Plant Physiol. (1998) 116: 681-686
Fusicoccin Counteracts the n-Ethylmaleimide and
Silver-Induced Stimulation of Oxygen Uptake in
Egeria densa Leaves1
Maria Teresa Marrè* and
Francesco Albergoni
Centro di Studio del Consiglio Nazionale delle Richerche sulla
Biologia Cellulare e Molecolare delle piante (M.T.M.), and Dipartimento
di Biologia, Università di Milano (F.A.), via Celoria 26, 20133 Milano, Italy
 |
ABSTRACT |
It was previously shown that a number
of sulfhydryl [SH] group reagents (N-ethylmaleimide
[NEM], iodoacetate, Ag+, HgCl2, etc.) can
induce a marked, transitory stimulation of O2 uptake
(QO2) in Egeria densa leaves, insensitive to
CN
and salicylhydroxamic acid and inhibited by
diphenylene iodonium and quinacrine. The phytotoxin fusicoccin (FC)
also induces a marked increase in O2 consumption in
E. densa leaves, apparently independent of the
recognized stimulating action on the H+-ATPase. In this
investigation we compared the FC-induced increase in O2
consumption with those induced by NEM and Ag+, and we
tested for a possible interaction between FC and the two SH blockers in
the activation of QO2. The results show (a) the different
nature of the FC- and NEM- or Ag+-induced increases of
QO2; (b) that FC counteracts the NEM- (and Ag+)-induced respiratory burst; and (c) that FC strongly
reduces the damaging effects on plasma membrane permeability observed in E. densa leaves treated with the two SH reagents. Two
alternative models of interpretation of the action of FC, in activating
a CN-sensitive respiratory pathway and in suppressing the
SH blocker-induced respiratory burst, are proposed.
| |
INTRODUCTION |
Previous investigations have shown that NEM and a number of other
SH group reagents are able to induce a remarkable respiratory burst in
Egeria densa Planchon leaves. This effect was not
inhibited by CN, SHAM, or propylgallate
added separately or in combination, and was additive with the
effect of the uncoupler
carbonylcyanide-m-chlorophenylhydrazone, thus ruling
out the participation of the mitochondrial (cytochromic and
alternative) electron transport pathways. It was, however, completely
suppressed by diphenylene iodonium and by quinacrine, two inhibitors of
the plasmalemma NADPH oxidase activated by pathogens in granulocytes
(Babior, 1992
) and in plants (Auh and Murphy, 1995). This indicated an
activating action of SH reagents on some redox systems that are
inactive under normal conditions (Albergoni et al., 1996; Bellando et
al., 1997).
To define experimental conditions able to influence the SH
reagent-induced increase in O2 consumption, we
studied the effects of the fungal toxin FC on the SH blocker-induced
increase in QO2. This choice was based on
previous evidence suggesting that FC might increase the reduction state
of NADP and thiol components in the cell (Marrè et al., 1989a,
1994) and also the finding that FC, in addition to stimulating the
H+-ATPase activity (Marrè et al., 1989b),
induces a marked increase in O2 consumption in
E. densa leaves, apparently independently of its stimulation
on the proton pump. Leaves treated with the toxin under experimental
conditions that are nonpermissive for proton extrusion had a
respiration rate significantly higher than controls treated under
conditions favorable for H+ extrusion (Beffagna
et al., 1989; Marrè et al., 1993). Thus, we thought it would be
interesting to compare this FC-induced increase in
O2 consumption with the similar effect induced by NEM and to test for a possible interaction between FC and the SH
blockers NEM and Ag+ in the activation of
QO2.
In this paper we present data concerning E. densa leaves
that demonstrate (a) the different nature of the FC- and the NEM- and
Ag+-induced increases of
QO2 and (b) the ability of FC to counteract the NEM- and Ag+-induced oxidative burst and
associated effects on plasma membrane permeability.
| |
MATERIALS AND METHODS |
Egeria densa Planchon plants were grown in flowing tap
water in a greenhouse. Young, fully expanded leaves were cut from
branches about 2 to 4 cm from the apex, randomized, and then grouped
into samples. The samples were preincubated for 1 h in 10 mL of
0.5 mm CaSO4, with continuous shaking
at 20°C in the dark. The solution was renewed after 30 min.
DCMU (5 µm) and, when applicable FC (0.1 mm)
were added during the last 30 min of pretreatment.
