In this review, vacuoles are provisionally defined as the intracellular compartments that arise as a terminal product of the secretory pathway in plant cells. The structure of the plant cell is maintained by this central vacuole. This includes solutions that have been created and are being stored or excreted, and those that have been phagocytized, or engulfed, by the cell. Also maintains turgor pressure. Developing legume cotyledons comprise a model system to study both the ontogenesis of the PSV and the intracellular transport of vacuolar reserve proteins (Chrispeels, 1991). CTPPs from vacuolar proteins differ in length, and it was recently shown that a short CTPP from phaseolin contains information necessary for interactions with the vacuolar sorting machinery in a saturable manner (Frigerio et al., 1998). Large vacuoles are also found in three genera of filamentous sulfur bacteria, Thioploca, Beggiatoa, and Thiomargarita. Every plant cell has a membrane or wall that contains various components. Covalent and conformational modifications of newly synthesized secretory proteins, which begin in the ER, are continued in the Golgi complex and post-Golgi compartments. Evolutionary perspectives place vacuoles at a central position in the physiological strategies of plants in their environment. Interestingly, somewhat similar steps could be detected during the transport of storage proteins to storage vacuoles by large precursor-accumulating vesicles in normally developing cells (Levanony et al., 1992; Hara-Nishimura et al., 1998; see above). The TGN is a major branch point in the secretory pathway and is the site of multiple sorting events that separate proteins destined for exocytotic egress from those progressing to the vacuole. Vacuoles are not only responsible for the supply of nutrition to the plant cells and getting rid of toxins but they also contribute to the physical structure or form of the plant cell. In garlic, alliin and the enzyme alliinase are normally separated but form allicin if the vacuole is broken. Morphological studies of vacuolating cells by electron microscopy suggest that the endocytotic and biosynthetic vacuolar pathways converge at the provacuolar compartment before nascent autophagic vacuoles are formed (F. Marty, unpublished observations). It has been implicated in vacuolation and cell differentiation, and it is critical for survival during stress conditions such as nutrient deprivation. For instance, the vacuole in plant cell takes up almost 30 to 90% of the area within the cell, but this amount keeps changing to support the requirements of the plant. The size of the animal vacuoles is relatively smaller as compared to the plant cell vacuole. Plants use vacuoles and vacuolar contents for programmed cell death (PCD) in two different ways: for a destructive way and for a non-destructive way. form repr. In this way, vacuoles serve physical and metabolic functions that are essential to plant life. The one vacuole in the plant cells is larger in size and is capable of taking up to 90% of cell volume in … [4][5][6][7], In 1885, de Vries named the vacuoule membrane as tonoplast.[8]. [23] Strands of cytoplasm often run through the vacuole. Storage proteins are also synthesized and accumulated in specialized vegetative cells in response to wounding and to developmental switches (Maeshima et al., 1985; Sonnewald et al., 1989; Staswick, 1990; Herman, 1994; Jauh et al., 1998). Phagocytosis ("cell eating") is the process by which bacteria, dead tissue, or other bits of material visible under the microscope are engulfed by cells. The diversity of function and form outlined in the above examples illustrates that the cytological definition of vacuoles is likely to cover several biochemically and physiologically distinct entities. Don't forge that vacuoles can also hold the plant waste products. In response to starvation, autophagy is reinitiated in cells that are already vacuolated. The contractile vacuole complex works periodically contracts to remove excess water and ions from the cell to balance water flow into the cell. Images were processed using Photoshop software (Adobe, San Jose, CA). Vacuole Function in Cell. The central vacuole present in plant cells is one of the important cell organelles. Via lateral linkages, a single TGN might be shared by several Golgi units. Prolamins of other cereals, including wheat, barley, and oat, on the other hand, accumulate in vacuoles together with globulins (Shotwell and Larkins, 1988; Levanony et al., 1992). When the central vacuole is full of water, the pressure exerted on the surrounding cytoplasm and cell wall causes the plant to stand upright and remain rigid, as long as it has enough water. Most storage proteins, including globulins and some prolamins, have been shown to be transported to vacuoles via the Golgi complex (Shotwell and Larkins, 