa), and the
flow measured again. This measurement was expressed
as a percentage of the initial flow. The curves of Fig. 6
were constructed from measurements at increasing values
of air pressure and the two other stresses. All three stresses induced an abrupt change in conductance from high
to low values over a narrow range of stress, and the stress
level at which this happened was characteristic of the
species. The authors argue that they have demonstrated
that the water in the conduits withstands negative pressure (generated by any of the three stresses) up to a
threshold value which varies from 215 bar (1.5 MPa) to
around 240 bar (4 MPa). This is the cohesion-theory
interpretation.
The compensating pressure theory proposes that the xaxis of Fig. 6 should be labelled, not as negative water
pressure, but as the compensating pressure applied to the
conduits to protect them from cavitation in response to
drying, and to refill them when they do cavitate. The

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OF A THEORY OF WATER TRANSPORT

905

mum pressure that can be applied to refill the conduits is

the osmotic pressure of the ray cells and xylem parenchyma, so the cavitation threshold for each species
should correspond approximately with the osmotic pressure of the ray cells. The rays of poplar, willow, and
maple with sharp thresholds should have fairly uniform
osmotic pressures, while in those of the two conifers (Fig.
6d) they would be expected to be high and variable. Second, the high conductance in the part of the curve up to
the threshold is maintained by refilling of conduits cavitated at low stress levels when water is supplied to the
dehydrated wood from the solution used to measure conductance. Third, the activity of living cells is necessary.
Experiments. Prediction 1: Check by measurements on fresh hand
sections of the wood. The high values of osmotic pressure deduced
for these ray cells accord with the determinations by Kny (1909)
and Ursprung and Blum (1916) already noted. Note also, the correspondence of the cavitation threshold with the osmotic pressure
of the living cells, in the data of Sperry and Saliendra (1994, their
Fig. 5) showing that the turgor pressure of the leaf cells of birch
falls to zero at just that value of P where the threshold change in
conductance occurs. Prediction 2: Check by varying the osmotic
pressure of the conductance-measuring solution; the higher this
osmotic pressure, the lower the expected threshold of critical stress.
Prediction 3: Check by adding a poison to the conductance solution, which should shift the cavitation threshold to its unprotected
level of around 23 bar (2300 kPa) and prevent refilling. Also,
follow the changes in percentage of embolized vessels during a
conductance measurement by direct observation in the CSEM.
Figs. 78. Figures from Sperry and Saliendra (1994) reproduced by
permission of the editors of Plant, Cell and Environment. 7. Apparatus
for measuring vulnerability curves on single hydrated stems using air
pressure. The stem (SEGMENT) was sealed in a double-ended steel
bomb with both ends protruding. From their Fig. 1. 8. The correlation
between compensating pressure (P) applied to the vessels (reducing
cavitation and refilling embolized vessels) and the mean hydraulic vessel diameter for individual root, trunk, and twig segments from a single
individual of Betula occidentalis. Redrawn, with the y-axis relabelled,
and omitting the data on hydraulic conductances, from their Fig. 4.

centrifuging is a drying stress, just like the air drying.

The pressurization technique will also dry the branch. Air
was being forced through it at up to 40 bar (4 MPa)
pressure for 10 min. The amount of drying will be roughly proportional to the applied air pressure. From what is
now known about the capacity of living cells to push
water back into empty vessels, the whole concept of a
vulnerability curve becomes suspect. The apparatus
shown in Fig. 7 pushes water through a dehydrated tissue.
While the xylem parenchyma is able to function as shown
in Fig. 2, embolized vessels will be refilled in a few minutes, and the conductance will rise during the act of measurement. What the graphs tell us is that up to a threshold
value of drying stress there is little or no effect on the
hydraulic conductance, that is, that the compensating
pressure of the living cells is able to restore the drying
damage and refill any cavitated vessels during the conductance measurement when the branch is supplied with
water. Beyond the threshold of stress the living cells have
been irreversibly damaged, they cannot repair the cavitations, and the conductance stays at zero.
Note the consequences of this interpretation and the
predictions that may be made to test it. First, the maxi-

