Russian Journal of Plant Physiology, Vol. 51, No. 4, 2004, pp. 547555. Translated from Fiziologiya Rastenii, Vol.

51, No. 4, 2004, pp. 607616.

Original Russian Text Copyright 2004 by Zyalalov.

REVIEW

Water Flows in Higher Plants:

Physiology, Evolution, and System Analysis
A. A. Zyalalov
Institute of Ecology of Natural Systems, Tatarstan Academy of Sciences, Daurskaya ul. 28, Kazan, 420087 Russia;
e-mail: zyalalov@iens.kcn.ru
Received February 7, 2003

AbstractWater movement in higher plants is treated as a symplastic fluid flow incorporated into a unified
hydrodynamic system comprising the apoplast and vessels (or tracheids). Since water flow is of vital necessity
for algae (phylogenetic ancestors of higher plants), it can be stated that higher plants colonized land, still keeping connections with their former water habitat. It is argued that colonization of terrestrial areas by plants
became possible due to the appearance and maintenance of a gradient of water chemical potential between the
rhizosphere and atmosphere, which drives water flows. Autonomization of flows in the symplast is considered
as a vector of evolution, whereas the gradient of water activity is a factor of evolution. The osmotic models of
water uptake by roots are analyzed; the role of potassium circulation in water-transporting system is determined; and a mechanism of automatic coupling between CO2 uptake through stomata and water evaporation
from leaves is presented. An inherent property of the systems to explicitly or implicitly duplicate its structural
or functional elements substantiates possible interactions between the mechanisms underlying opposite water
flows in plants.
Key words: higher plants - water flow - evolution - physiology - system

INTRODUCTION
Transpiration is as a unique biological phenomenon
in the aspect of physical meaning of momentum. Annually 35 1012 tons of water is transported through the
higher plants of our planet [1]. Within 24 h each plant
renews its water over 2030 times [2]. Considering the
average velocity of water flow in the xylem, the front
edge of the transpiration flow covers a single cell distance in the xylem parenchyma within 1020 ms.
The modern ecological physiology abandoned the
viewpoint on transpiration as a plant defense mechanism against overheating or as inevitable expenses for
providing the plant with carbon dioxide [3]. Transpiration is known to decline typically at noon, i.e., at the
period when the protection against overheating is most
urgent. On the other hand, transpiration remains quite
high even at cool weather, when air temperature does
not reach optimum values. The view on transpiration as
inevitable side effect of photosynthesis was also invalidated by studies of photosynthesis and transpiration in
relation to movement of stomatal guard cells [4].
According to contemporary views, the main role of
transpiration is the delivery of mineral nutrients and
organic substances, produced in roots, to the sink tissues; i.e., the exchange between tissues and organs [5].
Besides, water flow can also fulfill a signaling function,
since it occurs within the unified hydrodynamic system
of plant, which includes vessels (or tracheids) and free
water spaces between the cell walls (apoplast).

WATER MOVEMENT AS A PRECONDITION

FOR LIFE ACTIVITY OF HIGHER PLANTS
AND THEIR ANCESTORS
An important aspect of movement of huge amounts
of water in higher plants is the position of this phenomenon in the system of general biological knowledge.
Solving this problem requires an evolutionary approach
as an important methodological basement of modern
biology [6]. The development of water relations in
higher plants is a striking manifestation of a fundamental tenet of the evolutionary theory concerning development of the organism towards its higher independence
of stochastic environmental factors [7]. The basic pathway of biological progress is an expansion of capacities
to resist the external factors by attaining new properties
of more general importance. According to contemporary concepts, vascular plants originated as a result of
symbiosis between fungi and green algae.
Intimate relations between fungi and algae led to the
fusion of their heterotypic nuclei [8], which gave rise to
a nucleus of dual nature with a mixed genome. Subsequent proliferative processes led to the development of
a chimeric organism, which consisted of algal and fungal cells, together with intermediate type cells.
An assumption that plants colonized land by emerging from water habitat seems to be well-grounded. Terrestrial plants preserved all physiological processes that
were present in their ancestors: growth, photosynthesis,
respiration, and mineral nutrition. In addition, higher
plants developed the process of transpiration, which

