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A Review of Plant Vacuoles: Formation, Located Proteins, and Functions

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A Review of Plant Vacuoles: Formation, Located Proteins, and Functions plants Review A Review of Plant Vacuoles: Formation, Located Proteins, and Functions Xiaona Tan , Kaixia Li, Zheng Wang, Keming Zhu, Xiaoli Tan * and Jun Cao * Institute of Life Sciences, Jiangsu University, Zhenjiang 212013, China * Correspondence: [email protected] (X.T.); [email protected] (J.C.) Received: 19 July 2019; Accepted: 4 September 2019; Published: 5 September 2019 Abstract: Vacuoles, cellular membrane-bound organelles, are the largest compartments of cells, occupying up to 90% of the volume of plant cells. Vacuoles are formed by the biosynthetic and endocytotic pathways. In plants, the vacuole is crucial for growth and development and has a variety of functions, including storage and transport, intracellular environmental stability, and response to injury. Depending on the cell type and growth conditions, the size of vacuoles is highly dynamic. Different types of cell vacuoles store different substances, such as alkaloids, protein enzymes, inorganic salts, sugars, etc., and play important roles in multiple signaling pathways. Here, we summarize vacuole formation, types, vacuole-located proteins, and functions. Keywords: plant vacuole; lytic vacuole; protein storage vacuole; vacuole iron transporter 1. Discovery History of the Vacuoles The term “vacuole” was first proposed by the famous French biologist Félix Dujardin and was used to represent the blank space of protozoan contractile vesicles [1]. A similar blank space was also observed in the leaves and roots of plants. Thus, the term was also adopted by plant biologists. In the early stages of vacuole research, methods of microscopic observation and neutral-red staining indicated that the vacuole was an acidic environment surrounded by membranes. At the end of the 19th century, de Vries believed that vacuoles were formed by special plastid-like precursors, called tonoplasts [2]. The vacuole is an important part of many cells. Mature cells of all terrestrial plants, most fungi, and algae (except prokaryotic cells) have vacuoles. However, there are no vacuoles in animal cells and in the immature plant cells, as well as some highly mature plant cells (such as stone cells). In mature plant cells, vacuoles can account for 90% of the cell’s volume. For a long time, the biochemical analysis of this organelle was hindered by a lack of technology, and the majority of knowledge came from the study of yeast bubbles. Some biochemical characterization of vacuole components and amino acid transport experiments were performed in yeast. In contrast, the study of plant vacuoles was limited to the localization of some vacuole components. In the early 1980s, the application of the method of separating vacuolar and purified vacuolar vesicles made biochemical and electrophysiological studies of plant vacuolar transporters feasible [3]. 2. Formation Processes of Vacuoles The early stages of vacuolar research were limited to examining vacuolar morphology, as described above. In recent years, however, improvements in technology have brought the research of vacuoles to the molecular level, including metabolomics, proteomics, T-DNA insertion mutants, and heterologous complementation. Experimental evidence indicates that the substances of the plant vacuole system come from the intracellular biosynthesis pathway and the endocytosis pathway. Biosynthesis pathways leading to vacuole formation include: (1) Early secretory pathway(from ER to late Golgi compartments): some Plants 2019, 8, 327; doi:10.3390/plants8090327 www.mdpi.com/journal/plants Plants 2019, 8, 327 2 of 11 Plants 2019, 8, x FOR PEER REVIEW 2 of 12 proteins located in the vacuole are separated from the proteins transported to the cell surface; (2) proteinsEndocytosis located of substances in the vacuole from are the separated plasma membrane; from the proteins (3) Autophagy; transported (4) Directto the transmissioncell surface; (2) of Endocytosiscytoplasm to of vacuoles. substances Ultimately, from the specificplasma proteinsmembra enterne; (3) the Autophagy; vacuole and (4) perform Direct transmission their functions of cytoplasmthrough sorting to vacuoles. and targeting Ultimately mechanisms, specific [proteins4]. As in enter animal the and vacuole yeast and cells, perform the vacuolar their transportfunctions pathwaythrough sorting in plants and begins targeting with mechanisms the endoplasmic [4]. As reticulum in animal (ER) and (Figure yeast 1cells,). A the conventional vacuolar transport route of vacuolepathway transport in plants consistsbegins with of a vesiclethe endoplasmic transport pathwayreticulum including (ER) (Figure endoplasmic 1). A conventional reticulum route output of vacuolemediated transport by vesicle