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Plant Physiol, March 2000, Vol. 122, pp. 945-956
Genotypical Differences in Aluminum Resistance of Maize Are
Expressed in the Distal Part of the Transition Zone. Is Reduced
Basipetal Auxin Flow Involved in Inhibition of Root Elongation by
Aluminum?1
Malte
Kollmeier,
Hubert H.
Felle, and
Walter J.
Horst*
Institute of Plant Nutrition, University of Hannover,
Herrenhäuser Strasse 2, D-30419 Hannover, Germany (M.K.,
W.J.H.); and Institute of General Botany and Plant Physiology,
University of Giessen, Senckenbergstrasse 17-21, D-35390 Giessen,
Germany (H.H.F.)
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ABSTRACT |
Short-term Al treatment (90 µM Al at pH 4.5 for 1 h) of the distal transition
zone (DTZ; 1-2 mm from the root tip), which does not contribute
significantly to root elongation, inhibited root elongation in the main
elongation zone (EZ; 2.5-5 mm from the root tip) to the same extent as
treatment of the entire maize (Zea mays) root apex.
Application of Al to the EZ had no effect on root elongation. Higher
genotypical resistance to Al applied to the entire root apex, and
specifically to the DTZ, was expressed by less inhibition of root
elongation, Al accumulation, and Al-induced callose formation,
primarily in the DTZ. A characteristic pH profile along the surface of
the root apex with a maximum of pH 5.3 in the DTZ was demonstrated. Al
application induced a substantial flattening of the pH profile moreso
in the Al-sensitive than in the Al-resistant cultivar. Application of
indole-3-acetic acid to the EZ but not to the meristematic zone
significantly alleviated the inhibition of root elongation induced by
the application of Al to the DTZ. Basipetal transport of exogenously
applied [3H]indole-3-acetic acid to the meristematic zone
was significantly inhibited by Al application to the DTZ in the
Al-sensitive maize cv Lixis. Our results provide evidence that the
primary mechanisms of genotypical differences in Al resistance are
located within the DTZ, and suggest a signaling pathway in the root
apex mediating the Al signal between the DTZ and the EZ through
basipetal auxin transport.
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INTRODUCTION |
The initial effect of Al toxicity is the inhibition of root
elongation, a dramatic effect occurring within minutes after
application. It is generally accepted that the root apex plays the
major role in Al perception and response (for recent reviews, see
Delhaize and Ryan, 1995 ; Horst, 1995 ; Kochian, 1995 ; Taylor, 1995 ;
Rengel, 1996 ). This is well demonstrated by the fact that: (a) Al
accumulation as an indicator of Al sensitivity occurs in the distal
parts of the root apex (Delhaize et al., 1993a ; Llugany et al., 1994 ;
Sivaguru and Horst, 1998 ); (b) Al-resistance mechanisms, such as the
release of Al-complexing organic compounds, are confined mainly
to the root apex (Horst et al., 1982 ; Delhaize et al., 1993b ; Pellet et
al., 1995 ); and (c) callose formation, as a sensitive marker of Al
sensitivity, is induced primarily in apical cells of the outer cortex
(Wissemeier et al., 1987 ; Zhang et al., 1994 ; Wissemeier and Horst,
1995 ; Sivaguru and Horst, 1998 ). However, the question of the primary
target of the Al effect remained open until recently.
Ryan et al. (1993) showed that the root tip was most Al sensitive.
Sivaguru and Horst (1998) presented evidence that the distal transition
zone (DTZ) is the most Al-susceptible zone of the primary root of the
Al-sensitive maize (Zea mays) cv Lixis. Subsequently, Sivaguru et al. (1999a) and Horst et al. (1999) showed that Al leads to
alterations in the organization of microtubules and actin microfilaments, which were most severe in the DTZ. Although it is still
a matter of debate whether Al affects the root symplastically or
apoplastically, evidence increases that the apoplast plays the major
role in Al perception (Horst, 1995 ). Al binds strongly to the cell wall
of root epidermal and cortical cells (Delhaize et al., 1993a ), and
Horst et al. (1999) demonstrated the role of pectin content in
different apical root zones of maize for the Al response. Apart from
negative charge properties of the cell wall and its cation exchange
capacity, the exudation of organic compounds complexing Al (Delhaize et
al., 1993b ; Basu et al., 1994 ; Pellet et al., 1995 ) and the maintenance
of higher apoplastic pH (Degenhardt et al., 1998 ) may play an
additional or even more important role in the response of different
species and genotypes to Al.
In this study we extend our former findings about the spatial
sensitivity of the primary root of maize on genotypical differences between the Al-sensitive maize cv Lixis and the Al-resistant cv ATP-Y.
We paid particular attention to the relationship between root surface
pH and root-growth dynamics as affected by Al. Furthermore, we
considered the role of indole-3-acetic acid (IAA) in Al toxicity, testing the hypothesis that Al might influence basipetal IAA
transport in the root cortex, which is considered to contribute
to the regulation of root growth and development (Hasenstein and Evans,
1988 ; Kerk and Feldman, 1994 ; Ruegger et al., 1997 ).
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MATERIALS AND METHODS |
Plant Material, Growth Conditions, and Experimental Treatments
Seeds of the maize (Zea mays L.) cv ATP-Y, which is
classified as Al resistant, and cv Lixis, which is classified as Al
sensitive by Llugany et al. [1994]; Horst et al. 1997 ), were soaked
in tap water for 8 h. Selected seeds of equal size and shape were
germinated in filter paper rolls moistened with nutrient solution for
3 d in a growth chamber under controlled environment conditions
with 70% relative air humidity, 30°C/28°C day/night temperature, a day/night cycle of 16 h/8 h, and a 300 µm m 2
s 1 photon flux density.
