Effects of Jasmonic Acid on Motor Cell Physiology in

Plant Cell Physiol. 35(3): 389-396 (1994) JSPP © 1994

Effects of Jasmonic Acid on Motor Cell Physiology in Mimosa pudica L. and Cassia fasciculata Michx Andree Bourbouloux, Pierrette Fleurat-Lessard and Gabriel Roblin Laboratoire de Physiologie et Biochimie Vege'tales, Institut de Biologie de Beau-Site, URA CNRS 574, University de POITIERS—Sciences, 25, Faubourg Saint-Cyprien, 86000 POITIERS, France

Key words: Cassia fasciculata — Ionic fluxes — Jasmonic acid — Mimosa pudica — Motor cell turgor — Pulvinus.

( — )-Jasmonic acid and its derivatives represent a new class of endogenous regulators of plant growth and development (Sembdner and Klose 1985, Vick and Zimmerman 1987). They are widely distributed among higher plants (Yamane et al. 1981, Meyer et al. 1984) and have physiological activities (reviewed by Sembdner et al. 1989) that indicate their hormonal-like properties. However, descriptions of the effects of JA in the literature are mainly restricted to long-term aspects of plant development, such as promotion of leaf senescence (Ueda et al. 1981), inhibition of seedling growth (Yamane et al. 1980) and of cell division (Ueda and Kato 1982), induction of rooting (Zimmermann et al. 1987) and tuberisation (Koda et al. 1991, Van der Berg and Ewing 1991). In these processes, it is conceivable that JA exerts its effects by acting at the level of specific genes. Expression of genes for specific polypeptides under the influence of JA has already been described (Weidhase et al. 1987, Parthier 1990, Staswick 1992). In contrast to previous studies, the present note was focused on the early events induced by JA in the cell. We examined the effects of JA on the physiology of the motor Abbreviations: FC, fusicoccine; JA, jasmonic acid; MeJ, methyl jasmonate; 12-oxo-PDA, 12-oxo-phytodienoic acid. 389

cells of pulvini, which are a convenient model for such a study. It is very easy to follow the movements of leaves, which are the macroscopic expression of motor cell activity. In various plants, in particular in Leguminosae, leaf movement can be induced by transferring plants from light to darkness (scotonasty) or from darkness to light (photonasty). These movements are the result of reversible variations in turgor in the cortical parenchyma cells, driven by the migration of ions (K + , Cl~, H + ) into or out of the motor cells (Satter et al. 1970, 1974). Few data have been reported on the effects of JA on cells that involve changes in turgor. Satler and Thimann (1981) reported that JA induces the closure of stomata in leaves of A vena and Tsurumi and Asahi (1985) showed that pulvinar reactions of Mimosa pudica are affected by JA. The results presented here demonstrate the effects of JA on proton fluxes and membrane potential in pulvini of Mimosa pudica and also on the scoto- and photonastic movements of pulvinar motor cells of Cassia fasciculata. The second set of results enables us to make valuable comparisons with data obtained previously from the same model after treatment with other classes of phytohormones (Everat-Bourbouloux et al. 1990), in particular with ABA.

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When applied to pulvini of Mimosa pudica, jasmonic acid (JA) affected neither proton fluxes nor the membrane potential of the motor cells. When added to leaflets of Cassia fasciculata, JA increased the rate of dark-induced pulvinar movements in a concentration-dependent manner. This effect was observed within as little as 15 min after a 1-h treatment that preceded the inducing signal. Treatments in buffered media at acidic pH resulted in the greatest physiological responses. Light-induced pulvinar movements were considerably reduced under the same conditions. With continuous illumination, JA induced a closing movement of the leaflets in a concentrationdependent manner. These results are discussed in relation to the ionic changes in the pulvinar motor cells and in relation to results obtained previously upon treatment of Cassia plants with ABA. Although ABA and JA have similar physiological effects on the dark-induced closure, they differ in the type of response elicited by brief treatment and with respect to light-induced opening.

