ISSN 1021-4437, Russian Journal of Plant Physiology, 2007, Vol. 54, No. 2, pp. 224–229. © Pleiades Publishing, Ltd., 2007.
Original Russian Text © I.F. Ionenko, A.V. Anisimov, 2007, published in Fiziologiya Rastenii, 2007, Vol. 54, No. 2, pp. 253–259.
RESEARCH
PAPERS
Radial Diffusion Transport of Water in Various Zones
of Maize Root and Its Sensitivity to Mercury Chloride
I. F. Ionenko and A. V. Anisimov
Kazan Institute of Biochemistry and Biophysics, Kazan Research Center, Russian Academy of Sciences,
ul. Lobachevskogo 2/31, Kazan, Tatarstan, 420111 Russia;
e-mail: [email protected]
Received June 20, 2006
Abstract—NMR–spin echo method was used for comparative study of radial water diffusion in various zones
of maize (Zea mays L., cv. Donskaya 1) primary root. Coefficients of water diffusion varied strongly along the
root length; the pattern of variations depended on the period during which the diffusion of water molecules was
traced. Water diffusion transport in various root zones was unevenly sensitive to mercury chloride, an aquaporin
inhibitor. The discovered variations in the mobility of water molecules were assigned to morphological and
functional features of cells and tissues in the root zones examined; they were interpreted in terms of variable
contribution and redistribution of water flows along several transport pathways. The decrease in diffusional
water flows could be caused by cell wall modifications (deposition of suberin) that emerge in the endoderm
regions distant from the root apex and diminish the contribution of apoplastic transport.
DOI: 10.1134/S1021443707020100
Key words: Zea mays - root zones - water diffusion - symplast - membrane permeability - aquaporins - NMR
method
INTRODUCTION
One of the most important functions of roots is the
delivery of water and mineral elements from the soil
solution to the aboveground plant parts. Water absorption by roots provides the major income to water balance, thus ensuring normal functioning of the whole
plant. The largest resistance to root water flow is associated with radial transport pathway, where live cells
account for 70–90% of the resistance and the remaining
part is attributed to xylem cells [1].
Numerous studies have shown that radial hydraulic
conductivity of roots changes substantially as a function of root age and the stage of development [1–4]. It
is also sensitive to external and internal factors such as
water stress and salt stress, shortage of mineral nutrients, temperature changes, and water demands for transpiration of aerial plant parts [5–9]. Several publications dealt with identification of the main barriers hampering water transport in roots [1, 10], but the opinions
on this matter are controversial. A commonly accepted
view of endoderm with Casparian strips as the main
obstacle for radial water transport [11–13] was questioned in a series of works [1, 10, 14, 15]. The authors
of these studies supposed that the resistance to water
flow is uniformly distributed over all live cells. This
view was formulated, for example, in the “uniform
resistance model” [16] for young maize roots with
Abbreviations: Def—effective coefficient of water self-diffusion;
R—relative amplitude of the echo; td—diffusion time.
immature exoderm. The localization of the main barrier
for radial water movement in the root is obviously
determined by several factors, such as the stage of root
development (age), the dominance of one or another
pathway for water transport in the root, qualities of
experimental material, and plant growth conditions
accounting for the appearance of additional barriers in
the form of cell wall modifications in the endo- and
exoderm.
A significant role in the radial water transport
through the root is currently assigned to water-conducting channels, aquaporins. More than 70% of transported water is supposed to move through these channels [17–19]. Aquaporins play an important role in
osmotic regulation of cells and in transcellular water
transport. Large quantities of aquaporins are concentrated in zones of fast cell division and rapid elongation
growth, as well as in regions with high rate of water
flow. More than 30 aquaporins have been identified in
maize [20]. The aquaporin activity varies depending on
cell type and cell specialization [21, 22]; it also changes
in response to external cues and stresses [6, 23, 24].