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ZYALALOV

was absent in their ancestors. The appearance of a new

process in physiologically similar organisms is quite
surprising. Does it mean that lower plants can survive
without the function performed by transpiration, i.e.,
without movement of aqueous solutions in the extracytoplasmic hydrodynamic system?
The analysis of algal ecology indicates that the
movement of surrounding water with dissolved mineral
and organic substances and with cell excretions is an
important condition for their survival. For instance,
water movement is a basic ecological factor for benthic
algae, which determines their growth, functional activity, and rates of physiological processes. This factor is
physiologically as important as light and temperature
[9, 10]. Water circulation can limit the propagation of
algae and determine the structure of their thalli [11, 12].
The displacement of body relative to surrounding
medium is also crucial for planktonic algae. By excreting various substances, algae actively contribute to the
formation of biocoenotic media and thus influence each
other. For instance, Fucus vesiculosus daily excrete
1.01.5 g of carbohydrates and 0.51.0 g of simple phenols per 1 kg dry wt [13, 14]. Many fucoids excrete substances with antibiotic activity [15]. Thus, the circulation of media is crucial for life functions of both algae
and terrestrial plants; it provides organisms with mineral elements, oxygen, carbon dioxide, signaling substances and removes the catabolic wastes.
The water phase of a unified hydrodynamic system,
as well as aquatic environment of algae surrounds and
bathes the ectoplasmic cell membranes confining the
symplast. Stems, leaves, and partly roots are covered
with cutinized tissues poorly permeable to water; i.e.,
the hydrodynamic system is separated from the environment. However, in the absorption zone of root and in
root hairs, the apoplast of higher plants is as accessible
to the environment as that in algae. This is because the
cell walls in these regions have not been altered by secondary modifications. According to Dittmer [16], the
total length of rye roots increases daily by 5 km,
whereas the root hairs increase by 80 km per day. Even
if we reduce these values by an order of magnitude, as
argued by Stankov [17], the total surface of root hairs
would exceed 10 m2. Thus, there is no principal difference in the relations rootrhizosphere and algae
aquatic environment. The only difference is that the
apoplast of bentic algae is washed by flows of aquatic
media, whereas higher plants get access to water by
perforating the media with their roots.
A paradox is remarkable that higher plants have colonized land, still remaining in ocean. It is noteworthy
that the thermodynamic state of water in the World
Ocean is characterized by chemical potential of
approximately 250 J/mol (an equivalent osmotic pressure is 3 MPa) and the chemical potential of water in
free spaces of higher plants also does not fall below
250 J/mol [1].