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(scotonastic movement). Switching on the light during nyctophase induces the opening of the leaflets (photonastic Plant growth conditions—Plants of Mimosa pudica L. movement). These pulvinar movements were followed for and Cassia fasciculata Michx were grown from seed in con- 2 or 3 h after dark- or light-induction, respectively. They trolled chambers kept at 28±1 C C with a relative humidity were monitored by measuring the distance between the tips of 10+5%. Light was provided for 14 h daily, either from of leaflets with callipers at given times. The measurements 07:00 to 21:00 h for plants with a normal photoperiodic cy- were converted into angular values as described by Bonnecle (used for scotonastic experiments) or from 19:00 to main et al. (1978). The angle between two leaflets is propor09:00 h for plants with an inverted photoperiodic cycle tional to the turgor of the pulvinar motor cells. The data (used for photonastic experiments). The photon flux den- presented are mean values obtained from at least 3 experisity (400-700 nm) provided by fluorescent tubes (ACEC ments with 8 individual leaves. Statistical treatment was Charleroi, Belgium) was 36^molm~ 2 s~' at the plant performed by Student's /-test. apex. For further details, see Everat-Bourbouloux et al. Monitoring of the diurnal positions of leaflets—Fully (1990). expanded leaves were excised at 09:00 h, as previously deMeasurement of variations in pH—For an examina- scribed, from Cassia plants in the photophase. They were tion of the excretion of protons, primary pulvini (400 mg) kept in distilled water for 30 min. Then the leaves were of Mimosa were excised at 11:00 h from plants with 6 or 7 transferred to solutions of JA or ABA at various concentrafully expanded leaves, divided into transverse sections (0.5 tions in a medium buffered at pH 4.7. The distance between to 1 mm in width) and preincubated for 1 h in 5 ml of medi- the leaflet tips was measured twice hourly for 10 h. Converum that contained 0.5 mM CaCl2 and 0.25 mM MgCl2 sion of the measurements and statistical treatment were per(Lado et al. 1976) before transfer to fresh medium. The formed as described elsewhere (Everat-Bourbouloux et al. variations in pH of the incubation medium were recorded 1990). in the light as described in Otsiogo-Oyabi and Roblin Chemicals—(±)-Jasmonic acid, obtained by alkaline (1984). JA was diluted in the same medium and added as in- hydrolysis of (±)-methyl jasmonate and subsequent purification, was kindly provided by Dr. O. Miersch (Institut fur dicated in Figure 1. Its effects were compared with those of FC, which is known to induce the active extrusion of pro- Biochemie der Pflanzen, Forschungsbereich Biowissenstons (Marre et al. 1974), and with those of IAA and ABA. chaften und Medizin, 4010 Halle, Germany) and by Dr. J. Electrophysiological measurements—A fully expand- Kitahara (Department of Agricultural Chemistry, Universied leaf was excised from the stem of a Mimosa plant at the ty of Tokyo, Japan). (±)-cis,fra/w-abscisic acid was purbase of the primary pulvinus during the photophase. The chased from Sigma (Paris, France). lateral quarter of the motor organ was slit with a razor JA and ABA were dissolved separately in absolute blade and discarded. Pulvinar tissues were covered with 3 ethanol. At the highest concentrations tested, the final conml of a buffered medium (2.5 mM MES-KOH, pH 5.5) that centration of ethanol was 0.02%. Final dilutions were percontained 0.5 mM CaCl2 and 0.25 mM MgCl2. A glass formed in 2.5 mM 7V-(2-hydroxyethyl)piperazine-A''-(2microelectrode (tip diameter, < 1 fim; tip resistance, from ethanesulfonic acid) (HEPES) buffer (pH7.5) or in 2.5 5 to 30 MQ) was stuck into a motor cell in the lower half of mM 2-(A/-morpholino)-ethanesulfonic acid (MES) buffer the pulvinus. The membrane potential was measured by the (for pH 3.5,4.7 and 6.0). The pH of solutions was adjusted classical electrophysiological method with equipment that with 1 M KOH or HC1. Previous studies indicated that was described previously by Mounoury et al. (1984). JA (or these buffered solutions did not significantly affect the ABA) in the same medium was added as indicated in Figure dark- or light-induced movements. Moreover, after a 2. week, no delayed necrosis was observed after application Measurements of dark- and light-induced pulvinar of the compounds in the cited range of concentrations. movements—Fully expanded leaves of Cassia were excised at 09:00 h from 3-month-old plants with about 20 leaves. Results They were kept for several hours with the petiole dipped in distilled water to recover from shock, either in the light or Effects of JA on the change in pH of the incubation in the dark according to their origin (normal or inverted medium—Slices of primary pulvini from Mimosa induced photoperiodic cycle). The leaves were then transferred to the spontaneous acidification of the incubation medium buffered solutions of JA for 5 min to 1 h before the induc- (Roblin and Fleurat-Lessard 1983). JA added at various ing signal (either in the dark for leaves in the day position, concentrations from 10~6 to 10~4 M did not affect the rate or in the light for leaves in night position) and they were of acidification (Fig. 1). Under identical conditions, ABA kept in the same medium. (at 10~4 M) also had no effect, whereas FC (at 10~6 M) and IAA (at 10~5 M) caused large decreases in pH (Fig. 1). During photophase, leaflets of Cassia are quite open; Effects of JA on the membrane potential of pulvinar when the light is switched off, the leaflets collapse upwards Materials and Methods