HYDRAULIC ARCHITECTURE
Just as the pressure chamber does not measure tension
in the xylem, so the traditional way of measuring hydraulic conductance does not measure conductance because the activity of the living cells alters the conductance during the measurement. If all the measurements
we have of pressure gradients are wrong, and all the measurements of hydraulic conductance are wrong, what to
we truly know about the hydraulic architecture of trees?
Measurements of C throughout the canopies of trees
with the pressure chamber have produced the broad generalization that C becomes more negative along the outward path from the trunks through branches of smaller
diameters to twigs and leaves (e.g., Borchert, 1994). The
gradient of C is seen as a manifestation of the pressure
gradient needed to drive the water flow along the outward
path. It agrees well with Zimmermanns demonstration
that the leaf specific conductance (i.e., the flow through
a portion of the wood pathway divided by the area of the
leaves it supplies) decreases along the same path, and so
does the diameter of the largest vessels (Zimmermann,
1983). This concept of tree hydraulic architecture has
been elaborated to map the pressure gradients necessary
to account for the distribution of leaf specific conductances in a number of different tree types (e.g., Tyree and
Ewers, 1991). The orthodox explanation of the gradient
of C is that there are junction constrictions where each
branch or twig joins a larger one, which would generate
an increase in the pressure gradient across the junction,
and negative pressure would increase outwards in the
canopy (Tyree and Ewers, 1991).
On the compensating pressure theory the gradients of

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pressure are much smaller than the gradients of C since

a major part of the measured C is the compensating pressure protecting the conduits. The gradient of C is rather
a gradient of compensating pressure applied to protect
the conduits as they decrease in diameter along the outward path. The junction constriction becomes, on this
view, a nonexistent entity, a piece of plumbing postulated
to explain a gradient that has another purpose. Checks of
the reality of junction constrictions by conductance measurements across the junctions seem to have been inconclusive (Tyree and Ewers, 1991; Tyree and Alexander,
1993).
There is a satisfying explanation of the need for this
greater protection as the diameter decreases, in terms of
the fluid mechanics of the system. The volume flow in a
conduit varies with the pressure gradient and the fourth
power of the diameter. So for a given perturbation in flow
rate the consequent change in the pressure gradient (and
hence the compensating pressure to protect against it)
will vary inversely as the fourth power of the diameter.
As the conduits decrease in diameter along the outward
path the compensating pressure necessary to protect them
will increase. But it will not increase as fast as the fourth
power of the diameter, because the number of conduits
increases along the outward path, and the perturbation of
flow is dispersed among a larger number of smaller conduits. This dispersal can be estimated from Murrays law,
a generalization about branching pipelines known to apply to such diverse systems as blood veins and capillaries,
tracheae and bronchi of the lungs, and vein systems of
leaves (see Murray, 1926; La Barbera, 1990; Canny,
1993). Murrays law says that the number of pipes increases as the cube of the ratio of diameters (i.e., the
product [number of pipes 3 diameter3] is a constant).
Therefore, the size of the fluctuation is reduced as the
cube of the decreasing diameters, and the necessary compensating pressure varies inversely only as the fourth minus the third, equals the first power of the diameter.
An elegant confirmation of this linear dependence of
compensating pressure on conduit diameter can be derived from the birch vulnerability curves of Sperry and
Saliendra (1994). What they interpret as cavitation tensions are interpreted on the new theory as maximum
compensating pressures. Reproducing their report with
this single alteration and omitting the figures not reproduced here, we have:
The within tree variation in vulnerability . . . was correlated with the vessel diameters of the same axes ... .
Vessels were widest in roots, narrowest in twigs, and intermediate in trunks ... . Furthermore, the breadth of the
distributions corresponded to the shape of the vulnerability curves. Cavitation in roots occurred over a wide
range of compensating pressures, and the vessels
showed a similarly wide range of diameters. Vulnerability
curves in trunks and twigs were steep and associated with
relatively narrow vessel diameter distributions. Finally,
the correlation between mean maximum compensating
pressure and mean hydraulic diameter was highly significant with an r2 of 0.87 (Fig. 4) (Sperry and Saliendra, 1974, p. 1237). Their Fig. 4 has been redrawn with
the relabelled y-axis as Fig. 8.

