JXB Advance Access originally published online on July 8, 2008
Journal of Experimental Botany 2008 59(11):3121-3129; doi:10.1093/jxb/ern166
RESEARCH PAPER |
Anion channel activity is necessary to induce ethylene synthesis and programmed cell death in response to oxalic acid
1LEM (EA 3514), Université Paris Diderot, 2 place Jussieu, 75251 Paris cedex 05, France
2UPMC Université Paris 06, EA 2388, Physiologie des semences, Site d'Ivry, 4 place Jussieu, 75252 Paris cedex 05, France
* To whom correspondence should be addressed. E-mail: francois.bouteau{at}univ-paris-diderot.fr
Received 18 March 2008; Revised 13 May 2008 Accepted 14 May 2008
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Abstract |
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Oxalic acid is thought to be a key factor of the early pathogenicity stage in a wide range of necrotrophic fungi. Studies were conducted to determine whether oxalate could induce programmed cell death (PCD) in Arabidopsis thaliana suspension cells and to detail the transduction of the signalling pathway induced by oxalate. Arabidopsis thaliana cells were treated with millimolar concentrations of oxalate. Cell death was quantified and ion flux variations were analysed from electrophysiological measurements. Involvement of the anion channel and ethylene in the signal transduction leading to PCD was determined by using specific inhibitors. Oxalic acid induced a PCD displaying cell shrinkage and fragmentation of DNA into internucleosomal fragments with a requirement for active gene expression and de novo protein synthesis, characteristic hallmarks of PCD. Other responses generally associated with plant cell death, such as anion effluxes leading to plasma membrane depolarization, mitochondrial depolarization, and ethylene synthesis, were also observed following addition of oxalate. The results show that oxalic acid activates an early anionic efflux which is a necessary prerequisite for the synthesis of ethylene and for the PCD in A. thaliana cells.
Key words: Anion channel, Arabidopsis thaliana, ethylene, oxalic acid, programmed cell death
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Introduction |
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The phytotoxin oxalic acid is found to be produced by many necrotrophic plant pathogens. The early stage of infection by these fungi involves the production and the accumulation of a large amount of oxalic acid which appears to be an essential determinant of pathogenicity (Noyes and Hancock, 1981; Dutton and Evans, 1996; Guimaraes and Stotz, 2004). Accumulation of oxalate often reaches millimolar concentrations (up to 10 mM) in infected tissues (Bateman and Beer, 1965; Marciano et al., 1983). Even if oxalic acid could be generated from ascorbic acid breakdown (Green and Fry, 2005), the apoplastic ascorbate concentration is close to 1 mM (Kollist et al., 2001; Pignocchi and Foyer, 2003) which is negligible compared with the concentration delivered by a pathogenic fungus (Bateman and Beer, 1965; Marciano et al., 1983). Once produced and accumulated, oxalate plays a key role, provoking some disease-like symptoms independent of pathogen presence (Bateman and Beer, 1965; Noyes and Hancock, 1981). Moreover, Sclerotinia sclerotium mutants deficient in oxalate synthesis are no longer pathogenic (Godoy et al., 1990) and transgenic plants expressing oxalate decarboxylase show enhanced resistance to phytopathogenic fungus that utilize oxalic acid during infection (Kesarwani et al., 2000; Livingstone et al., 2005). Acidification of plant tissues enhanced by oxalate accumulation drives the activation of various fungal enzymes including specific isoforms of endo-polygalacturonase (Manteau et al., 2003; Favaron et al., 2004; Kars et al., 2005) and proteinases (Manteau et al., 2003; ten Have et al., 2004). Oxalate was shown to block a signalling event in the oxidative burst pathway which could compromise the defence responses of the host plant independently of both its acidity and its affinity for calcium (Cessna et al., 2000).