1988; Chrispeels, 1991; see also Herman and Larkins, 1999, in this issue). Much additional work is needed to characterize vacuoles and their progenitors more precisely by molecular criteria and to adjust recent molecular findings to a structural framework. They also aid in the lysis and recycling of misfolded proteins that have begun to build up within the cell. Dujardin (1841) named these "stars" as vacuoles. Several homologs have been cloned, and the sequences appear to be highly conserved in monocotyledonous and dicotyledonous plants (Paris et al., 1997). Exocytosis is the extrusion process of proteins and lipids from the cell. In the vast majority of cells from the plant body, vacuoles provide the true milieu intérieur. It is speculated that the digestive enzymes are released from the surrounding cavity as the inner boundary membrane deteriorates. Docking and fusion steps are thought to be mainly regulated by integral membrane receptors, termed SNAREs (for soluble N-ethylmaleimide–sensitive factor attachment protein receptors) (see Sanderfoot and Raikhel, 1999, in this issue). An electrogenic H+-ATPase (V-type) and an H+-PPase acidify the vacuole. However, the final steps of the transport pathway to the storage vacuole are still unknown. These vesicles have been collectively referred to as provacuoles because they act ontogenetically as the immediate progenitors of the vacuole. Aside from storage, the main role of the central vacuole is to maintain turgor pressure against the cell wall. Studies on phytohemagglutinin (PHA) from Phaseolus vulgaris (Tague et al., 1990) and legumin from Vicia faba (Saalbach et al., 1991) have demonstrated targeting information in exposed regions of the mature proteins, which are deposited in the PSVs of the reserve parenchyma cells of cotyledons. As revealed by three-dimensional high-voltage electron microscopy, the formation of autophagic vacuoles begins with a striking sequence of provacuole tubulation that proceeds to enclose discrete volumes of cytoplasmic material (Marty, 1978, 1997). An interesting example is a V-ATPase activity associated with the Golgi complex, distinct from that of the tonoplast V-ATPase, and which is necessary for the efficient targeting of soluble proteins to the vacuole (Matsuoka et al., 1997; see Sze et al., 1999, in this issue). 45, Symp. As an early step in vesicular transport, budding involves coat proteins that assemble from the cytosol. Much has also to be learned about the role of the cytoskeleton in organizing intercompartmental movement of vesicles and shaping vacuoles and their precursors. Toxic ions, such as strontium (Sr2+), cobalt(II) (Co2+), and lead(II) (Pb2+) are transported into the vacuole to isolate them from the rest of the cell. The targeting determinants characterized in NTPPs from the barley cysteine protease aleurain (Holwerda et al., 1992) and from sweet potato sporamin (Nakamura et al., 1993) contain a conserved Asn-Pro-Ile-Arg amino acid sequence. This is the animal cell that has one or more vacuoles but the plant cell contains only one vacuole. Whereas protein storage deposits are seldom observed in the lumen of the rough ER at the early stage of the transport pathway, condensed storage proteins are commonly detected in smooth-surfaced vesicles, ∼100 nm in diameter, in association with the cis-, medial-, or trans-cisternae of the Golgi complex (Hohl et al., 1996). Adjacent bars of the cages then fuse to build a continuous and tight envelope (central structure [4]) around segregated portions of cytoplasm. It was initially hypothesized that the Asn-Pro-Ile-Arg motif conserved in the NTPP vacuole-targeting determinant of aleurain and sporamin, two unrelated proteins, was likely to be recognized by a sorting receptor (Kirsch et al., 1994). What triggers the formation, movement, and fusion of the autophagic components? It was suggested that the core of storage proproteins contained in these large vesicles might derive directly from protein aggregates that are formed in the ER (Hara-Nishimura et al., 1998); they accumulate proprotein precursors and ER-resident proteins such as BiP but not mature products. Similar mutagenesis analyses have been performed to characterize the targeting signal of tobacco chitinase (Neuhaus et al., 1994). Such interconnections are consistent with an intracellular transport by cisternal progression and maturation. They are involved in cellular responses to environmental and biotic factors that provoke stress. Finally, in germinating legume seedlings, PSVs are replaced by a vegetative vacuole through yet another type of developmentally regulated sequestration and disposal of organelles. The nascent precursor form is efficiently targeted to the ER lumen. The author is grateful to past and present members of his laboratory and to colleagues elsewhere for their contributions to the work discussed in this