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XYLEM-FEEDING INSECTS
As emphasized previously (Canny, 1995; Crews et al.,
1998), one of the strongest arguments against large negative xylem pressures is the extraction of xylem sap by
many species of insect. Mittler (1967) calculated the pressure that a leafhopper generated to suck sap through its
stylets at the rate it was excreted as 23 bar (2300 kPa),
and Raven (1983) estimated from the dimensions and
properties of the muscles of the cibarial pumps, a maximum suction of 3 bar (300 kPa). A detailed study of the
feeding of the leafhopper Homalodiscus on four plant
species (Andersen, Brodbeck, and Mizell, 1992) produced results that the authors have great difficulty in reconciling with the cohesion theory. These leafhoppers
sucked and exuded sap at the rate of up to 0.7 cm3/h
through stylet canals 12 mm wide, implying a velocity of
43 cm/sec and a pressure gradient along the 2 mm of
stylet of 0.48 bar (48 kPa). Feeding rates were strongly
correlated with the organic nitrogen in the sap, which
varied on a diurnal cycle, and was highest in the afternoon. The authors were puzzled to find that the feeding
rate increased at this time, just when the pressure chamber required the strongest balancing pressure. Feeding
rate increased as C became more negative down to
218 bar (21.8 MPa). In plants stressed beyond 218 bar
(21.8 MPa), when C reached values down to 232 bar
(23.2 MPa), the feeding rate was reduced.
By now, the reader will easily make the translation to
the alternative interpretation, that down to C values
equivalent to the threshold of xylem parenchyma osmotic
pressure (.18 bar[1.8 MPa]) the pressure in the conduits
is kept close to zero, any embolisms are quickly refilled,
and the leafhoppers are easily able to pump the sap with
its enhanced organic nitrogen at maximum rates. In the
stressed plants, as the compensating pressure runs out and
sap pressures fall to 23 bar (2300 kPa) and beyond, the
rate of extraction slows, embolisms cannot be refilled,
and excretion stops.
TYLOSES, TERMINATING VESSEL FUNCTION
In the frozen preparations of sunflower petioles, which
provided the data for the embolism studies (Canny,
1997a, b), tyloses were frequently observed. A full account of them is given in Canny (1997c). They were
forming in, and filling, the oldest, thick-walled vessels at
the inner ends of the xylem arcs, farthest from the phloem. These were just those vessels that were shown to be
most vulnerable to embolism during the first water stress
imposed by transpiration early in the day. In terms of the
compensating pressure theory these tyloses are readily
interpretable as a device to preserve tissue pressure, prevent its dissipation in compressible gas spaces, and conserve supplementary water by eliminating superfluous
sinks for it. Those vessels farthest from the pressurizing
phloem would be the most vulnerable to embolism. The
strategy to put them out of action, replace them with incompressible parenchyma, and form new ones near to the
phloem from the cambium, is entirely consistent with the
requirements of the theory and with the tactics of meeting
these requirements by pressurizing and supplying supplementary water with the available tissues.

July 1998]

CANNYAPPLICATIONS

OF A THEORY OF WATER TRANSPORT

THE SELF-SUSTAINING PIPELINE,

ULTRASTABILITY
Looked at in these ways, the xylem is not a vulnerable
pipeline on the edge of disaster exerting large forces on
strong threads of metastable water liable to breakage. It
is a self-sustaining pipeline that controls the flow of weak
water under varying evaporative demands, using at least
five levels of homeostatic response and adjustment. At
the first level, by applying the compensating tissue pressure P, and working downwards from a positive pressure,
it keeps the tension in the water threads in a range where
cavitation is restricted. At the second level, it maintains
a flow of supplementary water to refill embolisms when
they occur. At the third level, it responds to increased
evaporative demand by osmoregulating the available P
upwards, to raise the xylem pressure and to provide more
supplementary water. At the fourth level it maintains a
population of conduits of small diameter, which will refill
quickly, to ensure continuity of some water threads until
a rapid flux can be restored in the larger conduits. At the
fifth level, it works to eliminate gas spaces, conserve supplementary water, and preserve the hydrostatic pressure
within the organ, by terminating the activity of the conduits most vulnerable to cavitation and filling them with
living parenchyma cells. It is in fact what Ashby (1960)
distinguished as an ultrastable system, a system that is
not just a homeostat, but one that responds to environmental changes outside its previous operating experience
by changing the parameters of its operation and regaining
stability (Appendix 4). Living systems are ultrastable. For
example, a population of bacteria responds to an antibiotic that it has never encountered before and transforms
itself into a resistant strain. Plant water transport has
joined the living world.
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ASHBY, W. R. 1960. Design for a brain, 2d ed. Wiley, London.
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APPENDIX 1
THE PETIOLE AS A SOURCE OF SUPPLEMENTARY WATER
Consider a petiole of one of the sunflower leaves used in Canny
(1997a), with radius 4 mm and ;150 vessels whose median diameter
is 40 mm. The question is: what volume of water must be provided to
maintain a supplementary water supply for the day, and is it reasonable
to suppose that the petiole parenchyma can supply it by a modest volume shrinkage? If DP is the pressure difference between the parenchyma and the vessel lumen, and Lp is the hydraulic conductivity of the
plasma membranes of the cells surrounding a vessel, the volume needed
for unit length is
Lp 3 total vessel surface 3 DP 3 time.
We must select likely values for Lp and DP. In Canny (1997a) the value
chosen for the former was from the midrange of those measured for
midrib tissue of corn leaves by Westgate and Steudle (1985), Lp 5 1027
m3m22s21bar21 [1026 m3m22s21MPa21]. The value of DP must be
greater than the vapor pressure of water but need not be very large. In
the middle of the day the difference is reversed, because water flowed
out of the vessels. Suppose an average of 1/10 bar (10 kPa). Then for
1 m of petiole with 150 vessels of diameter of 40 mm and an 8-h day
the volume becomes,
1027 3 150p 3 40 3 1026 3 28 800 3 0.1 5 5.4 3 1026 m3.
This would require a 5% shrinkage in the diameter of the petiole.
Assuming a transpiration of 100 g/d from a leaf with 1 dm2 of lamina
and 20 cm of petiole, the supplementary water would be ;1% of the
transpiration flow.

