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Plant Physiol. (1999) 121: 147-152
Oligogalacturonic Acid and Chitosan Reduce Stomatal Aperture by
Inducing the Evolution of Reactive Oxygen Species from Guard Cells of
Tomato and Commelina communis1
Sumin Lee,
Hyunjung Choi,
SuJeoung Suh,
In-Suk Doo,
Ki-Young Oh,
Eun Jeong Choi,
Ann T. Schroeder Taylor,
Philip S. Low, and
Youngsook Lee*
Department of Life Science, Pohang University of Science and
Technology, Pohang 790-784, Korea (S.L., H.C., S.S.,
I.-S.D., K.-Y.O., E.J.C., Y.L.); and Department of Chemistry,
Purdue University, West Lafayette, Indiana 47907 (A.T.S.T.,
P.S.L.)
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ABSTRACT |
Stomatal opening provides access to
inner leaf tissues for many plant pathogens, so narrowing stomatal
apertures may be advantageous for plant defense. We investigated how
guard cells respond to elicitors that can be generated from cell walls
of plants or pathogens during pathogen infection. The effect of
oligogalacturonic acid (OGA), a degradation product of the plant cell
wall, and chitosan ( -1,4-linked glucosamine), a component of the
fungal cell wall, on stomatal movements were examined in leaf epidermis
of tomato (Lycopersicon esculentum L.) and
Commelina communis L. These elicitors reduced the size
of the stomatal aperture. OGA not only inhibited light-induced stomatal
opening, but also accelerated stomatal closing in both species;
chitosan inhibited light-induced stomatal opening in tomato epidermis.
The effects of OGA and chitosan were suppressed when EGTA, catalase, or
ascorbic acid was present in the medium, suggesting that
Ca2+ and H2O2 mediate the
elicitor-induced decrease of stomatal apertures. We show that the
H2O2 that is involved in this process is
produced by guard cells in response to elicitors. Our results suggest
that guard cells infected by pathogens may close their stomata via a
pathway involving H2O2 production, thus
interfering with the continuous invasion of pathogens through the
stomatal pores.
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INTRODUCTION |
Pathogens penetrate plant tissues by three different mechanisms:
by digesting cell walls, by entering through wounds, and by invading
natural openings (including stomata). Although many pathogens can force
entry through closed stomata, some can infect plants only when the
stomata are open (Agrios, 1997 ). Thus, narrow stomata may limit the
penetration of some pathogens, thereby conferring resistance to them.
Upon pathogen infection, plants commonly activate a variety of defense
mechanisms. Within a few minutes, the challenged plants frequently
evolve reactive oxygen species (ROS) such as superoxide and
H2O2, which in turn can
facilitate the expression of a hypersensitive response (Levine et al.,
1994). ROS can also damage pathogens directly by the oxidation of
important biomolecules (including cell membranes; Adam et al., 1989;
Keppler and Baker, 1989), and may induce additional defense mechanisms
in plant cells, such as cell wall fortification (Bradley et al., 1992),
defense-related gene expression (Levine et al., 1994; Jabs et al.,
1997), and the synthesis of phytoalexins (Bradley et al., 1992; Jabs et
al., 1997). Perhaps related to these functions is the observation that exogenously added superoxide and
H2O2 inhibit stomatal
opening and promote stomatal closing (McAinsh et al., 1996). The
intriguing question, however, remains whether guard cells can perceive
signals of pathogen infection directly and thus modify stomatal
responses in vivo in a way that contributes to plant defense.
Pathogen attack can be mimicked by elicitor molecules produced during
the infection process. Cell wall fragments from plants or pathogens can
serve as elicitors in many plant species. Oligogalacturonic acid (OGA),
a well-studied elicitor, is derived from plant cell walls (Nothnagel et
al., 1983). When added to cultured plant cells, it induces an oxidative
burst within minutes (Apostol et al., 1989), releasing ROS via a
pathway that involves receptor binding (Horn et al., 1989), activation
of a G-protein (Legendre et al., 1992), influx of
Ca2+ (Chandra et al., 1997), stimulation of
phospholipase C (Legendre et al., 1993b), and induction of a number of
kinases (Chandra and Low, 1995). Chitosan (-1,4-linked glucosamine)
is a deacylated derivative of chitin that is a component of the cell
walls of many fungi (Bartnicki-Garcia, 1970). It can be produced by the activity of the enzyme chitinase, one of the pathogenesis-related proteins that is activated during infection and is toxic to invading pathogens (Mauch et al., 1988). Chitosan induces phytoalexin production in pea pods, inhibiting fungal growth and promoting protection from
further infection (Hadwiger and Beckman, 1980).
