Journal of Plant Research

, Volume 126, Issue 3, pp 439–446

Transduction of pressure signal to electrical signal upon sudden increase in turgor pressure in Chara corallina

Authors

    • Department of Life Science, Graduate School of Life ScienceUniversity of Hyogo
  • Koreaki Ogata
    • School of MedicineUniversity of Occupational and Environmental Health
Regular paper

DOI: 10.1007/s10265-012-0537-z

Cite this article as:
Shimmen, T. & Ogata, K. J Plant Res (2013) 126: 439. doi:10.1007/s10265-012-0537-z
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Abstract

By taking advantage of large cell size of Chara corallina, we analyzed the membrane depolarization induced by decreased turgor pressure (Shimmen in J Plant Res 124:639–644, 2011). In the present study, the response to increased turgor pressure was analyzed. When internodes were incubated in media containing 200 mM dimethyl sulfoxide, their intracellular osmolality gradually increased and reached a steady level after about 3 h. Upon removal of dimethyl sulfoxide, turgor pressure quickly increased. In response to the increase in turgor pressure, the internodes generated a transient membrane depolarization at its nodal end. The refractory period was very long and it took about 2 h for full recovery after the depolarizing response. Involvement of protein synthesis in recovery from refractoriness was suggested, based on experiments using inhibitors.

Keywords

CharaDepolarizationDimethyl sulfoxideEthylene glycolMembrane potentialOsmolalityTurgor pressure

Abbreviations

APW

Artificial pond water

APW(200 DMSO)

APW supplemented with 200 mM DMSO

CHI

Cycloheximide

DMSO

Dimethyl sulfoxide

EAB

Potential difference between pools A and B

EG

Ethylene glycol

Пi

Intracellular osmolality

Πo

Extracellular osmolality

Introduction

In plant cells, turgor pressure is generated by an osmotic gradient across the plasma membrane. Turgor pressure is involved in various plant cell activities; maintenance of cell morphology, elongational growth, stomatal function, etc. Therefore, cells accurately control their turgor pressure. In order to control turgor pressure, cells must have a mechanism to sense turgor pressure. The charophyte, Lamprothamnium, can maintain a constant turgor pressure in a wide range of extracellular osmolalities by regulating its intracellular osmolality (Bisson and Kirst 1980a, b; Okazaki et al. 1984a, b; Okazaki and Tazawa 1987). When extracellular osmolality was decreased, a large depolarization of the plasma membrane was induced. This membrane depolarization was intimately concerned with turgor regulation. The Ca2+ increase in the cytoplasm acts as a secondary messenger to initiate turgor regulation (Okazaki and Tazawa 1987). Later, a similar mechanism was also reported in tissue cultured higher plant cells (Takahashi et al. 1997). Thus, characean cells significantly contributed to the elucidation of turgor sensing in plants.

Upon wounding, plants generate a membrane depolarization (Frachisse et al. 1985; Fromm and Eschrich 1993; Julien et al. 1991; Julien and Frachisse 1992; Mertz and Higinbotham 1976; Meyer and Weisenseel 1997; Rhodes et al. 1996; Robin and Bonnemain 1985; Robin 1985; Stahlberg and Cosgrove 1994). The mechanism by which this membrane depolarization is generated upon wounding in higher plants is poorly understood due to the complex structure of tissues. Transduction of pressure signals to electrical signals upon wounding has been reported in wheat (Malone and Stankovic 1991, Malone 1992). However, the mechanism of transduction of signals remained unclear. Previous work in our laboratory focuses on electrical response upon wounding in Chara coralline (Shimmen 2001, 2002). We prepared specimens composed of two tandem internodes, one as a victim cell and the other as a receptor cell. When the victim cell was cut, the receptor cell generated a membrane depolarization at its nodal end. It was suggested that two signals were released from the victim cell upon cutting, loss of turgor pressure and release of intracellular content. It was found that released K+ induced a long lasting depolarization (Shimmen 2005, 2006). On the other hand, a decrease in turgor pressure by application of sorbitol to the external medium of the victim cell induced a transient depolarization at its nodal end (Shimmen 2001). Later, we found that such transient depolarization was induced by applying sorbitol to the nodal end of a specimen composed of a single internode (Shimmen 2003). It was found that the refractory period was very long, more than 1 h (Shimmen 2011). In the presence of protein synthesis inhibitor, cells could not recover from refractoriness. It was suggested that some protein(s) are lost or inactivated upon membrane depolarization and that this factor is slowly synthesized during the refractory period (Shimmen 2011). Thus, characean cells are suitable model system for analyzing the transduction of a pressure signal to an electrical one.