A classic analysis by Tyree (1970) of transport in the symplast

through plasmodesmata, comparing diffusion and pressure flow, provides the notation (differing from that in the rest of this paper), basic
equations, and values for many of the variables used here.
For N pores of radius r and length l, pressure flux (JvP) of a liquid of
viscosity h with a pressure difference DP is
(1)

For the same pores, and concentration (strictly activity) difference DC

of substance whose diffusivity is D, diffusive flux (JvD) is
(2)

It is likely that Eqs. 1 and 2 are not applicable in very small spaces.
(1) must overestimate the flow in spaces so narrow that some of the
volume is occupied with vicinal water. Poiseuille flow develops in pipes
100 times longer than their diameter, which is roughly the ratio in the
desmotubule channels (below).
We are seeking the pore size that will effectively restrict JvP relative
to JvD. Suppose we choose to set JvD 5 100 JvP. Most of the variables
on the two sides cancel, and we are left with
r2 5 8hD DC/100 DP.

[Vol. 85
r2 5 8hD DC/5.5 3 106 DP.

(4)

Values of the variablesSelf diffusion coefficient of water (D)

Eisenberg and Kauzmann (1969) give values over a range of temperatures. At 258C, D 5 2.5 3 1029 m2/s. D is somewhat influenced by
viscosity, as considered by Tyree (1970). For small uncharged solutes
the effect is small, and their diffusivities in agar gel are little less than
in water. For water molecules the effect will be even less.
Difference of pressure (DP)As mentioned in the text, small overpressures of the order of 1 bar (100 kPa) would be sufficient to express
water into the xylem, and would suffice for most plants most of the
time. A moderate maximum value for the pressure which might be built
up within the endodermis by the osmotic energy of the living cells of
the stele relative to those in the cortex would be 10 bar (1 MPa). This
was the minimum pressure estimated by White (1938) to be generated
by his cultured tomato roots. This overpressure would push the flux
through into the xylem conduits in plants working under considerable
stress and probably satisfy most of the requirements of the pump. In
the SI units used for this calculation this is 106 Pa.
Difference of water concentration (DC)This is the reduction in water concentration (mole fraction) in the pericycle vacuoles compared
with that in the inner cortical vacuoles due to the difference in solute
concentration. The difference of 10 bar (1 MPa) in DP generated osmotically would require a difference in the mole fraction of water of
0.007, which is equivalent to a difference of water concentration, of
400 moles/m3.
Viscosity (h)This is the most uncertain of the variables, but may
not be relevant. The viscosity of water at 208C is 0.001 Pas. Cytoplasm
can vary from being very fluid to being a strong gel. Valberg and Albertini (1985) list a dozen published values that range from 0.001 to
105 Pas. Tyree (1970) mentions the range 5 3 1022 to 2 Pas, and also
recognizes that it is quite possible that the cytoplasm in the pores of
the plasmodesmata is completely gelled; in this case h would be infinite. If this were so pressure flow is zero and h is irrelevant. The
sensible choice is a value of h that gives a value of r comfortably larger
than the plasmodesmatal pores, so that the choice is not critical. Such
a value is h 5 20 Pas.
CalculationEntering these values in Eq. 4, we have
r 5 nm,

THE POROUS SEPTUM AS A ONE-WAY VALVE

JvD 5 Npr2 D DC/l.

BOTANY

r 2 5 8 3 20(2.5 3 10 29 ) 3 400/(5.5 3 10 6 3 10 6 )

APPENDIX 2

JvP 5 Np r4 DP/8h.