We investigated whether guard cells might be able to sense the presence
of elicitors and then respond by changing stomatal apertures. For this
purpose, we tested the effects of OGA and chitosan, common,
non-species-specific elicitors, on stomatal movements in two different
plant species, tomato (Lycopersicon esculentum L.) and
Commelina communis L. Both OGA and chitosan were found to
induce the production of ROS in guard cells and to reduce stomatal
aperture either by inhibiting stomatal opening or by inducing stomatal
closing.
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MATERIALS AND METHODS |
Plant Materials and Elicitors
Commelina communis L. and tomato (Lycopersicon
esculentum L.) plants were grown in a greenhouse or growth chamber
at 23°C with 16-h/8-h light/dark cycles. Fully expanded leaves of 3- to 4-week-old plants were excised, and epidermal pieces were obtained either by peeling abaxial epidermis of C. communis or by
blending tomato leaves in a solution containing 5 mM CaCl2, 10 mM MES (pH 6.0), and 0.1% (w/v) PVP-40.
The blending process destroyed epidermal cells but guard cells were
viable, as judged from staining with fluorescein diacetate. The
preparation and isolation of OGA have been previously reported
(Legendre et al., 1993a). Chitosan was purchased from Kumho Chemical
Laboratories (Taejeon, Korea) and dissolved as previously described
(Walker-Simmons et al., 1984).
Measurement of Stomatal Aperture
To study the effects of elicitors on light-induced stomatal
opening, initially small apertures of stomata were obtained by keeping
the plants in darkness overnight, and then floating the epidermal
tissue on 10 mM K+-MES (pH 6.1) in
darkness for 2 h. The tissues were then transferred to 10 mM K+-MES (pH 6.1) in a 50 mM (tomato) or 30 mM (C. communis)
KCl solution, and illuminated with 250 to 500 µmol
m 2 s1 light with or
without chemicals. To determine if elicitors can affect midday stomatal
closing, initially open stomata were obtained by floating the epidermal
pieces of leaves on 10 mM
K+-MES (pH 6.1) containing 50 mM (tomato) or 30 mM
(C. communis) KCl under light for 2 to 3 h, beginning
at h 3 to 4 of the photoperiod. Chemicals were added alone or together
to the same solution on which the epidermal tissues were floated. At
the time of chemical or elicitor treatment, the control stomata began
midday closing, possibly driven by the circadian clock. Stomatal
apertures were measured using an eyepiece micrometer.
Microphotography of Production of H2O2 in
Intact Guard Cells
The production of H2O2
by guard cells was examined by loading epidermal preparations with
2 ,7-dichlorofluorescin diacetate (H2DCF-DA). This nonfluorescent dye can cross the
plasma membrane freely, and is then cleaved to its
impermeable counterpart, dichlorofluorescin (H2DCF), by endogenous esterases.
H2DCF, which accumulates in the cell,
functions as a reporter of cytoplasmic
H2O2 by converting upon
oxidation to its fluorescent form, DCF (Ohba et al., 1994; Yahraus et
al., 1995; Naton et al., 1996; Allan and Fluhr, 1997; Kang et al.,
1998).
Tomato epidermal pieces were floated on 10 mM
K+-MES (pH 6.1), 50 mM KCl with or
without chitosan, and catalase or ascorbic acid for 30 min, then
transferred to and floated on 10 mM
K+-MES (pH 6.1) and 50 mM KCl
solution containing 50 µM H2DCF-DA for 10 min. After a brief wash with 10 mM
K+-MES (pH 6.1) and 50 mM KCl, the
guard cells were observed under a fluorescent microscope (Optiphot-2,
Nikon) equipped with filter blocks of a narrow band pass (excitation
465-495 nm, barrier 515-555 nm). Photographs were taken on T-MAX 400 film (Kodak) using a photographic attachment (Microflex UFX-DX, Nikon).
