Journal of Experimental Botany, Vol. 52, No. 355, pp. 361-368,
February 2001
© 2001 Oxford University Press
Original Papers |
Brief exposure to low-pH stress causes irreversible damage to the growing root in Arabidopsis thaliana: pectin–Ca interaction may play an important role in proton rhizotoxicity
Laboratory of Plant Cell Technology, Faculty of Agriculture, Gifu University, 1-1, Yanagido, 501-1193 Gifu, Japan
Received 7 June 2000; Accepted 15 September 2000
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Abstract |
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The viability of Arabidopsis thaliana (strain Landsberg) roots exposed to a low pH (4.5 or 4.7) solution that contained 100 µM CaCl2 was examined by staining with fluorescein diacetate-propidium iodide. The elongation zone of growing roots lost viability within 1–2 h following exposure to low pH, but non-growing roots showed no damage under the same treatment. Low-pH damage in growing roots was irreversible after 1 h incubation at pH 4.5 as judged by regrowth in growing medium at pH 5.6. Growing lateral roots also lost viability in the same treatment, whereas non-growing lateral roots remained viable during and after the treatment. The low-pH damage was ameliorated by the simultaneous application of calcium, indicating the involvement of a calcium-requiring process in overcoming proton toxicity. At pH 5.0, growing roots required 25 µM of calcium to maintain elongation, and at pH 4.8 and pH 4.5 more than 250 µM and 750 µM, respectively. The low-pH damage was ameliorated by divalent cations in the order of Ba2+
Sr2+
Ca2+>Mg2+. The monovalent cation K+ showed no ameliorative effect, but borate showed a strong ameliorative effect with Ca2+. These results indicate that the primary target of proton toxicity may be linked to a disturbance of the stability in the pectic polysaccharide network, where calcium plays a key role in plant roots. Key words: Arabidopsis thaliana, calcium-requiring, low-pH stress, root elongation, pectin network.
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Introduction |
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Rhizotoxicity in acid soil, which involves the action of Al3+, H+ and Mn2+, is considered to be a major environmental stress that limits world food production (Foy, 1984
; Robson, 1988). It is important to examine the mechanisms of metal toxicity and tolerance in plants to improve crop productivity in acid soil. Aluminium toxicity has been well investigated (Taylor, 1991; Delheize and Ryan, 1995; Kochian, 1995) and mechanisms of Al tolerance have been proposed (e.g. root exudates; Delheize et al., 1993; Pellet et al., 1995; Ma et al., 1997; protein alteration; Basu et al., 1994). In contrast, little has been reported (Fawzy et al., 1954) on proton rhizotoxicity.
A simple culture solution consisting of calcium chloride allows the precise computation of Al speciation (Kinraide and Parker, 1987; Kinraide et al., 1992), and is often used to study Al toxicity (Blancaflor et al., 1998). However, proton toxicity is also evident in this culture solution (Kinraide and Parker, 1990; Yokota and Ojima, 1995). Kinraide and coworkers indicated that proton toxicity (low pH) inhibited root elongation in several plant species (Kinraide and Parker, 1987; Kinraide et al., 1994), and proposed that Ca displacement by proton is part of the toxic action of proton rhizotoxicity (Kinraide et al., 1994). It has also been reported that root elongation of Arabidopsis thaliana is severely inhibited by low pH (pH 4.5–4.8) in the same culture solutions with a low ionic strength of Ca2+ (Koyama et al., 1995). Under these experimental conditions, the growing root apex of A. thaliana showed low viability after exposure to low pH solution (Koyama et al., 1995) suggesting that the target of proton action may be a Ca-requiring process in root growth, but the mechanism is still unclear.
It is well known that Ca2+ ions play an important role in plant cell growth (Schiefelbein and Somerville, 1990; Schiefelbein et al., 1992; Bush, 1995). It was reported that Ca-displacement by proton causes an inhibition of root elongation in wheat, and it was suggested that Ca2+ in the apoplast is one of the major targets of proton rhizotoxicity (Kinraide et al., 1994). Apoplastic Ca2+ affects membrane functions including membrane potentials (Mohr and Schopfer, 1995; Shimmen, 1997), as well as the cell wall network including pectin (Matoh and Kobayashi, 1998). To speculate on a mechanism for the Ca2+ amelioration of proton rhizotoxicity for the former, an actual evaluation was performed using a computation model (Gouy-Chapman-System model: see Kinraide, 1998). However, the toxic effect of proton on the latter is still unclear.