All experiments were conducted with intact plants. Uniform seedlings
with primary root lengths of about 7 to 10 cm were selected for the
experiments. Seedlings were adapted to low pH by stepwise lowering of
pH over 24 h before the beginning of the experiments.
Local Al treatment was provided by agarose blocks containing nutrient
solution and 0.6% (w/v) low-gelling-temperature agarose (Fluka,
Deisenhofen, Germany) (1.2% for the electrophysiological experiments
and measurements of the partial root elongation). The nutrient solution
had the following composition: CaSO4, 250 µM; KNO3, 400 µM;
MgSO4, 100 µM; FeEDDHA, 20 µM; MnSO4, 1 µM; ZnSO4, 0.2 µM;
CuSO4, 0.2 µM;
KH2PO4, 10 µM; H3BO3, 8 µM;
(NH4)6Mo7O24, 0.1 µM; and
NH4NO3, 200 µM (pH 4.3).
For the study on the short-term effects of Al, the treatment duration
was 1 h in all experiments at 30°C temperature in a growth
chamber, except for the electrophysiological experiments, which were
conducted under a 21°C to 23°C ambient temperature. The Al supply
was a 90 µM monomeric Al obtained from an Al atomic spectroscopy standard solution
(AlCl3·6H2O, 1,000 mg L 1, Fluka). To achieve a final monomeric Al
concentration of 90 µM in the agarose gel, 300 µM Al was added to the cooled solution (measured by means
of the aluminon method according to Kerven et al. [1989]; see also
Sivaguru and Horst, 1998 ).
Determination of Callose in 1-mm Root Segments
Al was applied to specific apical root zones using the
polyvinylchloride (PVC) block system previously described by Sivaguru and Horst (1998) . After the Al treatment, 2-cm root tips were fixed in
96% (v/v) ethanol to avoid the formation of wound callose. The
segments were then dissected, blotted dry, and transferred to Eppendorf
cups containing 1 mL of 1 M NaOH. Each sample containing two 1-mm root segments was ultrasonicated (Bandelin Sonopuls, Bandelin
Electronics, Berlin) for 40 s. Subsequently, the cups containing
the samples were heated in an 80°C water bath for 20 min to
solubilize the callose from the disintegrated cell walls, and were then
centrifuged for 12 min at 12,000 min 1 at room
temperature. Callose concentrations in the supernatant were quantified
fluorometrically (Hitachi f2000, Hitachi, Tokyo; excitation at 393 nm
and emission at 484 nm) according to the method described by Kauss
(1989) using aniline blue. The Al-induced callose content was
calculated from the callose content of Al-treated segments minus the
callose content in segments from control roots not treated with Al.
Determination of Al in 1-mm Root Segments
After three brief rinses of the excised root tips in ultrapure
water (18.3 M , E-pure, D4642, Barnstead, Dubuque, IA), individual 1-mm root segments were dissected under ultrapure water from fresh root
tips within 30 min after the Al treatment period. The root segments
were placed into Eppendorf cups (two segments each) containing 500 µL
of ultrapure water, frozen, and kept at 20°C until analysis. For
the Al analysis the samples were transferred into 10-mL Teflon cups,
and the ultrapure water was evaporated in a heating block at 120°C.
The samples were dissolved in 1 mL of ultrapure concentrated HNO3 and wet oxidized at 190°C until the acid
had completely evaporated. The ash was dissolved in 500 µL of
ultrapure HNO3 (1:30 in ultrapure water). The
samples were analyzed for Al using a graphite furnace atomic absorption
spectrometer (UNICAM 939 QZ, Analytical Technology, Cambridge, UK) with
Zeeman background compensation. Instrumental adjustments were optimized
for the highest sensitivity. The Al contents of Al-treated root
segments were corrected for mean Al contents from blanks and root
segments not treated with Al (control).
Electrophysiology
A modified electrophysiological setup was used (Peters and Felle,
1999 ). It was turned by an angle of 90°, allowing undisturbed positive gravitropism of the root. The seedling itself remained intact.
The electrical setup for the fabrication and application of
ion-sensitive microelectrodes has been described by Felle and Bertl
(1986) and Felle (1994 , 1998 ). pH-selective micropipettes were pulled
on a Getra instrument (vertical) from borosilicate tubing with solid
filament (Hilgenberg, Malsfeld, Germany). Tip diameters were 3 to 4 µm. The tips were blunt and heat-polished. Before filling, the
micropipette (apical 4 cm) was bent in a 30° angle, allowing
measurement in the modified setup. To give the ion-sensitive sensor in
the tip sufficient firmness to stay in place for repeated use, the
cocktail (Fluka) was dissolved in a mixture of 40 mg of PVC per mL of
tetrahydrofuran (THF) at a ratio of 30:70 (v/v). After evaporation of
the THF, the remaining firm gel was topped with the undiluted sensor
cocktail, followed by the reference solution (0.5 M KCl and
1 mM 2-([N-morpholino])-ethanesulfonic acid [MES], pH
6.0).