Unlike algae, the higher plant parts above the

absorption zone are covered with epidermal tissues
poorly permeable to water. The xylem sap and associated water phase, penetrating into the whole system of
intercellular spaces, form an autonomous aqueous
medium of a higher plant. The higher plants, as compared to algae, more actively control the composition
and the thermodynamic state of water in this medium.
Therefore, it is not a coincidence that the transpiration
coefficient remains at a relatively constant level.
The flow of surrounding medium is of crucial
importance for plants. The compartmentation separates
flows. These flows are clearly evident in the reticular
vacuolar continuum [18]. The intercellular flow via
plasmodesmata was proven by experiments [19] and
was simulated by virtue of physical and mathematical
models [20].
In plants, the apoplastic water is an internal medium
for the epidermal tissue and an external medium for the
symplast. Its movement in a vascular plant can be
defined as a flow of internal aquatic environment of live
cells. It is this flow that provides functioning of a plant
organism as an integrated entity [5].
OSMOTIC WATER UPTAKE
The driving force of water uptake in roots includes
metabolic and osmotic components. The modern phenomenology and the concept of metabolic mechanism
of water transport were thoroughly discussed by
Zholkevich at the 41st Timiryazev lecture [5].
A term metabolic component was suggested as a
substitute for the term nonosmotic component in
order to emphasize a highly sensitive controllability of
the magnitude of this component [21]. The term metabolic component is a synonym of active pressure
introduced by van Overbeek [22]. However, it should
be noted that the term suggested by van Overbeek does
not correspond to a widely accepted terminology in
contemporary plant physiology. Unlike passive processes, the processes recognized as active require
metabolic energy. Both osmotic and nonosmotic water
flows into the central cylinder of root absorption zone
are driven by metabolic energy. In the former case,
energy is spend on formation or transport of solutes,
rather than on water uptake per se. Therefore, the
osmotic water uptake could not be treated as a passive
flow in the modern sense of this term. The nonosmotic
or metabolic water uptake represents the flow driven
by hydrostatic pressure, which is also established at the
expense of metabolic energy. Zholkevich et al. documented the involvement of myosin and actin in this
energy transformation process [23, 24]. Further accumulation of data would allow researchers to estimate
the energetic efficiency of two mechanisms of water
transport. Currently we can only say that the energy
transduction pathway in the osmotic mechanism is
reduced to a minimum: respirationproton gradient

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gradient of solute concentrationsosmotic water

uptake. Therefore, the efficiency of osmotic mechanism
may exceed the efficiency of metabolic mechanism.
Currently, several competing models were proposed
to describe the osmotic water uptake by roots. These
models consider alternatives of a single membrane, a
double membrane with dissimilar membrane properties, and a double membrane with identical membrane
properties. In this context, a term membrane does not
mean a biological membrane, but designates a set of
barriers on the pathway of solute radial transport in the
root, which can be treated as a single osmotically active
membrane.
Single-membrane model. According to the first
model, the water flow between soil and the root metaxylem crosses only one membrane. The term membrane
applies to the passage cells of endodermis, with the Casparian strips restricting water movement through the cell
walls. Water moves towards the Casparian strips through
the apoplast of outer and cortical tissues [25]. The driving force of bleeding sap exudation from excised roots is
the difference of osmotic pressures between soil solution
and the metaxylem. The excessive osmotic pressure of
the xylem solution compared to that of soil solution, is
due to the uptake of solutes (mainly inorganic ions) from
the rhizosphere [26]. As an argument against this model,
Newman noted that the conductivity of cell walls is an
order of magnitude lower than is required to reach an
overall conductance of 40 nm/(MPa s) [27]. A supporter
of this model, Steudle [28], believes that its vulnerability
comes from defects of the model as a root equivalent. He
proposed a sophisticated transport model that envisages
parallel water flows via the apoplastic and symplastic
pathways.
Double membrane model. The osmotic concept
based on the double membrane model assumes that
water transport through the cortex occurs via the symplastic route, i.e., the cytoplasmic continuum ensured
by plasmodesmata [18, 29, 30]. Water crosses the membrane twice: at the entrance it is transported through the
plasmalemma of rhizodermis, and then it leaves
through the plasmalemma of passage cells. Two pathways of water transport from the passage cells to the
xylem walls are considered: through the apoplast and
via symplast of the central cylinder. The double membrane model was formulated in two versions. One of
them postulates the identity of properties of both membranes [3133], whereas the other assumes their difference [34, 35].
According to the double membrane model with dissimilar membrane properties, the outer membrane (plasmalemma of epidermal tissue) has low permeability,
whereas the inner one has high permeability to solutes.
The water inflow in the compartment is driven by local
uptake of ions from ambient soil solution, by synthesis of
low-molecular weight compounds (osmolytes) in the
cortex, and by their basipetal transport. The inflow of
water into the compartment enclosed by these two memRUSSIAN JOURNAL OF PLANT PHYSIOLOGY

