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First published online October 21, 2005; 10.1104/pp.105.067520 Plant Physiology 139:1207-1216 (2005) © 2005 American Society of Plant Biologists
The Dynamic Changes of Tonoplasts in Guard Cells Are Important for Stomatal Movement in Vicia faba1State Key Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, China Agricultural University, Beijing 100094, People's Republic of China (X.-Q.G., C.-G.L., P.-C.W., X.-Y.Z., J.C., X.-C.W.); and College of Life Science, Qufu Normal University, Qufu 273165, People's Republic of China (X.-Q.G.)
Stomatal movement is important for plants to exchange gas with environment. The regulation of stomatal movement allows optimizing photosynthesis and transpiration. Changes in vacuolar volume in guard cells are known to participate in this regulation. However, little has been known about the mechanism underlying the regulation of rapid changes in guard cell vacuolar volume. Here, we report that dynamic changes in the complex vacuolar membrane system play a role in the rapid changes of vacuolar volume in Vicia faba guard cells. The guard cells contained a great number of small vacuoles and various vacuolar membrane structures when stomata closed. The small vacuoles and complex membrane systems fused with each other or with the bigger vacuoles to generate large vacuoles during stomatal opening. Conversely, the large vacuoles split into smaller vacuoles and generated many complex membrane structures in the closing stomata. Vacuole fusion inhibitor, (2s,3s)-trans-epoxy-succinyl-L-leucylamido-3-methylbutane ethyl ester, inhibited stomatal opening significantly. Furthermore, an Arabidopsis (Arabidopsis thaliana) mutation of the SGR3 gene, which has a defect in vacuolar fusion, also led to retardation of stomatal opening. All these results suggest that the dynamic changes of the tonoplast are essential for enhancing stomatal movement.
Guard cells can perceive environmental and intracellular signals, such as atmospheric CO2 concentration, light intensity, humidity, auxin, Ca2+, extracellular calmodulin, and abscisic acid (ABA) to regulate the stomatal aperture and gas exchange (Blatt, 2000  ; Allen et al., 2001; Schroeder et al., 2001; Chen et al., 2004). The regulation of guard cell movement plays an important role in the optimization of photosynthesis and transpiration (Wang and Chen, 2001). Studies have shown that the vacuoles in guard cells are also involved in stomatal movement. Vacuoles are the primary calcium pool in guard cells. Ca2+ channels and transporters in the tonoplast contribute to Ca2+ movement between vacuoles and the cytoplasm. Such Ca2+ movements between the reservoir and the cytoplasm result in the spatiotemporal changes in [Ca2+]cyt, generating [Ca2+]cyt oscillations and [Ca2+]cyt waves that modulate stomatal movement(Allen et al., 2001; Schroeder et al., 2001). Vacuoles also are the largest H+ storage sinks in guard cells. The accumulation of H+ in the vacuoles is dependent on the tonoplast proteins, V-ATPase and H+-PPase (Gaxiola et al., 2002). Studies revealed that cytosolic pH could act as a second messenger in ABA signaling in guard cells (Blatt, 2000). The H+ electrochemical gradient across the tonoplast mediates the movement of other ions, such as K+, Cl–, Suc, or malate between vacuoles and the cytoplasm, resulting in the changes of the water potential in guard cells (Schroeder et al., 2001), which drives water influx and efflux across the tonoplast. Such a process results in the changes of turgor pressure in the guard cells, driving stomatal movement.
During stomatal movement, the volume of the guard cells can change by more than 40% (Shope et al., 2003
In spite of vacuolar importance to stomatal movement, little has been known about the regulatory mechanism underlying the change of the vacuolar surface area in response to rapid changes of vacuolar volume. There are a great number of small vacuoles in guard cells of the closed stomata, and only a few big ones in the guard cells of the fully opened stomata (Couot-Gastelier et al., 1984
The Small Vacuoles Fused with Each Other to Form Bigger Vacuoles in Guard Cells during Stomatal Movement To visualize the vacuoles in guard cells, we stained V. faba guard cells with 10 µM acridine orange (AO) and imaged the vacuoles using confocal laser scanning microscopy (CLSM). As can be seen in Figure 1A, the guard cells contained many small vacuoles when the stomata were closed. They were largely spherical and had a diameter of 1 to 5 µm (Fig. 1A). As stomata opening proceeded, the number of vacuoles decreased in each guard cell, but the size of vacuoles increased accordingly (Fig. 1, A–C).
