Plant Physiol. (1999) 119: 213-218
Electric Signaling and Pin2 Gene
Expression on Different Abiotic Stimuli Depend on a Distinct Threshold
Level of Endogenous Abscisic Acid in Several Abscisic Acid-Deficient
Tomato Mutants1
Oliver Herde,
Hugo Peña Cortés,
Claus Wasternack,
Lothar Willmitzer, and
Joachim Fisahn*
Max Planck Institut für Molekulare Pflanzenphysiologie, Karl
Liebknechtstrasse 25, D-14476 Golm, Germany (O.H., L.W., J.F.); Universidad de Santiago, Casilla 40, Correo 33, Santiago, Chile
(H.P.C.); and Institut für Pflanzenbiochemie, Weinberg 3, 06120 Halle/Saale, Germany (C.W.)
 |
ABSTRACT |
Experiments were performed on three
abscisic acid (ABA)-deficient tomato (Lycopersicon
esculentum Mill.) mutants, notabilis, flacca, and sitiens, to investigate the
role of ABA and jasmonic acid (JA) in the generation of electrical
signals and Pin2 (proteinase inhibitor II) gene expression. We selected
these mutants because they contain different levels of endogenous ABA.
ABA levels in the mutant sitiens were reduced to 8% of
the wild type, in notabilis they were reduced to 47%,
and in flacca they were reduced to 21%. In wild-type
and notabilis tomato plants the induction of
Pin2 gene expression could be elicited by heat
treatment, current application, or mechanical wounding. In
flacca and sitiens only heat stimulation induced Pin2 gene expression. JA levels in
flacca and sitiens plants also
accumulated strongly upon heat stimulation but not upon mechanical
wounding or current application. Characteristic electrical signals
evolved in the wild type and in the notabilis and
flacca mutants consisting of a fast action potential and
a slow variation potential. However, in sitiens only
heat evoked electrical signals; mechanical wounding and current
application did not change the membrane potential. In addition,
exogenous application of ABA to wild-type tomato plants induced
transient changes in membrane potentials, indicating the involvement of ABA in the generation of electrical signals. Our data strongly suggest
the presence of a minimum threshold value of ABA within the plant that
is essential for the early events in electrical signaling and mediation
of Pin2 gene expression upon wounding. In contrast,
heat-induced Pin2 gene expression and membrane potential changes were not dependent on the ABA level but, rather, on the accumulation of JA.
| |
INTRODUCTION |
The plant hormones ABA and JA play a predominant role in the
conversion of environmental signals into changes in plant gene expression. An increase in endogenous ABA and JA levels precedes and is
involved in Pin2 (proteinase
inhibitor II) gene expression upon wounding
(Peña-Cortés et al., 1989
, 1991, 1995, 1996; Farmer and
Ryan, 1992; Farmer et al., 1992). This increase in ABA and JA is not
restricted to the tissue damaged directly but can also be detected in
the nonwounded, systemically induced tissue
(Peña-Cortés et al., 1989; Peña-Cortés and
Willmitzer, 1995). The accumulation of ABA and JA have been described
for several plant species, including potato, tomato, and tobacco
(Sanchez-Serrano et al., 1991; Peña-Cortés and Willmitzer,
1995).
Further evidence for the involvement of ABA and JA in wound-induced
Pin2 gene expression was provided by a series of experiments in which potato plants were sprayed with ABA or JA and Pin2
mRNA accumulated in the absence of any wounding
(Peña-Cortés et al., 1989; Hildmann et al., 1992). Both
nonsprayed leaves and leaves that were sprayed directly showed
increased Pin2 mRNA levels with a pattern identical to the
one described for wounded plants (Peña-Cortés et al., 1988;
Peña-Cortés and Willmitzer, 1995). Conclusive evidence for
the involvement of ABA in wound-induced Pin2 activation was
obtained from mutants impaired in ABA biosynthesis. Consequently, wound
induction of Pin2 was not observed in the droopy
mutant of potato or the sitiens mutant of tomato
(Peña-Cortés et al., 1989). However, in these mutants
treatment with ABA caused a return of the accumulation of
Pin2 mRNA to levels normally found in wild-type plants upon
wounding (Peña-Cortés et al., 1991).
