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Plant Physiol, July 2001, Vol. 126, pp. 1055-1060
Role of Auxin-Induced Reactive Oxygen Species in Root
Gravitropism1
Jung Hee
Joo,
Yun Soo
Bae, and
June Seung
Lee*
Center for Cell Signaling Research, Department of Biological
Sciences, Ewha Womans University, Seoul 120-750, South Korea
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ABSTRACT |
We report our studies on root gravitropism indicating that reactive
oxygen species (ROS) may function as a downstream component in
auxin-mediated signal transduction. A transient increase in the
intracellular concentration of ROS in the convex endodermis resulted
from either gravistimulation or unilateral application of auxin to
vertical roots. Root bending was also brought about by unilateral
application of ROS to vertical roots pretreated with the auxin
transport inhibitor N-1-naphthylphthalamic acid. Furthermore, the scavenging of ROS by antioxidants
(N-acetylcysteine, ascorbic acid, and Trolox) inhibited
root gravitropism. These results indicate that the generation of ROS
plays a role in root gravitropism.
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INTRODUCTION |
Since Cholodny (1926) and Went
(1926) discovered that directional auxin transport occurs upon
gravistimulation, the mechanism of auxin transport is well
established. According to the mechanism, the gravitropic stimulation
induces asymmetric auxin movement, and the localized auxin in turn
causes gravitropic curvature (Young et al., 1990; Dolan, 1998; Rosen et
al., 1999). These results indicate that auxin is indeed essential for
gravitropism. Several lines of evidence suggest that the second
messengers, Ca2+ and inositol 1,4,5-triphosphate
(IP3), are involved in root gravitropism (Lee et
al., 1983; Perera et al., 1999). However, the relationship between
auxin and second messengers is still unknown.
Although reactive oxygen species (ROS) such as superoxide anions and
H2O2 are generally
considered to be toxic byproducts of respiration, recent evidence
suggests that the production of ROS might be an integral component of
intracellular signaling (Krieger-Brauer and Kather, 1992; Finkel, 1998;
Rhee et al., 2000). In mammalian cells, a variety of extracellular
stimuli have been shown to induce a transient increase in the
intracellular concentration of ROS, and specific inhibition of the ROS
generation results in a complete blockage of stimulus-dependent
signaling (Sundaresan et al., 1995; Bae et al., 1997). Also, several
lines of evidence suggest that ROS serve as signaling molecules in
plants. It has been shown that ROS mediate systemic signal
networks for plant defense (Chen et al., 1993; Greenberg, 1996;
Pennell and Lamb, 1997; Alvarez et al., 1998). ROS stimulate cell wall
stiffening and apoptosis in infectious regions, preventing the
transmission of infectious particles (Lamb and Dixon, 1997; Delledone
et al., 1998; Potikha et al., 1999; Grant and Loake, 2000). Recent
evidence suggests that the plant hormone abscisic acid-mediated
H2O2 generation and the
H2O2-activated
Ca2+ are important in stomatal closing (Pei et
al., 2000). However, the potential of ROS as a second messenger in root
gravitropism is still unclear. In this report, we reveal the role of
ROS in root gravitropism.
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RESULTS AND DISCUSSION |
Gravity Induces Asymmetric ROS Generation
To verify the role of ROS in plant gravitropism, the generation of
ROS in maize (Zea mays) primary root was investigated
following gravistimulation by placing the root horizontally. Upon
gravistimulation of maize primary root, the intracellular concentration
of ROS, as measured by the oxidation of ferrous ion
(Fe2+) to ferric ion
(Fe3+), increased by 3-fold within 1 h and
then declined to the basal level (Fig.
1A). The portion of the root we refer to
as zone 1 is the apical 4 mm of the root and includes the root cap,
meristem, and the apical half of the root elongation zone. Zone 2 extends from 4 to 8 mm from the root tip and includes the basal half of the elongation zone. ROS appeared in zone 1 of primary roots in response to gravity, whereas there was little change in ROS in zone 2. Longer gravistimulation of the root also led to the accumulation of ROS
in zone 2. As ROS are very diffusible molecules, it is likely that the
accumulation of ROS in zone 2 results from diffusion of ROS into zone 2 from the zone 1. Salicylic acid is a well-known inducer of ROS
production in plants (Chen et al., 1993). However, no difference of ROS
generation in salicylic acid-treated root was detectable between the
zone 1 and zone 2. It is likely that the generation of ROS following
gravistimulation is more specific to zone 1 than to zone 2.