To facilitate the description of the dynamic changes in vacuole number and size during stomatal movement, we arbitrarily divided the movement of stomata into three particular stages according to the size of the stomatal aperture: stage I, <5 µm; stage II, 5 to 8 µm; and stage III, >8 µm. At stage I, on the average, more than 18 vacuoles could be found in each guard cell and the average diameter of the vacuoles was less than 3 µm. However, at stage III, they had less than four vacuoles with an average diameter of more than 15 µm (Fig. 1, D and E).
To confirm AO labeling of vacuoles, we also used LysoTracker Red DND-99 (an acidic organelle-selective cell-permeable probe; Molecular Probe) to stain the vacuoles of guard cells of V. faba, and similar results were obtained (Fig. 1F). In addition, AO staining pattern (Fig. 1, G1) of Arabidopsis (Arabidopsis thaliana) guard cell vacuoles was similar to that of V. faba, suggesting that AO can be used to label guard cell vacuoles in Arabidopsis. Fluorescein diacetate (FDA) can be deesterified by esterase in the cytoplasm, giving rise to the polar fluorescein that can't enter vacuoles (Fricker et al., 2001 To understand the mechanism underlying the changes of vacuole numbers and sizes, we examined the motility of vacuoles and tonoplasts during stomatal movement by monitoring their structural changes using time-lapse imaging of FDA-stained cells. As shown in Figure 2, A and B, individual small vacuoles fused into bigger vacuoles during stage I of stomatal opening. Among the 52 observed V. faba guard cells at this stage, 88% of the cells showed the typical changes. In the opening stomata, the fusion of small vacuoles with each other (Fig. 2C) and the tonoplast remnants in the fusing vacuole lumen (Fig. 2D) also could be observed in TEM images. To test whether the dynamic changes in vacuoles are reversible, we investigated the change of vacuoles in the guard cells in closing stomata. Indeed, large vacuoles did split into many small vacuoles during stomatal closing induced by 10 µM ABA in V. faba (Fig. 2E). Thirty-six out of 44 guard cells showed the foregoing changes treated with ABA.
Fusion of Small Vacuoles Was Correlated to Stomatal Opening
We also investigated whether the dynamic changes in vacuole morphology and size are required for stomatal movement using chemicals to inhibit vacuole fusion or mutation that is defective. To study the correlation between vacuole development and stomatal movement, first we used a membrane-permeable Cys protease inhibitor, (2s,3s)-trans-epoxy-succinyl-L-leucylamido-3-methylbutane ethyl ester (E-64d). Application of E-64d to the root cells of barley (Hordeum vulgare) caused the accumulation of starvation-induced autolysosomes (Moriyasu et al., 2003
To further confirm the above finding, we used an Arabidopsis mutant, sgr3-1, to study the correlation between vacuole fusion and stomatal movement. The Arabidopsis SGR3 gene encodes a syntaxin, SYP22 (syntaxin of plants 22), also called AtVAM3, which is localized in the prevacuole and the tonoplast (Uemura et al., 2002 ; Rojo et al., 2003; Carter et al., 2004). It is commonly believed that SGR3 protein plays an important role in transporting vesicles to vacuoles as well as the vacuolar fusion (Sato et al., 1997; Sanderfoot et al., 1999; Surpin and Raikhel, 2004). We found a significant reduction in the fusion of vacuoles in the guard cells of sgr3-1 (Fig. 3, E–H). The stomatal opening under light in sgr3-1 was slower compared to that in the wild type and the complementary line sgr3-1/gSGR3, especially obvious at the early stage of stomatal opening (Fig. 3I).This result further indicates that vacuolar fusion is involved in the stomatal movement.
To further understand the structural basis for the dynamic changes in vacuolar morphology during stomatal movement, we next investigated the changes of vacuolar structure during stomatal opening. In the guard cells at stage I of stomatal opening, the small vacuoles with the diameters of 1 to 3 µm were spherical. In contrast, those with a diameter of more than 4 µm tended to be irregular (Fig. 4A). The guard cells also contained many complex membrane structures in their lumen, for example, foldings of the tonoplast (Fig. 4A). TEM images showed that the foldings of the tonoplast resulted from the invagination of the cytoplasm into the vacuolar lumen (Fig. 4B), generating ripple-like fringe in the vacuole (Fig. 4, C1 and C2). To visualize the spatial configuration of vacuoles in a readily accessible image, the three-dimensional (3D) projection was performed from a series of Z-axis optical section by CLSM. As shown in a 3D projection image of the guard cells in Figure 4, C1, the surface of globular vacuole was not smooth, but wavy (Fig. 4, C3).