Like wounding, the application of electrical current was able to
initiate ABA and JA accumulation in wild-type plants but not in
ABA-deficient plants (Herde et al., 1996). These results suggested
that, like wounding, electrical current requires the presence of ABA
for the induction of Pin2 gene expression (Herde et al.,
1996). In contrast to wounding and electrical current, burning of
leaves activated Pin2 gene expression in sitiens
mutants by directly triggering the biosynthesis of JA via an
alternative pathway that is independent of endogenous ABA levels (Herde
et al., 1996).
To determine the endogenous levels of ABA that are sufficient to
mediate electrical current-, heat-, and wound- induced Pin2 gene expression via electrical signals, we used several tomato mutants
containing progressively reduced levels of ABA. The effects of these
attenuated ABA levels on JA content and membrane potentials and the
expression pattern of Pin2 genes were analyzed. Analysis of
JA content was conducted to confirm the existence of an alternative pathway that is independent of endogenous ABA levels in the different ABA-deficient mutants.
| |
MATERIALS AND METHODS |
Plant Material and Growth Conditions
Wild-type and the ABA-deficient mutants flacca,
notabilis, and sitiens (generously donated by Dr.
Maarten Koornneef, Wageningen, The Netherlands) of tomato
(Lycopersicon esculentum Mill. cv Moneymaker [MM]) were
grown in the greenhouse at 26°C day/20°C night temperatures, 70%
to 80% RH, and 14 h of light. Characterization of the mutants and
determination of the endogenous levels of ABA were published previously
(Taylor, 1987). Two weeks after germination, the mutants were wrapped
in plastic to provide 100% humidity. All measurements were performed
on 21- to 28-d-old plants at 100% humidity.
Mechanical Wounding, Current Application, Heat Treatment, and
Elicitation by ABA
Mechanical damage to plants was due to dialysis clamps applied as
described by Sanchez-Serrano et al. (1986). For current application a
direct-current power supply provided 10 V for 30 s, as described
by Herde et al. (1995). Current was supplied extracellularly through
Ag/AgCl surface electrodes. Heat treatment was performed on the tip of
a leaf. Approximately 1 cm2 was burned as
described by Malone and Stankovic (1991) and Herde et al. (1996).
In all experiments stimuli were applied on leaf 4, which we refer to as
"local." Leaf 2 is referred to as "systemic" (not treated).
Treatment of plants was at 4 PM; at 10 PM
tissue samples were taken for analysis of Pin2 gene
expression and ABA and JA contents.
Application of ABA was via a microincision in the major vein of a leaf
2 cm from the point of measurement. Cutting was with a high-frequency
microcauter (hf SURG, Meyer-Haake, Oberursel, Germany), which provided
a surgical tip 1 µm in diameter. No alterations in the membrane
potential upon cutting could be detected. The experimental solution was
water buffered with Tris-HCl at pH 7.5, with a final concentration of
10 µM ABA. A drop containing 10 µL of this solution was
introduced in the microincisions.
ABA and JA Quantification
Endogenous ABA and JA levels were determined as described by
Lehmann et al. (1995). In this ELISA an antibody highly specific for
(
)-JA and L-amino acid conjugates of ()-JA, as
specified by Knöfel et al. (1990), was used. ABA/JA sample
quantitation values given are averages ± SD
(n = 5).
Gel-Blot Analysis of RNA
Total plant RNA was isolated and subjected to electrophoresis (10 µg of RNA per slot) in agarose-formaldehyde gels as described by
Logemann et al. (1987). Blotting and hybridization conditions were as
described by Amasino (1986). Probes used for radioactive labeling
consisted of potato Pin2 (cDNA 1; Sanchez-Serrano et al.,
1986). Each experiment was repeated independently at least five times.