Jasmonic acid and turgor regulation

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Fig. 1 Typical examples of the effects of JA on the time-course of changes in pH of the incubation medium of slices of Mimosa primary pulvini after addition of JA (arrow) at 10~4 M (O). Effects are also shown of ABA (at 1(T4 M; A), IAA (at 10~5 M; O) and fusicoccin (at 10~6 M; •). (•) Control. Identical results were obtained in four replicate experiments. motor cells—Under our conditions, the resting transmembrane potential of Mimosa motor cells was 104±19mV (n=40). Addition of JA at concentrations from 10~6 to 2 x 10~4 M did not significantly alter the transmembrane potential (Fig. 2). In order to confirm the bioelectrical viability of each impaled motor cell, FC was added (at 2 x 10~6 M) to the medium and it induced strong hyperpolarisation of the same cell (Fig. 2). Under identical conditions, ABA at 10~4 M had similar effects to those of JA whereas IAA (at 10~6 M) enhanced the transmembrane potential considerably (Fig. 2). Effects of JA on the scotonastic movement of Cassia leaflets—Treatment of Cassia leaves with JA at 5 x 10~5 M in MES at pH 4.7 for 5 min to 1 h before the light was switched off increased the rate of the scotonastic closure (Fig. 3A). One hour after lights-off, noticeable increases in the extent of dark-induced closure were observed after a 15-min and a 30-min pretreatment with JA, but the changes were without statistical significance (for P=0.05). After a 1-h pretreatment before the dark signal, a maximum effect was observed as little as 15 min (inset) after the dark signal (stimulation of closure of 31%, as compared to the control). Under these conditions, the initial position of the leaflets was affected, in the direction of closure, by JA (about 9% compared to the control when the lights-off signal was given). Thus, a 1-h treatment with JA was