Many vesicle-like structures (named as bulb by Saito et al. [2002] ) with diameters of 0.5 to 1.5 µm were found in spherical vacuole lumen (Fig. 5, A and B), bound with the single or double layer membrane. To study the full-view structure of the vesicle-like structures, we performed Z-axis optical sections at different foci on the guard cells stained with FDA. We found that a close, vesicle-like structure in vacuolar lumen (0 µm) was open at the 1.2-µm optical section (Fig. 5C). This result implied that these vesicle-like structures might come from the coalescence of tonoplast foldings. In addition, a guard cell also had tubular vacuolar membranes (TVMs) with the diameters of 0.5 to 1.5 µm in not fully opened stomata (Fig. 5D). Most of the TVMs were located at the central part of the guard cells. However, TVMs were not observed in the TEM images. The possible reason might be that the TVM structures had been destroyed by the conventional chemical fixation (Ashford and Allaway, 2002).
The number of tonoplast foldings and vesicle-like structures in guard cells varied in different stages of stomatal aperture. As shown in Figure 6A, the average number of vesicles observed in the central optical section of a guard cell decreased from 4.1 to 1.3 when stomatal aperture proceeded from stage I to stage III. The largest average number of foldings was recorded at stage II, which then decreased as stomatal aperture proceeded to stage III. The statistical results showed a strong correlation between the emergence of tonoplast structures in guard cells and stomatal aperture (Fig. 6B). The proportion of guard cells containing vesicles in vacuolar lumen decreased from 49.3% to 6.7% when stomatal aperture developed from stage I to stage III. The guard cells with foldings were counted as more than 50% of the total guard cells at stage I and stage II. However, they occupied only 26.7% of the total guard cells at stage III. The percentage of guard cells with TVMs also decreased as the stomatal opening proceeded. When the stomata opened wider than 8 µm, the TVMs in guard cells disappeared.
To find the disappearance process of these tonoplast structures, we captured a series of time-lapse CLSM images during stomatal opening. The results showed that the foldings of the tonoplast disappeared, possibly due to the fact that they reverted to the tonoplast as stomatal opening proceeded (Fig. 6C). The vesicle-like structures probably fused with outer tonoplasts during stomatal opening and disappeared (Fig. 6D). The TVMs were converted to spherical vacuoles with the increase of stomatal aperture (Fig. 6E). These tonoplast structures were observed again in the vacuolar lumen of guard cells when stomata were closing.
To examine the spatial relationship among vacuoles in a whole guard cell, a 3D projection for a series of Z-axis optical sections of stomata of V. faba at stages II and III was created. Lumens of two separated vacuoles in an optical section of Z-axis were interconnected in the vertical optical section (Fig. 7, A2). This finding suggested that the lumens of these two vacuoles might be connected with each other. As shown in Figure 7, A3, a projection image of the stoma in Figure 7, A1, a canal-like structure connected to the vacuoles at the two poles of a guard cell. In a single optical section, TVMs also were found linked to the spherical vacuoles (Fig. 7B). From a series of optical sections at different foci of a stomata stained with FDA, we found two separated small vacuoles at the 0-µm section (Fig. 7, C1) were connected at the 0.9-µm section (Fig. 7, C4). The projection image of another stoma stained with FDA (Fig. 7, D3) showed that the lumens of some vacuoles were interconnected, although they were found separated in the single optical section (Fig. 7D, 1 and 2). To gain further insight into the structural relationship between vacuolar lumens in a guard cell, photobleaching was performed with the strongest excitation light. As shown in Figure 8A, the fluorescence intensities of both a photobleached vacuole and a nearby vacuole were decreased after bleaching, indicating that the lumens of these two neighboring vacuoles were connected with each other. In another stoma, when the vacuoles at one end of the guard cell were bleached, the AO fading was observed in the vacuole lumen at the other end of the guard cell (Fig. 8B). These results indicated that TVMs might bridge the lumens of these vacuoles. We defined more than 20% of changes in fluorescence intensity of the nearby vacuole between pre- and after bleach as fluorescence intensity decreases. Among the 35 V. faba guard cells for this experiment, 69% of the cells showed the typical fluorescence intensity changes. Taken all together, we suggest that the lumens of different vacuoles in the same guard cell were interconnected, and their saps could flow freely.