The micropipettes were connected through a Ag/AgCl half-cell to a
high-impedance amplifier (FD 223, World Precision Instruments, Sarasota, FL). Signals were recorded on a chart recorder (L
2200, Linseis, Selb, Germany). Experiments were carried out under
constant perfusion (1 mL min 1) in a specially
designed plexiglass chamber at room temperature (22°C 23°C). The
measurement solution consisted of distilled water containing 200 µM each of CaCl2 and KCl, and 1 mM MES. The pH was adjusted to 4.5. The pH profiles were
measured at a distance of 20 µm from the root surface and in 200-µm
intervals for the first 5 apical mm. Control measurements were carried
out 15 min after the roots had been attached to the measurement
cuvette. Only roots showing the specific basic pH profile were selected for further experiments. The Al treatment lasted 60 min at a
concentration of 90 µM. Either the whole root or specific
1-mm root zones were treated with Al using a specially designed
adjustable agarose block in plexiglass that was movable along the root
in the plexiglass cuvette.
Partial Elongation of 1-mm Root Zones
The experimental setup for the electrophysiological experiments
allowed simultaneous measurement of pH profiles and elongation growth
of specific 1-mm root zones. Before the seedlings were attached to the
measurement cuvette the root was marked with ink (Bruynzeel Permanent
fine, Bruynzeel, The Netherlands) dots in 1-mm intervals. The distances
between the dots and the width of the dots were measured at the
beginning and during the course of the experiment, and then the
elongation rate of the specific root zone was calculated. The ink used
did not detach during the course of the experiment and did not affect
root elongation or disturb the pH measurements, as confirmed in
preliminary experiments. The precision of the measurements was 20 µm
at a 64-fold magnification against a scale. Due to the vertical setup
of the measurement cuvette, root bending did not occur.
Exogenous Application of IAA and Determination of Root Elongation
Rate
The setup for the determination of the effect of exogenous IAA
application on Al-induced inhibition of root growth was a modification of the PVC block system described by Sivaguru and Horst (1998) for the
specific purposes of the experiments conducted. This included a
smoothly moveable tray on which the PVC plates to which the plants were
attached could be moved along the binocular (20-fold magnification;
Stemi SV8, Zeiss, Oberkochen, Germany). Gravity-induced curvature did
not complicate the measurements due to the vertical attachment of the
seedlings to the PVC plates. Ninety micromolar monomeric Al or 10 µM of the IAA transport inhibitor 2,3,5-triiodobenzoic acid (TIBA) was applied via agarose blocks to the 1- to 2-mm apical root zone, while agarose blocks (1.2% [w/v] agarose)
containing nutrient solution and 10 7
M IAA were positioned either around the meristematic zone
(MZ) (0-1 mm) or the main elongation zone (EZ) (2.5-3.5 mm). This IAA concentration has been selected as most enhancing root elongation from
a range of preliminary experiments in which IAA concentrations have
been varied from 10 9 to
10 3 M (data not shown).
Exogenous Application of [3H]IAA and Localization in
Specific Root Segments
Al (90 µM monomeric) or 10 µM of the
IAA transport inhibitors TIBA or N-1-naphthylphthalamic acid
(NPA) was applied to the DTZ of primary roots of intact plants in the
PVC system as described before. [3H]IAA (777 GBq/mmol, Amersham Pharmacia Biotech, Freiburg, Germany) was applied to
the MZ in 64-µL agarose blocks (1.2% [w/v] with nutrient
solution) for 30 min. Then, 2 × 10 8
M tritiated IAA was mixed with untritiated IAA
(Sigma, Deisenhofen, Germany) to reach a final IAA
concentration of 10 7 M.
After application, the roots were carefully removed from the system and
rinsed in distilled water for 3 s from the base to the tip.
Afterward, the segments were cut and frozen in 4 mL of distilled water
in separate scintillation vials overnight. After reaching room
temperature again, 8 mL of scintillation cocktail (Lumasafe Plus, Lumac
LSC B.V., Groningen, The Netherlands) was added. Radioactivity was
determined in a liquid scintillation counter (RackBeta 1217, LKB Wallac
OY, Turku, Finland) allowing 10 min of integration time per specimen.
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RESULTS |
Effect of Al on Root Growth
When Al was applied to the entire root apex, the root-elongation
rate was significantly inhibited in both cultivars (Fig. 1). However, growth inhibition was more
severe in cv Lixis (44.4%) than in cv ATP-Y (18.2%), reflecting the
greater Al resistance of cv ATP-Y. Al treatment of the 1- to 2-mm
apical root zone (the DTZ) led to a slightly stronger inhibition of
root elongation than the treatment of the whole root apex (cv Lixis:
55.5%; cv ATP-Y: 27.3%). Furthermore, the genotypical differences in
Al resistance were maintained. Al treatment of the 0- to 1-mm root zone
significantly reduced root elongation only in the Al-sensitive cv
Lixis; treatment of the 2.5- to 3.5-mm root zone did not affect root
elongation in either cultivar.

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Figure 1.
Effect of Al application (90 µM
Almono in 0.6% [w/v] agarose gel) for 1 h to
the entire root apex or to specific 1-mm root segments on the root
elongation rate of primary roots of the maize cv ATP-Y (Al-resistant)
and cv Lixis (Al-sensitive). Values are means of five independent
replicates ± SD. The results shown are representative
of three independent experiments. Different letters indicate
significant differences at P < 0.05 (Tukey's
test). White bars, 0 µM Al; black bars, 90 µM Al.
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Effect of Local Al Application on Al Content and Callose
Formation
The particular Al sensitivity of the 1- to 2-mm apical root zone
and the higher Al sensitivity of cv Lixis compared with cv ATP-Y was
related to significantly higher Al accumulation (Fig. 2) and Al-induced callose formation (Fig.