Pectic polysaccharides are one of the major constituents containing Ca2+ at the polygalacturonic acid zone, which has a possible function to stabilize the cell wall network (Carpita and Gibeaut, 1993). Although the biological role of pectic polysaccharides has not yet been clarified, another cross-linkage of pectic polysaccharides at the rhamnogalacturonan II region, that is mediated by borate (RG-II: Kobayashi et al., 1996; O'Neill et al., 1996; Williams et al., 1996) has been reported. Recently, Fleisher et al. reported tobacco cell death (lost of viability) caused by borate deprivation (Fleisher et al., 1998). On the other hand, the low pH of the apoplast has been reported to stimulate pectin solubilization in tomato fruit during development (Chun and Huber, 1998). These results raised a question as to whether the loss of viability in growing root tips from proton rhizotoxicity is due to the depletion of Ca2+ from the pectin network at low pH. To test this possibility, proton rhizotoxicity was examined in the growing root of A. thaliana, which is highly sensitive to proton rhizotoxicity (Koyama et al., 1995). Although the nature of Ca2+-mediated cross-linkage of pectin in growing cells is uncertain, an ‘egg-box model’ has been proposed from an in vitro study (Grant et al., 1973), and the ameliorative effects of divalent cations on proton rhizotoxicity fits well in this model. Borate, which cross-links pectin at the rhamnogalacturonan II region (O'Neill et al., 1996; Matoh et al., 2000), also strongly ameliorated the effect of low pH damage, suggesting that the disturbance of the pectin network may be one of the primary targets of proton rhizotoxicity.
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Materials and methods |
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Hydroponic culture of Arabidopsis thaliana
Arabidopsis thaliana plants were cultured according to the method of Toda et al., which permits the measurement of root viability while minimizing mechanical damage (Toda et al., 1999
). Arabidopsis thaliana, ecotype Landsberg, seeds were surface-sterilized with 1% sodium hypochloride solution for 1 min, and were then kept at 4 °C for 2 d before planting to synchronize germination as described previously (Koyama et al., 1995). About 100 seeds were placed on the culture apparatus, which consisted of a nylon mesh (50 mesh per inch) supported by a plastic photo slide mount as described previously (Toda et al., 1999). Each apparatus was floated on 100 ml basal culture solution containing calcium chloride (100 µM) or 1/10 strength of MGRL nutrients (Fujiwara et al., 1992). Seedlings were grown under 12 h illumination per day (PPDF: 150 µmol m-2 s-1) at 24–26 °C.
Measurement of root length and elongation rate
Seedlings were gently pulled from the apparatus at the designated time. Each seedling was soaked in 5 ml of test solutions in a multi-well plate (Sumilon MS-80060, Sumitomo Bakelite, Tokyo) and incubated at 25 °C. For the measurement of root length, each seedling was settled on the well bottom, covered with a micro coverslip (21x21 mm) and an image of the plant was captured by a microscope video camera (Pico Scopeman, Kenis, Tokyo, Japan). The root length was measured on a monitor by using a multiple measure-unit (MC-300, Kenis) and the elongation rate was calculated from the values measured at intervals.
Test solutions used for short-term treatments
A series of simple test solutions was prepared by adding MgCl2, CaCl2, SrCl2 (200 µM each), KCl (400 µM) or boric acid (100 µM) to the basal test solution (100 µM CaCl2). Solutions containing only CaCl2 or SrCl2 or MgCl2 or BaCl2 were also prepared to determine the direct effect of divalent cations. Test solutions containing a set of nutrients, with different ionic strength, were prepared by a series of dilution of MGRL nutrients. The initial pH was adjusted by adding 0.1 N HCl in the presence of 5 µM of MES.