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branes (assemblage of cells of rhizodermis and primary

cortex) produces a hydrostatic pressure, which filtrates
the solution into the root vessels.
This model was criticized on the following grounds.
No membrane with low hydraulic conductivity was
found in stems, and the reflection coefficient of cell
membranes for physiological solutions is so close to
unity that there is no justified reasons to build up a
model on the assumption of different properties of
these membranes [36, 37].
The other version of the double membrane model
envisages asymmetrical membranes and postulates the
active transport of solutes into the xylem; i.e., localization of active ion transport at the inner membrane [29,
37, 38]. This model develops a notion that active secretion of solutes is directed into the interfibrillar spaces in
the cell walls of stele, rather than directly into the vessels. These interstices are clogged with suberin at the
endodermal side; i.e., only the pore endings adjacent to
the xylem remain open [39, 40].
Based on the double membrane model with symmetrical membranes, Lyalin proposed the theory of reverse
osmotic uptake of water by roots [33]. The outer membrane, composed of the membranes of rhizodermal and
cortical cells, separates the symplast from soil solution,
whereas the inner membrane, the plasmalemma of
stele, delimits it from the xylem vessels. The outer
membrane functions as the membrane of osmotic cell,
while the inner one operates in the mode of reverse
osmosis. Filtration of solutes through the inner membrane into the vessels is driven by turgor pressure build
up in the double membrane system.
Despite complete identity of both membranes, some
asymmetry still arises in this system. This is because
the volume of compartment from which solutes are
delivered into the xylem is negligibly small as compared to the volume of the rhizosphere.
According to the model of Meleshchenko [41], the
root consists of two compartments: zone 1, which represents a symplast of the rhizodermis and the primary
cortex, and zone 2, which is a symplast of the stele. As
for the kinematics of bleeding sap exudation, it should
be noted that the osmotic and turgor pressures in zone
1 are increasing due to metabolic attraction. The turgor pressure is transmitted to zone 2 through an elastic
endodermis. As a result of this and because the osmotic
pressure in zone 2 is lower than in the external compartment, the chemical potential of water in zone 2
increases, which drives the flow from the symplast to
the metaxylem vessels. This process has a relaxational
and periodical behavior.
All described models have a solid physicochemical
basis and account for possible consequences of osmotic
phenomena. Plants possess all elements of the osmotic
system (water, solutes with various dimensions of molecules and ions, and membranes with different permeabilities to various particles); therefore, the occurrence
of osmotic flows in plants is undoubted.
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ZYALALOV

POTASSIUM CIRCULATION COMPENSATES

FOR THE EFFLUX OF SOLUTES
The following requirements and features are common to all the osmotic models: the osmotic pressure of
bleeding sap should not be zero and the rate of sap exudation is typically described by direct, other than
inverse, dependence on solute concentrations.
Plants dispose a wide range of osmotic solutes and
a highly efficient mechanism of their formation, which
is activated in response to environmental stimuli. These
solutes, the osmoprotectants, are various organic substances [42]. However, the principal osmotic processes
in plants are driven by inorganic ions and, particularly,
by potassium ion. Potassium concentrations in the cytosol and vacuoles of rhizodermal cells exceed 100 and
60 mM, respectively [43]. With the allowance for bidirectional fluxes, these concentrations correspond to
osmotic pressures of 0.45 and 0.25 MPa.
Potassium concentrations in corn root exudates
reach 37 mM [44]. The xylem sap collected at the level
of root collar contained 1015 mM K+ in sunflower
plants [45] and 817 mM in tomato plants [46]. By considering potassium ions and their counterions, one can
easily calculate that the osmotic pressures of these solutions should be 0.035 to 0.154 MPa. Potassium is
dragged with the transpiration flow, but there is a considerable discrepancy in the potassium balance. Almost
all water is evaporated from transpiring organs to the
atmosphere, whereas solutes, including potassium,
remain in the plant. To compensate losses of solutes,
the root must constantly (as long as transpiration takes
place) take up potassium. In order to produce 1 g of dry
matter, the growing plant should transfer at least 300 g
of water with the transpiration flow (transpiration coefficient is 300) [3]. Taking the aforementioned value of
transpiration coefficient and the potassium concentration in the xylem equal to 10 mM, 1 g of dry matter
should contain 0.12 g or 12% of potassium. The average potassium content in plant tissues is usually an
order of magnitude lower. This discrepancy led to an
assumption that a considerable fraction of potassium is
retransported to the root without reaching leaves, and
such an explanation was proved by experiments [45,
47, 48]. Later, other authors confirmed the performance
of this physiological process [49, 50].
Potassium returned to the root is reinvolved in the
ascending flow, and then again enters the conductive
tissue to be transported in the basipetal direction. The
circulation of potassium within the plant is specially
essential for plant life. Due to this process, the
osmolytes in the root absorption zone are permanently
replenished and, therefore, the osmotic potential is
maintained (osmoregulation at the organism level). The
metabolic energy is presumably spent at the stage of
potassium transport from the xylem into the phloem,
because its activity in the phloem is typically higher
than that in the xylem [51], and because potassium is
transported against the concentration gradient.