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Figure 1.
Generation of ROS during gravitropism in maize
roots. A, Time course of gravistimulation-induced ROS generation. The
roots were oriented horizontally for the indicated time and then cut
into two parts. Zone 1 (black bars) contains the apical end of root to
0.4 cm, and zone 2 (hatched bars) contains 0.4 to 0.8 cm from root tip.
SA, Salicylic acid-treated maize roots. The segments were subjected to
ROS measurement assay (OXIS, Portland, OR). Values are the
means ± SE for five independent experiments. B,
Asymmetric generation of ROS by gravistimulation. Gravistimulated or
control roots were dissected and stained with a 0.003% (w/v)
dihydrorhodamine-123 solution for 10 min. Fluorescence intensity of
oxidized rhodamine was observed with a fluorescence microscope (Zeiss,
Jena, Germany; excitation = 485 nm, emission = 535 nm). Experiments were repeated at least five times with similar
results.
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Gravistimulation-induced ROS were monitored using the
oxidation-sensitive fluorescent probe dihydrorhodamine-123 and a
fluorescence microscope. Upon gravistimulation of the primary maize
roots, ROS were observed in the lower cortex of the root within 30 min (Fig. 1B). Prolonged gravistimulation of the root also led to the
generation of ROS in the lower and upper cortex. This indicates that
asymmetric production of ROS in the early stages following gravistimulation could play a role in the gravitropic growth response. To test this possibility further, we investigated the effect of exogenous H2O2 on the
gravitropic response. Placing
H2O2-containing agar on the
upper side of the root tips inhibited gravitropic curvature, whereas
placing the agar on the lower side of the root stimulated gravitropic
curvature (Rashotte et al., 2000; Fig. 2A). Furthermore, the asymmetric
application of H2O2 to the
tips of vertical roots induced curvature toward the
H2O2 source (Fig. 2B).
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Figure 2.
Effect of asymmetric application of
H2O2 on root curvature. A,
Induction of curvature in horizontal roots by asymmetric application of
H2O2. Agar (1.5%,
w/v) blocks were immersed into 1 mM
H2O2 in 5 mM
MES buffer [2-(N-morpholino)ethanesulfonic acid, pH 6.8]
and then put on the lower side ( ) or the upper side ( ) of roots
held horizontally.  , Control root showing normal gravitropism.
Values are the means ± SE for five
independent experiments. B, Induction of curvature in vertical roots by
asymmetric application of
H2O2.
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Scavenging of ROS Inhibits Maize Root Gravitropism
We next assessed the effect of N-acetyl-Cys (NAC), an
antioxidant, on the gravitropic response. Scavenging of ROS by
treatment with 1 mM NAC inhibited root
gravitropism (Fig. 3, A and B) without affecting root growth (data not shown). To further strengthen the
evidence that asymmetric generation of ROS may play a role in root
gravitropism, the effects of asymmetric treatment of the root with NAC
were investigated. Placing NAC-containing agar on the upper side of the
root enhanced gravitropic curvature relative to controls, whereas
placing NAC on the lower side of the root impaired gravitropism (Fig.
3C). We investigated the effect of other antioxidants on gravitropism.
Membrane-permeable antioxidants such as 3 mM
ascorbic acid and 100 µM trolox,
pyrrolidinedithiocarbamate have an inhibitory effect on gravitropism
similar to that of NAC (data not shown). However, treatments of the
root with catalase, which cannot permeate the epidermal layer of roots,
had no effect on the inhibition of gravitropism (data not shown). These
results suggest that the ROS are generated inside the cells.
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Figure 3.
Effect of NAC on gravitropic root curvature. A and
B, Suppression of gravitropic curvature by pretreatment with NAC. Roots
were immersed in 1 mM NAC for 2 h and then oriented
horizontally to induce gravitropism.  , Control maize roots; ,
NAC-treated roots. C, Induction of curvature by asymmetric application
of NAC. Agar (1.5%, w/v) block was soaking into 10 mM NAC solution in 5 mM MES buffer (pH 6.8) and
then put on the lower side () or the upper side () of roots held
horizontally. , Control roots, which were subjected to
gravistimulation. Values are the means ± SE for five
independent experiments.