Measurement of root viability
Seedlings were gently transferred to 100 ml of test solutions and, following the incubation in the test solutions, viability of root tip cells was determined by fluorescein diacetate (FDA)–propidium iodide (PI) staining or PI staining according to the method of Jones and Senet (Jones and Senet, 1985) with minor modifications as described previously (Toda et al., 1999). FDA is permeable to the intact plasma membrane and is converted to a green fluorescent dye, fluorescein, by a function of internal esterase(s), in turn to showing green colour in viable cells. By contrast, PI is impermeable to the intact plasma membrane. Damaged cells having pores on the plasma membrane incorporate the dye, and generate a red fluorescence by forming a PI–nucleic acid conjugate. Root staining with FDA–PI was observed with a confocal microscope (LSM510, Carl-Zeiss, Germany) equipped with an argon-HeNe laser. The wavelengths for excitation and emission for fluorescein diacetate (FDA) were 488 nm and 505–530 nm, respectively, and those for propidium iodide (PI) was 543 nm and 585 nm, respectively. Image processing was completed using the software supplied by the confocal microscope manufacture. For evaluation of ameliorative effects of metals on proton rhizotoxicity, root staining with PI was also observed with a fluorescent microscope (IMT-2–21-RFL; Olympus, Tokyo) equipped with a dichroic mirror unit [IMT-2-DG; Olympus] and with a density filter (ND6, Olympus).
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Results |
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Short-term exposure to low pH solutions caused damage in the apex of growing roots
The viability of root tips of seedlings was examined at various developmental stages to determine the sensitivity to low pH using FDA-PI staining, which showed high sensitivity for estimating rhizotoxicity of metals (Toda et al., 1999
). After this treatment, viable cells fluoresce bright green (FDA), while damaged cells fluoresce a bright red colour (PI) (Fig. 2).
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In the basal culture solution (100 µM CaCl2 alone: pH 5.6), the primary roots stopped growing after 6 d from planting (Fig. 1
). In contrast, the primary roots continued growing for at least 9 d in the solution supplemented with 1/10 strength of MGRL nutrients (Fig. 1). When the roots of seedlings grown in basal culture solution were immersed for 3 d, typical low-pH damage was observed in root tips after exposure to the simple solution (100 µM CaCl2 only) with low pH (pH 4.5) for 2 h (Fig. 2c
). However, no damage was observed in the roots after day 6, when primary root growth had stopped (Fig. 2a). The primary roots, which continued growing for at least 9 d in 1/10 strength MGRL culture solution, were also highly sensitive to low pH (Fig. 1). Thus, the growing primary roots seemed to be more sensitive to low pH than non-growing roots.
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As described previously, seedlings grown in medium MGRL nutrient medium can develop healthy lateral roots about 15 d after planting on the culture apparatus (Toda et al., 1999
). In the preliminary experiment, damage in growing lateral roots was observed after an exposure to low pH solution (Fig. 2d). To examine the relationship between the developmental stage of the lateral root and low-pH sensitivity, any low-pH damage of lateral roots that had different elongation rates during the 12 h before low-pH treatment was examined. The percentage of damaged lateral roots strongly increased with increasing lateral root growth rate (Fig. 3). This implies that the low-pH damage was observed only in growing roots for both primary and lateral roots.
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Short-term low-pH stress irreversibly terminated root elongation
Confocal images of FDA-PI fluorescence in roots exposed to pH 4.5 for 30 min (Fig. 2b) showed that the pH damage occurred not only in the epidermis but also in internal tissues. After 2 h exposure to a low pH, the central part of the root tip was also damaged (Fig. 2c, d). To determine whether this damage caused an inhibition of root growth, the re-growth of roots following exposure to low pH solutions was examined. The seedlings whose roots had been exposed to low pH solutions (100 µM CaCl2, at pH 4.5 or 4.7) for various periods were transferred to 1/10 MGRL medium (pH 5.6), and root elongation during the subsequent 24 h was examined. As shown in Fig. 4, primary root elongation was suppressed with increased exposure to a low pH. A 1 h exposure to pH 4.5 completely suppressed subsequent elongation, and a 2 h exposure to pH 4.7 also severely suppressed subsequent elongation (Fig. 4). These results clearly showed that the damage caused by brief exposure to a low pH (Fig. 2c, d) is not reversed even after the seedlings were transferred to a non-stressed condition (Fig. 4).