OF

(3)

Before proceeding we must get the units right. The units of JvP are
volume flow units, m3/sec, while those of JvD are mass transfer units,
e.g., moles/sec. To equate the two fluxes they must be measured in the
same units, which can be achieved by multiplying JvP by the number of
moles of water in a cubic metre, 5.5 3 104. With this change, Eq. 3
becomes

while for water,

r 0.04 nm.
Comparison with experimentally determined pore sizesThe detailed
structure of plasmodesmata and the sizes of the pores in them have
been the subject of much experiment and debate (Robards and Lucas,
1990). An extensive study by Terry and Robards (1987) measured the
rates of diffusion of fluorescent probes of various molecular sizes
through plasmodesmata of Abutilon nectary trichomes. They concluded
that the annulus around the desmotubule is probably divided into 10
20 cylindrical channels, each of radius ;1.5 nm. It is also clear (Hake
and Char, 1997; Kragler, Lucas, and Monzer, 1998) that the size of pores
in plasmodesmata is under cellular control, and the exclusion limit for
molecules can vary from ,1000 Da to at least 40 000 Da.
APPENDIX 3
WATER FLUX THROUGH THE ENDODERMAL VALVE
Measured water flux through plasmodesmataA fairly complete set
of data exists on water flux through the endodermis of the branch roots
of corn. Wang, McCully, and Canny (1995) combined their measurements of the number of plasmodesmata through the endodermis, with
the rates of water uptake by the branch roots measured by Varney and
Canny (1993), to express the flux through the endodermis per plasmodesma (plasmo). From Table 3 of Wang, McCully, and Canny (1995),
the water flux was 0.1 to 0.4 pLh21plasmo21. Converting this to moles
of water we have

July 1998]

CANNYAPPLICATIONS

OF A THEORY OF WATER TRANSPORT

522 pmolh21plasmo21.
This may be compared with a calculated possible diffusive flux.
Calculated water flux through the endodermal valveFrom Eq. 2 in
Appendix 2 and continuing with the notation used there
JvD 5 Npr2 D DC/l.
Values of the variablesWe have already (Appendix 2) settled on
values for D 5 2.5 3 1029 m2/s, and DC 5 400 mol /m3. The value for
l was not needed in Appendix 2, but can be taken from Tyree (1970)
as 5 3 1027 m. For the pore radius r, the argument of Appendix 2 was
that values of r less than 5 nm would turn the endodermal plasmodesmata into the one-way valve for water movement. The value of JvD
depends very critically on the value of r. The estimate of Terry and
Robards (1987) for the Abutilon nectary trichomes was that in each
plasmodesma there was an annulus of 1020 cylindrical pores each with
r 5 1.5 nm.
CalculationInserting these values in Eq. 2 gives a flux of
JvD 5 1 pmolh21plasmo21
while the generous maximum value of r 5 5 nm gives
J 5 10 pmolh21plasmo21.
ConclusionThe proposed mechanism is at the threshold of possibility and deserves more detailed consideration. If the endodermal plasmodesmata have channels somewhat larger than 1.5 nm, the diffusive
flux with the assumed values for the other variables would comfortably
supply water at the middle range of measured rates. To achieve fluxes

909

at the higher end of the range wider channels, a steeper gradient of

water concentration or some other modification of the conditions would
be needed.
APPENDIX 4
ULTRASTABLE SYSTEMS
A complex example of an ultrastable system is your blood temperature. The internal homeostats that regulate blood flow through capillaries, sweating, rates of heat production by respiration, etc., have evolved
to accommodate a large range of temperature conditions. You have
learned to extend these conditions almost indefinitely by (for example
on the cold side) putting on more clothes, seeking or constructing shelters and insulation, lighting fires, constructing elaborate heating systems, migrating to warmer climes. Each of these steps provides a change
of the parameters within which the basic bodily thermostats work.
Ashby (1960) defines an ultrastable system as follows: Two systems
of continuous variables (that we called environment and reacting
part) interact, so that a primary feedback (through complex sensory
and motor channels) exists between them. Another feedback, working
intermittently and at a much slower order of speed, goes from the environment to certain continuous variables which in their turn affect
some step-mechanisms, the effect being that the step-mechanisms
change value when and only when these variables pass outside given
limits. The step-mechanisms affect the reacting part; by acting as parameters to it they determine how it shall react to the environment (p.
136).
In the xylem system the four levels of regulation above the basic
compensating pressure homeostat correspond with four sets of Ashbys
step mechanisms, whose parameters may be changed over longer time
scales to sustain the flow of water.