Fig. 2 Typical recordings of changes in membrane potential induced in Mimosa pulvinar motor cells by addition (black arrow) of JA (•) or ABA (©). JA and ABA were used at 10"6 to 2 x 4 10~ M with similar results. FC was applied (white arrow) at 2x 10"6 M (after JA) and at 10~5 M (after ABA). Results are also shown for IAA (at 10~6 M; D); no FC was added in this case. Identical results were obtained in five replicate experiments. chosen for further experiments. Applied in buffered medium at various pH values, JA at 10~4 M enhanced the rate and the amplitude of the scotonastic response, in particular under acidic conditions (Fig. 3B). The largest increase was obtained at pH 3.5 and pH 4.7, but the dark-induced response was also modified in the same way at closer to neutral pH, in particular at pH 6.0 (inset). For further experiments, a pH of 4.7 was chosen because it is closer to the physiological apoplastic pH and corresponds to the pKa of JA. Applied in MES at pH 4.7 for 1 h before the lights-off signal, JA enhanced the rate of the scotonastic closure in a concentration-dependent manner (Fig. 3C). The effect was highly significant after 15 min for JA at 10~4 M and 10~5 M (t value in Student's test = 3.76 and 2.71, respectively; inset) and after 30 min with JA at 10~6M (t=l.96). Effects of JA on the photonastic response—The parameters identified as the most suitable for scotonastic experiments (i.e. 1-h treatment with JA at pH 4.7) were retained for a study of the influence of JA on the regulation of the photonastic movement. Under these conditions, JA inhibited the rate and the amplitude of leaflet opening in a concentration-dependent manner from 10~6 M to 10~4 M (Fig. 3D) within as little as 1 h after the lights-on signal (inset). Effects of JA and ABA on the diurnal positions of leaflets—Under continuous illumination, JA induced a closing movement of Cassia leaflets as little as 30 min after its


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Fig. 3 (A) Effect of the duration of treatment with JA on scotonastic movement of Cassia leaflets. JA was applied (arrows) at 5 x 10~~5 M (in MES 2.5 mM, pH 4.7) at different times before the lights-off signal. (•) Control (without JA), (A) 5 min, (•) 15 min, (O) 30 min, (D) 1 h. (D): The light was switched off at the middle of the photophase of the photoperiodic cycle. The inset shows the change in angle for each different set minus the control value (i.e. the enhancement of the dark-induced closure) 15 min after the dark signal. Vertical bars = SE, n = 32. (B) Effect of JA at 10~4 M in media at various pH values on the scotonastic closure of leaflets. JA was applied (•) Control; (A) MES, pH 3.5; (•) MES, pH 4.7; (O) MES, pH 6.0; (•) HEPES, pH 7.5. (D): (arrow) 1 h before the lights-off signal. As in Fig. 3A. The inset shows the change in angle for each different set minus the control value 30 min after the dark signal. Vertical bars=SE, n=24. (C) EffectsofJA at various concentrations on the scotonastic movement of leaflets. JA was applied (arrow) in MES at pH 4.7 for 1 h before the lights-off signal. (•) Control, (A) JA at 10"7 M, (T) JA at 10" 6 M, (O) JA at 10" 5 M, (•) JA at 10~4 M. (D): As in Fig. 3A. Vertical bars = SE, n = 3 2 . The inset shows the change in angle for each different set minus the control value 15 min after the lights-off signal. Vertical bars = SE, n = 32. (D) Effects of JA at various concentrations on the photonastic opening of leaflets. JA was applied (arrow) under the same conditions as in Fig. 4C before the lights-on signal. Symbols are the same as in Fig. 3C. (L): The light was switched on in the middle of the nyctophase. The inset shows the inhibition of the light-induced opening 1 h after the lights-off signal. Vertical bars=SE, n=24.

application (Fig. 4 at 10:00 h). This reaction was concentration-dependent, the threshold concentration being 10~6 M (Fig. 4). Moreover, it appeared that the effect of JA increased considerably with time during the second half of the photophase. Indeed, the rate of closure was 2.5 times

higher during the second period than during the first 4 hours of the experiment. The effects of ABA at 10~5 M and 10~4 M on leaflets from the same sets of Cassia plants appeared earlier than those of JA (Fig. 5A), and the difference was highly signifi-


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cant after 3-h treatments with ABA or JA at 10 4 M {t — 3.26) or at 10~5 M (r=3.14) (Fig. 5A). However, after a 9-h treatment, only the final closures induced by these compounds at 10~5 M were significantly different from each other (t=2.41); (Fig.5B). Discussion Pulvinar movements are the macroscopic expression