Several studies revealed different and nonuniform sensitivity of radial hydraulic conductance along the growing root to mercury chloride, an aquaporin inhibitor
[16, 26]. These data implied possible alterations in predominant pathways of water movement during root
development. Nevertheless, the contributions of individual transport pathways during water uptake by roots
and fundamental events in regulation of root absorbing
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RADIAL DIFFUSION TRANSPORT OF WATER
capacity remain insufficiently characterized and puzzling issues.
Our previous NMR–spin echo studies with the
pulsed magnetic field gradient revealed that the diffusional water flow in maize roots is sensitive to mercury
chloride, an inhibitor of water channels [26, 27]. Based
on these studies, we suggested approaches to investigation of water diffusion in different compartments of
plant tissue [28].
Considering that changes in water transport parameters are based on structural differences related to cell
and tissue differentiation along the root axis and taking
into account functional features and differential contribution of various water-conducting pathways, we
intended to study diffusional water transport in various
zones of growing maize root and to assess the sensitivity of this transport to an aquaporin inhibitor, mercury
chloride.
MATERIALS AND METHODS
Growth conditions and preparation of samples.
Experiments were performed on roots of 9-day-old
maize seedlings (Zea mays L., cv. Donskaya 1). Seeds
were germinated for two days on trays between layers
of filter paper moistened with fourfold diluted Hoagland–Arnon nutrient solution. The germinated seeds
were spread on sheets of wet filter paper (15 × 50 cm)
at a distance of 2 cm from each other and 1 cm from the
sheet edge. The paper sheets were then rolled and
placed into cylindrical glass vessels with nutrient solution covering their bottoms. The seedlings were raised
in these rolls for 7 days at 22 ± 2°ë at irradiance of
40 W/m2 and 12-h photoperiod. Experiments were conducted with primary roots of maize seedlings measuring 12–15 cm; root segments were cut from various
root zones (Fig. 1). Zone I is the apical root segment
measuring 1.5–2.0 mm that included the meristem and
the transition zone (the distal part of the extension
zone); zone II is the root region with a length of 7 mm
excised from the extension zone (the root region adjoining to zone I); zone III is the root segment measuring
8 mm and located at a distance of 60–70 mm from the
root apex (zone of differentiated cells). In order to measure diffusion coefficients, samples from the respective
zones were placed into a measuring ampoule (30 segments per ampoule for zones II and III and 50 segments
per ampoule for zone I samples).
Mercury chloride was used as an inhibitor of water
channels; it was found effective for the majority of
aquaporins [6, 16, 18, 30, 31]. In order to study effects
of this agent on diffusional transport of water, the roots
of intact maize seedlings were immersed for 15 min
into the nutrient medium containing 0.1 mM HgCl2.
After the end of incubation period, the seedlings were
removed from the solution; the roots were excised and
cut into respective zones. The optimal concentration of
HgCl2 and the length of incubation period were
RUSSIAN JOURNAL OF PLANT PHYSIOLOGY
Vol. 54
Zone I
Zone II
225
Zone III
Fig. 1. Schematic view of the primary maize root and the
root zones investigated.
Zone I (the root apex measuring 2 mm) comprised the root
cap, the apical meristem, and the transition zone (according
to [30]). The cells of this zone had isodiametric shape and
were almost uniform in size (d = 10–15 µm). Zone II (the
root segment with a length of 7 mm located above zone I)
contained the elongation zone and a part of the differentiation zone. The cells were elongated along the root axis and
contained central vacuoles. The diameter of cortex cells in
the radial direction was 30–45 µm. Zone III (a root part at a
distance of 60–70 mm from the tip) consisted of differentiated cells that completed the stage of maturation. This zone
was characterized by the presence of endoderm with the
Casparian strips (dashed line) and suberin lamellae (solid
line). In some roots the exoderm was formed. A horizontal
bar in the center shows position of the xylem conducting
vessels (the mature early metaxylem appeared at a distance
of about 25 mm from the root tip [1]).
selected according to publications of other authors [18,
19, 30]. These studies established that the rate of water
flow decreased substantially after 15-min incubation of
roots in the presence of HgCl2 and reversed under subsequent treatment with mercaptoethanol. This concentration did not cause significant side effects [27], was
nontoxic [32], and did not damage the membranes [33].