3) when Al was applied to this apical
root zone. Al application to the 0- to 1-mm zone also led to enhanced
Al accumulation and callose formation; however, the cultivars did not
differ significantly. Al application to the more basal root zones only
led to slight or no increases in Al and callose contents, respectively.

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Figure 2.
Al contents of specific 1-mm segments of the
primary root apex of the Al-sensitive maize cv Lixis ( ) and the
Al-resistant cv ATP-Y ( ). Ninety micromolar Almono was
applied for 1 h in agarose gel to specific 1-mm root zones, as
indicated by arrows. Values are means of three independent
replicates ± SD. The results shown are representative
of two independent experiments. Stars indicate significant genotypical
differences at P < 0.05 (Tukey's test).
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Figure 3.
Al-induced callose formation in specific 1-mm
segments of the primary root apex of the Al-sensitive maize cv Lixis
( ) and the Al-resistant cv ATP-Y ( ). Ninety micromolar
Almono was applied for 1 h in agarose gel to specific
1-mm root zones, as indicated by arrows. Values are means of five
independent replicates ± SD. The results shown are
representative of three independent experiments. Stars indicate
significant genotypical differences at P < 0.05 (Tukey's test).
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Effect of Al on Partial Elongation of Specific 1-mm Root Zones
For the measurement of the effect of Al application to the entire
root apex or to individual 1-mm root zones on the partial elongation
rate of individual apical root zones, a specially developed cuvette was
used, which also allowed the simultaneous measurement of pH profiles
along the root apex. In both maize cultivars the main EZ was 2.5 to 5 mm behind the root apex (Fig. 4). When Al was applied to the entire root apex, root elongation was inhibited over
the entire EZ. The higher Al resistance of cv ATP-Y was expressed as a
less-severe inhibition over the entire zone. The application of Al only
to the 1- to 2-mm apical root zone, a zone that only slightly
contributes to root elongation, produced the same inhibition of root
elongation. The genotypical differences in Al sensitivity were
similarly expressed. Application of Al to the 0- to 1-mm and the 2.5- to 3.5-mm root zones induced significantly less or no inhibition of
root elongation, respectively.

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Figure 4.
Effect of Al supply (90 µM
Almono, 1 h) to the entire root apex or specific 1-mm
apical root zones on partial elongation rates of apical 1-mm root
segments of the primary roots of the maize cv ATP-Y (Al-resistant) and
cv Lixis (Al-sensitive). Values are means of five independent
measurements ± SD. The results shown are
representative of two independent experiments. Different letters
indicate significant differences at P < 0.05 (Tukey's test). , Control (Al); 0 to 1 mm zone; , 1 to 2 mm
zone; , 2.5 to 3.5 mm zone; , entire apex.
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Effect of Al on the pH Profile along the Root Surface
Roots of both maize cultivars growing in the absence of Al at pH
4.5 in the bulk solution developed a typical and stable pH profile at
the root surface along the 5-mm root apex (Fig.
5). The pH increased steeply, from 4.8 at
the root tip to about 5.3 at a 1-mm distance from the tip, dropped to
the bulk solution pH at 3 mm from the tip, and then rose again to pH
4.7 in the 4- to 5-mm zone. Al application for only 15 min induced a
substantial flattening of the pH profile in both cultivars. Longer Al
treatment increased this effect only in the Al-sensitive cv Lixis. The
application of Al to the 1- to 2-mm apical root zone induced a similar
flattening of the pH profile along the root apex (Fig.
6). The flattening was more pronounced in
cv Lixis, especially in the 1- to 2-mm root zone. Application of Al to
the 0- to 1-mm or the 2.5- to 3.5-mm zones did not affect the pH
profiles in either cultivar.

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Figure 5.
Effect of Al application to the entire root apex
on the root surface (distance 20 µm) pH profiles along the primary
root of the maize cv ATP-Y (Al-resistant) and cv Lixis (Al-sensitive).
Ninety micromolar Almono was supplied in a solution
containing KCl and CaCl2 at 200 µM each for
15 ( ), 30 ( ), and 60 ( ) min. , Control ( Al) The bulk
solution pH was adjusted to 4.5. The values are means of three
independent replicates ± SD. The results shown are
representative of three independent experiments.
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Figure 6.
Effect of Al application (90 µM
Almono in agarose gel) for 1 h to specific root zones
on the root surface (distance 20 µm) pH profiles along the primary
roots of the maize cv ATP-Y ( ; Al-resistant) and cv Lixis ( ;
Al-sensitive). The pH of the bulk solution containing KCl and
CaCl2 at 200 µM was adjusted to 4.5. Values
are means of three independent replicates ± SD. The
results shown are representative of three independent experiments. The
shaded areas indicate the zone of Al application.
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Effect of Exogenous IAA Application on Al-Induced Inhibition of
Root Growth
Application of IAA to the 0- to 1-mm MZ as well as to the 2.5- to
3.5-mm EZ significantly enhanced root elongation in both maize
cultivars (Fig. 7A). Al applied to the 1- to 2-mm zone (the DTZ) reduced the root elongation rate in cv Lixis
significantly more than in cv ATP-Y, as shown above. When IAA was
applied to the MZ of Al-treated roots, absolute root elongation was
significantly enhanced only in the Al-resistant cv ATP-Y. Root
elongation relative to the IAA-treated control without Al was not
significantly affected in either cultivar (Table
I). However, when IAA was applied to the
EZ, Al-induced inhibition of root elongation was significantly reduced
(Fig. 7B, Table I). TIBA treatment of the DTZ led to an inhibition of
root elongation comparable to that caused by Al in both cultivars (Fig.