In our previous works, we have induced a depolarization by decreasing the turgor pressure via addition of sorbitol to the external medium (Shimmen 2001, 2003, 2011). Later, we noticed that turgor pressure increases upon wounding of wheat (Malone and Stankovic 1991; Malone 1992). Preliminary experiments examining the effect of increasing turgor pressure on membrane potential was performed as follows. Cells were first incubated in media containing sorbitol. Upon removal of sorbitol from the external medium, internodes received a stimulus of increasing turgor pressure. We noted that a transient membrane depolarization was induced at the nodal end upon removal of sorbitol. However, the responses were sometimes very irregular, probably resulting from the fact that the cells were kept in turgor-less (unusual) situation for a long period. Recently, we developed a unique method to induce membrane depolarization by increasing turgor pressure. Dimethyl sulfoxide (DMSO) is a small neutral molecule that permeates through the lipid bilayer and to small extent through the water channels (Steudle and Henzeler 1995). Consequently, after the cell is exposed to DMSO, the external and internal concentrations equilibrate with time and the turgor pressure returns to pre-exposure level. Upon removal of external DMSO, the turgor increases quickly. Then, DMSO leaks out and again the turgor returns to the original level. Thus, at the moment of removal of external DMSO, the cell receives a stimulus of quick increase in turgor pressure. In the present study, we analyzed the depolarization generated by increasing turgor pressure of internodes which had been incubated in the medium supplemented with DMSO.

Materials and methods

Chara corallina was cultured in an air-conditioned room (23–25 °C) as described previously (Mimura and Shimmen 1994). Internodes were prepared by removing neighboring internodes and branchlet cells with scissors. They were kept in artificial pond water (APW) containing 0.1 mM KCl, 0.1 mM NaCl and 0.1 mM CaCl2 (pH 5.6), at least for 2 days before use. It must be noted that nodal cells are attached at both ends of internodes. Hereafter, an internode including nodal cells was simply referred to as “internode”.

Changes of intracellular osmolality (Пi) during incubation were followed using a basal medium containing either dimethyl sulfoxide (Wako Pure Chemical Industries, Osaka, Japan) or ethylene glycol (Wako Pure Chemical Industries, Osaka, Japan). In the following experiments, APW buffered with 5 mM HEPES–Tris (pH 7.0) was used as an external medium. Hereafter, APW buffered with 5 mM HEPES–Tris (pH 7.0) was referred to as APW. Internodes were incubated in APW supplemented with either 200 mM dimethyl sulfoxide (DMSO) or 200 mM ethylene glycol (EG). At each time, internodes were taken out and their surface was gently blotted with a sheet of filter paper to remove the medium. One end of the internode was cut with scissors and the intracellular content of internodal cell was squeezed out by hand. The osmolality of the cell content was measured using an osmometer (Vapor Pressure Osmometer 5520; Wescor Inc, Utah USA). The osmolality of 200 mM DMSO or 200 mM EG was 179 ± 2 or 183 ± 3 mOsm, respectively.

Measurement of the electrical response caused by osmotic stimulation was carried out as reported previously (Shimmen 2011). Internodes were mounted on a measuring chamber composed of two pools, A and B (Fig. 1). An internode was mounted so that the node (n) in pool A was attached to the partition (P). By attaching the node to P (by shortening the length of flank region in pool A), an electrical signal from the nodal region can be selectively monitored (Shimmen 2002). Pools A and B were electrically insulated by embedding the cell into the groove of P, using petroleum jelly (Wako Pure Chemical Industries, Ltd., Osaka Japan). Both pools were filled with APW supplemented with either DMSO or EG. Internodes mounted on a measuring chamber were incubated overnight at room temperature. During the incubation, internodes accumulated DMSO or EG and Пi attained a constant value. The potential difference between pools A and B (EAB) was measured using agar electrodes connected to Ag–AgCl wire via 3 M KCl solution. The tip of the electrode in pool A was located very close to the node. When the external medium in pool A was removed for replacement, a small amount of medium connected the node and the electrode tip. Therefore, the electrical potential could be monitored continuously during replacement of the medium. The resting membrane potential was measured according to Shimmen and Wakabayashi (2008). The electrical potential was amplified with an amplifier (Microelectrode Amplifier MEZ7101, Nihon Kohden, Tokyo, Japan) and recorded using a pen-writing recorder (VP-6358A, National Panasonic, Tokyo, Japan).
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Fig. 1