The northern blots and ABA/JA quantification shown in the figures are
representatives of the average.
Membrane Potential Recordings
Quartz glass capillaries with a solid filament (Hilgenberg,
Malsfeld, Germany) were pulled on a laser-heated pulling device (P2000,
Sutter Instruments, Navaro, CA), resulting in a tip diameter of 150 nm.
These capillaries were filled with 0.1 M KCl, as described by Fisahn et al. (1986). For recordings of the membrane potential, these capillaries were mounted on the headstage of a gene-clamp amplifier (model HS 2A, Axon Instruments, Foster City, CA). The ground
reference consisted of an Ag/AgCl wire electrode that was attached to
the stem as described by Fromm et al. (1995). For a detailed
description of the protocol for membrane potential recordings, see
Herde et al. (1998).
| |
RESULTS |
Pin2 Gene Expression Occurs in flacca and
sitiens Only after Heat Treatment
Whole plants were mechanically wounded, treated with electrical
current, or gently burned at the tip of a leaf. After 6 h, the
time at which wound-induced JA accumulation reached its highest levels,
treated and nontreated systemic leaves were harvested and analyzed for
Pin2 gene expression by northern analysis (Fig. 1). As expected, mechanical damage and
electrical current application led to a local and systemic accumulation
of Pin2 mRNA in wild-type plants (Fig. 1).
notabilis exhibited the same pattern of Pin2 gene
expression as the wild type with all three stimuli. In contrast, the
flacca and sitiens mutants activated
Pin2 gene expression only with heat treatment (Fig. 1).
Further extended exposure of the autoradiograms did not reveal
accumulation of Pin2 mRNA in sitiens plants
following either wounding or electrical current application (data not
shown).
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| Figure 1.
Mechanical wounding, electrical current, and heat
treatments initiate the local and systemic accumulation of
Pin2 mRNA. Wild-type (MM) and ABA-deficient
(notabilis, flacca, and
sitiens) mutant tomato plants were wounded or treated
with electrical current or heat. Six hours after treatment, total RNA
was isolated from the treated leaves (L) and from leaves located distal
(S) to the treated ones. The autoradiogram shows the result of a
gel-blot hybridization of total RNA (10 µg per slot) against
radioactive Pin2 (Sanchez-Serrano et al., 1986).
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Differential Accumulation of ABA and JA
Endogenous levels of ABA and JA in the mutants
notabilis, flacca, and sitiens were
determined with all three stimuli. In particular, hormone concentration
was measured 6 h after treatment in both treated leaves (local)
and leaves located distal (systemic) of the treated ones. As expected,
ABA and JA accumulated in wild-type tomato plants following wounding,
current application, and heat treatment (Figs.
2 and 3). Because of inhibition in ABA
biosynthesis, the mutants flacca and notabilis
produced less ABA than the wild type (Fig. 2). Furthermore, these
mutants exhibited reduced levels of ABA compared with the wild type
upon mechanical wounding, current application, or heat treatment (Fig.
2). The sitiens mutants were unable to substantially
increase their ABA levels upon elicitation (Fig. 2).
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| Figure 2.
ABA content in tomato plants. Wild-type (MM) and
ABA- deficient (notabilis, flacca, and
sitiens) mutant tomato plants were wounded or treated
with electrical current or heat. Both directly treated (local) and
nontreated distal leaves (systemic) were harvested after 6 h.
Endogenous levels of ABA were determined as described in ``Materials and Methods'' and are indicated as means ± SE
(n = 5). FW, Fresh weight.
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| Figure 3.
Effect of wounding, electrical current, and heat
treatment on endogenous levels of JA. Wild-type (MM) and ABA-deficient
(notabilis, flacca, and
sitiens) mutant tomato plants were wounded or treated
with electrical current or heat. Both directly treated (local) and
nontreated distal leaves (systemic) were harvested after 6 h.