7, Table I). Genotypical differences did not occur. The TIBA effect
could be compensated significantly in both cultivars by IAA application
to the EZ.

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Figure 7.
Effect of exogenous IAA supply (0.1 µM in 1.2% [w/v] agarose blocks containing
nutrient solution) for 1 h to different apical root zones (A, MZ
0-1 mm; B, EZ 2.5-3.5 mm) on Al-induced inhibition of elongation of
primary roots of the maize cv ATP-Y (Al-resistant) and cv Lixis
(Al-sensitive). Ninety micromolar monomeric Al (gray bars) or 10 µM TIBA (black bars) in 0.6% (w/v) agarose gel
was applied to the 1-to 2-mm root zone (DTZ). White bars, Control
( Al). Values are means of five independent replicates ± SD. The results shown are representative of three
independent experiments. Different letters indicate significant
differences at P < 0.05 (Tukey's test).
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Table I.
Effect of exogenous application of 10 7
M IAA in agarose blocks to the apical root zones MZ (0-1
mm) or EZ (2.5-3.5 mm) on inhibition of root elongation induced by
application of 90 µM monomeric AI or 10 µM
TIBA to the DTZ (1-2 mm) relative to control roots treated only with
nutrient solution in agarose blocks
Values are the means of five independent replicates ± SD. Different letters indicate significant differences at
P < 0.05 (Tukey test).
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Effect of Al on Uptake and Distribution of [3H]IAA
Within 30 min of treatment, basipetal
[3H]IAA transport did not go beyond the first
10 mm of the root apex in either cultivar. The application of either
TIBA or NPA to the DTZ led to a significant decrease in basipetal
transport of [3H]IAA. Total (Fig.
8) and relative contents (Fig.
9) in the EZ (2-5 mm) were significantly
lower than in the nontreated control roots. In contrast to the EZ, in
the MZ and DTZ (0-2 mm), [3H]IAA contents
consistently accumulated. Roots treated with Al showed effects similar
to those treated with the IAA transport inhibitors: accumulation in
more apical root zones and lower contents of
[3H]IAA in the EZ especially in the
Al-sensitive cultivar. The effects of Al and IAA transport inhibitors
applied to the DTZ on basipetal [3H]IAA
transport from the MZ to the EZ are illustrated in Figure 9.

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Figure 8.
Effect of Al on uptake and basipetal distribution
of [3H]IAA in the apex of primary roots of the maize cv
ATP-Y (Al-resistant) and cv Lixis (Al-sensitive). Application of 90 µM monomeric Al, 10 µM NPA, or 10 µM TIBA in nutrient solution, pH 4.3, in 0.6%
(w/v) agarose gel to the DTZ for 30 min. Control roots were
treated only with nutrient solution in agarose blocks, pH 4.3. [3H]IAA (0.1 µM in 1.2% [w/v]
agarose blocks containing nutrient solution) was applied to the MZ for
30 min. Values are means of five independent replicates ± SD. The results shown are representative of three
independent experiments. Different letters indicate significant
differences at P < 0.05 (Tukey's test).
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Figure 9.
Effect of Al on [3H]IAA
distribution relative to entire IAA uptake into the apex of primary
roots of the maize cv ATP-Y (Al-resistant) and cv Lixis (Al-sensitive).
Application of 90 µM monomeric Al, 10 µM
NPA, or 10 µM TIBA in nutrient solution, pH 4.3, in 0.6%
(w/v) agarose gel to the DTZ for 30 min. Control roots were
treated only with nutrient solution in agarose blocks, pH 4.3. [3H]IAA (0.1 µM in 1.2% [w/v]
agarose blocks containing nutrient solution) was applied to the MZ for
30 min. Values are means of five independent replicates ± SD. The results shown are representative of three
independent experiments. Different letters indicate significant
differences at P < 0.05 (Tukey test).
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DISCUSSION |
The setup for the determination of partial elongation of specific
1-mm root zones revealed that the main EZ is located within 2.5 to 5 mm
from the root tip, with a maximum at 4 mm (Fig. 4), thus confirming the
findings of Pilet et al. (1983) , Collings et al. (1992) , Evans and
Ishikawa (1997) , and Blancaflor et al. (1998) . The 1- to 2-mm zone
contributed only very little to root elongation, so it appears
justified to classify this zone as DTZ. In this root zone, cells are
changing their mitotic mode and undergo a preparatory phase for rapid
elongation (Balu ka et al., 1996 ). This zone is most responsive
to a variety of environmental stimuli such as gravitropism and auxin
(Meuwly and Pilet, 1991 ; Ishikawa and Evans, 1993 ), as well as
thigmomorphism (Ishikawa and Evans, 1990 ).
In the present study we confirmed our previous results (Sivaguru and
Horst, 1998 ; Sivaguru et al., 1999a ) and verify and substantiate that
the DTZ is the most Al-sensitive apical root zone in maize. Application
of Al to the DTZ inhibited root elongation similarly to Al application
to the whole root apex. The application of Al to the 0- to 1-mm root
zone (the MZ) was significantly less inhibitory, and application to the
adjacent EZ (2.5-3.5 mm from the root tip) was not inhibitory at all
(Figs. 1 and 4). The lower Al sensitivity of the MZ may be due to
protection of the MZ through root-cap mucilage, which strongly binds Al
(Archambault et al., 1996 ), thus protecting the MZ from Al injury
(Horst et al., 1982 ). The low Al sensitivity of the EZ is not yet
understood, but appears to be in agreement with the much lower Al
sensitivity of stationary phase compared with log phase cells (Sivaguru
et al., 1999b ).
