Osmocytosis and Vacuolar Fragmentation in Guard Cell Protoplasts: Their Relevance to Osmotically-lnduced Volume Changes in Guard Cells

Diekmann, Wilfried; Hedrich, Rainer; Raschke, Klaus; Robinson, David G.

doi:10.1093/jxb/44.10.1569

Cited by 36 publications

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“…Also, in the protoplast study, vesicles were clearly observed, whereas in our study vesicles may have been present but could not be unequivocally identified. An earlier study using intact guard cells (Diekmann et al, 1993) found no evidence of vesicle formation during osmotically induced decreases in volume. In that study, the fluorescent dye, lucifer yellow, which is water soluble and generally assumed not to cross the plasma membrane, was used as an indicator for vesicle formation, so membrane internalization that was not accompanied by vesicle formation would not have been visible.…”

Section: Discussionmentioning

confidence: 81%

“…Furthermore, the energy requirement for vesicle formation should be less for smaller vesicles (Saxton and Breidenbach, 1988) or for flattened vesicles (Fricke et al, 2000). Despite these theoretical considerations and the data showing reversible membrane internalization in protoplasts, no evidence for endocytosis was observed in intact, turgid guard cells when lucifer yellow was used as an indicator of endocytotic vesicle formation and stomata were closed using osmotically induced changes in guard cell volume (Diekmann et al, 1993).…”

mentioning

confidence: 98%

“…Thus, guard cells must either: (a) change shape such that plasma membrane surface area remains nearly constant while volume changes, or (b) move membrane between the plasma membrane and internal sources within the cell to accommodate changes in surface area. Although the literature on guard cells assumes the latter solution (Diekmann et al, 1993;Homann, 1998;Blatt, 2000), examples of both solutions can be found in animal cells. For example, mammalian erythrocytes change shape to maintain a constant surface area as volume is changed osmotically, but neurons continuously shuttle membrane between the endomembrane system and the plasma membrane to vary both surface area and volume (Morris and Homann, 2001).…”

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confidence: 99%

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Changes in Surface Area of Intact Guard Cells Are Correlated with Membrane Internalization

2003

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Guard cells must maintain the integrity of the plasma membrane as they undergo large, rapid changes in volume. It has been assumed that changes in volume are accompanied by changes in surface area, but mechanisms for regulating plasma membrane surface area have not been identified in intact guard cells, and the extent to which surface area of the guard cells changes with volume has never been determined. The alternative hypothesis-that surface area remains approximately constant because of changes in shape-has not been investigated. To address these questions, we determined surface area for intact guard cells of Vicia faba as they underwent changes in volume in response to changes in the external osmotic potential. We also estimated membrane internalization for these cells. Epidermal peels were subjected to external solutions of varying osmotic potential to shrink and swell the guard cells. A membrane-specific fluorescent dye was used to identify the plasma membrane, and confocal microscopy was used to acquire a series of optical paradermal sections of the guard cell pair at each osmotic potential. Solid digital objects representing the guard cells were created from the membrane outlines identified in these paradermal sections, and surface area, volume, and various linear dimensions were determined for these solid objects. Surface area decreased by as much as 40% when external osmotic potential was increased from 0 to 1.5 MPa, and surface area varied linearly with volume. Membrane internalization was approximated by determining the amount of the fluorescence in the cell's interior. This value was shown to increase approximately linearly with decreases in the cell's surface area. The changes in surface area, volume, and membrane internalization were reversible when the guard cells were returned to a buffer solution with an osmotic potential of approximately zero. The data show that intact guard cells undergo changes in surface area that are too large to be accommodated by plasma membrane stretching and shrinkage and suggest that membrane is reversibly internalized to maintain cell integrity.Guard cells regulate stomatal pore size to allow CO 2 uptake while controlling water loss. To accomplish this, they respond to environmental factors such as light and CO 2 concentration and to chemical signals such as ABA, which may originate in other parts of the plant. Guard cells respond to these factors by regulating ion fluxes across the plasma membrane, and the resulting movement of water causes changes in cell volume, turgor pressure, and shape, leading to changes in the pore aperture. The changes in guard cell turgor pressure and volume caused by these processes can be quite large. In Vicia faba, guard cell turgor pressure has been shown to vary between 1.0 and 4.0 MPa (Franks et al., 1998(Franks et al., , 2001) as stomata go from closed to wide open, and volume has been shown to change by as much as 40% (Raschke and Dickerson, 1973;Franks et al., 2001). These changes can occur over a time period of minutes.An often-un...

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Section: Discussionmentioning

confidence: 81%

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confidence: 98%

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confidence: 99%

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Changes in Surface Area of Intact Guard Cells Are Correlated with Membrane Internalization

2003

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“…In hypertonie medium protoplasts endocytose excess plasma membrane in the form of large vesicular structures, and in addition form tethered spheres or bleb-like structures on the outside of the protoplast (Figure 7; [35,61,108]). On reswelling or in hypotonic medium these extrusions disappear while the endocytosed vesicles remain in the cytoplasm.…”

Section: Pressure-induced Exocytosismentioning

confidence: 99%

Exocytosis in plants

Thiel

Battey

1998

Protein Trafficking in Plant Cells

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Exocytosis is the final event in the secretory pathway and requires the fusion of the secretory vesicle membrane with the plasma membrane. It results in the release to the outside of vesicle cargo from the cell interior and also the delivery of vesicle membrane and proteins to the plasma membrane. An electrophysiological assay that measures changes in membrane capacitance has recently been used to monitor exocytosis in plants. This complements information derived from earlier light and electron microscope studies, and allows both transient and irreversible fusion of single exocytotic vesicles to be followed with high resolution in protoplasts. lt also provides a tool to investigate bulk exocytotic activity in single protoplasts under the infiuence of cytoplasmic modulators. This research highlights the role of intracellular Ca 2 +, GTP and pressure in the control of exocytosis in plants.In parallel to these functional studies, plant proteins with the potential to regulate exocytosis are being identified by molecular analysis. In this review we describe these electrophysiological and molecular advances, and emphasise the need for parallel biochemical work to provide a complete picture of the mechanisms controlling vesicle fusion at the plasma membrane of plant cells.

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“…Recent studies on leaf epidermis and guard cell protoplasts have revealed that endocytotic vacuoles (or vesicles) were formed as the guard cell volume and cell surface area decreased. These small vacuoles (or vesicles) could fuse with the plasma membrane, increasing its surface area as guard cell volumes increase (Diekmann et al, 1993;Homann, 1998;Kubitscheck et al, 2000;Shope et al, 2003). Moreover, scanning electron microscopy also showed that the exocytotic extrusions on the plasma membrane appeared in shrunk protoplasts but disappeared in swelled protoplasts, indicating that these extrusions may be involved in the dynamic change of the surface area in the guard cells (Lambrechts et al, 1992).…”

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The Dynamic Changes of Tonoplasts in Guard Cells Are Important for Stomatal Movement inVicia faba

et al. 2005

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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-epoxysuccinyl-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.

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Osmocytosis and Vacuolar Fragmentation in Guard Cell Protoplasts: Their Relevance to Osmotically-lnduced Volume Changes in Guard Cells

Cited by 36 publications

References 0 publications

Changes in Surface Area of Intact Guard Cells Are Correlated with Membrane Internalization

Changes in Surface Area of Intact Guard Cells Are Correlated with Membrane Internalization

Exocytosis in plants

The Dynamic Changes of Tonoplasts in Guard Cells Are Important for Stomatal Movement inVicia faba

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