H2DCF-DA was dissolved in dimethylformamide. The
final concentration of the solvent was 0.5% (v/v), which did
not induce any significant change in guard cell viability or stomatal
aperture.
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RESULTS |
Effects of OGA on Stomatal Movements in Tomato Leaves
The effects of OGA, a plant cell wall-derived elicitor, on
stomatal movements were tested in tomato epidermal tissues. Tomato is
one of the best-characterized plant systems employed in studying plant-pathogen interactions. Treatment of leaf epidermal tissues with 5 µg/mL OGA, a concentration known to induce an oxidative burst in
cultured soybean and tomato cells (Legendre et al., 1992), inhibited
light-induced stomatal opening (Fig. 1).
Following 120 min of treatment with OGA, the stomatal aperture was 46%
(Fig. 1A) and 63% (Fig. 1B) of that of control plants illuminated
without OGA. To determine whether the effect of OGA on stomatal
movements might involve ROS known to participate in elicitor-induced
defense responses, tomato epidermal tissues were treated with OGA in
the presence of either catalase or ascorbic acid, both of which remove or reduce the level of ROS (Bradley et al., 1992; Levine et al., 1994).
As noted in Figure 1, both agents reversed the inhibitory effects of
OGA on stomatal opening, indicating that OGA inhibits light-induced
stomatal opening via a mechanism involving ROS. Treatment of the
epidermis with catalase or ascorbic acid alone did not induce any
change of stomatal aperture (data not shown).
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| Figure 1.
Effects of OGA on light-induced stomatal opening
in tomato leaf epidermis. Note that 3 mg/mL catalase (A) and 5 mM ascorbic acid (B), which reduce the level of ROS,
reversed the inhibitory effect of OGA (5 µg/mL) on stomatal opening.
Experimental procedures are described in ``Materials and Methods''.
Results are the averages ± SE (n = 120) of four independent experiments.
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ROS has been reported to reduce stomatal aperture via a pathway
involving a Ca2+ increase in cytosol (McAinsh et
al., 1996). Therefore, we addressed whether Ca2+
is also involved in elicitor-induced changes in stomatal movements. Stomatal opening was inhibited by 5 µg/mL OGA (Figs. 1 and 2A), while
midday stomatal closing was accelerated by 50 µg/mL OGA (Fig.
2B). In the presence of EGTA, however,
the effects of OGA on both stomatal opening (Fig. 2A) and closing (Fig.
2B) were completely reversed, suggesting an important role of
Ca2+ in the OGA-induced reduction of stomatal
aperture. EGTA alone induced a slight stomatal opening over untreated
controls (data not shown), as was reported previously (Schwartz, 1985).
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| Figure 2.
Involvement of Ca2+ in OGA-induced
narrowing of stomata in tomato leaves. In light-induced opening (A) and
midday closing (B) experiments, the inhibitory effect of OGA (5 µg/mL) on opening and the enhancing effect of OGA (50 µg/mL) on
closing of stomata were reversed by EGTA (2 mM).
Experimental procedures are described in ``Materials and Methods''.
Results are the averages ± SE (n = 120) of four independent experiments.
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Effects of Chitosan on Stomatal Movements of Tomato Leaves
Because OGA is a plant-derived elicitor, we questioned whether
pathogen-derived elicitors may have similar effects on stomatal movements. Chitosan (100 or 200 µg/mL), an elicitor that can be generated from the degradation of fungal cell walls, inhibited light-induced opening (Fig. 3). Following
120 min of chitosan treatment, the stomatal aperture was 59% (Fig. 3A)
and 62% (Fig. 3B) of that of the controls illuminated in the absence
of chitosan. This effect of chitosan on stomatal opening was also
suppressed by catalase and ascorbic acid (Fig. 3), as seen previously
with OGA (Fig. 1).
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| Figure 3.
Effect of chitosan on light-induced stomatal
opening in tomato leaf epidermis. Note that 3 mg/mL catalase (A) and 10 mM ascorbic acid (B) suppressed the inhibitory effect of
chitosan (100 µg/mL in A or 200 µg/mL in B) on stomatal opening.
Experimental procedures are described in ``Materials and Methods''.