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) for 30, 60 or 120 min and were then cultured in the 1/10 strength MGRL solution at pH 5.6 for 24 h. Y-axis shows the elongation of roots after the low-pH stress. Means ±SD (n=7) are indicated.
Requirement of Ca2+ for maintaining root tip viability and root growth in low pH solutions
To determine whether lowering of solution pH increases the Ca2+-requirement for root growth, seedlings with growing roots were soaked in solutions containing Ca2+ at various concentrations at pH 5.3, 5.0, 4.8 or 4.5, and root elongation was measured 6 h after exposure. Root elongation as a function of Ca2+ concentration at pH 5.0 and 5.3 had sharp peaks at 25 µM, and then slightly decreased at higher Ca2+ concentrations (Fig. 5). In contrast, the growth curves for seedlings grown in solutions at pH 4.8 and pH 4.5 showed no clear peaks. Root elongation increased as the Ca2+ concentration was increased up to 250 µM and 750 µM, at pH 4.8 and 4.5, respectively (Fig. 5).
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), 4.8 (
) or 4.5 (
) for 6 h. Means of relative values and SD values are indicated (n=7).When the Ca2+ concentration was lower than 25 µM root tip viability was strongly decreased within 3 h. Following 3 h exposure to 10 µM CaCl2, about 30% of seedlings showed damage at pH 5.0 or 5.3 (data not shown). The same level of damage was observed with 150 µM and 500 µM of calcium at pH 4.8 and 4.5, respectively (data not shown). Thus, the Ca2+ requirement of growing roots strongly increased by lowering the pH.
Ameliorative effects of Ca, Sr, Ba, and borate on short-term pH damage
To examine whether proton rhizotoxicity is caused by the weakening of Ca2+-mediated cross-linkage of pectin, the ameliorative effect of metals known to mediate cross-linkage in pectin was examined. First, the ameliorative effect of metals in the presence of CaCl2 at pH 4.7 was examined. During the 2 h incubation in basal test solution (100 µM CaCl2) only 2 out of 45 roots maintained viability in the root tip (Table 1). Under such conditions, the addition of 200 µM CaCl2 or SrCl2 known to bind with pectin strongly ameliorated low-pH damage. By contrast, excessive addition of K+ showed no ameliorative effect and Mg2+ partially ameliorated proton rhizotoxicity. Borate strongly ameliorated low pH stress in the presence of Ca2+. Only 9 out of 45 roots showed low-pH damage after adding 100 µM borate to the basal test solution (Table 1).
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To determine the ameliorative effect of divalent cations more directly, root damage was examined after exposure to solutions containing divalent cations alone. Because high Ba2+ concentrations can damage in the growing root, moderate low-pH stress was used (1 h at pH 4.8) in this experiment. The divalent cations, Ca2+, Sr2+ and Ba2+ strongly ameliorated low-pH stress, but Mg2+ showed a very weak ameliorative effect (Fig. 6
). The ameliorative effect of Sr2+ and Ba2+ was higher than that of Ca2+.
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Low-pH damage in nutrient solution
To examine whether Ca2+-dependent proton rhizotoxicity would occur in a nutrient solution with a more natural and complex compositions, the low-pH damage was examined after exposure to MGRL nutrient solution (1 h, pH 4.8) with a series of dilutions. Concentration of CaCl2 in normal, 1/25 and 1/50 MGRL solutions was 2 mM, 80 µM and 40 µM, respectively. Only 1 out of 90 seedlings showed the low-pH damage during the 1 h incubation in normal strength and in 25 times diluted MGRL (Table 2). By contrast, about 40% of seedlings showed low-pH damage after exposure to 50 times diluted MGRL solution. This value was almost similar to that observed with the same treatment (pH 4.8 for 1 h) in a simple culture solution containing 40 µM CaCl2 alone (Fig. 6). Under these conditions, elimination of Ca2+ from the solutions caused about 90% damage for the seedlings (Table 2). However, the degree of damaged roots with -Mg2+ and -K+ treatments was similar to those with a control treatment (Table 2). These results suggest Ca2+-dependent proton rhizotoxicity occurs in nutrient solution and is comparable to that with a simple culture solution.