The existence of coupling between water flows in

plants and the retransport of potassium was proved by
experimental evidence. The aerial organs were treated
with potassium salts, and the aftereffect of this treatment on the bleeding from the stumps of sunflower
stems and from the maize root tips were studied. It was
found that, in the case when sunflower leaves were wetted with potassium sulfate solution and then the shoot
was cut off above the root collar, the rate of bleeding
sap exudation increased with time, whereas in control
(untreated) plants the exudation rate decreased. The
amount of potassium released with the bleeding sap in
the treated plants also increased in time. The correlation
analysis revealed positive correlation between the exudation rate and the potassium content in the bleeding
sap. Measurements of exudation rate from the root tips
in plants after loading the undetached aerial organs
with potassium (by the method suggested by Solovev
and Verenchikov [44]), revealed different time-courses
of exudation in treated and untreated plants. In
untreated (control) plants, the rate of exudation from
the root tips slowly decreased, but in the treated plants
the exudation rate increased rapidly 7080 min after
spraying leaves with potassium and continued to gradually increase. Potassium amounts in the exudate also
increased in the treated plants.
Thus, both experimental approaches gave similar
results: the treatment of aerial organs with potassium
increased the uptake and long-distance transport of
water. This supported the idea that the plant controls
water flows at the organismal level by virtue of regulated potassium circulation [48]. In addition, data were
obtained on the involvement of phytohormones (IAA
and ABA) in regulation of potassium circulation and,
consequently, water transport [52].
The process of potassium circulation was found
both in monocotyledonous and dicotyledonous plants,
which suggests its general importance for physiology.
Judging from the facts that potassium circulation not
only maintains the osmolality of xylem sap, but also is
coupled with assimilate loading into the phloem, this
process apparently has multiple functions.
ENERGETICS OF WATER FLOWS
Irrespective of the mechanism (osmotic or nonosmotic), water uptake is associated with expenditures of
metabolic energy. The energy costs are minimal at optimum level of water chemical potential in soil (at oxygen sufficiency) and become higher when water activity
decreases. Similarly to water movement in algae, water
entering the xylem in the root tip moves along the symplast without metabolic energy expenses, i.e., downhill
the gradient of its chemical potential between the rhizosphere and atmosphere. This gradient between soil and
the atmosphere is huge. Even at relative humidity of
94%, the gradient of water chemical potential is
150 J/mol, which is equivalent to osmotic pressure of
8.3 MPa. At a typical summer noon in the continental