A wide variety of phytotoxins have also been shown to induce programmed cell death (PCD) in plant cells, among them AAL-toxin (Gechev et al., 2004), FB1 (Asai et al., 2000), fusicoccin (Malerba et al., 2003), and victorin (Curtis and Wolpert, 2004). These toxins are able to induce defence signalling pathways which are dependent on reactive oxygen species (ROS), jasmonic acid (JA), and ethylene (ET), and which lead to PCD. Recently, detailed analyses carried out with the phytotoxin fusaric acid demonstrated the induction of early defence-related responses, such as an increase in [Ca2+]cyt, plasma membrane (PM) depolarization, an increase in anion current, an extracellular alkalization, and a production of ROS, followed by accumulation of phytoalexin (Bouizgarne et al., 2006) and PCD (Samadi and Shahsavan Behboodi, 2006). Anion channel-mediated anion effluxes were also shown to be an essential component of cryptogein-induced cell shrinkage during PCD (Wendehenne et al., 2002; Gauthier, 2007). However, transduction of the signals that are involved in PCD activation seems to be dependent on the stimuli. We are still far from fully understanding the phytotoxin-specific cell death mechanisms even if DNA fragmentation and cell shrinkage, mediated by a net efflux of water caused by the release of ions, seem to be major hallmarks of the PCD process in plant and animal cells (Maeno et al., 2000; Lam, 2004; Okada et al., 2006).
There is a lack of information concerning the induction of PCD by oxalate in plant cells. The purpose of this work was (i) to investigate whether oxalate could induce PCD and (ii) to detail the transduction of the PCD signal induced by oxalic acid. The study unambiguously shows that oxalate can induce PCD in Arabidopsis thaliana plant cells and that this PCD is regulated by the activation of an anion channel and by the synthesis of ET.
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Materials and methods |
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Chemicals
The pH of oxalic acid (ethanedioic acid) solution was systematically adjusted to 5.8 with KOH before addition to the culture medium.
Cell culture conditions
For this study, A. thaliana L. (ecotype Columbia) suspension cultures were used. Suspension cells have been shown to be a convenient system for identifying early physiological events induced by pathogens or their derived elicitors (Cessna et al., 2000; Wendehenne et al., 2002; Bouizgarne et al., 2006; Samadi and Shahsavan Behboodi, 2006; Gauthier, 2007; Reboutier et al., 2007). They show physiological responses to various stimuli, similarly to the autonomous cellular responses in intact tissues, especially the morphological features of dying cells during PCD (van Doorn and Woltering, 2005), and thus allow the observation of events in each single cell or the real-time behavioural monitoring of large populations of cells. Arabidopsis thaliana suspension cells were grown in Gamborg medium (pH 5.8). They were maintained at 22±2 °C, under continuous white light (40 µE m–2 s–1) and continuous shaking (gyratory shaker) at 120 rpm. Cell suspensions were subcultured weekly using a 1:10 dilution. All experiments were performed at 22±2 °C using log-phase cells (4 d after subculture).
Cell viability assays
Cell viability was assayed using the vital dye neutral red. Cells (50 ml) were incubated for 5 min in 1 ml of phosphate buffer pH 7 with neutral red to a final concentration of 0.01%. Cells that did not accumulate neutral red were considered dead. Cell viability was also assayed using the vital dye, Evans blue, in the presence of oxalate alone or with the appropriate pharmacological effectors. Cells (50 ml) were incubated for 5 min in 1 ml of phosphate buffer pH 7 supplemented with Evans blue to a final concentration of 0.005%. Cells that accumulated Evans blue were considered dead. At least 1000 cells were counted for each independent treatment.
Cell death was also quantified using the fluorescein diacetate (FDA) spectrofluorimetric method (Reboutier et al., 2007). Briefly, 4-d-old A. thaliana suspension cells were collected and washed by filtration in a suspension buffer containing 175 mM mannitol, 0.5 mM CaCl2, 0.5 mM K2SO4, and 10 mM HEPES (H10 medium) adjusted to pH 5.8 (with KOH). A 1 ml aliquot of cell suspension was incubated in the presence of oxalate. At each incubation time, 500 µl of the suspension was diluted in 1.5 ml of H10 medium in a quartz cuvette. Then, FDA was added at a final concentration of 12 µM and the fluorescence increase was monitored over a 2 min period using a Hitachi F-2000 spectrofluorimeter. The slope of fluorescence increase, representing cell viability, was calculated for each treatment, and directly compared with non-treated cells. Cell death was calculated as follows: % of cell death = 100x(slope of treated cells/slope of non-treated cells). The experiment was repeated at least four times for each condition.