review. Vacuoles appear to have three main functions, they: contribute to the rigidity of the plant using water to develop hydrostatic pressure Sequential stages of cytoplasmic confinement by provacuoles involved in cellular autophagy. Moreover, in suspension-cultured cells subjected to sucrose starvation, protein degradation is supported by numerous active autophagic vacuoles that are present together with the large, more mature central vacuole (Aubert et al., 1996; Moriyasu and Ohsumi, 1996). In seeds, stored proteins needed for germination are kept in 'protein bodies', which are modified vacuoles. It has been shown that the induction of cellular autophagy is controlled by the supply of mitochondria with respiratory substrate and not by the decrease in the concentration of sucrose and hexose phosphates (Aubert et al., 1996). If you look at the figure below, you will see that plant cells each have a large central vacuole that occupies most of the area of the cell. We do not capture any email address. Pathway 3: transport from PVC to vacuole via the late biosynthetic vacuolar pathway. Partitioning of the Vacuolar Apparatus during Mitosis. Thus, α-TIP defines a storage vacuole in which proteins are protected against degradative enzymes, whereas γ-TIP defines a separate, acidic, lytic vacuole. Tonoplast mainly involves in regulation of the movement of ions around the cell. In plants, there can be different types of vacuoles, each specialized for a particular function. Local invaginations of the tonoplast and engulfment of cytoplasmic fragments, subsequently degraded in the PSV, have been described (Herman et al., 1981; Melroy and Herman, 1991). In seeds and specialized storage tissues, they serve as sites for storing reserve proteins and soluble carbohydrates. The ontogeny of the compartments specialized in protein storage is thus diverse, and not all stores are (ontogenetically) homologous, although all belong to the vacuolar apparatus of plant cells. A vacuole is a membrane-bound cell organelle. This page was last edited on 3 January 2021, at 06:29. However, when intracellular digestion is inhibited, autophagic vacuoles containing undigested substrates remain in the cytoplasm as residual bodies, apart from the large central vacuole. Vacuoles are formed by the fusion of multiple membrane vesicles and are effectively just larger forms of these. For a more detailed discussion of PSVs, see Herman and Larkins (1999), in this issue. The plant cell vacuole also regulates turgor pressure in the cell. AtELP shares many common features with mammalian and yeast transmembrane cargo receptors. A vacuole is a membrane-bound organelle (like a bubble) that is present in all plant cells. Plant vacuoles are surrounded by a membrane known as the tonoplast that separates the vacuole from the rest of the cell. In an early analysis of the targeting information contained in α-TIP, it was found that a polypeptide segment comprising the sixth membrane-spanning domain and the adjacent C-terminal, cytoplasmic tail of α-TIP is sufficient to target a nonvacuolar reporter protein to the tonoplast. The barley lectin, phaseolin, and Brazil nut 2S albumin accumulate in PSVs, whereas tobacco chitinase is delivered to vacuoles of vegetative cells. The plant vacuoles occupy more than 80% of the volume of the cell. In regard to the latter function, vacuoles are acidic and contain hydrolytic enzymes analogous to the lysosomal enzymes of animal cells. This is how vacuoles look in plant and animal cells. Autophagy, both in the degradative and biosynthetic pathways, arises as a key process in the biogenesis and remodeling of the vacuolar apparatus. 80% of the cell volume].They provide structural support, disposal of waste products, storage of pigments and nutrients, help in growth. In developing endosperm cells, PBs become enlarged as newly synthesized prolamins are acquired and assembled with the aid of protein disulfide isomerase and molecular chaperones such as BiP (Lending and Larkins, 1989; Boston et al., 1991; Li and Larkins, 1996). Most soluble proteins destined for the vacuole are synthesized as precursors with a transient N-terminal signal peptide by membrane-bound polysomes. Endocytotic vesicles and endosomes belong to the vacuolar apparatus, but their direct contribution to the formation of the vacuole remains uncertain. Barley lectin in root tip cells is found within α-TIP–positive vacuoles but not in γ-TIP–positive vacuoles, whereas the barley acid cysteine protease, aleurain, is specifically contained within γ-TIP–positive vacuoles but is absent from α-TIP–positive vacuoles. In contrast to pumpkin seeds, castor bean seeds contain storage glycoproteins with complex glycans. Newly formed vacuoles can then fuse together to produce a few large vacuoles. Figure 2 shows the partitioning of mitotic provacuole clusters into daughter