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Discussion |
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A number of studies have shown that simple culture solutions containing only CaCl2, with a low ionic strength, enhance proton rhizotoxicity (Koyama et al., 1995
; Yokota and Ojima, 1995; Kinraide, 1998). Using this solution as the test medium and combining visual measures of root tip viability to increase the sensitivity of the technique for measuring the toxic action of proton on root elongation, it has been demonstrated that A. thaliana displays high sensitivity to short-term proton rhizotoxicity (Figs 2, 4; Table 1). A visual low-pH damage was detectable within a short term, such as 1 h (Figs 2, 6), and the results are comparable to those obtained using inhibition of root elongation as an indicator for rhizotoxicity, which requires a longer term (Fig. 5). It appears that the experimental system described here is a suitable model system for examining proton rhizotoxicity.
Low-pH exposure caused irreversible damage in primary and lateral growing roots of A. thaliana, but not in non-growing roots (Figs 2, 3). This observation suggests that the primary target of proton in rhizotoxicity is the disturbance of biological functions involved in root elongation. Higher concentrations of Ca2+ were required for maintaining root tip viability (Fig. 6) and root elongation of A. thaliana at low pH (Fig. 5). Thus, it is speculated that the major target of proton rhizotoxicity in growing roots of A. thaliana seems to be Ca2+-requiring processes involved in root elongation, which could easily be disturbed by low pH. Using growing root hairs as a model for studying cell elongation (tip growth) of A. thaliana, it was reported that the Ca-gradient in the cytosol was necessary to maintain elongation (Wymer et al., 1997). However, internal Ca stores could support normal root hair growth for at least an hour, even if Ca uptake was terminated by the addition of the Ca-channel blocker verapamil. This suggests that the internal function of Ca could be maintained during short-term treatment, such as an hour employed in the current study (Fig. 6). In fact, verapamil treatment, with Ca2+, showed no effect on root tip viability (data not shown). Also, seedlings soaked in Sr2+ and Ba2+ solutions, without Ca2+, maintained normal root growth for at least 2 h (data not shown). These results suggest that, under the experimental conditions used, internal Ca stores supported normal root function. Thus, the low-pH damage observed in the growing root of A. thaliana is not considered to be caused by deprivation of Ca in the symplast, but rather in the apoplast.
The ameliorative effect of Ca2+ has been investigated for rhizotoxic metals, such as Al and Na (Kinraide, 1998). Mechanism of Ca-amelioration has been proposed both for the symplast and for the apoplast from the toxic action of metals. For example, some metals, such as Al (Kochian, 1995), inhibit Ca-uptake and Ca-homeostasis, and therefore the addition of Ca into the toxic medium may result in amelioration by maintaining Ca influx. Another important mechanism of Ca-amelioration, proposed as the ‘Ca-displacement hypothesis’, may be involved in the apoplast. Low-pH damage under the experimental conditions used in this study, as described above, may be caused by Ca-deprivation from the apoplast, and thus this hypothesis was considered for explaining the ameliorative effects of Ca2+. The Ca-displacement hypothesis for metal toxicity has been proposed for proton (Kinraide et al., 1994), Al (Reid et al., 1995) and other ions (Cramer et al., 1985). As reported recently (Kinraide, 1998), the change in Ca2+ activity at the action site, including the membrane surface, is one of the major factors affecting proton rhizotoxicity. Given the ameliorative effects of several metals other than Ca2+, another action site for the Ca2+ amelioration of proton rhizotoxicity may be negatively charged cell wall pectin. A series of amelioration studies on low-pH damage supported this possibility.