The cultivar differences in Al resistance were only clearly expressed
when Al was applied to either the whole root apex or to the DTZ (Figs.
1 and 4), clearly indicating that this root zone plays an outstanding
role in the expression of Al toxicity and Al resistance mechanisms in
maize roots.
The high Al sensitivity of the DTZ and genotypical differences in Al
sensitivity were characterized by higher Al accumulation and Al-induced
callose formation (Figs. 2 and 3). This is in agreement with results
showing a positive relationship between Al sensitivity and Al
accumulation in root tips (Rin on and Gonzales, 1992 ; Delhaize et
al., 1993a ; Llugany et al., 1994 ) and Al-induced callose formation
(Wissemeier et al., 1987 ; Zhang et al., 1994 ; Horst et al., 1997 ). Our
results are consistent with the view that Al resistance requires
exclusion of Al from the apoplast and Al sensitivity is due to enhanced
binding of Al to Al-sensitive binding sites of the apoplast (Blamey et
al., 1992 ; Grauer and Horst, 1992 ; Horst et al., 1997 ).
Externally applied Al rapidly binds to the cell walls of root cells
(Zhang and Taylor, 1989 ; Blamey et al., 1990 ; Delhaize et al., 1993a ),
where the main binding sites are the negative charges on carboxylic
groups of the pectic matrix. These charges yield an electrical
potential gradient determining binding and distribution of ions in the
apoplast (Kinraide, 1993 ). Horst et al. (1999) showed that the spatial
Al sensitivity of the root apex is positively correlated with the
pectin contents of the root zones, with the exception of the MZ, but
those results might have been due to contamination of the MZ with
mucilage. The role of pectin content and its degree of methylation
(and, thus, negative charge) on Al toxicity and resistance were further
confirmed by N. Schmohl and W.J. Horst (unpublished results). Binding
of Al may lead to impairment of the physical properties of the cell wall, leading to changes in extensibility and permeability (Blamey et
al., 1993 ; Pritchard, 1994 ). It may also lead to mechanical stress,
which could transduce a signal to the cytoskeleton via transmembrane
proteins assumed to connect the cell wall and cytoskeleton (Nick,
1999 ), inducing severe disintegration of the microtubule and actin
network (Blancaflor et al., 1998 ; Horst et al., 1999 ; Sivaguru et al.,
1999a ).
Our results do not support the recently expressed view that Al
accumulation in root tip vacuoles is a major mechanism of Al resistance
(Vázquez et al., 1999 ). However, we do not exclude the
possibility that longer-term adaptation to Al supply will also require
such a tolerance mechanism. However, in a normally growing root (2 mm
h 1), the cells within the DTZ will not be
exposed to Al for more than 1 h.
Cell wall pH is difficult to measure directly (Degenhardt et al., 1998 ;
Peters et al., 1998 ), so it has been frequently calculated indirectly
from pH changes in the incubation medium. However, these measurements
cannot be expected to yield results that can be directly referred to as
cell wall or apoplastic pH (Peters et al., 1998 , and refs. therein).
Using ion-sensitive microelectrodes, as proposed by Felle and Bertl
(1986) and Felle (1994 , 1998 ), we measured root surface pH directly in
the 20-µm distance from the surface and related it to root growth in
specific zones of the primary root. The pH profile we found is in
agreement with the findings of Pilet et al. (1983) , Collings et al.
(1992) , and Felle (1998) in the maize root apoplast and is consistent
for both cultivars. It is particularly remarkable, however, that the roots seem to be capable of maintaining this pattern within a vast
range of bulk solution pH from 7.9 (Felle, 1998 ) over 6.8 (Pilet et
al., 1983 ) to 4.5 (our results). The finding that the roots maintained
this pH profile even after 24 h of adaptation to low pH shows that
it is not a transient effect due to seedling manipulation in the
experimental setup. Effects of gravistimulation were also excluded by
the vertical setup. It is of particular interest that the maize root is
capable of either acidifying or alkalizing specific root zones
depending on the pH of the surrounding medium, because the root
response involved must therefore be understood as a powerful adaptation
mechanism to transient changes in medium pH. This view is in agreement
with findings by Yan et al. (1998) showing that maize roots are capable
of coping with extremely low external pH if carefully adapted.
Miyasaka et al. (1989) , Ryan et al. (1992) , and Collings et al. (1992)
explained the pH pattern along the rhizoplane as resulting from
endogenous ionic currents traversing the root tip. Collings et al.
(1992) discussed the role of the currents observed in transducing the
gravitropic stimulus from the root cap to the EZ. By removing K+, Na+,
Ca2+, or Cl ions from the
bathing solution or by applying the Ca2+ channel
blocker lanthanum, they could demonstrate that the currents measured
were primarily composed of protons, a finding that is in accordance
with Ryan et al. (1992) . Ca2+ influx and
Cl efflux contribute to these currents to a
lesser extent (Iwabuchi et al., 1989 ; Ryan et al., 1992 ).