QO2 Measurements
QO2 was measured on four leaves (about 30 mg
fresh weight) in 2 mL of medium by using a Clark-type
O2 electrode (unit KW2, control box CB1,
Hansatech, Norfolk, UK), modified to allow quick (every 5-10 min)
changes of the incubation solution. The electric current generated by
the O2 consumption was applied to an mV recorder connected to a computerized unit differentiating continuous
measurements. Data output were simultaneously converted to
O2 consumption rate values expressed as nanomoles
of O2 decrease per minute in the measurement
chamber.
Measurements were carried out in a medium containing: 0.5 mm CaSO4, 5 µm DCMU,
and 10 mm Mes buffer, pH 6.0, with BTP. Other reagents were
added at the concentrations specified in the legends to the figures.
The data represent a group of at least five experiments for each
experimental condition; the se did not exceed 10%.
Electrolyte Leakage Measurements
After pretreatment, samples of leaves (200 mg fresh weight) were
incubated in 10 mL of a stirred solution, thermoregulated at 20°C,
that contained 0.5 mm CaSO4, 5 µm DCMU, and 10 mm Mes buffer, pH 6.0, with
BTP. Other reagents were added at the concentrations specified in the
legends to the figures. The conductivity of the medium was measured
continuously for the required time by means of a conductivity meter
(model MO 101, Analytical Control, Milan, Italy) connected to a chart
recorder. The data represent the change in medium conductivity
(
µS) from the value (taken as zero) of conductivity at the end of
the equilibration period. The data presented are those of a
typical experiment out of at least five measurements for each set
of experimental conditions. The se did not exceed 6%.
Electrophysiological Measurements
A single leaf held in a 5-mL plexiglass chamber was irrigated with
a continuously flowing (approximately 15 mL
min1) aerated medium, thermoregulated at
20°C, that contained 0.5 mm CaSO4,
5 µm DCMU, and 10 mm Mes buffer, pH 6.0, with
BTP. Other reagents were added at the concentrations specified in the
legends to the figures.
Micropipettes (tip resistance 10-20 m
) filled with 1 m KCl were used as microsalt bridges of Ag/AgCl electrodes
and inserted vertically into the tissue by means of a micromanipulator
(Leitz, Wetzlar, Germany). Transmembrane electric potential difference was measured with a high-impedance electrometer amplifier (WPI K5-700,
WP Instruments, New Haven, CT) connected to a chart recorder. The data
presented are those of a typical experiment out of at least four
experiments for each set of experimental conditions. The se
did not exceed 6%.
Variations in Titratable H+ and K+
Concentrations in the Medium
Following pretreatment, the samples (120 mg fresh weight) were
incubated in 7 mL of solution containing 0.5 mm Mes
adjusted to pH 6.0 with BTP, 0.5 mm
CaSO4, 0.25 mm
K2SO4, and 5 µm DCMU with 0.1 mm FC and/or 0.2 mm NEM when applicable. After 45 min of incubation the
leaves were removed from the medium, which was divided into two
aliquots to determine titratable H+ extrusion
(
H+) and K+ net uptake
(K+) by the tissue.
H+ extrusion was determined by back titration of
4 mL of the medium from the final pH value to the initial value after
removal of CO2, as described by Lado et al.
(1981). K+ uptake was determined in 3 mL of
the medium using an atomic absorption-flame spectrophotometer
(model AA12175, Varian Techtron, Melbourne, Australia).
Experiments were run in triplicate and repeated three times.
| |
RESULTS |
Figure 1 shows the changes induced
by FC, or alternatively by NEM or Ag+, on the
rate of O2 consumption by E. densa
leaves. The substitution of the control solution, with one containing
0.2 mm NEM or 2 µm Ag+,
caused the typical respiratory changes previously described for
E. densa and Potamogeton crispus (Albergoni et
al., 1996; Bellando et al., 1997). With NEM an initial phase in which a
slight QO2 decrease occurred was followed by the
onset of a marked but transitory stimulation of
O2 consumption, whereas with
Ag+, no lag phase was usually observed. The NEM-
or the Ag+-induced respiratory burst was
essentially unchanged, even in conditions of drastic inhibition of the
basal QO2 induced by combined treatment with
CN and SHAM (Bellando et al., 1997; Fig. 3B,
control curve). The effect of FC on respiration had a completely
different pattern. As shown in Figure 1, a stimulation of
QO2 was already measurable 15 min after the toxin
was added and reached its maximum in about 50 min, remaining constant
for more than 2 h. This FC-induced increase in respiration was not
influenced by SHAM (Fig. 2A) but was
completely suppressed by CN alone (Fig. 2B) or
in combination with SHAM (Fig. 2C). Even more interesting was the
finding that FC completely suppressed the NEM-induced stimulation of
QO2 both in the absence and in the presence of
CN and SHAM (Fig.