The diffusion was measured in the radial direction
of root, with an exception for zone I samples (very
small sizes of these root segments precluded their
proper alignment). All measurements were performed
at 22°ë.
NMR measurements of water diffusion coefficients.
Water diffusion measurements were conducted with a
spin-echo NMR relaxometer–diffusometer at a frequency of 16 MHz with a pulsed magnetic field gradient. The method of NMR-stimulated echo is based on
the recording of translational path length for the diffusion of water molecules over a certain experimental
period of observation in the sample volume marked
with the magnetic field gradient [34]. During experiment, we recorded the diffusional decays of spin echo
signals as a function of parameters characterizing the
pulse sequence: the amplitude of magnetic field gradient pulses (g), pulse duration (δ), and the interpulse
period (td), called conventionally “the diffusion time.”
For quantitative description of the experimental results,
we applied the formalism for effective coefficient of
water self-diffusion (Def). The essence of Def formalism
is the following. The diffusional decay is described by
the equation that is valid for unrestricted diffusion. The
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2007
226
IONENKO, ANISIMOV
1
10
Coefficient of water diffusion, Def × 10–5 cm2/s
(a)
0.1
0.01
Relative echo amplitude, R
1
0.001
3
2
1
(b)
0.1
9
8
7
6
5
1
4
2
3
3
0
100
200
300
400
Diffusion time, td, ms
500
3
2
0.01
1
0
10
20
30
40
50
60
Amplitude of the gradient pulses, g2, T2m2
Fig. 2. Relative amplitude of the echo signal R as a function
of gradient pulse amplitude g2 at diffusion times (a) td =
15 ms and (b) td = 500 ms for various zones of maize root.
(1) Zone I; (2) Zone II; (3) Zone III. The diffusional decay
curves were averaged over seven accumulations of echo signal amplitudes.
further interpretation of Def takes into account the
dependence of diffusional decay on multiple factors
(the nature of transmembrane flows, diffusion rates,
and the influence of restricting factors). Average values
of effective diffusion coefficient were calculated from
the slope of tangent to the curve of the diffusional decay
at g
0 with the use of the known equation:
R = exp[–γ2δ2g2(td – 1/3δ)Def],
where R is the relative echo amplitude, which is equal
to the ratio of echo amplitude in the presence and
absence of magnetic field gradient (A(g)/A(0)) and γ is
a gyromagnetic ratio. The physical meaning of the
apparent diffusion coefficients was interpreted according to the chosen td value. In the series of experiments
the signal attributed to the vacuolar water was excluded
from the total NMR signal. This was accomplished by
applying selective sequences of stimulated echo; the
basics and examples of this method were described in
previous studies [26, 28].
The diffusometer data were processed with a computer. Each diffusional decay curve represents the mean
of seven accumulated signals of echo amplitude. All
experiments were performed in triplicate.
Fig. 3. Dependence of water diffusion coefficients Def on
the diffusion time td in maize roots.
(1) Zone I; (2) Zone II; (3) Zone III. Data are mean values
for three replicate measurements. Bars designate standard
errors.
RESULTS AND DISCUSSION
The decay curves of the relative echo amplitude R
plotted against the amplitude of gradient pulses g2were
nonexponential, irrespective of the diffusion time td, for
all root zones of 9-day-old maize seedlings (Fig. 2).
Such nonexponential patterns are characteristic of live
heterogeneous systems where water diffusion is
restricted by the presence of compartments of various
dimensions. The curves of diffusional echo decay differed for various root zones; namely, the slopes of these
curves were different indicating variations in the water
diffusion coefficients Def. Figure 3 shows dependences
of Def on td for various root zones. The shapes of these
curves were obviously different. In the case of zone I,
two clearly different regions were seen: (1) the region
of restricted diffusion at td < 100 ms, where Def
decreased rapidly with td, and (2) the region of hindered
diffusion at td > 100 ms, where Def was independent of
td (Fig. 3, curve 1). In the region of hindered diffusion,
Def values are known to depend on permeability of
membranes to water; therefore changes in water permeability were manifested as changes in the slope of the
diffusional decay. For zones II and III the region of hindered diffusion was observed at td > 400 ms; this was
due to much larger cell sizes in these zones compared
to the meristem zone (Fig. 3, curves 2, 3).