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Fig. 5 Comparison of the effects of JA and ABA on the diurnal position of Cassia leaflets after a 3-h (A) and a 9-h (B) period. The products were applied as described in the legend to Fig. 4. (m) Control, (CD) ABA at 10" 5 M, ( H ) ABA at 10"4 M, ( B ) JA at 10"5 M, (Dm) JA at 10~4 M. Vertical bars=SE, n=24.

of reversible variations in turgor in the cortical parenchyma cells of the motor organs, being driven by the migration of ions (K + , Cl~, H + ) into or out of the motor cells. This system can provide insight into the way in which a compound can influence the regulation of the permeability of plant cells to water and ions. To our knowledge, the present results relating to the control by jasmonic acid of dark-induced movements in plants are the first in the literature. In Cassia, JA increased the rate of movement in a concentration-dependent manner, an indication that the decrease in cell turgor triggered by the lights-off signal was accelerated by the compound. This effect suggests that the efflux of K + ions from the symplast of the motor cell is facilitated. Fifteen min of pretreatment with JA at 10~4 M were sufficient to cause a significant increase in the extent of dark-induced closure 1 h after the lights-off signal, suggesting that the initial impact of this compound might be felt at the plasmalemma. The effect was enhanced with increasing duration of treatment, perhaps as the result of a cascade of cytoplasmic events. In the same range of concentrations (10~6 to 10~4 M), JA strongly decreased the rate and the amplitude of the light-induced opening of Cassia leaflets in a concentration-dependent manner. Similarly, using JA at 10~ 4 M, Tsurumi and Asahi (1985) observed the almost complete inhibition of the light-induced opening of Mimosa pulvini that had been separated from pinnules and rachillae. The impairment of the light-induced increase in turgor of the pulvinar cells might be explained either by a stimulatory effect on the outward flux of protons generated by the plasmalemma ATPase, or by an inhibitory effect of JA on the


Fig. 4 Effects of JA on the diurnal position of Cassia leaflets. JA was applied (arrow) in MES at various concentrations, at pH 4.7, 30 min after the excision of leaflets. The symbols are the same as in Fig. 3C. Numbers above the curve represent time during the photophase (09:00 to 19:00 h) of the day-night cycle. QD corresponds to the middle of the photophase. Vertical bars = SE, n=24.

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deed, our experiments in acidic buffered media gave the highest physiological response. However, a clear response was noted at pH 6.0, which might reflect the activity of a JA carrier or/and the permeability of the plasmalemma to the anionic form of the compound at this pH. JA and ABA exhibit similarities as well as differences in their physiological activities (Staswick 1992, Sembdner and Parthier 1993). In our experiments, both compounds increased the rate of the dark-induced reaction in a concentration-dependent manner, but they differed in terms of the responses to treatments of brief duration (present results and Everat-Bourbouloux et al. 1990). Their effects also differed dramatically since ABA was ineffective in the lightinduced opening of Cassia leaflets (Everat-Bourbouloux et al. 1990). In Mimosa pulvini, examined under similar conditions, the JA-induced inhibition was also greater than that induced by ABA (Tsurumi and Asahi 1985). The JA-induced decrease in turgor of pulvinar cells kept in continuous light was delayed in comparison with that initiated by ABA at the same concentrations. A similar delay was also observed in Avena leaves treated with MeJ or with ABA at 2xlO~ 4 M (Satler and Thimann 1981). However, in our material, since the effect of JA was enhanced during the second half of the photophase, the final closures induced by ABA and JA at 10~4 M were similar after a 9-h treatment. This enhanced decrease in turgor during the second half of the photophase might be related to that observed during the same period in experiments with young Mimosa plants (unpublished data) in which JA caused anticipation of the nyctohemeral rhythm (endogenous angle variation linked with the alternation of day and night) by favouring the night position of the leaflets. Moreover, no re-opening of the Cassia leaflets (unpublished data) or of Avena stomata occurred after treatment with JA, unlike the case with ABA (Satler and Thimann 1981). Taken together, these results suggest that JA and ABA do not act via the same mechanism even though the final results seem the same. The physiological activity of JA may also be compared with that of other products that originate from the same precursor molecule. The precursor to jasmonic acid, 12oxo-PDA, has a structure quite similar to that of prostaglandins (Anderson 1989) and most plant tissues can probably metabolize 12-oxo-PDA rapidly to JA (Vick and Zimmerman 1984). The physiological effects of prostaglandins added to plant tissues can be expected to include changes in membrane permeability and/or ion transport (Larqu6-Saavedra 1979, Roblin and Bonmort 1984). However, as the light-induced rate of opening of Cassia leaflets is enhanced by prostaglandins (Roblin and Bonmort 1984) and, conversely, is hindered by JA (our results), it appears that this compound exhibits a regulatory role distinct from that of prostaglandins. JA has been previously considered on the one hand as an extracellular messenger that is trans-