Results are the averages ± SE (n = 120) of three to four independent experiments.
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Although the initial and/or final apertures of stomata varied
between experiments, the effects of elicitors and other chemicals on
stomatal movements were consistent (Figs. 1 and 3). The variation in
stomatal aperture may have been due to seasonal changes in growth
conditions or to a slight difference in the preparation of epidermal
tissue pieces.
Effects of OGA on Stomatal Movements in C. communis Leaves
If the regulation of stomatal movements is an important plant
defense mechanism, then this response should be exhibited by many
species. Therefore, we also tested whether the OGA elicitor might
affect stomatal movements in C. communis leaf epidermal tissues. C. communis is the most widely used plant for
studying guard cell physiology. We found that OGA inhibited
light-induced stomatal opening and enhanced stomatal closing in a
concentration-dependent manner in C. communis (Fig.
4). In the opening experiment, after 3 h of illumination, stomatal apertures of epidermis treated with 10 and 50 µg/mL OGA were 85% and 35% of control, respectively. In
the closing experiment, stomatal apertures after 90 min of treatment
with 10 and 50 µg/mL OGA were 55% and 41% of control. Therefore,
our data suggest that the effects of OGA on stomatal movements are not
unique for tomato, but may have also evolved in other species.
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| Figure 4.
Effects of OGA on stomatal movements in C. communis. OGA effects on both stomatal opening (A) induced by
white light of 500 µmol m2 s1 and midday
stomatal closing (B) were tested. Note that OGA inhibited stomatal
opening (A) and enhanced stomatal closing (B) in a
concentration-dependent manner. Results are the averages ± SE (n = 120) of four independent
experiments.
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H2O2 Production by Guard Cells in Response
to OGA and Chitosan
Reversal of the effects of OGA and chitosan by catalase and
ascorbic acid suggests that ROS, especially
H2O2, are involved in
elicitor-inhibited stomatal opening and elicitor-enhanced stomatal closing. We questioned whether guard cells themselves could produce H2O2 using the dye
H2DCF-DA.
H2O2 evolution was evident
throughout the entire surface of tomato guard cells treated with
chitosan for 30 min (Fig. 5, B and F). In
contrast, control guard cells showed fluorescence only in regions where
chloroplasts were located (Fig. 5, A and E). Chloroplasts are well
known for the formation of ROS during photosynthetic electron
transport. In the present study, chitosan-induced
H2O2 evolution became
apparent from 10 to 20 min after the onset of the treatment and
continued until 30 to 60 min, after which time the dye was
bleached. In the presence of catalase (Fig. 5C) and ascorbic
acid (Fig. 5D), chitosan-induced H2O2 production was
suppressed and the fluorescence existed only in regions where
chloroplasts were enriched (Fig. 5, G and H), as was also seen in
control cells. OGA also induced the production of
H2O2 in tomato guard cells
(data not shown).
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| Figure 5.
Chitosan-induced production of
H2O2 by guard cells of tomato leaf. Epidermal
pieces of tomato leaf without (control) (A and E) or with 30 min of
treatment with chitosan alone (B and F), with chitosan and catalase (C
and G), or with chitosan and ascorbic acid (D and H) were loaded with
50 µM of H2DCF-DA for 10 min. After a brief
wash with 50 mM KCl and 10 mM
K+-MES (pH 6.1), photographs were taken for a
representative pair of guard cells from each treatment using
fluorescence microscopy (A-D) or light microscopy (E-H). The bar in A
is 10 µm, and applies to all photographs.
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DISCUSSION |
Some pathogens penetrate into plant tissues only through open
stomata (Agrios, 1997). Since guard cells govern access to this port of
entry, they are likely to be the first cells to come into contact with
these pathogens. Our results suggest that guard cells might have
evolved the capability to detect and respond to signal molecules
generated during such contact. We have shown that guard cells can
recognize common, non-species-specific elicitors of both plant and
pathogen origin, can generate ROS, and can respond to ROS by narrowing
stomatal apertures. Furthermore, OGA was shown to stimulate the same
stomatal changes in two different plant species. These observations
suggest the possibility that elicitor-induced changes in stomatal
properties may not be isolated responses but, rather, are a
characteristic of many plants following the detection of pathogen
attack.