At pH 4.5, an increase in rhizosphere pH of 0.1 to 0.2 units leads to
considerable decrease of phytotoxic Al3+ activity
(Martell and Motekaitis, 1989 ; Kinraide, 1991 ), and the
capability of roots to increase rhizosphere pH has been suggested as a
possible mechanism of Al resistance (Miyasaka et al., 1989 ; Degenhardt
et al., 1998 ). This is difficult to reconcile with the particularly
high Al uptake and Al sensitivity of the DTZ and the highest pH at the
root surface observed in this study (Figs. 2 and 5). Rather, it appears
that the pH increase primarily led to less competition of
Al3+ with H+ for apoplastic
binding sites, thus enhancing Al toxicity, as suggested by Grauer and
Horst (1992) and Kinraide (1993) . In this context it is important to
consider that Al application to the entire root apex or specifically to
the DTZ led to a flattening of the alkalization peak (1-2 mm) in both
cultivars after 15 min of application and remained relatively constant
for the succeeding 45 min. This may explain why in the presence of Al,
the pH increase in the DTZ was not sufficient to inactivate
Al3+ especially in the Al-sensitive cultivar,
where Al application led to a greater flattening of the pH peak in the
DTZ than in the Al-resistant cultivar. However, we believe that the
genotypical differences are the consequence rather than the cause for
the differences in Al resistance, a conclusion shared by Miyasaka et
al. (1989) after measuring ion fluxes with lower spatial resolution in
the rhizosphere of two wheat cultivars differing in Al resistance.
The alkalization peak in the DTZ may be due to: (a) enhanced anion
uptake, e.g. an H+/anion symport, which is in
agreement with the findings of Collings et al. (1992) and Ryan et al.
(1992) comparing two wheat cultivars differing in Al resistance; (b)
enhanced respiration and thus bicarbonate production; and (c) enhanced
release of organic acid anions, which at the low ambient pH in the
apoplast will bind free protons. However, the release of organic anions
appears unlikely to account for alkalization in the Al-sensitive
cultivar, because it is well established that this will lead to Al
resistance through complexation, as shown for malate in wheat (Delhaize
et al., 1993b ; Basu et al., 1994 ; Ryan et al., 1995a , 1995b ), citrate
in maize (Pellet et al., 1995 ), and oxalate in buckwheat (Zheng et al., 1998 ).
The capacity of the Al-resistant cultivar to better maintain the
alkalization peak in the DTZ may be explained by two factors: (a) the
physiological properties for maintenance of ionic currents are less
affected by Al in the Al-resistant than in the Al-sensitive cultivar
(Miyasaka et al., 1989 ) or (b) an Al exclusion mechanism is switched on
in the Al-resistant cultivar promoting release of organic acid anions.
They might bind free protons in the rhizosphere and hence lead to an
increase in surface pH. At the prevailing cytoplasmic pH (>7.0) both
malate and citrate are mainly present in dissociated form as anions.
Since the external concentration of these anions is much lower and
because of the negative membrane potential, transport of these anions
into the external solution is a thermodynamically passive process along
a steep electrochemical gradient. Hence, gating of anion channels
permeable for these anions would allow considerable efflux within a
short time (Schmidt and Schroeder, 1994 ; Papernik and Kochian, 1997 ;
Ryan et al., 1997 ). Even though there is agreement about the role of
adequate cell wall pH in root elongation (Rayle and Cleland, 1992 ;
Zieschang et al., 1993 ; Kutschera, 1994 ; Felle, 1998 ), a causal
relation between the changes in pH profile observed and Al-induced
inhibition of root growth remains a matter of debate (Ryan et al.,
1992 ).
The finding that Al applied to the DTZ, which does not contribute
significantly to root elongation, severely inhibits cell elongation in
the EZ not in contact with Al (Fig. 4) strongly suggests a signaling
pathway mediating the Al signal between DTZ and EZ. It is clearly
established that coordinated auxin transport is involved in the
regulation of root growth, morphology, and the gravitropic growth
response (Hasenstein and Evans, 1988 ; Kaufmann et al., 1995 ; Evans and
Ishikawa, 1997 ; Ruegger et al., 1997 ; Müller et al., 1998 ). Auxin
is transported from auxin-synthesizing shoot tissues via the phloem
toward the root apical meristems, where it is proposed to be unloaded
from the central stele into cortical and epidermal cells and then
translocated basipetally to the EZ (Hasenstein and Evans, 1988 ;
Estelle, 1998 ). Inhibition of basipetal auxin flow has been implicated
in severe effects on root growth and morphology. These include swelling
of root tips through uncontrolled periclinal divisions (Blancaflor and Hasenstein, 1995 ; Ruegger et al., 1997 ) as a consequence of auxin accumulation in the MZ and DTZ and suppression of the gravitropic response (Müller et al., 1998 ; Hasenstein et al., 1999 ) due to insufficient auxin accumulation and thus growth inhibition on the lower
side of the bending root.
Similar effects on growth and morphological changes have been reported
in Al-treated roots (Blancaflor et al., 1998 ; Sivaguru et al., 1999a ).
Although Hasenstein and Evans (1988) clearly demonstrated inhibition of
basipetal transport of [3H]IAA in maize roots
by Al, the implications of these results in the understanding of Al
rhizotoxicity have not been followed up on to date. The results
presented in this study confirm those findings by showing that local
application of Al, as well as TIBA or NPA, to the DTZ led to reduced
[3H]IAA contents in the EZ, while contents
relative to control roots were elevated in the MZ/DTZ (Figs. 8 and 9).
The involvement of Al/auxin transport interaction in the expression of
Al-induced inhibition of root elongation is further substantiated by
the result that exogenous application of IAA in root-growth-stimulating doses to the EZ alleviated inhibition of root elongation caused by Al
or TIBA applied to the DTZ (Fig. 7; Table I). The stronger inhibition
of [3H]IAA transport by Al in the Al-sensitive
compared with the Al-resistant cultivar supports this assumption.