Fusion of Small Vacuoles Is Required for Stomatal Opening In this study, we reported that the fusion of small vacuoles to form big vacuoles contributed to the increase of vacuolar volume in guard cells during stomatal opening. Inhibiting the fusion of small vacuoles by the inhibitor and the mutation of vesicle fusion gene inhibited not only the increase of vacuolar volume, but also the stomatal aperture in V. faba and Arabidopsis. This result indicates that the fusion of small vacuoles to form a bigger vacuole in the guard cell is required for the stomatal opening.
However, the mechanism for vacuolar fusion is still not clear. One possibility is that the uptaking of water results in the increase of vacuolar sizes that drives the two neighboring vacuoles to contact physically and fuse with each other passively. Another possibility is that there may be a regulatory mechanism that activates the fusion of the small vacuoles into the big vacuoles in the guard cells during the stomatal opening. The Arabidopsis SGR3 protein was involved in transporting vesicles to vacuoles as well as the vacuolar fusion (Sato et al., 1997 As the number of vacuoles decreased, the volume per vacuole increased accordingly during stomatal opening. Only a few big vacuoles were found in each guard cell of the fully opened stomata. However, it is unclear why the change of cell volume required big vacuoles instead of multiple small vacuoles in V. faba. The possible explanation is that a big vacuole has a larger total volume than many small vacuoles when they have the same surface area. Therefore, the big vacuole is good for taking up more water than multiple small vacuoles under the condition of an unchangeable amount of tonoplasts. Alternatively, the formation of the big vacuoles via the fusion of small vacuoles may be also regulated by the physical and spatial signals. Nevertheless, our study clearly shows a strong correlation of the big vacuole formation to the stomatal opening. Taken all together, we conclude that the fusion of small vacuoles to form big vacuoles is required for the stomatal opening. The process may be regulated by the physical and cellular signals in guard cells.
It is usually believed that the plant vacuole is a large compartment with a smooth surface. However, several recent studies have revealed that it might not be true. Using the technologies of cryofixed and freeze-substituted fluorescence dye labeling, transgenic plants expressing green fluorescent protein combined with CLSM and 3D reconstruction, several research groups have found that the tonoplasts of plant cells actually have many complex and intricate structures, such as foldings of tonoplasts (Cutler et al., 2000
TVMs, another type of vacuolar structure found in many plant tissues, also appeared in the guard cells in V. faba. They formed in the guard cells of the opening stomata and disappeared in the fully opened stomata. As TVMs have been found to transform to spherical vacuoles during stomatal opening, we conjectured that TVMs in guard cells may also serve as a reservoir of tonoplasts for the increase of vacuolar volume. Many studies support this hypothesis. TVMs also were found in many dividing or growing cells, such as the cultured evacuolated oat (Avena sativa) mesophyll protoplasts (Newell et al., 1998
Our results showed that vacuoles in guard cells were interconnected and the spherical vacuoles were linked together with TVMs in V. faba. The photobleaching further confirmed that the vacuoles in the guard cells formed a continuum in V. faba. Several studies have shown that membrane linkage among the cells or organelles is important for cell signaling and cell function. Plasmodesmata, plasma-membrane-lined tubule-like channels, mediated the direct cell-to-cell communication in plants by facilitating the direct intercellular transport (Lucas and Lee, 2004
The changes of vacuolar morphology also were observed in the moving motor cell of Mimosa pudica pulvini, which contained two kinds of vacuoles, tannin vacuoles and aqueous vacuoles. When pulvini motor cells shrunk, the tannin vacuoles formed many connected tubules and the aqueous vacuoles formed many invaginations (Fleurat-Lessard et al., 1997 In conclusion, the fusion of small vacuoles to form big vacuoles in guard cells is important for the stomatal opening. However, it is not the only mechanism that is involved in the rapid increase of vacuolar volume during the stomatal opening. The complex tonoplast structures may also serve as a reservoir of tonoplast, which plays a role in the rapid change of vacuolar volume in the guard cells during the stomatal opening.
Plant Materials The plants of Vicia faba were grown in a growth chamber with 12 h of light and 12 h of darkness, with a photon flux density of 300 µmol m–2 s–1, and day and night temperature cycles of 25°C ± 2°C and 20°C ± 2°C, respectively. The fully extended leaves at the apex of V. faba plants were collected from 3- to 4-week-old plants for the analyses. The plants of Arabidopsis (Arabidopsis thaliana) wild type (Colombia ecotype), AtVAM3 mutant, sgr3-1, and it's complementary line sgr3-1/gSGR3 (which was sgr3-1 transformed with a 4-kb genomic fragment of SGR3) were grown in a growth chamber with 12 h of light and 12 h of darkness, with a photon flux density of 300 µmol m–2 s–1, at 22°C ± 2°C. Fully expanded rosette leaves of 4- to 6-week-old Arabidopsis plants were used for epidermal strip bioassay.