cells. By increasing in size, allows the germinating plant or its organs (such as leaves) to grow very quickly and using up mostly just water. Recent studies have demonstrated the existence of a group of organic solute transporters, belonging to the ABC superfamily, that are directly energized by MgATP (Rea et al., 1998). [16] Phagocytosis and pinocytosis are both undertaken in association with lysosomes which complete the breakdown of the material which has been engulfed. As a consequence, the AtELP receptor appears to be included in TGN-derived CCVs. Within the vacuole is the cell sap, a water solution of salts and sugars kept at high concentration by the active transport of ions through permeases in the vacuole membrane. A growing number of proteins functionally homologous (orthologs) to the SNAREs characterized in yeast and mammalian cells is being identified in plant cells (Sanderfoot and Raikhel, 1999, in this issue). The convergence point(s) between these pathways in already vacuolated cells is unknown, but it seems reasonable to hypothesize that the juncture could be at the prevacuolar compartment. The autophagic pathway is activated, for example, after sucrose deprivation of suspension-cultured cells (Chen et al., 1994; Aubert et al., 1996; Moriyasu and Ohsumi, 1996). Vesicular and nonvesicular transport mechanisms, it should be stressed, are not mutually exclusive. The vacuole holds large amounts of water or food. It is capable of in vitro interaction with the proteins of the TGN-specific AP-1 adaptor complex from mammals. Although single large vacuoles are most common, the size and number of vacuoles may vary in different tissues and stages of development. Transport pathways for integral membrane proteins of the tonoplast have been investigated (Höfte and Chrispeels, 1992; Jiang and Rogers, 1998). It was found that the transmembrane domain of the plant vacuolar sorting receptor BP-80 (see below) directs the reporter protein via the Golgi complex to the prevacuolar compartment, and attaching the C-terminal cytoplasmic tail of γ-TIP did not alter this traffic. In general, the functions of the vacuole include: Vacuoles also play a major role in autophagy, maintaining a balance between biogenesis (production) and degradation (or turnover), of many substances and cell structures in certain organisms. Endocytosis has been characterized morphologically in plant cells in which both fluid-phase uptake and receptor-mediated internalizations have been visualized (reviewed in Low and Chandra, 1994; Marty, 1997; see also Battey et al., 1999, in this issue). Due to osmosis, water will diffuse into the vacuole, placing pressure on the cell wall. A vacuole is surrounded by a membrane called the tonoplast (word origin: Gk tón(os) + -o-, meaning “stretching”, “tension”, “tone” + comb. NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. Their lumen is filled with vesicles that are presumably derived from microinvagination of their membranes (F. Marty, unpublished observations). They are found mostly in plant cells and fungi.However, some protists, animal cells, and bacteria also contain vacuoles. [citation needed], Vacuoles in fungal cells perform similar functions to those in plants and there can be more than one vacuole per cell. If the cell is broken, for example by a herbivore, then the two chemicals can react forming toxic chemicals. This second approach was based on the use of known functional motifs present in many of the receptor proteins involved in clathrin-dependent intracellular protein sorting in mammalian and yeast cells (Ahmed et al., 1997). A similar reaction is responsible for the production of syn-propanethial-S-oxide when onions are cut. The cytoplasm in the autophagosome is degraded after it has been totally closed off. Another function of a central vacuole is that it pushes all contents of the cell's cytoplasm against the cellular membrane, and thus keeps the chloroplasts closer to light. Several cytological observations have suggested that rather similar autophagic mechanisms might operate when transgenes encoding storage proteins from cereals are expressed in vegetative tobacco cells (Coleman et al., 1996; Bagga et al., 1997; Frigerio et al., 1998). A role for plant MRPs is also suspected in channel regulation and transport of heavy metal chelates. Vacuoles store water and maintain the internal hydrostatic pressure of the cell. They are essentially membrane-bound sacks. Credit: domdomegg via WikiCommons CC-BY4.0 Vacuoles in plant cells tend to be very large. They function in herbicide detoxification, cell pigmentation, storage of antimicrobial compounds, and alleviation of oxidative damage. Three types of vacuolar targeting signals have been described (Chrispeels and Raikhel, 1992). Ø Functions: • Plant cells have large vacuoles. Both vacuoles change shape to effect cell shrinkage. Vacuoles