Although the results presented here suggest an involvement of
auxin-transport inhibition in the expression of Al toxicity, the
mechanism by which Al affects root apical basipetal IAA transport needs
to be further elucidated.
In conclusion, the results shown convey substantial evidence that the
DTZ of the maize primary root plays an outstanding role in the Al
response, and that the primary mechanisms of genotypical differences in
Al resistance are located within the DTZ. Furthermore, they provide
circumstantial evidence for the existence of a signaling pathway in the
root apex mediating the Al signal between DTZ and EZ through
alterations in basipetal auxin transport. The nec-essary elucidation of
the physiological processes responsible for Al sensitivity and for
genotypical differences in Al resistance of the DTZ and of the Al
signal is the subject of our ongoing research.
 |
ACKNOWLEDGMENTS |
The maize cv Lixis was kindly donated by Force Limagrain
(Montpellier, France), and cv ATP-Y by Dr. Charles Thé
(Institut de la Recherche Agronomique pour le Development, Cameroon).
We also thank R diger Sachse (Zentrum für Strahlenschutz
and Radioökologie, Hannover, Germany) for his assistance on the
Wallac RackBeta.
 |
FOOTNOTES |
Received July 27, 1999; accepted November 9, 1999.
1
This work was supported by the Deutsche
Forschungsgemeinschaft within the Special Research Program 717 ("The
Apoplast of Higher Plants").
*
Corresponding author; e-mail
horst{at}mbox.pflern.uni-hannover.de; fax 49-511-762-3611.
 |
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Overexpression of an auxilin-like gene (F9E10.5) can suppress Al uptake in roots of Arabidopsis
J. Exp. Bot.,
February 1, 2007;
58(3):
497 - 506.
[Abstract]
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P. Illes, M. Schlicht, J. Pavlovkin, I. Lichtscheidl, F. Baluska, and M. Ovecka
Aluminium toxicity in plants: internalization of aluminium into cells of the transition zone in Arabidopsis root apices related to changes in plasma membrane potential, endosomal behaviour, and nitric oxide production
J. Exp. Bot.,
December 1, 2006;
57(15):
4201 - 4213.
[Abstract]
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A Stass, Y Wang, D Eticha, and W. Horst
Aluminium rhizotoxicity in maize grown in solutions with Al3+ or Al(OH)4- as predominant solution Al species
J. Exp. Bot.,
December 1, 2006;
57(15):
4033 - 4042.
[Abstract]
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T. B. Kinraide, D. R. Parker, and R. W. Zobel
Organic acid secretion as a mechanism of aluminium resistance: a model incorporating the root cortex, epidermis, and the external unstirred layer
J. Exp. Bot.,
July 1, 2005;
56(417):
1853 - 1865.
[Abstract]
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S. Doncheva, M. Amenos, C. Poschenrieder, and J. Barcelo
Root cell patterning: a primary target for aluminium toxicity in maize
J. Exp. Bot.,
April 1, 2005;
56(414):
1213 - 1220.
[Abstract]
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Y. Wang, A. Stass, and W. J. Horst
Apoplastic Binding of Aluminum Is Involved in Silicon-Induced Amelioration of Aluminum Toxicity in Maize
Plant Physiology,
November 1, 2004;
136(3):
3762 - 3770.
[Abstract]
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V. Ermolayev, W. Weschke, and R. Manteuffel
Comparison of Al-induced gene expression in sensitive and tolerant soybean cultivars
J. Exp. Bot.,
December 1, 2003;
54(393):
2745 - 2756.
[Abstract]
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S. J. Ahn, M. Sivaguru, G. C. Chung, Z. Rengel, and H. Matsumoto
Aluminium-induced growth inhibition is associated with impaired efflux and influx of H+ across the plasma membrane in root apices of squash (Cucurbita pepo)
J. Exp. Bot.,
September 1, 2002;
53(376):
1959 - 1966.
[Abstract]
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M. A. Pineros, J. V. Magalhaes, V. M. Carvalho Alves, and L. V. Kochian
The Physiology and Biophysics of an Aluminum Tolerance Mechanism Based on Root Citrate Exudation in Maize
Plant Physiology,
July 1, 2002;
129(3):
1194 - 1206.
[Abstract]
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M. Kollmeier, P. Dietrich, C. S. Bauer, W. J. Horst, and R. Hedrich
Aluminum Activates a Citrate-Permeable Anion Channel in the Aluminum-Sensitive Zone of the Maize Root Apex. A Comparison Between an Aluminum- Sensitive and an Aluminum-Resistant Cultivar
Plant Physiology,
May 1, 2001;
126(1):
397 - 410.
[Abstract]
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P. Wenzl, G. M. Patiño, A. L. Chaves, J. E. Mayer, and I. M. Rao
The High Level of Aluminum Resistance in Signalgrass Is Not Associated with Known Mechanisms of External Aluminum Detoxification in Root Apices
Plant Physiology,
March 1, 2001;
125(3):
1473 - 1484.
[Abstract]
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M. Sivaguru, T. Fujiwara, J. Samaj, F. Baluska, Z. Yang, H. Osawa, T. Maeda, T. Mori, D. Volkmann, and H. Matsumoto
Aluminum-Induced 1right-arrow3-beta -D-Glucan Inhibits Cell-to-Cell Trafficking of Molecules through Plasmodesmata. A New Mechanism of Aluminum Toxicity in Plants
Plant Physiology,
November 1, 2000;
124(3):
991 - 1006.
[Abstract]
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