DNA extraction and analysis
Frozen cells were ground in liquid nitrogen, and genomic DNA was extracted according to the cetyltrimethyl ammonium bromide (CTAB) method of Haymes et al. (2004). DNA electrophoresis was performed to assess DNA fragmentation. DNA samples (5 mg per lane) were loaded on a 1.8% agarose gel, and stained with 0.2 mg ml–1 ethidium bromide.
Electrophysiology
Individual cells were impaled and voltage-clamped in the culture medium using an Axoclamp 2B amplifier (Axon Instruments, Foster City, CA, USA) for discontinuous single electrode voltage clamp experiments as previously described (El-Maarouf et al., 2001; Reboutier et al., 2002; Brault et al., 2004). Voltage and current were digitized with a personal computer fitted with a Digidata 1320A acquisition board (Axon Instruments). The electrometer was driven by pClamp software (pCLAMP8, Axon Instruments). The experiments were conducted on 4-d-old cultures (main ions in the medium after 4 d of culture: 9 mM K+, 11 mM NO3–) (Reboutier et al., 2002). Experiments were performed at 22±2 °C.
Mitochondrial membrane potential measurement
Arabidopsis thaliana cells were prepared as described for FDA measurement (0.1 g FW ml–1) in a medium containing 50 mM HEPES, 0.5 mM CaCl2, 0.5 mM K2SO4, and 10 mM Glc (pH 7.0). Before treatment, cells were first stained with the mitochondrial membrane potential probe JC-1 by incubating 2 ml of cell suspensions for 15 min (24 °C in the dark) with 2 µg ml–1 JC-1 (3 µM). JC-1 from Molecular Probes Inc. (Eugene, OR, USA) was dissolved and stored according to the manufacturer's instructions. Treated cells without prior washing were subjected to analysis using a Hitachi F-2000 spectrofluorimeter. The excitation wavelength used was 500 nm. Fluorescence signals were collected using a bandpass filter centred at 530 nm and 590 nm.
Ethylene measurement
A 4 ml aliquot of cells was subcultured in 10 ml flasks tightly closed with serum caps, maintained at 22 °C under constant shaking. After 2 h, a 2 ml gas sample was taken from each flask and injected into a gas chromatograph (Hewlet Packard 5890 series II) equipped with a flame ionization detector and an activated alumina column (6 mm in internal diameter, 50 cm long, 50–80 mesh) for ethylene determination. Results are presented as means of four measurements ±SD, and are expressed as picomoles of ethylene produced per 1 g of fresh matter.
Statistics
Significant differences between treatments were determined by the Mann–Whitney test, and P-values <0.05 were considered significant.
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Results |
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Oxalate induces programmed cell death
Millimolar concentrations of oxalate (up to 10 mM), close to those found in infected tissues (Bateman and Beer, 1965; Marciano et al., 1983), were tested on host cell viability using A. thaliana suspension-cultured cells. Three different methods were used in parallel to analyse cell death in order to obtain reliable measures (Rizhsky et al., 2004): the live/dead staining methods with combinations of FDA, neutral red staining, and Evans blue staining. Albeit that these detection methods lead to a small variability in oxalate-induced cell death, a 24 h treatment with increasing concentrations of oxalate resulted in dose-dependent cell death (Fig. 1c, d). In order to discriminate between the effects of oxalic acid itself as an inducer of PCD and a putative cytosol acidification due to diffusion of oxalic acid into the cytosol, the impact of acetic acid on A. thaliana cell death was tested. Acetic acid up to 12 mM only slightly affects the cell viability when compared with oxalic acid (Fig. 1e). The percentage of dead cells, quantified with FDA, reached a plateau after 8 h of treatment with 6 mM oxalate (Fig. 1f). Oxalate-induced vacuole shrinkage (Fig. 1a, right-hand picture) led to a complete collapse of the dead cells (Fig. 1b, right-hand picture). In order to check whether oxalate-induced cell death is an active mechanism requiring active gene expression and cellular metabolism, A. thaliana cell suspensions were treated with actinomycin D (AD), an inhibitor of RNA synthesis, or with cycloheximide (Chx), an inhibitor of protein synthesis, 15 min prior to 6 mM oxalate addition. Although pre-treatments of A. thaliana cells with these inhibitors resulted in a slight increase in cell death (Fig. 1g), AD and Chx significantly reduced the oxalate-induced cell death (24 h after oxalate treatment) from 97% to 54% and 46%, respectively (Fig. 1g). These results indicated that the oxalate-induced cell death required active cell metabolism, namely gene transcription and de novo protein synthesis. In order to check whether this active cell death displays other apoptotic features, a putative nuclear DNA cleavage was looked for in a ladder of internucleosomal fragments. Gel analysis of DNA extracted from cell suspensions after a 12 h treatment with 6 mM oxalate showed a typical DNA laddering (Fig. 1h). This specific DNA cleavage induced by 6 mM oxalate has been shown to be dependent on active gene expression and de novo protein synthesis since it was not detected after addition of AD or Chx to the suspension cell cultures (Fig. 1h). Taken together, these data clearly indicate that millimolar concentrations of oxalate induce PCD in A. thaliana cells.