3). A similar suppression of the
respiratory burst was observed when FC was added 5-8 min after the
addition of NEM (data not shown). Figure
4 shows that FC was equally able to
inhibit the increase in QO2 induced in E. densa leaves by Ag+.
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| Figure 1.
Changes in the rate of QO2 induced in
E. densa leaves by the presence of 104
m FC and of 0.2 mm NEM, or 2 µm Ag+, in the incubation medium. Basal
composition of the medium was 0.5 mm CaSO4, 5 µm DCMU, and 10 mm Mes-BTP buffer, pH 6.0, and Ag+ was added as the SO42
salt. gr F.W., Grams fresh weight.
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| Figure 3.
Counteracting effect of FC on the oxidative burst
induced by 0.2 mm NEM in E. densa leaves in
the absence (A) and in the simultaneous presence (B) of 2 mm NaCN and 1 mm SHAM. Other experimental
conditions were as described for Figure 1. gr F.W., Grams fresh
weight.
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| Figure 2.
Effects of 2 mm NaCN and 1 mm SHAM, fed separately or in combination, on the basal and
FC-induced increase in O2 consumption. Other experimental
conditions were as described for Figure 1. gr F.W., Grams fresh
weight.
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| Figure 4.
Counteracting effect of FC on the respiratory
burst induced by 2 µm Ag+ in E. densa leaves. Other experimental conditions were as described for Figure 1. gr F.W., Grams fresh weight.
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In a further exploration of this clear-cut antagonism between FC action
and the ability of NEM to induce the respiratory burst, we investigated
how FC influenced the effects of NEM on the membrane electrical
potential and on electrolyte leakage: two responses to NEM or other SH
blockers usually associated with that of QO2 (Bellando et al., 1997; for the toxic effect of SH blockers on plasma
membrane functionality, see Delrot et al., 1980; Lichtner and
Spanswick, 1981; Loos and Lüttge, 1984). Figure
5A shows that FC efficiently, but only
partially, inhibited the NEM-induced increase in electrolyte leakage,
in contrast to its ability to completely suppress the NEM-induced
respiratory activation. The effect of FC on the membrane potential of
the NEM-treated cells is more complex, and the interpretation is
difficult because of the interference of the strong hyperpolarizing
action of FC. Figure 5B highlights two phases in the phenomenon. In an
earlier phase (lasting approximately 25 min after the addition of NEM
to the FC-pretreated leaves), the presence of FC does not prevent the NEM-induced depolarization; however, the cells treated with FC and NEM
remain hyperpolarized by about 40 mV above those treated with NEM
alone. In a second phase, the FC-induced hyperpolarization disappears
as well; therefore, after 90 min the same transmembrane electric
potential difference values are reached by all samples, independently
of the presence of FC. A possible interpretation could be that NEM acts
on more than one target and that its initial action on membrane
potential is not suppressed by FC, whereas in the second phase, it
attacks other systems, in particular the H+-ATPase, the activation of which is responsible
for the hyperpolarizing action of FC (Marrè et al., 1989b; for
the inhibition by NEM of the H+-ATPase, see
Brooker and Slayman, 1982).
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| Figure 5.
Counteracting effect of FC on the increase in
medium conductivity and on membrane depolarization induced by 0.2 mm NEM in E. densa leaves. Basal medium
consisted of 0.5 mm CaSO4, 5 µm DCMU, and 10 mm Mes buffer, pH 6.0, with BTP.
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The contrast between the total inhibition of the respiratory response
to NEM and the partial inhibition of the electrolyte response is
similar to the behavior previously observed in treatments with the two
oxidase inhibitors diphenylene iodonium and quinacrine, which only
partially inhibit NEM-induced electrolyte leakage and depolarization,
while completely suppressing the respiratory burst (Bellando et al.,
1997). In both cases, the simplest interpretation is that of a relative
independence of the effects of the SH blocker on both the general
organization of the membrane and on the enzyme system responsible for
the respiratory burst (Bellando et al., 1997). The results reported in
Table I that show that FC only partially
counteracted the basification of the medium, and the marked release of
K+ induced by NEM in E. densa leaves
are in agreement with this interpretation.