The epidermic strips from V. faba or Arabidopsis were peeled from the lower epidermis of leaves and cleaned up by gently brushing away the mesophyll cells. The cleaned strips were submerged in 10 mM MES (pH 6.1) and treated with the following procedures: For studying the vacuolar dynamic during stomatal movement, the closed stomata were induced to open under a halogen cold-light source (Colo-Parmer), and the opened stomata were induced to close in 10 µM ABA. For studying the effects of E-64d on stomatal opening of V. faba, the strips with closed stomata were transferred to 10 mM MES (pH 6.1) buffer with or without 100 µM E-64d (Sigma) diluted from 100 mM stock in methanol for 1 h, then transferred into 10 mM MES (pH 6.1) with 50 mM KCl to induce stomatal opening under a halogen cold-light source (Colo-Parmer). For studying the stomatal opening difference between sgr3-1, sgr3-1/gSGR3, and wild type of Arabidopsis, the strips with closed stomata were transferred to 10 mM MES (pH 6.1) buffer with 50 mM KCl to induce stomatal opening under a halogen cold-light source. Stomatal apertures were measured under a microscope at indicated times with more than 50 randomly selected stomata. Each assay was repeated three times.
Leaves of V. faba with different stomatal apertures were cut into small pieces about 1 mm2, then prefixed in the fixation solution containing 4% (v/v) glutaraldehyde and 1% (w/v) tannic (Komis et al., 2002
For vacuole fluorescent staining, the lower epidermal strips of V. faba and Arabidopsis leaves were dipped into 10 µM AO (Fluka; in MES buffer, pH 6.1) for 10 to 15 min, 1 µM FDA (Sigma; in MES buffer, pH 6.1) 5 to 10 min as described by Mathur et al. (2003)
The epidermal strips stained with AO or FDA were observed under MRC 1024 CLSM (Bio-Rad) or LSM 510 CLSM (Zeiss) equipped with an argon ion laser as the excitation source. With an excitation laser of 488 nm, a series of images were captured with a 505 to 550 nm band-pass filter. The epidermal strips stained with LysoTracker were observed under LSM 510 CLSM (Zeiss) equipped with a Helium/Neon laser as the excitation source. With an excitation laser of 543 nm, images were captured with a 560- to 615-nm band-pass filter. To register the dynamic of vacuoles in guard cells during stomatal movement, the epidermal strips preloaded with AO or FDA were treated for 10 to 15 min with 1 mg L–1 fusicoccin (Sigma) for stomatal opening or 10 µM ABA (Sigma) for stomatal closing, then observed under CLSM. Fusicoccin or ABA also was added directly to the buffer in which the strips were placed. The photobleaching was performed with the vacuoles stained with AO bleached 50 to 100 times with strong excitation light of 488 nm under the control of LSM 510 Meta (Zeiss). The images of prebleach and postbleach were collected. 3D projections were obtained from a series of 0.2 to 0.5 µm interval continuous optical sections with LSM 510 Meta (Zeiss). All images were processed using Confocal Assistant version 4.02 (Bio-Rad) or LSM 510 image browser version 3.0 (Zeiss) and were exported as TIFF files. The optical sections of X- or Y-axis were obtained from a series of Z-axis optical sections at different foci, using the ORTHO function of LSM 5 image browser version 3.0. Adobe Photoshop 6.0 was used for further processing of all the images.
We thank Dr. De Ye (China Agricultural University) and Dr. Zhenbiao Yang (University of California, Riverside) for their helpful discussion and critical reading of the manuscript. We also thank Dr. Masao Tasaka and Dr. Miyo T. Morita (Nara Institute of Science and Technology, Japan) for the generous gift of Arabidopsis seeds of sgr3-1 and sgr3-1/gSGR3. Received June 22, 2005; returned for revision August 26, 2005; accepted August 26, 2005.
1 This work was supported by the National Basic Research Program of China (grant nos. 2006CB100100 and 2003CB114300) and the National Science Foundation of China (grant nos. 30370129 and 30421002).  The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Xue-Chen Wang (xcwang{at}cau.edu.cn). Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.105.067520. * Corresponding author; e-mail xcwang{at}cau.edu.cn; fax 86–10–62733450.
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