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WATER FLOWS IN HIGHER PLANTS

climatic zone, this gradient is about 1500 J/mol or

100 MPa of equivalent pressure. It was shown in experiments that plants spend considerable amounts of
energy to compensate for the absence of external driving force for water movement, when chemical potential
of water in the rhizosphere is close to its value in the
atmosphere [53, 54]. There are reasons to believe that a
similar force is applied to drive water uptake by the
root. This view is suggested by measurements of turgor
pressure and osmotic potential along the root radius.
Under sufficient irradiance and the transpiration rates
above 3 mmol/(m2 leaf area), considerable gradients of
turgor pressure across the cortex and of water potential
across the epidermis and stele were found in maize
plants. The suppression of transpiration led to dissipation of the gradients of turgor pressure and of water
chemical potential [55].
NONCLASSICAL VIEW ON STOMATAL
TRANSPIRATION
The gradient of chemical potential of water between
the leaf and the atmosphere is undoubtedly the driving
force of the upper end motor. According to conventional views, 7585% of water is evaporated through the
stomata. The cuticular transpiration accounts for 25
15% of total one. Water is evaporated from cell surfaces
into the substomatal cavity; air is saturated with moisture, which diffuses through the stomatal aperture outward. This process is regulated by closing and opening
(narrowing and widening the aperture) of stomatal pore.
This view is, however, in conflict with the following
data.
(1) It was shown experimentally that water moves in
the leaf from the tracheal endings of vascular bundles
through the cell walls of sheath and mesophyll cells to
the epidermis. A smaller portion of water, after reaching the epidermis, moves through the periclinal cell
walls and is evaporated through the cuticle. The most
part of water is evaporated through the anticlinal cell
walls of epidermal cells adjacent to stomata and partly
of stomatal guard cells [5659].
(2) Cell walls that form the substomatal cavity are
cutinized [60, 61]; i.e., the nature provided a barrier to
water evaporation into this cavity (although this barrier
is presumably more permeable than that of the epidermal cell cuticle).
(3) The humidity of air in the substomatal cavity
does not reach maximum values. The relative humidity
was reported to decrease to 60% [62].
(4) The stomatal movement is rather slow [4].
(5) The rate of stomatal transpiration is often independent of the stomatal aperture [63].
These data suggest that a considerable amount of
water is transferred during stomatal transpiration from
the leaf into the atmosphere through the anticlinal walls
of epidermal cells in the vicinity of stomata [59]. Consequently, CO2 diffuses through the stomatal pore withRUSSIAN JOURNAL OF PLANT PHYSIOLOGY

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out an appreciable counterflow of water. According to

Rahi [64], the surface area of mesophyll cells lining the
substomatal cavity is 79 times larger than the surface
area of leaf. This means that the rate of stomatal transpiration per unit surface area is not higher than that of
cuticular transpiration. A characteristic feature of stomatal transpiration is that it is canalized.
PHYSIOLOGICAL SIGNIFICANCE
OF CANALIZATION OF WATER TRANSPORT
FROM THE LEAF TO ATMOSPHERE
Since evaporation occurs from the outer surface of
cell walls of near-stomatal cells, the canalization localizes a temperature gradient around the stomatal pore.
Apparently, such localization is of decisive significance. Diffusion flows are known to arise in nonuniformly heated system. The difference in thermal motion
of molecules, caused by differences in their effective
cross sections, leads to unequal numbers of molecules
of different kinds that cross unit area downhill and
uphill the gradient of temperature. It is noteworthy that
this phenomenon provides the basis for a thermogravitational method of isotope separation. Two regions with
different concentrations of gas components arise as a
result of thermodiffusion; i.e., the process of thermodialisis occurs. It is arbitrarily assumed that air consists of
heavy (slow) and light-weight (fast) molecules
[65]. The heaviest is the molecule of carbon dioxide
(0.044 kg/mol), whereas the molecules of other air components are light (average value of 0.029 kg/mol).
According to the rules of thermodiffusion, a lighter gas
moves towards the warm side, whereas a heavier gas
diffuses towards the cold side. Therefore, in the presence of temperature gradient, which arises due to evaporation, carbon dioxide is concentrated in the stomatal
pore. It is also important for plant life activity that, in
the absence of transpiration, the CO2 dialysis would
proceed in the reverse direction: its concentration in the
pore would become lower than in the ambient air [66].
Table shows calculated increments of CO2 concentration in the stomatal pore as a function of temperature
gradient at the leafair interface. The increment in CO2
concentration of about 0.51.0% corresponds to the
published values of temperature gradients [67, 68].
Besides, it was shown that, in the absence of transpiration, CO2 concentration in intercellular spaces
decreased. Nevertheless, these values should not be considered as quantitative estimates of the transpiration
effect on the entry of carbon dioxide into the mesophyll.
Absolute and specific increments of the CO2 concentration in
the stomatal pore at various average temperature gradients at
the leafair interface [66]
T, C
N 1016 molecule/cm3
N/2 709 1019
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3
13.6
5.0