Schematic upper view of chamber for electrical measurement. An internode (cell) was separated into pools A and B. It was mounted so that the node (n) in pool A was attached to the partition (P). The potential difference between pools A and B (EAB) was measured with agar electrodes. The tip of the electrode in pool A was located very close to the node. For further explanation, see the text. (modified from Shimmen (2011))

Stock solutions of cycloheximide (Wako Pure Chemical Industries, Osaka, Japan), tetracycline (Sigma-Aldrich co. St. Louis, MO, USA) and erythromycin (Wako Pure Chemical Industries, Osaka, Japan) were prepared in methanol (Wako Pure Chemical Industries, Osaka, Japan). Stock solutions of anisomycin (Wako Pure Chemical Industries, Osaka, Japan), chloramphenicol (Wako Pure Chemical Industries, Osaka, Japan) and kanamycin (Wako Pure Chemical Industries, Osaka, Japan) were prepared in pure water. The concentration of all stock solutions was 10 mM. Methanol per se did not affect the response at the concentration used: 0.1 % (v/v).

Experiments were carried out at room temperature (24–27 °C) under dim light (about 90 lux).

Results and discussion

Change of Пi during incubation in APW supplemented with 200 mM DMSO [APW(200 DMSO)] was followed. Figure 2b shows a change of Пi. At each time, Пi of more than five replicate internodes were measured. Before incubation in APW(200 DMSO), Пi was 244 ± 2 mOsm. During the incubation in APW(200 DMSO), Пi gradually increased and attained a steady value after about 3 h. When internodes were incubated overnight in APW(200 DMSO), they maintained Пi of the same level (data not shown). Upon replacement of the external medium with APW 6 h after the start of DMSO-incubation, Пi gradually decreased. Five hours after removal of DMSO from the external medium, Пi attained a value (249 ± 3 mOsm) close to that before incubation in the medium supplemented with DMSO (244 ± 2 mOsm). Thus, increase in Пi during incubation in the medium supplemented with DMSO was reversible, suggesting that cell maintained the mechanism of osmoregulation. Figure 2c shows a difference between Пi and extracellular osmolarity (Пo), which suggests a transient decrease and increase in turgor pressure upon addition and removal of DMSO, respectively. This quick change of turgor pressure upon addition and removal of DMSO was confirmed according to Ogata (2010) (data not shown).
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Fig. 2

Increase in intracellular osmolarity in the presence of 200 mM DMSO. Internodes were incubated in APW supplemented with 200 mM DMSO. At various time after start of incubation in the medium containing DMSO, intracellular osmolarity (Пi) was measured. a Change of extracellular osmolarity (Пo). At time zero, incubation in APW supplemented with 200 mM DMSO was started. After 6 h, internodes were transferred to APW lacking DMSO. b Change of Пi. c Change of difference between Пi and Пo. SD was smaller than the size of closed circles at all points. For further explanation, see the text

When turgor pressure of internodes bathed in APW was decreased by replacing the medium in pool A with sorbitol solution, a transient depolarization was induced (Shimmen 2011). A similar depolarization was also induced upon addition of 200 mM DMSO. In Fig. 3, the external medium of pools A and B (Fig. 1) was initially APW. When the external medium in pool A was replaced with APW(200 DMSO), a transient depolarization was induced (Fig. 3a) as in the case of sorbitol (Shimmen 2011). Both pools were filled with APW(200 DMSO) and incubated for 4 h. When the external medium in pool A was replaced with APW lacking DMSO, a transient depolarization was also induced (Fig. 3b). Generation of transient depolarizations upon both addition and removal of DMSO was confirmed in more than 10 internodes.
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Fig. 3