Endogenous levels of JA were determined as described in ``Materials and Methods'' and are indicated as means ± SE
(n = 5). FW, Fresh weight.
|
|
JA was measured to confirm the existence of an alternative pathway that
is independent of endogenous ABA levels and was found to accumulate to
a minor extent after elicitation by mechanical wounding or current
application in notabilis, flacca, and
sitiens mutants compared with wild- type plants (Fig.
3). This reduction in JA levels resembled
the decrease in endogenous ABA in notabilis and
flacca mutants upon mechanical wounding or current
application (Figs. 2 and 3). Conversely, JA accumulation upon heat
treatment was not influenced by endogenous levels of ABA. All of the
mutants exhibited JA contents comparable to those observed in wild-type plants in the absence of elicitation (Fig. 3).
Membrane Potential Recordings
In the signal transduction cascade mediating elicitor- induced
Pin2 gene expression, membrane transport events precede
hormone biosynthesis and changes in gene expression patterns. To
measure relaxation kinetics of membrane potentials, a microelectrode
was targeted to the region of the most negative membrane potential within the major vein of a tomato leaf (Herde et al., 1998). Upon arrival of the microelectrode in the target region and establishment of
a steady-state recording of the membrane potential, one of the three
stimuli was applied to a remote leaf and the electrical signal was
recorded (Herde et al., 1998). In wild- type tomato plants all three
stimuli resulted in an initial rapid depolarization that was followed
by a second time constant (Herde et al., 1998). A prolonged
depolarization was observed during this second phase.
The relaxation kinetics of the membrane potential that were generated
in notabilis and flacca plants upon wounding,
current application, and heat treatment resembled those of wild-type
plants (Fig. 4; Herde et al., 1998). In
addition to this similarity, two differences became most obvious: (a)
the depolarization of the slow component within the ABA-deficient
plants was not as pronounced as in the wild type, in accordance with
the endogenous levels of ABA; and (b) the absolute values of the
membrane potential were more negative in the ABA-deficient plants, in
accordance with decreasing levels of endogenous ABA within the mutants
(Fig. 4; Herde et al., 1998). No changes in the membrane potential upon mechanical wounding or current application occurred in the mutant with
the lowest endogenous ABA content (sitiens). In contrast, application of a heat stimulus to sitiens resulted in
relaxation kinetics of the membrane potential that consisted of a fast
initial depolarization followed by a second, slow depolarization (Herde et al., 1998). Similar to the mechanisms of the heat- induced Pin2 gene expression, generation of electrical signals upon
heat stimulation also seemed to be independent of endogenous ABA
levels.
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| Figure 4.
Characteristic membrane potential relaxation
kinetics in the main vein of a leaf of ABA-deficient tomato mutants
caused by mechanical wounding (indicated by an arrow). Membrane
potential recordings caused by current application and heat treatment
resembled those after mechanical wounding (data not shown). The results
shown are characteristic examples of a pool of 30 measurements per
plant.
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|
Application of exogenous ABA to microincisions of the major vein of
wild-type tomato leaves induced characteristic changes of the membrane
potential (Fig. 5). In particular, ABA
treatment resulted in a rapid depolarization followed by a period of
damped oscillations lasting for 10 to 15 min. In contrast, application of the experimental solution without ABA had no effect on the membrane
potential.
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| Figure 5.
Characteristic membrane potential relaxation
kinetics in the main vein of a wild-type tomato plant caused by
exogenous application of ABA (indicated by an arrow) . The results
shown are characteristic examples of a pool of 30 measurements per
plant.