At short diffusion time, td = 15 ms (Figs. 2a, 3), the
Def values in zones II and III were considerably higher
than Def values in the apical part of the root (zone I).
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No. 2
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RADIAL DIFFUSION TRANSPORT OF WATER
227
Effect of mercury chloride on diffusional water transport in various zones of maize roots at different diffusion times (td)
Root zone
I
II
III
HgCl2 , 100 µM
–
+
–
+
–
+
Coefficient of water diffusion (Def × 10–5 cm2/s)
15 ms
100 ms
300 ms
700 ms
7.0 ± 0.2
7.5 ± 0.15
9.2 ± 0.2
9.4 ± 0.2
8.8 ± 0.2
9.0 ± 0.1
4.9 ± 0.2
5.9 ± 0.3
6.2 ± 0.2
5.4 ± 0.2
5.7 ± 0.15
5.2 ± 0.1
4.8 ± 0.15
5.4 ± 0.2
4.6 ± 0.15
3.3 ± 0.2
4.2 ± 0.2
2.8 ± 0.2
–
–
4.2 ± 0.15
2.9 ± 0.1
3.3 ± 0.2
1.9 ± 0.1
Note: Sign (–) designates no treatment; sign (+) refers to roots that were immersed for 15 min into solution with 100 µM HgCl2 , dissected
into respective zones, and sampled for measurements.
* Data represent average values (± standard error) calculated from three replicate experiments.
The diffusional path length of water molecules X at a
given td was estimated from the relation
X2 = 2Dtd,
and was found equal to 10–15 µm; i.e., it did not exceed
the average dimension of one cell. It is known that cell
elongation is accompanied by sharp activation of cell
metabolism, formation of the central vacuole, and drastic cytoplasm fluidization (owing partly to a significant
decrease in concentration of cytoplasmic proteins)
[35]. The differences in water diffusion coefficients for
zone I and zones II and III (at td = 15 ms) were likely
caused by combination of all these factors. Evidence
for the view that the cytoplasm fluidization (the
decrease in viscosity) could elevate the diffusivity of
water was obtained in experiments with the use of
selective program of stimulated echo [29]. This experimental protocol allowed us to exclude the signals attributed to vacuolar water. We found that Def was consistently lower in zone I (Def = 1.4 × 10–5 cm2/s) than in
zones II and III (Def = 1.7 × 10–5 cm2/s).
At higher td values, a different pattern of changes in
water diffusion coefficients was observed (Figs. 2b, 3).
Namely, the Def values were lower in zones II and III
than in zone I. In this case, the diffusional path length
of water molecule X (at td = 500 ms) was equal to 70–
80 µm, which is more than two times higher than the
average dimension of root cells in the radial direction
(especially for zone I cells). In this case, the differences
in Def values at td = 500 ms for various root zones could
be due to disparate tissue morphologies and membrane
permeabilities. Namely, the water permeability of cell
membranes seems lower in zone II and especially in
zone III compared to zone I. French et al. [36] concluded that root tissues become less permeable for cellto-cell water flows during root development. They
observed the decrease in hydraulic conductivity of
maize roots by a factor of 5 and 10 upon the displacement from the root apex to a distance of 25 and 100 mm,
respectively. The higher water permeability of meristematic cells in zone I may promote faster transmembrane exchange of extra- and intracellular water, thus
RUSSIAN JOURNAL OF PLANT PHYSIOLOGY
Vol. 54
ensuring adequate conditions for cell transition to the
elongation stage. An elevated mobility of water molecules in the meristem at higher td compared to other
root zones could also result from larger contribution of
the symplastic route to water flows. Data presented by
Hukin et al. [25] support this assumption and provide
evidence for the effective symplastic communications
between cells near the apex of maize root (3-mm region
from the apex) and for gradual loss of such communications in distant regions (5 and 20 mm from the root
apex).