Transient depolarizations upon addition and removal of DMSO. Both pools of Fig. 1 were APW lacking DMSO. When medium in pool A was replaced with APW supplemented with 200 mM DMSO, a transient depolarization was induced (a). Both pools were filled with APW supplemented with 200 mM DMSO and incubated for 4 h. When the external medium in pool A was replaced with APW lacking DMSO, a transient depolarization was also induced (b). For further explanation, see the text

In the previous study, both pools had been filled with APW (Fig. 1) and a transient depolarization was induced by replacing the medium in pool A with APW supplemented with sorbitol (Shimmen 2003). The question arose whether the depolarization was induced by decrease in turgor pressure or transcellular osmosis. This question was solved by an experiment to replace medium of both pools with APW supplemented with sorbitol (Shimmen 2003). Since a similar depolarization was induced by the stimulation, it was concluded that the depolarization upon addition of sorbitol to pool A was induced via decrease in turgor pressure and not transcellular osmosis. The same question arose in the present study, i.e. whether depolarization upon removal of DMSO from pool A was induced by increase in turgor pressure or transcellular osmosis. To solve this question, we carried out the following experiment. Internodes equilibrated with 200 mM DMSO were set on a measuring chamber and both pools were filled with APW(200 DMSO). The medium of both pools, A and B (Fig. 1), was replaced with APW. Upon replacement of the medium in both pools A and B, a transient depolarization [90 ± 4 mV (n = 5)] was induced, implying that the depolarization upon removal of DMSO from pool A (Fig. 3b) was induced by a decrease in turgor pressure but not transcellular osmosis.

The dose–response relation between stimulus intensity and amplitude of depolarization was studied (Fig. 4). After internodes were set on a chamber, both pools were filled with APW(200 DMSO) and incubated overnight. The internodes were stimulated by replacing the media in pool A with APW supplemented with various concentrations of DMSO. In Fig. 4, the abscissa shows the decrease in DMSO concentration, i.e. 200 mM means that the DMSO concentration was decreased from 200 to 0 mM. As is evident in Fig. 4, the amplitude of the depolarization increased in a stimulus-dependent manner. In other words, this is an analogue sensing mechanism rather than a digital one. Depolarization induced by addition of sorbitol had also analogue one (Shimmen 2011).
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Fig. 4

Dose–response relation between stimulus intensity and amplitude of depolarization induced by decrease in DMSO concentration. Both pools were filled with APW supplemented with 200 mM DMSO and incubated overnight. The external medium of pool A was replaced with APW supplemented with DMSO of various concentrations. Abscissa shows the decrease in DMSO concentration. Average value of 5–6 cells are shown with SD. For further explanation, see the text

In a previous paper, we reported a very long refractory period for depolarization induced by decreasing turgor pressure (Shimmen 2011). In the present study, we examined the refractory period for depolarization induced by increase in turgor pressure (removal of DMSO) (Fig. 5). After internodes had been bathed in the measuring chamber containing APW(200 DMSO) overnight, the medium in pool A was removed (not shown). When APW(200 DMSO) was added (1), membrane potential became slightly more positive. When APW(200 DMSO) in pool A was removed (2), membrane potential became more negative. Thus, a small potential change was induced just by replacement of the medium. However, this is not the case for all culture batches. The electrical response of internodes to the replacement of the medium was variable. In some culture batches, no response, in other culture batches, a small response was induced (Fig. 3). Reason for this variable response to replacement of the external medium remained unclear. When APW was added to pool A (3), a small depolarization due to addition of medium, and then a large depolarization due to osmotic stimulation were generated (Fig. 5). After the membrane had almost repolarized, the external medium in pool A, APW, was removed (4) and APW(200 DMSO) was added (5). No significant change in membrane potential was induced by these procedures, except for a small change due to replacement of the external medium. After the internode was incubated in APW(200 DMSO) for 10 min, the external medium in pool A was removed (not shown). When APW was added to the pool, only a small depolarization due to addition of external medium was induced without response to osmotic stimulation. Thus, the internode entered the refractory period after the first depolarization. The same results were obtained in all specimens examined, more than 10 internodes.
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Fig. 5