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Activation of anion channels is a crucial early event for oxalate-induced cell death
Cell shrinkage is a major hallmark of PCD. This process may be mediated by a net efflux of water resulting from the release of anions and K+ (Maeno et al., 2000). Indeed, anion efflux, detectable as a current increase, has been reported to be a necessary event to achieve cell death in tobacco suspension cells subjected to a treatment with cryptogein (Wendehenne et al., 2002; Gauthier, 2007). We undertook an electrophysiological approach in order to determine the role of oxalate on cell membrane potential and on anion currents. The value of the resting membrane potential (Vm) of control cells in their culture medium was –47±5 mV (n=96), similar to values found in previous studies (Reboutier et al., 2002, 2007; Bouizgarne et al., 2006). Oxalate induced a rapid depolarization of the cell PM (Fig. 2a), reaching a maximal value within 2±1 min (n=10). This PM depolarization was concentration dependent (Fig. 2b). Previous electrophysiological studies and pharmacological analyses had identified an anion current which displays the main characteristics of slow anion channels (Reboutier et al., 2002) in the PM of A. thaliana cells. This current was shown to be sensitive to structurally unrelated anion channel inhibitors, 9-anthracene carboxylic acid (9-AC), glibenclamide (gli), and niflumic acid (NA) (Reboutier et al., 2002, 2007; Brault et al., 2004; Reboutier et al., 2007). Oxalate also induced a concentration-dependent increase of anion current (not shown) reaching 580% at 6 mM (Fig. 2c–e) from a mean control value of –0.28±0.08 nA (n=45). The increase in anion current might explain the depolarization due to oxalate since pre-treatment of cells with gli or 9-AC (200 µM) reduced it to almost zero (Fig, 2e). The effects of anion channel blockers on the induction of cell death by oxalate were also tested. Oxalate (6 mM) induced
90% of cell death within 24 h (Fig. 1c, d). When treated with anion channel blockers, only a slight cell death was induced (Fig. 2f, g), thus significantly lowering the level of oxalate-induced cell death (Fig. 2f, g). These results suggested that the anion current increase was a required upstream event in the signalling pathway leading to oxalate-induced cell death.
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Mitochondrial depolarization is involved in oxalate-induced cell death
Since alterations of mitochondrial function, notably a mitochondrial membrane potential (
m) loss, might also play a role in the early stages of PCD induction in both plants and animals (Vianello et al., 2007), an investigaton was carried out to check whether oxalate could lead to a decrease in the 
m. The K+ ionophore valinomycin (1 µM, Fig. 3a) was used as a positive control of m decrease. In untreated cells, the JC-1 fluorescence ratio of mitochondria displaying a high m versus mitochondria presenting a low m was largely >1 (Fig. 3a). This ratio decreased in a time- and a concentration-dependent manner upon addition of oxalate, reaching a value <1, indicating that oxalate induced a significant decrease of m in most mitochondria (Fig, 3a). Since the mitochondrial m decrease during cell death was reported to be due to the formation of the mitochondrial permeability transition pore (PTP) (Vianello et al., 2007), the effect of cyclosporin A (CsA), a well-known inhibitor of the PTP, on oxalate-induced mitochondrial depolarization and oxalate-induced cell death was tested. A pre-treatment with CsA significantly reduced the oxalate-induced mitochondrial depolarization after 2 h (Fig. 3b), indicating that mitochondrial PTP was involved in oxalate-induced mitochondrial depolarization. Although treatment with CsA only increased cell death to a certain level (35% of oxalate-induced cell death), pre-treatment with CsA significantly inhibited the oxalate-induced cell death by 20% (Fig. 3c) after 24 h. Interestingly, the oxalate-induced decrease of m was not inhibited by 9-AC or gli (Fig. 3d), indicating that the early anion current increase was not involved in the signalling pathway leading to the oxalate-induced mitochondrial formation of the PTP, and further suggesting that at least two different pathways could be involved in the oxalate-induced cell death.