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Auxin-Mediated ROS Generation
It is well established that redistribution of auxin plays an
important role in plant gravitropism (Young et al., 1990; Rashotte et
al., 2000). To test for a possible link between auxin redistribution and generation of ROS in gravistimulated roots, we investigated the
effect of applied auxin on ROS generation in the root tip using
fluorescence microscopy. Placing indole-3-acetic acid (IAA)-containing agar on one side of the root tip stimulated ROS generation in the
treated region (Fig. 4A). We next asked
whether auxin can induce ROS generation in root protoplasts directly
(Sheen, 1990). The generation of ROS by auxin was measured with DCF-DA
and flow cytometry (Bae et al., 1997). Stimulation of the ROS
generation in the protoplasts with auxin resulted in a time-dependent
increase in the intensity of DCF fluorescence, with the maximal
2.5-fold increase within 10 min after stimulation; fluorescence had
returned to the baseline value after 20 min (Fig. 4B). These results
suggest that the redistribution of auxin by gravity induces an increase in the gravitropic curvature in maize root through the generation of
ROS. NPA is an inhibitor of auxin transport inhibitor and is known to
inhibit gravitropism (Rashotte et al., 2000). Therefore, we examined
the effect of NPA on the ability of asymmetric application of
H2O2 to enhance root
gravitropism. NPA-treated roots did not show gravitropism. However,
placing H2O2-contaning agar
on the lower side of NPA-pretreated roots induced curvature toward the site of application (Fig. 4C). These results indicate that the action
of asymmetrically applied
H2O2 in causing root
curvature does not depend upon auxin redistribution, suggesting that
ROS play a role as a downstream component in the auxin-mediated
signaling pathway.
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Figure 4.
Auxin-induced ROS generation. A, Agar blocks
(1.5%, w/v) were incubated in 5 µM IAA in 5 mM MES (pH 6.8) and then placed on the indicated region.
ROS generation was detected by fluorescence microscopy. B, Transient
generation of ROS by auxin. Intracellular ROS generation in protoplast
was measured by 5 µM 2',7'-dichlorofluorescein diacetate
(DCF-DA; Molecular Probes, Eugene, OR) and flow cytometry (FACScan,
Becton-Dickinson, Bedford, NJ). Shaded area means control
fluorescence intensity. Protoplasts were incubated with 5 µM IAA for 5 min (thin line), 10 min (thick line), 20 min
(dashed line), or 30 min (dot line). C, Effect of
N-(1-naphthyl)phthalamic acid (NPA) on ROS-induced
gravitropism. Roots were immersed in 5 µM NPA
in 5 mM MES buffer (pH 6.8) and then
gravistimulated.
H2O2-containing () or
control agar () was then placed on the lower side of roots held
horizontally. Values are the means ± SE for
five independent experiments.
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It is well established that ROS enhance the phosphorylation and
activation of a number of proteins, including mitogen-activated protein
kinase (MAPK), in mammalian and plant cells (Sundaresan et al., 1995;
Bae et al., 1997; Kotvun et al., 2000). Our current results indicate
that gravistimulation elicits a transient increase in intracellular ROS
and a rapid phosphorylation of ZmMAPK5 in maize root (data not shown).
ZmMAPK5 has sequence homology with AtMAPK6 in Arabidopsis, which is
activated by oxidative stress (Kotvun et al., 2000). Furthermore, NAC
pretreatmment of roots abolishes the activation of ZmMAPK5 by
gravistimulation (data not shown).
Based on the work reported here, we propose a novel role of ROS in
plant gravitropism. Gravity induces asymmetric movement of auxin within
60 min, and then the auxin stimulates ROS generation to mediate
gravitropism. Several lines of evidence indicate that calcium (Lee at
al., 1983) and IP3 (Perera et al., 1999) as
second messengers are also involved in the gravitropic response of
roots. Gravitropism stimulated the transient generation of
IP3, which then promoted the opening of an
IP3-induced Ca2+ channel to
increase intracellular Ca2+ (Perera et al.,
1999). Furthermore, asymmetric application of exogenous
Ca2+ caused gravitropic-like curvature of maize
roots. How molecular mechanisms involving ROS and
Ca2+ are integrated into a physiological signal
that leads to the gravitropic curvature remains to be elucidated.
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MATERIALS AND METHODS |
Plant Materials and Growth Conditions
Caryopses of maize (Zea mays L. cv Golden
Cross Bantam) were soaked in distilled water for 12 h before
planting. The grains were placed between wet paper towels held between
opaque trays mounted in a vertical position and germinated at
28°C ± 1°C in the dark. The primary roots of maize were used
2 d after planting (about 2 cm long).