Presence of refractory period. Both pools were filled with APW supplemented with 200 mM DMSO and incubated overnight. The external medium of pool A was removed (not shown). When APW supplemented with 200 mM DMSO was added to pool A, a small depolarization was induced (1). Upon removal of the external medium in pool A, a small repolarization was induced (2). Upon addition of APW lacking DMSO (3), a small initial depolarization was followed by a larger depolarization. At the time shown with 4, the external medium of pool A was removed and membrane potential slightly changed to the negative direction. When APW supplemented with 200 mM DMSO was added (5), membrane potential became slightly more positive. The cell was incubated in APW supplemented with 200 mM DMSO for 10 min. The external medium in pool A was removed (not shown). Upon addition of APW lacking DMSO (6), only a small depolarization was induced due to addition of the external medium

A systematic analysis was carried for the refractory period. Internodes had been bathed in APW(200 DMSO) overnight. They were stimulated by replacing the medium in pool A with APW. After the first stimulation, both pools were filled with APW(200 DMSO). At various time after the first stimulation, internodes were stimulated by replacing the external medium of pool A with APW. In Fig. 6, amplitude of the response induced by the second stimulation is shown as a relative value to that induced by the first stimulation. After 15 min, no depolarization was induced. By resting the internodes without stimulation, the amplitude increased with time and after 2 h, responses of original amplitude was generated.
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Fig. 6

Systematic analysis of refractory period. Both pools were filled with APW supplemented with 200 mM DMSO and incubated overnight. Internodes were stimulated by replacing the medium of pool A with APW lacking DMSO. After the end of depolarization, both pools were filled with APW supplemented with 200 mM DMSO. At various time after the first stimulation, internodes were stimulated by replacing the medium in pool A with APW lacking DMSO. The amplitude of the depolarization induced by the second depolarization is shown as a relative value to that induced by the first stimulation. Average value of 5–10 cells are shown with SD

Thus, refractory period was long as in the case induced by decreasing turgor pressure (Shimmen 2011). In the previous paper, we reported that inhibitors of protein synthesis inhibited the recovery from refractoriness. In the present study, we also examined the effect of protein synthesis inhibitors. Internodes had been bathed in APW(200 DMSO) overnight. The first depolarization was induced by replacing the medium of pool A with APW. The amplitude of the depolarization was 94 ± 8 mV (n = 6). After the end of the depolarization, the external medium of both pools were replaced with APW(200 DMSO) supplemented with 10 μM CHI and incubated for 4 h. The cell was stimulated by replacing the external medium of pool A with APW. The amplitude of the depolarization was 0 ± 0 mV (n = 6). Thus, recovery from refractory period was completely inhibited in the presence of 10 μM CHI. The external medium of both pools were replaced with APW(200 DMSO) lacking CHI and incubated for 4 h. When internodes were stimulated by replacing the external medium of pool A with APW, a significant depolarization was induced [78 ± 16 mV (n = 6)]. In 5 internodes, amplitude close to that of the first stimulation was induced. In one internode, no depolarization was induced at all. Thus, inhibition by CHI was reversible.

The effect of another inhibitor of eukaryote-type protein synthesis, anisomycin, was examined. Cells were bathed in APW(200 DMSO) overnight. An initial depolarization was induced by replacing the external medium in pool A with APW. The amplitude of the depolarization was 92 ± 15 mV (n = 6). After the end of the depolarization, the external medium of both pools were replaced with APW(200 DMSO) supplemented with 10 μM anisomycin and incubated for 4 h. The cell was stimulated by replacing the external medium in pool A with APW. The amplitude of the depolarization was 4 ± 3 mV (n = 6). Thus, recovery from refractoriness was severely inhibited in the presence of anisomycin. All inhibitors of prokaryote-type protein synthesis, chloramphenicol, tetracycline, erythromycin, streptomycin and kanamycin (all 10 μM) did not inhibit the recovery from refractoriness at all (data not shown). Thus, it is suggested that some protein(s) is lost or inactivated upon membrane depolarization and that the factor is slowly synthesized during the refractory period, as in the case of depolarization induced by decrease in turgor pressure (Shimmen 2011).