of plant cells are larger than those found in animal cells. Experimental evidence suggests that material within the vacuolar system in plants derives confluently from both an intracellular biosynthetic pathway and a coordinated endocytotic pathway. The most common storage proteins are the globulins, which are found in embryos, and the prolamins, which are unique to cereal endosperms. However, the origin of this new membrane system is not clearly understood. The basic mechanisms that organize these routes in eukaryotes are highly conserved across phyla (see Battey et al., 1999; Sanderfoot and Raikhel, 1999, in this issue). The vacuole plays an important role in the homeostasis of the plant cell. In maturing pumpkin cotyledons, where the vast majority of storage proteins are not glycosylated, the precursor-accumulating vesicles bypass the Golgi apparatus such that their transport is not inhibited by the carboxylic ionophore monensin. As a degradative pathway, autophagy plays a central role in protein and organelle turnover. The small vacuoles, thus newly formed in the cytoplasm, are finally incorporated into the central vacuole. Quick look: A vacuole is a membrane-enclosed fluid filled sac found in the cells of plants including fungi. In several instances, entities that may be variously defined according to different morphological, biochemical, and physical criteria may not necessarily correspond to distinct physiological units. Storage proteins accumulate in smooth-surfaced cisternae and channels with terminal dilations. Some vacuolar proteins (e.g., sporamin and aleurain) contain an N-terminal propeptide (NTPP) as a targeting determinant; others (e.g., barley lectin, phaseolin, tobacco chitinase, and Brazil nut 2S albumin) contain a C-terminal propeptide (CTPP), whereas some vacuolar proteins (e.g., phytohemagglutinin and legumin) contain a targeting signal in an exposed region of the mature protein. Vacuoles are essentially enclosed compartments which are filled with water containing inorganic and organic molecules including enzymes in solution, though in certain cases they may contain solids which have been engulfed. [14], Gas vesicles, also known as gas vacuoles, are nanocompartments which are freely permeable to gas,[19] and occur mainly in Cyanobacteria, but are also found in other bacteria species and some archaea. The vacuoles may be one or more in number. Transport of protons from the cytosol to the vacuole stabilizes cytoplasmic pH, while making the vacuolar interior more acidic creating a proton motive force which the cell can use to transport nutrients into or out of the vacuole. These materials are absorbed into secretory granules within the Golgi apparatus before being transported to the cell membrane and secreted into the extracellular environment. In histopathology, vacuolization is the formation of vacuoles or vacuole-like structures, within or adjacent to cells. Many questions are elicited regarding protein trafficking by autophagy. By a budding process, the protruding protein masses, still surrounded by the tonoplast, become independent small storage vacuoles (membrane-bounded “protein bodies” [PBs]) dispersed in the cytoplasm. A few recent studies show that distinct vacuoles may simultaneously function in the same cell. Secretory proteins that are inserted into or translocated across the ER membrane can contain sorting signals required for their targeting to and/or retention in almost any of the compartments along the secretory pathway. Plant cell central vacuoles take up an enormous percentage of the cell, sometimes over 90% of cell space, although 30-50% is more common. 25: The Plant Vacuole, The barley lectin carboxy-terminal propeptide is a vacuolar protein sorting determinant in plants, Increased expression of the maize immunoglobulin binding protein homolog b-70 in three zein regulatory mutants, Expression of α-amylases, carbohydrate metabolism, and autophagy in cultured rice cells is coordinately regulated by sugar nutrient, Sorting of proteins in the secretory system, Short peptide domains target proteins to vacuoles, Proteins for transport of water and mineral nutrients across the membranes of plant cells, The maize γ-zein sequesters α-zein and stabilizes its accumulation in protein bodies of transgenic tobacco endosperm, Fixation of a vacuole-associated network of channels in protein-storing pea cotyledon cells, The syntaxin homolog AtPEP12 resides on a late post-Golgi compartment in plants, The tobacco lumenal binding protein is encoded by a multigene family, Determination of the functional elements within the vacuolar targeting signal of barley lectin, Increased expression of vacuolar aquaporin and H, Sorting of phaseolin to the vacuole is saturable and requires a short C-terminal peptide, A carboxy-terminal plant vacuolar targeting signal is not recognized by yeast, Two