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|
| |
DISCUSSION |
Previous studies revealed local and systemic induction of
Pin2 gene expression and JA accumulation upon mechanical
wounding and electrical current in wild-type tomato plants (Fig. 1). In contrast, sitiens mutants were unable to respond to
mechanical damage or electrical stimulation in terms of JA accumulation
and Pin2 gene expression. However, burning leaves of
sitiens mutants gave rise to local and systemic accumulation
of JA (Herde et al., 1996). Our findings suggest that (a) wound- or
electrically induced JA accumulation might depend on distinct levels of
ABA that exist in wild-type plants but not in sitiens plants
and (b) heat-induced JA accumulation does not require elevated levels
of ABA.
Since exogenous application of JA did not evoke an elevation in ABA
(Peña-Cortés et al., 1996), the accumulation of this hormone in wild-type plants upon heat treatment demonstrated that elicitation by heat has the capacity to activate two biosynthetic pathways independently (i.e. ABA and JA biosynthesis). Furthermore, the
accumulation of JA in sitiens plants indicated that heat
treatment was able to activate JA biosynthesis independently of the
internal levels of ABA (Fig. 3). Convincing evidence has been reported showing the involvement of JA in several stress responses of higher plants (Sembdner and Parthier, 1993). A model was proposed by Farmer
and Ryan (1992) in which the release of the peptide systemin as a
result of tissue damage may lead to an activation of a lipase in the
plasma membrane. The subsequent release of linolenic acid would then
produce a rapid accumulation of JA, which in turn may trigger the
activation of wound-responsive genes. Based on this proposed model, we
investigated the role of JA in wound-, current-, and heat-induced
Pin2 gene expression and in the process of generating electrical signals.
By analyzing tomato mutants that were progressively impaired in ABA
biosynthesis, we obtained additional information concerning a minimal
content of ABA required for stress-induced Pin2 gene expression (Fig. 1). In notabilis tomato mutants, which have
an ABA content that is 47% of the wild type, all three stimuli induced Pin2 gene expression. In contrast, flacca tomato
mutants, which have an ABA content that is 21% of the wild type,
resembled the Pin2 gene expression pattern found in
sitiens tomato mutants, which have an ABA content that is
8% of the wild type. Only heat treatment led to the accumulation of
Pin2 mRNA in sitiens mutants; mechanical wounding
and current application did not (Fig. 1). Since Pin2 mRNA
was not detected upon wounding or current application in mutants with
progressive attenuation in ABA content, it could be suggested that a
certain threshold value of ABA exists, functioning as an on/off switch
for wound-induced Pin2 gene expression (Fig. 1). Therefore,
the ABA level functioning as the threshold value for the ABA-dependent
pathway that leads to Pin2 gene expression upon wounding and
current application was between 21% and 47% of that found in
wild-type plants.
The ABA level that accumulated in wounded and current-treated plants
was roughly reflected by the respective JA content of wild-type and
mutant plants after these treatments. These findings are in line with
the results of Peña-Cortés et al. (1995), who demonstrated
that the application of ABA is able to induce JA biosynthesis and,
furthermore, that JA is located downstream of ABA in the signal
transduction cascade leading to Pin2 gene expression. Conversely, unwounded control plants of the wild type and the notabilis, flacca, and sitiens mutants
had almost identical levels of JA, suggesting that JA biosynthesis is
not influenced by endogenous levels of ABA. Harms et al. (1995)
reported that high endogenous levels of JA in transgenic plants
overexpressing a flax allene oxide synthase cDNA did not induce
constitutive Pin2 gene expression. One possible explanation
for these phenomena is that endogenous ABA and JA are stored in
cellular compartments different from those where ABA and JA accumulate
upon wounding. JA biosynthesis is suggested to occur in the chloroplast
(Harms et al., 1995), which implies that accumulation of JA in this
organelle is not sufficient to lead to changes in the expression of
JA-responsive genes such as Pin2.