DMSO is generally used as a solvent in preparing stock solutions of hydrophobic drugs in various studies of cell biology. When the stock solution was added to an aqueous solution for experiment, the concentration of DMSO is 0.1–1 %(v/v). The molar concentration of 1 % (v/v) DMSO is about 140 mM, significantly high. Therefore, absence of the effect of DMSO, per se, on the target phenomenon must be examined. Various physiological effects of DMSO have been reported (Yu and Quinn 1994). Any ill effects other than increase in Пi might be caused by DMSO in the present study. Therefore, we examined the effect of DMSO on the resting membrane potential and cytoplasmic streaming. Internodes were incubated in APW(200 DMSO) for 20 h. The resting membrane potential incubated in APW(200 DMSO) was −224 ± 3 mV (n = 5), which was close to that of cells incubated in the absence of DMSO [−228 ± 2 mV (n = 5)]. The velocity of cytoplasmic streaming of cells incubated in APW(200 DMSO) was 114 ± 4 μm (n = 5), which was also close to that of cells incubated in the absence of DMSO [114 ± 4 μm (n = 5)]. Thus, DMSO did not affect, at least, electrogenesis and motility.

We further suspected that increase in Пi may be a DMSO-specific phenomenon. To examine this possibility, experiments using ethylene glycol (EG) were carried out. The value of Пi before incubation in EG was 246 ± 7 mOsm (n = 6). When internodes were incubated in APW supplemented with 200 mM EG, Пi gradually increased and attained a value of 385 ± 5 mOsm (n = 9) after 4 h incubation. The Пi value stayed at the level during incubation (6 h). Upon removal of extracellular EG, Пi gradually decreased (data not shown). Electrophysiological experiments were carried out using EG. After internodes were incubated in APW supplemented with 200 mM EG overnight, they were stimulated by replacing the external medium in pool A with APW lacking EG. A significant depolarization was induced as in the case of DMDO (data not shown). Thus, depolarization by increasing turgor pressure was not specific to DMSO.

When internodes of C. corallina were incubated in a medium of high Пo, they maintained a constant Пi (Bisson and Bartholomew 1984), supporting the reports that fresh water Characeae regulates Пi but not turgor pressure (Kiyoswa and Okihara 1988; Tazawa 1961). On the other hand, Пi increased when Chara internodes were incubated in a medium containing concentrated KCl (Davenport et al. 1996; Kiyosawa 1993a; Wittington and Smith 1992). It is suggested that internodes lost their function to regulate Пi in unusually high KCl solution. In the presence of either DMSO or EG, Пi also increased (Fig. 2). However, the mechanism of Пi increase in the presence of KCl will be different from that in the presence of DMSO (EG). While it took 2 days for Пi increase in the presence of concentrated KCl (Kiyosawa 1993a), it took only 3 h in the presence of DMSO (EG). In the former case, internodes had to be illuminated during the incubation, indicating an active process (Kiyosawa 1993a). On the other hand, Пi increase in the presence of DMSO normally occurred in the dark (data not shown). Kiyosawa (1993b) reported high permeability of Chara membrane to EG. It is suggested that DMSO and EG entered the cell via non-specific passive diffusion.

Upon removal of extracellular DMSO, a sudden increase in turgor pressure and a membrane depolarization were induced. Characteristics of the depolarization induced by removal of DMSO (increase in turgor pressure) and that induced by addition of sorbitol (decrease in turgor pressure) were similar. In both cases, the response was transient and dose-dependent. A long refractory period was observed and protein synthesis inhibitors hampered the recovery from refractoriness in both cases. In addition, inhibitors of eukaryote-type protein synthesis were effective while inhibitors of prokaryote-type protein synthesis were ineffective. Thus, it seems likely that some protein factor(s) are inactivated or lost upon induction of membrane depolarization and synthesized during the refractory period. The present study showed that internodes of C. coralline can be used as a model system for studies on transduction of pressure signal to electrical one for both increase and decrease in turgor pressure.

Acknowledgments

The authors thank Prof. Nobuaki Yanagihara (School of Medicine, University of Occupational and Environmental Health) for his kind supports of the present experiments.

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© The Botanical Society of Japan and Springer Japan 2012