Divalent cations with large ionic radii and borate ameliorate low-pH damage (Table 1; Fig. 6). According to the ‘egg-box model’, divalent cations can cross-link pectic polysaccharides through the formation of coordinate bonds with uronate residues, but monovalent and divalent cations with a small ionic radius (such as Mg2+) cannot. The polygalacturonic acid zone is thought to provide an ‘egg-box’ for stabilizing pectin (Carpita and Gibeaut, 1993). The ameliorative effects of several cations are in agreement with this model (Table 1; Fig. 6). Monovalent cation, K+ showed no effect and the divalent cation, Mg2+ (ionic radius: 0.66 Å) showed lower ameliorative effects than Ca2+ (0.99 Å). Both Ba2+ (1.34 Å) and Sr2+ (1.12 Å) with large ionic radii strongly ameliorated proton damage in growing roots. The decreasing order of ameliorative effects of these ions [Ba2+Sr2+Ca2+>Mg2+ (Fig. 6)] match the selectivity co-efficient of pectate for each ion [
(7.0), 
(9.6) and 
(10.1)] (Haug and Smidsrød, 1970). Under our experimental conditions, borate, which cross-links pectin at the rhamnogalacturonan II region (Kobayashi et al., 1996; Williams et al., 1996), also ameliorated low-pH stress in the presence of Ca2+ (Table 1). However, borate provided no amelioration of low-pH stress when applied without Ca2+ (data not shown). This Ca2+ requirement of borate amelioration fits the mechanism of cross-linkage of pectic polysaccharides with borate, which requires Ca2+ (O'Neill et al., 1996). Although the internal effects of metals [Sr affects Ca release from the internal Ca stores (Bauer et al., 1998) and borate increases ascorbate synthesis (Lukaszewski and Blevins 1996)] have been reported, these results indicate that short-term proton rhizotoxicity is caused by weakening of Ca-mediated cross-linkage of pectin due to low pH. In the experimental conditions used here, pectolyase treatment (pH 5.3, 500 µM Ca2+, 0.01% pectolyase for 1 h) caused severe damage in the root tip of growing roots (data not shown), suggesting that the pectin network plays an important role for root tip viability. The necessity of the pectin network in cell growth has been reported in cell cultures of Chenopodium album L. (Fleisher et al., 1998) and mutant tomato (Shedletzky et al., 1990). Unfortunately, there are no reports showing that development of the pectin network is essential for root elongation. Further analysis is needed to test this hypothesis in relation to the vital importance of the development of the pectin network for root growth.
Under the experimental conditions used here, low-pH damage was not evident in solutions containing the normal levels of nutrients (Table 2), as similar to previous reports (Koyama et al. 1988; Osaki et al., 1997) which used growth as the indicator for estimating low-pH damage. However, low-pH damage was again clear in a 50-fold diluted nutrient solution (50 times dilution) with a low ionic strength of CaCl2 (40 µM). The degree of low pH damage of this condition was almost similar to that in a simple test solution containing CaCl2 alone (Table 2; Fig. 6). Thus, it could be speculated that Ca2+-dependent proton rhizotoxicity may occur in a solution with more natural and complex compositions, such as a soil solution. Whether short-term proton rhizotoxicity is a serious problem in the natural environment remains unknown. However, similar short-term rhizotoxicity has been observed in other plants including woody species (data not shown). In addition, acid precipitation decreases Ca availability in some soils (Knoepp and Swank, 1994; Likens et al., 1997), and also occasionally lowers soil pH below 4.7 (Radojevic and Brunei, 1997). Rapid and irreversible rhizotoxicity associated with brief exposure to low pH should be considered a potential risk of acid precipitation.
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Acknowledgments |
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We wish to thank Dr Neil S Harris at the University of Alberta and Dr SS Kantha for critical reading of the manuscript. We wish to thank Dr H Suga of Gifu University Gene Research Center for his kind technical support for confocal microscopic analysis. Part of this work has been financially supported by a Grant in-aid for Scientific Research from the Ministry of Education Science and Culture of Japan (for HK 10760036).
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Notes |
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1 To whom correspondence should be addressed. Fax: +81 582932911. E-mail: koyama{at}cc.gifu\|[hyphen]\|u.ac.jp
2 HK and TT contributed equally to this study.
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