A considerable decrease in Def upon the increase in
the diffusion time was noted for zone III. This could be
due to the formation in this zone of additional barriers
for water movements, such as the endoderm with developed Casparian strips and suberized cell walls, and,
possibly, the exoderm. Young roots of maize seedlings
grown in hydroponic culture usually contain no exoderm but develop it under aeroponics conditions [37,
38]. In our experiments the seedling roots were not
immersed into solution but were placed into wet filter
paper (see conditions of plant growth). Such growth
conditions could favor the formation of exoderm,
which represents a considerable barrier for radial water
transport in the root [1, 4].
Effects of aquaporin blocker HgCl2 on water diffusion were different in various root zones and depended
on the diffusion time td (table). At large td the inhibitory
effect of mercury chloride was revealed in zones II and
III, which was manifested as a large decrease in Def values. The results are consistent with our earlier studies
[26, 27], which showed that water diffusion is sensitive
to membrane permeability changes induced by the
aquaporin blocker. The inhibitory effect of HgCl2 on
Def is presumably attributed to the blocking of waterpermeable membrane pores [18, 30, 31]. According to
these authors, Hg2+ ions interact with free sulfhydryl
groups of proteins engaged in the membrane pore structure and induce closing of water-conducting pores.
A different profile of changes was observed in zone I
cells. Instead of inhibiting the diffusion rate, HgCl2
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IONENKO, ANISIMOV
caused a slight increase in Def (especially at td = 100 ms).
Such an effect of HgCl2 is probably related to specificity of cell responses in the transition zone [29] upon the
action of adverse factors. Ishikawa and Evans [39]
noted “specific” physiological properties of cells in this
zone (the distal part of the elongation zone), which
were often opposite to cell properties in the real elongation zone (for example, water stress induced equivocal
responses in these cells). The increase in water diffusion coefficients after the treatment of zone I with
HgCl2 might also originate from compensatory
increase in water diffusion along the symplastic route.
Other researchers also noticed varying sensitivity of
cell hydraulic conductivity to HgCl2. For example, in
experiments with onion roots [16], in contrast to our
observations, HgCl2 had insignificant influence on root
regions distant from the root tip. The apparent contradiction to our results might be caused by specificity of
plant materials used and by the mismatch of root
regions examined (no measurements were made for the
root apex in [16]). At the same time, Hukin et al.
reported [25] that hydraulic conductivity of maize root
cells became more sensitive to the inhibitor as the distance from the root apex was increased. This phenomenon was explained as the consequence of symplastic
isolation of cells.
Differential effects exerted by HgCl2 in various root
zones provide evidence that dominant pathways for
radial water transport may differ in these root regions.
In the meristem, the symplastic route seems predominant, while in the distant regions above the apex, the
contribution of transmembrane transport increases. The
elevated sensitivity of water flow to HgCl2 inhibition in
the cell elongation zone correlates with the enhanced
activity (gene expression) of aquaporins in this zone
established in some studies [25]. The strongest inhibition of water flow was observed at long diffusion times
td in root regions remote from the apex, where the vacuolar water is the main contributor to the diffusional
decay (the relaxation time of the vacuolar water T1 =
700–800 ms). This finding suggests that the inhibiting
effect of mercury is mainly attributed to its action on
the vacuolar membrane, the tonoplast.
CONCLUSION
During root cell development (i.e., cell transitions
from the meristematic zone to the elongation zone and
differentiated cell zone), the symplastic, apoplastic, and
the transmembrane routes contribute variable fractions
to the radial water transport. The symplastic transport
seems preferential in the root apex, whereas HgCl2-sensitive aquaporin-mediated transmembrane pathway
becomes increasingly important during cell elongation.
Modifications of cell walls in the endoderm (suberin
deposition), which arise at increasing distances from
the root apex and reduce the apoplastic transport, could
account for the retardation of diffusional water transport.
ACKNOWLEDGMENTS
This work was supported by the Russian Foundation
for Basic Research, project no. 04-04-49350.
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