The results presented here indicate an involvement of ABA in the early
events of the signal transduction cascade mediating wound-induced
Pin2 gene expression. In particular, wild-type tomato plants
generated an electrical signal upon all three stimuli, mechanical
wounding, current application, and heat treatment. Similarly, the
relaxation kinetics of the membrane potential that were generated in
notabilis and flacca plants upon these stimuli resembled those of wild-type plants (Fig. 4; Herde et al., 1998). Exogenous application of ABA to wild-type tomato plants induced transient changes in membrane potential as well. These changes in the
membrane potential consisted of a fast, transient depolarization followed by a period of damped oscillations lasting for 10 to 15 min
(Fig. 4). Like the initial fast depolarization, these oscillations could have been due to an influx of Ca2+ into the
cytosol. Oscillations in Ca2+ are often observed
in animal cells, especially when phosphoinositide metabolism is
stimulated (Berridge and Galione, 1988; Berridge et al., 1988).
In the mutant with the lowest endogenous ABA content,
sitiens, there were no changes in the membrane potential
upon mechanical wounding or current application (Herde et al., 1998).
In contrast, application of a heat stimulus resulted in relaxation
kinetics of the membrane potential consisting of a fast depolarization followed by a second time constant. The results of the Pin2
gene expression analysis suggested that the generation of electrical signals upon heat treatment is independent of endogenous ABA levels. Moreover, the depolarization of the slow component within the ABA-deficient plants was not as pronounced as in the wild type, which
is in agreement with a progressive reduction in endogenous levels of
ABA within the different mutants. Like wound-induced Pin2
gene expression, there was a distinct threshold value required for
propagation of electrical signals within the plant. Compared with the
role of ABA in wound-induced Pin2 gene expression, two differences are obvious: (a) the variation potential generated upon
mechanical damage or current application became less pronounced in
correlation with progressive attenuation in endogenous ABA levels,
indicating a graduated response to different levels of ABA; and (b) the
ABA threshold value required for a change in the membrane potential
upon wounding and current application (between 8% and 21% of the wild
type) was below that required for an induction of Pin2 gene
expression (between 21% and 47% of the wild type). Resting membrane
potential is also dependent on ABA levels. In parallel to progressive
decreases in ABA content, the resting membrane potentials became more
negative (Fig. 4; Herde et al., 1998).
The results presented in this report suggest that the ABA-dependent
pathway leading to Pin2 gene expression upon wounding and
current application requires ABA levels ranging between 21% and 47%
of those found in wild- type tomato plants. Within these ranges, a
distinct threshold value seems to exist, functioning as an on/off
switch for the subsequent Pin2 gene activation. In contrast,
heat-induced Pin2 mRNA accumulation is regulated by triggering directly the biosynthesis of JA by an alternative pathway that is independent of normal levels of ABA. In terms of the membrane potential, two major differences emerged between wild-type and ABA-deficient tomato plants. First, ABA-deficient mutants were not able
to generate electrical signals upon wounding and current application
below a certain threshold value of endogenous ABA. Conversely,
stimulation by heat induces the generation of electrical signals
independently of ABA. Unlike the threshold level of ABA required for
Pin2 gene expression, the threshold level of ABA for
membrane transporter activation ranged between 8% and 21% of the wild
type. Second, resting membrane potential was more negative in ABA-
deficient mutants, in accordance with decreasing levels of endogenous
ABA. Exogenous application of ABA to wild-type tomato plants induced
transient changes in membrane potentials, indicating the essential role
of ABA in the generation of electrical signals within plants.
| |
FOOTNOTES |
1
This work was supported by Deutsche
Forschungsgemeinschaft grant no. 571/2 to J.F. and H.P.C.
*
Corresponding author; e-mail fisahn{at}mpimp-golm.mpg.de; fax
49-331-977-2301.
Received June 8, 1998;
accepted October 14, 1998.
| |
ABBREVIATIONS |
Abbreviation:
JA, jasmonic acid.
| |
ACKNOWLEDGMENTS |
We thank C. Gebhardt and Dr. R. Atzorn for JA and ABA
measurements.
| |
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