McAinsh et al. (1996) showed that externally applied
H2O2 induces stomatal
closing in C. communis, as well as an increase in cytosolic
free Ca2+ in guard cells. We observed that the
elicitor-stimulated inhibition of stomatal opening and the
elicitor-enhanced stomatal closing were both inhibited by extracellular
EGTA. Ca2+ is an important regulator of guard
cell movements (for review, see Mansfield et al., 1990; Assmann, 1993),
and an increase in cytosolic Ca2+ from
intracellular or extracellular sources is closely correlated with
stomatal closing (Gilroy et al., 1990; McAinsh et al., 1995). Our data
support the idea that Ca2+ serves as a common
component of signal transduction pathways induced by many different
stomatal closing signals.
Treatment with elicitors generally renders a plant more resistant to
subsequent pathogen attack. Indeed, elicitor stimulation has been
observed to induce the hypersensitive response (Bradley et al., 1992),
PR gene expression (Broekaert and Peumans, 1988; Jabs et al., 1997),
phytoalexin biosynthesis (Nürnberger et al., 1994; Jabs et al.,
1997), and cell wall stabilization (Bruce and West, 1989; Bradley et
al., 1992), all of which are plant defense responses. All of these
defense mechanisms depend at least in part on ROS (Bradley et al.,
1992; Jabs et al., 1997). Our data now suggest that stomatal closure is
similarly triggered by elicitor-induced ROS, which may also contribute
to plant defense.
Although Figure 5 clearly shows that ROS were present inside the
elicitor-treated guard cells, inhibition of both the elicitor-induced stomatal narrowing responses (Figs. 1 and 3) and
H2O2 evolution of guard
cells (Fig. 5) by externally applied catalase (240 kD), which is not
likely to cross the plasma membrane, indicates that H2O2 may also act outside
of the plasma membrane of guard cells. This is consistent with studies
showing high permeability of the membrane to
H2O2 (Yamasaki et al.,
1997). It was recently reported that epidermal cells of tobacco
leaves produce H2O2 in
response to a peptide elicitor, cryptogein, and that the product can
diffuse to neighboring cells (including guard cells) (Allan and Fluhr, 1997). Because the tomato leaf preparation employed in our study did
not maintain the viability of the epidermal cells, it was not possible
to evaluate whether epidermal cells of tomato also participate directly
in elicitor-stimulated ROS production. Nevertheless, the guard cells in
the same preparations were highly viable and responded to elicitation
with a significant oxidative burst. Further studies are necessary to
understand the site of H2O2
production in guard cells.
As shown previously, H2O2
biosynthesis involves the induction of a sequence of second messengers,
including G-proteins, Ca2+ influx, phospholipase
C, and protein kinases (Legendre et al., 1992, 1993b; Schwacke and
Hager, 1992; Chandra and Low, 1995; Chandra et al., 1997). In view of
the mobilization of these signaling components, it may seem surprising
that guard cells still use H2O2 as a signal to trigger
their elicitor-stimulated closure. However, one distinct advantage of
relying on H2O2 to promote stomatal closure is that if initially infected guard cells or adjacent
epidermal cells can respond to pathogen attack with an oxidative burst,
then the product, H2O2,
rapidly diffusing in the apoplastic pathway (as shown in tobacco
epidermal tissue; Allan and Fluhr, 1997) might induce narrowing of
neighboring stomata before more of the same or similar pathogens can
find other open stomata. In this manner, elicitor-stimulated stomatal
closure might provide one of the most rapid mechanisms to thwart
pathogen invasion.
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FOOTNOTES |
1
This work was supported by a Korea-United States
cooperative research grant from the Korea Science and Engineering
Foundation (no. 966-0500-007-2 awarded to Y.L.) and by a grant from
the National Science Foundation of the United States (nos. INT-9600183
and MCB-9725934 awarded to P.S.L.).
*
Corresponding author; e-mail ylee{at}postech.ac.kr; fax
82-562-279-2199.
Received January 21, 1999;
accepted May 12, 1999.
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ACKNOWLEDGMENTS |
We thank Dr. Ro-Dong Park for information concerning chitosan
and Shi-In Kim for management of plants.
| |
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Top
Abstract
Introduction