5
22.7
8.4

7
31.8
11.7

9
40.9
15.1

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ZYALALOV

At a first glimpse one can get an impression that the

notion presented above brings us back to former ideas
on the cooling role of transpiration. However, such an
impression is entirely wrong. In earlier studies, only an
antistress role was assigned to transpiration: protection
against overheating. In our case, transpiration ensures
the operation of a mechanism that enhances CO2 transport into the substomatal cavity.
The presence of separate pathways for water and
CO2 transport in stomatal complexes accounts for the
existence of independent stomatal mechanisms for regulation of CO2 concentration and transpiration. Irrespective of water content in leaf, the increase in CO2
concentration leads to closing of stomatal pores, which
does not affect transpiration in the near-stomatal
region. Near-stomatal transpiration is controlled by the
narrowing of interfibrillar spaces in anticlinal cell walls
and by the disappearance of ectodesmata. The regulation of stomatal conductance activated by various triggers (CO2, vapor pressure deficit at the leafair interface, drought) relies on mechanisms that are interrelated, cosubordinated, and, apparently, speciesspecific. For example, stomatal conductance actively
responds to changes in CO2 concentration under
weather conditions with low vapor pressure deficit,
whereas this response is almost absent on days with
high vapor pressure deficit [69, 70]. Under drought
conditions, some species do not respond to CO2 in a
wide range of vapor deficit, whereas in other species the
elevation of CO2 level additionally lowers the stomatal
conductance. These data suggest that the mechanism
triggered by drought (and mediated by ABA) represents
the primary hierarchical level; the mechanism triggered
by air dryness is secondary; and the mechanism of CO2
triggering is tertiary. Species-specific differences could
be explained by the fact that the loss of stomatal activity
depends on the organ age and is related to cutinization
of cell walls lining the substomatal cavity. When the
cell walls turn dehydrated due to air dryness, not only
the stomatal conductance is lowered [71], but also the
conductance of mesophyll cells decreases. Changes in
water potential of apoplast regulate the activity of water
channels in plasmalemma by phosphorylation of aquaporins [72]. Narrowing of interfibrillar spaces, which
reduces water conductance, can be triggered both by
the decrease in air humidity [73], and by the reduced
water flow into the root [74].
As a response to the decreased air humidity, the epidermis reduces its surface area within few seconds.
Under conditions of humidity variations, cells can presumably regulate the elasticity of cell walls by synthesizing proteins and their secretion into the intercellular
space [75]. Under water-sufficient conditions, the aperture of stomata, as the pathway for CO2 entry, is regulated by changes in linear dimensions of microtubules
in guard cells [76].