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Table I.
Effects of NEM and FC on titratable proton extrusion
(H+) and on K+ net uptake
(K+) in E. densa leaves
Basal composition of the medium (control) consisted of the following:
0.5 mm Mes adjusted to pH 6.0 with BTP, 0.5 mm
CaSO4, 0.25 mm K2SO4,
and 5 µm DCMU, with 0.1 mm FC and/or 0.2 mm NEM when present.
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DISCUSSION AND CONCLUSION |
The respiratory activation by the SH blockers NEM and
Ag+, and by FC, involve two clearly distinct
oxidative pathways: a nonmitochondrial, CN-
and SHAM-insensitive one and one completely blocked by
CN. The finding that FC completely blocks the
respiratory effect of NEM even in the presence of
CN and SHAM (in spite of the total inhibition
of the effects of FC on respiration under these conditions) indicates
that the stimulation of CN-sensitive
respiration by the toxin is not a necessary step in the repression of
NEM capability to induce the oxidative burst. A possible interpretation
of the action of FC, both in activating a
CN-sensitive respiratory pathway and in
suppressing the NEM- and Ag+-induced respiratory
burst, is that the toxin could primarily interact with a receptor
located in the plasma membrane. Recently, this FC receptor has been
identified with a protein belonging to the 14-3-3 group (Korthout and
De Boer, 1994; Marra et al., 1994; Oecking et al., 1994), several
members of which have been shown to be involved in the regulation of a
number of enzyme activities (Aitken et al., 1992; Moorhead et al.,
1996; De Boer, 1997). The FC-receptor complex might then be responsible
for the activation of CN-sensitive respiration
and also, independently, for the repression of the effects of SH
blockers on QO2 and electrolyte leakage.
The hypothesis that the primary interaction of FC with its receptor
might give rise to a multiplicity of effects (De Boer, 1997), beyond
the well-established one on the H+-ATPase (De
Michelis et al., 1996), has already been proposed to interpret the FC
effect on respiration (Marrè et al., 1993). The ability of FC to
efficiently counteract the effects of SH blockers demonstrated here is
in agreement with previous evidence suggesting that FC increases the
reduction state of NADP and thiol compounds (Rasi-Caldogno et al.,
1978; Trockner and Marrè, 1988; Marrè et al., 1989a, 1994),
a view also supported by some recent results from this laboratory
showing a statistically significant increase (20%) of NADPH in
E. densa leaves treated with FC in the absence of
K+ (P. Vergani, personal communication). Because
the respiratory burst induced by NEM or by other SH blockers depends on
the reaction between these reagents and the SH groups of cell
components, the suppression of the respiratory effect of SH blockers by
FC might be due to its capability to increase the reducing power of the pyridine coenzyme-SH system in the cell, thus protecting SH groups from
attack by the SH blockers. In this respect it is worth pointing out
that a well-conserved Cys is present in a definite region of the 14-3-3 proteins so far studied (Oecking et al., 1994), thus suggesting the
hypothesis of an involvement of this protein family in both the effects
of FC and of SH reagents on respiration.
An interesting aspect of the results reported here is that they
converge with recent reports (De Boer, 1997) that propose that the
model in which FC specifically influences the plasma membrane
H+-ATPase should be corrected to a new one. In
this model FC would primarily bind to a 14-3-3 protein, modifying it so
as to give rise to a series of responses, including activation of the
H+ pump, inhibition of nitrate reductase
(Moorhead et al., 1996), stimulation of respiration, and the protection
of SH groups from SH blockers. This interpretation is depicted in
Figure 6A, where the interaction between
FC and the SH blockers would occur at the level of some SH
group-containing cell components.
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| Figure 6.
Alternative models of the interaction between FC
and SH blockers. The interaction occurs at the level of the SH systems
redox state in A, and at the level of ion transport and membrane
polarization in B.
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The present data are also open to a different interpretation, which is
depicted in Figure 6B. Recent reports suggest that the induction of the
oxidative burst by pathogenic elicitors might be caused by changes in
ion fluxes at the membrane level (Jabs et al., 1997; for the role of
Ca2+ transport in oxidative burst, see Atkinson
et al., 1990; Schawacke and Hager, 1992; Levine et al., 1996). If the
view is accepted that in our system as well the effects of NEM or
Ag+ on ion transport and membrane potential
mediate the activation of NADPH oxidase, then the interaction between
FC and SH blockers might be interpreted as occurring at the ion
transport level. Here the stimulation of K+ and
Cl uptake and of H+
extrusion and the hyperpolarization of the membrane induced by the
toxin counteract the release of K+ and
Cl, the increase in H+
influx, and the depolarization induced by the SH blockers (Table I;
Fig. 5; Bellando et al., 1997).