Assay of ROS
The portion of the root we refer to as zone 1 is the apical 4 mm
of the root and includes the root cap, meristem, and the apical half of
the root elongation zone. The portion we refer to as zone 2 extends
from 4 to 8 mm from the root tip and includes the basal half of the
elongation zone. Zone 1 (0-4 mm from root tip) or zone 2 (4-8 mm from
root tip) of the gravistimulated primary roots was homogenized in
distilled water with a pellet disrupter. Supernatants were collected by
microcentrifugation of the extract. Total ROS concentration was
determined by a Bioxytech H2O2-560 assay
kit. This assay is based on the oxidation of ferrous ion (Fe2+) to ferric ion (Fe3+) by ROS under acidic
conditions; the ferric ion binds with indicator dye xylenol
orange to form a stable colored complex, which can be measured
at 560 nm.
Fluorescence Microscope
For the microscopic measurements, gravistimulated or control
roots were bisected longitudinally and stained with 0.003%
(w/v) dihydrorhodamine-123 solution for 10 min. Fluorescence
intensity of oxidized rhodamine was observed with a fluorescence
microscope (Zeiss; excitation = 485 nm, emission = 535 nm;
Potikha et al., 1999). Experiments were repeated at least five times
with similar results. The selected pictures are parts of the
microscopic field, which is representative of the entire field.
Photographs were taken with PIXERA visual communication suite
(version 1.1.0 for Macintosh operating systems, Pixera, Los Gatos, CA).
Determination of Curvature and Elongation of Maize Root
Curvature and elongation were measured using the digital
color camera system (HFG, version 1.1, Yongmacom, Seoul, South
Korea) that connected to the computer for the gravitropism
measurement. Several pretreated or untreated maize seedlings were
mounted in vertical or horizontal position in a clear plastic petri
dish under near saturating humidity. Curvature and elongation were recorded and displayed automatically by a custom software program (picture measurement system, version 1.1, Yongmacom).
Preparation of Maize Root Protoplast
Etiolated maize root protoplasts were a modified method as
described (Sheen, 1990). Protoplasts were isolated from 2-d-old etiolated maize seedlings. Zone1 (0-4 mm from root tip) of the roots
was digested in an enzyme solution containing 2% (w/v) cellulase Onozuka RS (Yakult Pharmaceutical Company, Tokyo), 2% (w/v)
Cellulysin (Calbiochem/Behring Diagnostic, La Jolla, CA), 0.026% (w/v)
pectolyase Y23 (Sigma, St. Louis), 0.6 M mannitol, 10 mM MES (pH 5.7), 1 mM CaCl2, 1 mM MgCl2, 10 mM
 -mercaptoethanol, and 0.1% (w/v) bovine albumin (Sigma) for 5 h at 22°C. Protoplasts were separated from the partially digested
tissues by passage through a mesh. The protoplast was washed three
times with solution of 0.45 M mannitol and 1 mM
CaCl2 and stored in the dark.
Flow Cytometry
Protoplasts were incubated with 5 µM auxin. After
various incubation times, cells were loaded with 5 µM
DCF-DA (Molecular Probes). This compound is converted by intracellular
esterases to 2',7'-dichlorofluorescin, which is then oxidized by
H2O2 to the highly fluorescent DCF. The
fluorescence intensity was measured by FACScan (Becton-Dickinson) with
excitation and emission settings of 488 and 530 nm, respectively.
Counting of cells stopped at 30,000. Gating was performed prior to the
collection of data to remove apoptotic cells and cellular debris. All
experiments were repeated three times.
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ACKNOWLEDGMENTS |
We thank Drs. Sue Goo Rhee, Bin Goo Kang, Karl Hassenstein, and
Michael Evans for critical reading and encouragement.
| |
FOOTNOTES |
Received December 14, 2000; accepted April 2, 2001.
1
This work was supported by the Center of
Excellence grant (to J.S.L. and Y.S.B.), by the BK21 program (to
Y.S.B.) from Ministry of Education, and by the Korea Research
Foundation (grant to J.S.L.) made in the program year of 1998.
*
Corresponding author; e-mail jslee{at}mm.ewha.ac.kr; fax
82-2-3277-3760.
| |
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TOP
ABSTRACT
INTRODUCTION