It was also shown that the actin cytoskeleton in protoplasts of guard cells is sensitive to light and involves
in gating K+-channels [77].
Thus, the progress in studies of subcellular mechanisms of osmotic and nonosmotic regulation of stomatal CO2 conductance is obvious. But the mechanism
of stomatal response to changes in water regime is not
yet clear. Therefore, the problem of controlled water
relations in plants is still far from being resolved [78].
CONCLUSION
The phenomenon of water relations in plants is intimately related to a global event in the history of biosphere, the colonization of land by plants. There was
nothing principally new in life activities of terrestrial
plants as compared to their ancestors. Both terrestrial
plants and their aquatic ancestors perform identical
physiological processes and should meet the same
requirements for realization of physiological functions.
In fact, even the range of environmental conditions
appropriate for plant survival did not change drastically. The life activity of algal and higher plant cells is
only possible within the same narrow range of chemical
potentials of water in the extracellular medium. A vital
factor for algae is the flow of medium. Owing to a specific morphology of higher plants, a considerable part
of their surface area (the root absorption zone covered
with root hairs) directly contacts the soil solution
(water medium). In terrestrial plants, likewise in algae,
the cell walls contacting the outer medium have not
undergone secondary modifications; i.e., the symplast
is actually bathed by the medium.
In higher plants the flow of water medium is driven
by transpiration. The structural framework for the
medium is a hydrodynamic system that includes the apoplast and the vessels or tracheids. The composition of
this medium is affected by bathed cells [79], the root
cells and cells of photosynthesizing organs in particular.
The general strategy of adaptations is to make ontogenetic, morphogenetic, physiological, and biochemical processes comparatively independent of the environmental factors [8082]. Based on this assumption it
appears that, in both animal and plant kingdoms, this
strategy is mainly implemented through the improvement of the system where the cells are functioning.
The unified hydrodynamic system with a moving
aqueous phase inside it can be considered an external
medium with respect to the symplast and as an internal
medium with respect to the environment. This view is in
accord with Bernards idea (cited after [83]) on the internal medium and with the Cannons doctrine of homeostasis [84]. According to Cannon, homeostasis is the
state of organism stability, the maintenance of which is
the main function of autonomous aqueous medium.
The squeezing of huge amounts of water through the
plant is driven largely at the expense of the gradient of
water chemical potential between the rhizosphere and

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atmosphere; i.e., the free energy of the media is utilized.

Consequently, terrestrial plants can only survive on condition that the atmospheric humidity is unsaturated. It means
that a new environmental factor, formerly inaccessible to
ancestors, was put under control. This supports the natural
selection theory, according to which the evolutionary
advance is attributed to those biological entities that can
better utilize environmental energy resources [85].
The insight into phenomenon of water balance in
plants is related to the concept of their self-organization.
The question arises of whether the plants can be treated
as systems, self-organization of which is based on their
inherent internal mechanisms of regulation, or their selforganization is unrelated to the presence or internal controller and is realized by virtue of direct local interactions
between the components of the system.
The preference should presumably be given to the
plant as a system, in which physiological processes are
capable of self-arranging for a certain synergetic activity (Wiener) [86]. Apparently, the hormonal regulation
should be also considered in this aspect, although modern plant physiology has only fragmental knowledge on
exerting the hormonal controlling.
The recognition of symbiotic origin of higher plants
from fungi and algae and the autonomy of plastids and
mitochondria inclines us to a view that regulation in
plants is polycentric; i.e., relatively autonomous systems are organized in a dynamic network. This notion
is likely to represent a correct view on the autonomy of
water system in higher plants.
The notion that the redundancy of functional components of a system increases its stability has a direct bearing to the acceptance or rejection of osmotic or nonosmotic theories of water uptake by the root; it is also relevant to the ideas on the pumping function of stem, on
water column suspension by transpiration, and on multiple functions of transpiration. Many elements of the system are explicitly or implicitly duplicated in structure
and function. By adopting this viewpoint and considering the plant as a system, one must admit that both
osmotic and nonosmotic mechanisms of water uptake
operate concurrently in the root. The revelation of border
conditions imposed on functioning and interactions of
these mechanisms is a challenge for plant science.
Interactions of various regulatory mechanisms in
water relations provide adaptation of plants to one of
the most dynamic environmental factors, the water
regime.
The mobile internal aqueous medium in plants fulfils a communicative function that remains unexplored
so far.
Also the mechanism of coupling of water to CO2
transport in stomatal complexes at the organismal level
remains unelucidated.
Thus, the consideration of water relations in plants
as a system is contiguous to the problem of organism
integrity, which, according to Schmalhausen [87], is
one of the central problems of theoretical biology.
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