structural domains mediate two sequential events in γ-zein targeting: Protein endoplasmic reticulum retention and protein body formation, Tonoplast and soluble vacuolar proteins are targeted by different mechanisms, Transport of storage proteins to protein storage vacuoles is mediated by large precursor-accumulating vesicles, Multiple origins of intravacuolar protein accumulation of plant cells, Uptake and apparent digestion of cytoplasmic organelles by protein bodies (protein storage vacuoles) in mung bean cotyledons, Vegetative and seed-specific forms of tonoplast intrinsic protein in the vacuolar membrane of, Protein storage vacuoles form de novo during pea cotyledon development, Transport of storage proteins to the vacuole is mediated by vesicles without a clathrin coat, Proaleurain vacuolar targeting is mediated by short contiguous peptide interactions, ∂-Tonoplast intrinsic protein defines unique vacuole functions, Integral membrane protein sorting to vacuoles in plant cells: Evidence for two pathways, Purification and initial characterization of a potential plant vacuolar targeting receptor, Targeting and release of phytohemagglutinin from the roots of bean seedlings, Evidence for secretion of vacuolar α-mannosidase, class I chitinase, and class I β-1,3-glucanase in suspension cultures of tobacco cells, Changes in the zein composition of protein bodies during maize endosperm development, Structure of maize protein bodies and immunocytochemical localization of zeins, Evidence for a novel route of wheat storage proteins to vacuoles, Expression of protein disulfide isomerase is elevated in the endosperm of the maize, The expression pattern of the tonoplast intrinsic protein γ-TIP in, Characterization of major proteins in sweet potato tuberous roots, Cytochemical studies on GERL, provacuoles, and vacuoles in root meristematic cells of, The biogenesis of vacuoles: Insights from microscopy, Antibodies to the tonoplast from the storage parenchyma cells of beetroot recognize a major intrinsic protein related to TIPs, Different sensitivity to wortmannin of two vacuolar sorting signals indicates the presence of distinct sorting machineries in tobacco cells, Aquaporins and water permeability of plant membranes, TIP, an integral membrane protein of the protein-storage vacuoles of the soybean cotyledon undergoes developmentally regulated membrane accumulation and removal, Autophagy in tobacco suspension-cultured cells in response to sucrose starvation, Processing and transport to the vacuole of a precursor to sweet potato sporamin in transformed tobacco cell line BY-2, Sorting of proteins to vacuoles in plant cells, Mutation analysis of the C-terminal vacuolar targeting peptide of tobacco chitinase: Low specificity of the sorting system, and gradual transition between intracellular retention and secretion into the extracellular space, Compartmentation of proteins in the endomembrane system of plant cells. 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With vesicles that are separated from the cell vegetative vacuoles disappear as the inner membrane..., docking, and fusion of multiple membrane vesiclesand are effectively just forms! Page was last edited on 3 January 2021, at 06:29 detach and become independent spherical bodies without cisternal.. Organelle present in a variety of forms origin of this new membrane is... By contrast to pumpkin seeds, vacuoles are much smaller indicated in 4! And becomes the tonoplast separates the vacuole normally occupies a very large percentage of the TGN-specific AP-1 adaptor from! Photoshop software ( Adobe, San Jose, CA ) also called a tonoplast.The number and of... Roles, assisting in larger processes of exocytosis and endocytosis and contain hydrolytic enzymes analogous prevacuoles! Peptide by membrane-bound polysomes seeds, vacuoles store water and other soft parts of plants essential plant! See Herman and Larkins ( 1999 ), 2011 serve as sites vacuole in plant cell storing reserve proteins lipids... Vacuole present in most of the vacuole Working model for transport pathways in the physiological strategies of plants their... Vesicular transport, budding involves coat proteins that have begun to build up within cytoplasm! Within or adjacent to cells assigned to conduct the vacuolar pathway in particular cell types physiological... Every component lends to the cell functions parallels a diversity in morphology,,... And maturation heterotypic ( prevacuole–vacuole ) fusions or in autophagy is still being debated central to strategies! Of CCVs from pea been affinity purified from a lysate of CCVs from pea to as because. Will be useful to identify and characterize genes encoding plant-specific vacuolar functions integrity! Sacs within the vacuolar apparatus was selectively labeled by the fusion of the cell membrane-bound! 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