consists and Golgi of a andvesicle post-Golgi transpor transportt pathway [5 ,including6]. For example, endoplasmic the tonoplast reticulum potassium output mediatedchannel AtTPK1 by vesicle in Arabidopsis and Golgi formsand post-Golgi dimers, is transport controlled [5,6]. by ER For quality example, control, the tonoplast and then reachespotassium the vacuolechannel throughAtTPK1 thein Arabidopsis Golgi apparatus forms dimers, [7]. An unconventionalis controlled by pathwayER quality of control, vacuolar and transport then reaches is the thedirect vacuole transport through from the ERGolgi to theapparatus vacuole [7]. without An un involvingconventional Golgi pathway and Golgi-posterior of vacuolar vesiclestransport [8, 9is]. theStudies direct have transport shown from that the vacuole ER to biogenesis the vacuole and without transport involving of plastid Golgi proteins and Golgi-posterior and lipids can vesicles occur [8,9].directly Studies from have theER shown without that Golgivacuole involvement biogenesis [and10]. transport It is clear of that plastid these proteins pathways and arelipids highly can occurconserved directly in eukaryotesfrom the ER [without11]. Recent Golgi studies involvement have reviewed[10]. It is clear the commonalities that these pathways and di arefferences highly conservedbetween di ffinerent eukaryotes eukaryotic [11]. transport Recent studies systems have from reviewed the perspective the commonalities of plants and and have differences discussed plantbetween vacuole different substitution eukaryotic and transport trafficking systems pathways from [9,12 the]. Proteinsperspective with of N-terminal plants and leading have sequencesdiscussed plantor transmembrane vacuole substitution domains and are secretedtrafficking by conventionalpathways [9,12]. protein Proteins secretion with pathways. N-terminal In contrast,leading proteinssequences lacking or transmembrane signaling peptides domains are secretedare secreted by unconventional by conventional protein protein secretion secretion pathways pathways. [8,13 In]. contrast,In addition, proteins some studieslacking havesignaling introduced peptides two ar newe secreted glycosylated by unconventional vacuolar GFP (greenprotein fluorescent secretion protein)pathways markers [8,13]. [In14 ].addition, some studies have introduced two new glycosylated vacuolar GFP (green fluorescent protein) markers [14]. Figure 1. ModelModel for for the formation of plant vacuoles. (1) (1) Endocytosis Endocytosis from from the the cell cell surface to a prevacuolar compartmentcompartment (PVC).(PVC). (2)(2) Early Early secretory secretory pathway pathway from from the the endoplasmic endoplasmic reticulum reticulum (ER) (ER) to tothe the late late Golgi Golgi compartment. compartment. (3) (3) Proteins Proteins are are sorted sorted into into the the PVCPVC byby anan earlyearly biosyntheticbiosynthetic vacuolar pathway. TheThe GolgiGolgi apparatus apparatus/trans-Golgi/trans-Golgi network networ (TGN)k (TGN) system system is important is important for biosynthetic for biosynthetic traffic. (4)traffic. PVC (4) is transferredPVC is transferred to vacuoles to vacuoles via the latevia biosyntheticthe late biosynthetic vacuole pathway.vacuole pathway. (5) PVC enters(5) PVC vacuoles enters vacuolesthrough autophagicthrough autophagic vacuoles (AV) vacu byoles degradation (AV) by degradation or biosynthetic or pathways.biosynthetic (6) pathways. Direct transport (6) Direct from transportER to vacuole. from (7)ER Transportto vacuole. of (7) ions Transport and solutes of ions on vacuoleand solutes membrane. on vacuole membrane. 3. Different Types of the Vacuoles Vacuoles account for most of the volume of mature cells in plants. Two types of vacuole, lytic vacuoles (LV) and protein storage vacuoles (PSV), appear sequentially during embryogenesis [15,16]. LVs contain hydrolases to degrade unwanted cellular substances, while PSVs accumulate Plants 2019, 8, 327 3 of 11 3. Different Types of the Vacuoles Vacuoles account for most of the volume of mature cells in plants. Two types of vacuole, lytic vacuoles (LV) and protein storage vacuoles (PSV), appear sequentially during embryogenesis [15,16]. LVs contain hydrolases to degrade unwanted cellular substances, while PSVs accumulate large amounts of defense and storage proteins. Because of the degradation and storage functions exhibited by LVs and PSVs, respectively, some labeled proteins are used to distinguish them [15,17]. Recent studies have indicated that these two types of vacuoles share a transport protein [18,19]. They also noticed that in maturing seeds, the LVs were turned into PSVs, which was reversed during germination [20]. Most vacuolar soluble proteins are synthesized into larger precursors in the ER and then transported into vacuoles, in which become mature following the intervention of vacuolar processing
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