The choice between the two interpretations presented cannot be made on
the basis of available data, and a more detailed description of the ion
fluxes (in particular of Ca2+) and of the
electrophysiological parameters of the phenomenon are required.
| |
FOOTNOTES |
1
This work was supported by the Ministero
Italiano dell' Università e della Ricerca Scientifica e
Tecnologica (40%).
*
Corresponding author; e-mail teamarre{at}imiucca.unimi.it; fax
39-2-26-60-43-99.
Received July 14, 1997;
accepted October 28, 1997.
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ABBREVIATIONS |
Abbreviations:
BTP, 1,3-bis
Tris(hydroxymethyl)methylamino-propane.
FC, fusicoccin.
NEM, N-ethylmaleimide.
QO2, O2
uptake.
SH, sulfhydryl.
SHAM, salicylhydroxamic acid.
| |
ACKNOWLEDGMENTS |
We are grateful to Prof. Erasmo Marré for useful advice
and to Prof. Ida de Michelis for critical reading of the manuscript. Thanks are also due to Prof. Robert Jennings for revising the English
manuscript.
| |
LITERATURE CITED |
Aitken A,
Collinge DB,
Van Heusden BPH,
Isobe T,
Roseboom PH,
Rosenfeld G,
Soll J
(1992)
14-3-3 proteins: a highly conserved, widespread family of eukaryotic proteins.
Trends Biochem Sci
17:
498-501
[CrossRef][ISI][Medline]
Albergoni F,
Rocco P,
Bellando M,
Sacco S,
Marrè MT
(1996)
The induction of oxidative burst in Elodea densa by sulfhydryl reagents is independent of the inhibiting action of these reagents on photosynthesis.
Rend Fis Acc Lincei
9:
171-177
Atkinson MM,
Keppler LD,
Orlandi EW,
Baker CJ,
Mischke CF
(1990)
Involvement of plasma membrane calcium influx in bacterial induction of the K+/H+ and hypersensitive responses in tobacco.
Plant Physiol
92:
215-221
[Abstract/Free Full Text]
Auh CK,
Murphy TM
(1995)
Plasma membrane redox enzyme is involved in the synthesis of O2 and H2O2 by Phytophthora elicitor-stimulated rose cells.
Plant Physiol
107:
1241-1247
[Abstract]
Babior BM
(1992)
The respiratory burst oxidase.
Adv Enzymol
65:
49-95
Beffagna N, Romani G, Marrè E (1989) ATP level and proton
pump activity in Elodea leaves. In J Dainty, MI De Michelis, E Marrè , F Rasi-Caldogno, eds, Plant Membrane
Transport: The Current Position. Proceedings of the Eighth
International Workshop on Plant Membrane Transport, Venice, Italy, June
25-30, 1989
Bellando M,
Sacco S,
Albergoni F,
Rocco P,
Marrè MT
(1997)
Transient stimulation of oxygen uptake induced by sulfhydryl reagents in Egeria densa and Potamogeton crispus leaves.
Bot Acta
110:
388-394
Brooker RJ,
Slayman CW
(1982)
Inhibition of the plasma membrane H+-ATPase of Neurospora crassa by N-ethylmaleimide. Protection by nucleotides.
J Biol Chem
257:
12051-12057
[Abstract/Free Full Text]
De Boer B
(1997)
Fusicoccin
a key to multiple 14-3-3 locks?
Trends Plant Sci
2:
60-66
Delrot S,
Despeghel JP,
Bonnemain JL
(1980)
Phloem loading in Vicia faba leaves: effects of N-ethylmaleimide and parachloromercuribenzenesulfonic acid on H+ extrusion, K+ and sucrose uptake.
Planta
149:
144-148
De Michelis MI,
Rasi-Caldogno F,
Pugliarello MC,
Olivari C
(1996)
Fusicoccin binding to its plasma membrane receptor and the activation of the plasma membrane H+-ATPase.