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Ethylene synthesis is involved in oxalate-induced cell death
In A. thaliana, resistance to the oxalate-producing pathogen Botrytis cinerea depends on ET signalling (Glazebrook, 2005). As ET is also known to modulate cell death (Overmyer et al., 2003; Lam, 2004), experiments were conducted to determine whether an inhibitor of ET synthesis could act on oxalate-induced cell death. Treatment of suspension cells by aminooxyacetic acid (AOA), an inhibitor of ACC synthase (Yu et al., 1979), or by
-aminoisobutyric acid (AIB), an inhibitor of ACC oxidase (Satoh and Esashi, 1980), at 200 µM for 24 h induced a 25% increase in cell death (Fig. 4a). However, both inhibitors significantly reduced the level of oxalate-induced cell death, especially AIB which reduced cell death by 30% (Fig. 4a). Thus ET synthesis was investigated. Oxalic acid at 6 mM did not induce ET production after 1 h of treatment (not shown). However, after 2 h a 100% increase in the amount of ET was observed in the cell culture flask (Fig. 4b). The effects of anion channel blockers on ET synthesis by oxalate were also tested. Treatment with anion channel blockers inhibited ET synthesis by oxalate and led to a decrease in the control ET level (Fig. 4b). These results suggest that an anion current-dependent ET synthesis is involved in the pathway leading to oxalate-induced cell death.
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Discussion |
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Oxalate is essential for the development of disease symptoms and pathogenicity of various necrotrophics among the most damaging plant pathogens (Dutton and Evans, 1996). The pathogenicity of fungal oxalate was previously ascribed to its acidity, which is believed to aid fungal invasion by direct cellular toxicity or by the establishment of a more suitable apoplastic pH for cell wall-degrading enzymes (or both) (Dutton and Evans, 1996). Although oxalate-induced cell death develops more rapidly without adjusting the pH of the oxalate solution (data not shown), the activity remained even when acidification was prevented. This suggests that acidification is not the only mode of oxalic acid action bringing about deleterious effects. Indeed, oxalate-induced cell death has been shown to be achieved and completed at concentrations measured in leaf materials infected with pathogenic strains of Sclerotinia (Marciano et al., 1983). Here it is demonstrated that oxalate induces drastic cell death which fulfils the criteria for PCD in cultured A. thaliana cells, in a fashion similar to that initiated by other phytotoxins. First, it was shown that oxalate induced a genetically controlled PCD in A. thaliana cultured cells that required active gene expression and de novo protein synthesis, and that this was associated with apoptosis-like features, such as cleavage of nuclear DNA. These data fulfil the widely accepted criteria for PCD, described as the genetically controlled and ordered processes that require active metabolism. The oxalate-induced cell shrinkage, another hallmark of the PCD process in both plant and animal cells (Maeno et al., 2000; Lam, 2004), was probably due to a large activation of anion channels by oxalate. This activation of anion release appears important since various anion channel blockers, previously shown to be effective in A. thaliana suspension cells (Reboutier et al., 2002, 2007; Brault et al., 2004), decreased the oxalate-induced cell depolarization, anion channel increase, and finally cell death. Such an efflux of anions would drive water efflux, leading to cell shrinking. In various mammalian cell types, apoptotic volume decrease, which is mediated by water loss caused by activation of anion channels and the ensuing K+ efflux, is an early prerequisite for apoptotic events including cell shrinkage, cytochrome c release, activation of proteases (including caspase) and nucleases, and ultimately leading to PCD (Okada et al., 2006). Involvement of ion release via ION flux modulation is considered to be most essential among the earliest responses of plant cells to avirulent pathogens or elicitors capable of inducing PCD (Lam, 2004). Recently it has been shown that the involvement of anion channels, a critical component of the cell death process in cryptogein-induced cell shrinkage during PCD of tobacco suspension cells, promoted the accumulation of vacuolar processing enzymes showing caspase-1 activity involved in the disruption of vacuole integrity observed during this cell death (Gauthier, 2007). As a whole, these data suggest that the oxalate-induced anion channel activation is not a passive secondary aspect of PCD, but an event that inevitably drives the whole process. These data are reminiscent of those observed in response to cryptogein (Wendehenne et al., 2002; Gauthier, 2007) and pointed out a critical role for anion channels in the signalling response to pathogens. Anion channels are now becoming recognized as important players in signalling pathways associated with adaptation of plant cells to abiotic and biotic environmental stresses (de Angeli et al., 2007), and here this evidence is further strengthened. In addition, it is shown that anion current increase is a necessary upstream event in oxalate-induced ET synthesis. Moreover, this event is certainly linked to the oxalate-induced PCD since it involves ET synthesis, as evidenced by using blockers of ACC synthase and ACC oxidase, two key enzymes in the ET synthesis pathway (Wang et al., 2002). Interestingly, anion effluxes are also necessary for the oxalate-related induction of ET-dependent defence-related genes (e.g. PDF1-2, not shown) in seedlings. The present data are in agreement with previous reports indicating that ET synthesis is involved in elicitor-induced cell death (Quin and Lan, 2004), victorin-induced PCD (Curtis and Wolpert 2004), and developmentally induced PCD (Overmyer et al., 2003), and more generally during the interaction between plants and necrotrophic pathogens, especially the oxalate-producing pathogens (Glazebrook, 2005).
It is further shown that oxalate-induced cell death processes could involve an alteration of mitochondrial functions caused by the activation of the PTP that results in the dissipation of mitochondrial electrical potential (m), since oxalate-induced mitochondrial depolarization and cell death were attenuated in the presence of CsA. Literally, PTP can be defined as a voltage-dependent, high-conductance mitochondrial membrane channel (Vianello et al., 2007). These data are consistent with our increasing knowledge that supports the importance of plant mitochondria in the control of PCD (Lam et al., 2004; Vianello et al., 2007), where a mitochondrial permeability transition precedes PCD (Curtis and Wolpert, 2004; Vianello et al., 2007) by allowing the release of proteins from the mitochondrial inter-membrane space. However, at this time, the role of PTP in apoptosis is quite controversial, since recent studies show that sustained PTP opening is predominantly involved in necrosis (Nakagawa, 2005) and would be a consequence rather than an initiator of PCD (Kinnaly, 2007). Recently, CsA was shown to decrease cannabinoid-induced plant cell death greatly in those plants displaying necrotic characteristics by inhibiting PTP formation (Morimoto, 2007). CsA only slightly reverses the effect of oxalate-induced mitochondrial depolarization and cell death. Thus, it cannot be excluded that a small part of the cell population undergoes a necrotic cell death pathway in response to oxalate whereas the majority of the cells undergo a PCD pathway possibly involving a CsA-independent m decrease. Further studies are needed to elucidate this point, but such different behaviours were reported on cultured saffron plant cells in response to fusaric acid (Samadi and Shahsavan Behboodi, 2006). Nevertheless, the data clearly show that oxalate, a toxin from necrotrophic fungi, can induce plant cell PCD in an ET- and anion channel activity-dependent way.
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Acknowledgements |
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We wish to thank H El Maarouf-Bouteau for her technical help in DNA laddering experiments, T Kawano for fruitful discussions and critical reading of the manuscript, and M Hodges (IBP, UMR CNRS 8616, Université Paris Sud 11, Orsay, France) for reading the manuscript. Financial support was provided to EA3514 by MENSR, PRAD 04-02 and AUF6301PS615.
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Abbreviations |
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9-AC, 9-anthracene carboxylic acid; AD, actinomycin D; AIB,
-aminoisobutyric acid; AOA, aminooxyacetic acid; Chx, cycloheximide; CsA, cyclosporin A; ET, ethylene; FDA, fluorescein diacetate; m, mitochondrial membrane potential; gli, glibenclamide; NA, niflumic acid; PCD, programmed cell death; PM, plasma membrane; PTP, permeability transition pore; ROS, reactive oxygen species; Vm, plasma membrane potential. |
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