entry of K + ions into the symplast, or both. The first of these alternatives was tested by following the changes in pH in the incubation medium of Mimosa pulvini after addition of JA at 10~4 M. This compound did not have any significant effect compared to the control. Nevertheless, the apparent absence of an effect does not allow us to conclude that JA does not affect the extrusion of protons because of a possible buffering effect of the medium created by other extruded materials. Experiments to examine this issue are now under way. The second alternative was checked by Gordon et al. (1991) who used excised roots of spring wheat incubated in a solution of MeJ (at 10~5 M). No leakage of K + ions into the medium was observed by these authors. Furthermore, JA (at concentrations from 10~6 to 2 x 10~4 M) did not significantly alter the transmembrane potential of the pulvinar motor cells in our study, a result that suggests that the electrogenic status of the plasmalemma was not affected. Nevertheless, this method provides only an overall result for the electrical balance between the inside and the outside of the cell and does not allow us to quantify the different ionic fluxes across the plasmalemma. Thus, potential fluxes of K + ions must be determined specifically. In Cassia, JA induced a decrease in turgor of the pulvinar cells, as shown by the closing of the leaflets kept in continuous light. This induced closure might be explained once again by an accelerated outward movement of K + ions and water from the symplasm of the motor cell towards the apoplast, through the plasma membrane. Similar results were obtained within 1 h with Mimosa pulvini kept in the light for concentrations of JA above 10~4 M (Tsurumi and Asahi 1985). Furthermore, treatment of Avena (Satler and Thimann 1981) and barley leaves (Popova et al. 1988, Horton 1991) with JA and/or MeJ increased the stomatal resistance that elicited stomata closure. No re-opening of the stomata was observed in these earlier studies. The threshold concentrations differ among the various plant species and may also depend on the molecular form of the compound: JA at 2.5 x 10~5 M increased stomatal resistance by about 77% over that in control barley plants (Popova et al. 1988), whereas exposure to MeJ at 10~3 M for 5 h was necessary to obtain inhibition of stomatal opening in the same species (Horton 1991). However, the fact that the acid form is more active than the methyl ester has been questioned, for example, by Staswick (1992). The keto-acids JA and ABA exhibit some similarities in terms of structure, molecular weight, solubility properties and pK value (the pK of ABA is 4.7; Anderson 1989). According to the theory of diffusive uptake, proposed for other lipophilic weak acids (Goldsmith 1977), JA might enter the cell in its undissociated form as does ABA (Everat-Bourbouloux et al. 1984) and would remain predominantly in the cytoplasm (Astle and Rubery 1985). In-


ported via the vascular tissues (Anderson 1989) and acts as a long-distance signal and, on the other hand, as a second messenger (Staswick 1992). In fact, JA is a derivative of the products generated by lipoxygenase from linolenic acid (Anderson 1989, Vick and Zimmerman 1984), a widespread fatty acid in plants. More data are now needed to determine whether or not a-linolenic acid is involved in turgor regulation in Cassia, as it is in the process of tendril coiling (Falkenstein et al. 1991, Weiler 1993) and in the activation of the synthesis of wound-inducible inhibitors of proteinases (Farmer and Ryan 1992).

References

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