Plant Physiol
110:
957-964
[Abstract]
Jabs T,
Tschöpe M,
Colling C,
Hahlbrock K,
Scheel D
(1997)
Elicitor-stimulated ion fluxes and O2 from the oxidative burst are essential components in triggering defense gene activation and phytoalexin synthesis in parsley.
Proc Natl Acad Sci USA
94:
4800-4805
[Abstract/Free Full Text]
Lado P,
Cerana R,
Bonetti A,
Marrè MT,
Marrè E
(1981)
Effects of calmodulin inhibitors in plants. I. Synergism with fusicoccin in the stimulation of growth and H+ secretion and in the hyperpolarization of the transmembrane electric potential.
Plant Sci Lett
23:
253-262
[CrossRef]
Levine A,
Pennell RI,
Alvarez ME,
Palmer R,
Lamb C
(1996)
Calcium-mediated apoptosis in a plant hypersensitive disease resistance response.
Curr Biol
6:
427-437
[CrossRef][ISI][Medline]
Lichtner FT,
Spanswick RM
(1981)
Electrogenic sucrose transport in developing soybean cotyledons.
Plant Physiol
67:
869-874
[Abstract/Free Full Text]
Loos S,
Lüttge U
(1984)
Effects of HgCl2 on membranes of Lemna gibba in the energized and non-energized state.
Physiol Veg
22:
171-179
Korthout HAAJ,
de Boer AH
(1994)
A fusicoccin binding protein belongs to the family of 14-3-3 brain protein homologs.
Plant Cell
6:
1681-1692
[Abstract]
Marra M,
Fullone M,
Fogliano V,
Pen J,
Mattei M,
Masi S,
Aducci P
(1994)
The 30-kilodalton protein present in purified fusicoccin receptor preparations is a 14-3-3-like protein.
Plant Physiol
106:
1497-1501
[Abstract]
Marrè E,
Bellando M,
Albergoni F,
Sacco S
(1993)
Stimulation of oxygen uptake by fusicoccin in conditions of inhibited H+ extrusion.
Rend Fis Acc Lincei
9:
173-178
Marrè E,
Marrè MT,
Moroni A,
Venegoni A,
Albergoni F
(1994)
Metabolism-mediated control of ATP-driven H+ extrusion: some evidence and a working hypothesis.
In
D Chiatante,
J Gallon,
C Smith,
G Zocchi,
eds, Biochemical Mechanisms Involved in Growth Regulation, Phytochemical Society of Europe.
Oxford University Press, Milan, Italy, pp 245-258
Marrè MT,
Albergoni FG,
Moroni A,
Marrè E
(1989a)
Light-induced activation of electrogenic H+ extrusion and K+ uptake in Elodea densa depends on photosynthesis and is mediated by the plasma membrane H+-ATPase.
J Exp Bot
40:
343-352
[Abstract/Free Full Text]
Marrè MT,
Albergoni FG,
Moroni A,
Pugliarello MC
(1989b)
On the involvement of the ATP-driven H+ pump in H+ extrusion in Elodea densa leaves.
Plant Sci
62:
21-28
Moorhead G, Douglas P, Morrice N, Scabel M, Aitken A, MacKintosh C
(1996) Phosphorylated nitrate reductase from spinach leaves is
inhibited by 14-3-3 proteins and activated by fusicoccin. Curr Biol
6: 1104-1113
Oecking C,
Eckerskorn C,
Weiler EW
(1994)
The fusicoccin receptor of plants is a member of the 14-3-3 superfamily of eukaryotic regulatory proteins.
FEBS Lett
352:
163-166
[CrossRef][ISI][Medline]
Rasi-Caldogno F, Lado P, Colombo R, Cerana R, Pugliarello MC
(1978) Changes in Cellular Metabolism Associated with the Activation of
H+/K+ Exchange by Auxin or
FC in Pea Internode Segments. Proceeding of the Inaugural Meeting of
the Federation of European Societies of Plant Physiology, Edinburgh,
Scotland, pp 438-439
Schawacke R,
Hager A
(1992)
Fungal elicitors induce a transient release of active oxygen species from cultured spruce cells that is dependent on Ca2+ and protein-kinase activity.
Planta
187:
136-141
Trockner V,
Marrè E
(1988)
Plasmalemma redox changes and H+ extrusion. II. Respiratory and metabolic changes associated with fusicoccin-induced and with ferricyanide-induced H+ extrusion.
Plant Physiol
87:
30-35
[Abstract/Free Full Text]
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Abstract
Introduction
