Plant Vacuoles

Abstract

Vacuoles can represent 90% or more of the total volume of a mature plant cell. Derived from the endoplasmic reticulum and Golgi complex and delimited from the cytosol by the vacuolar membrane (tonoplast), they are versatile dynamic organelles capable of assuming different morphologies and serving a wide range of functions in different cells or in the same cells at different times. Many cells contain just one central vacuole, others contain several that differ in their relative contributions to lytic and storage functions and a few contain compound vacuoles – vacuoles within vacuoles – by means of which lytic and storage functions are partitioned within a single vacuole. The many processes in which vacuoles participate include the maintenance of tissue water balance and turgor regulation for growth, mechanical support, stomatal aperture control and thigmotropic responses; inorganic and organic nutrient storage and retrieval; macromolecule turnover and salvage; cytosolic inorganic ion and metabolite homeostasis; storage excretion and detoxification of endogenous waste products, heavy metals and other xenobiotics. Although most of the carrier‐ or channel‐mediated transport processes that occur across the vacuolar membrane are driven by the H+ electrochemical gradient (proton motive force, PMF) established by ATP (adenosine triphosphate)‐energised V‐type H+‐ATPases and inorganic pyrophosphate‐energised H+‐PPases (V‐PPase), there are many that are directly energised by ATP through the action of P‐type ATPases or ATP‐binding cassette (ABC) transporters.

Key Concepts

  • Vacuoles often represent much of the volume of a plant cell.
  • As components of the endomembrane system, vacuoles are derived from the endoplasmic reticulum and/or Golgi complex.
  • Depending on their function and contents, plant vacuoles fall into two categories: lytic vacuoles (LVs) or protein storage vacuoles (PSVs). LVs, whose contents are acidic and dominated by degradative enzymes, primarily serve a lysosomal function. Protein storage vacuoles (PSVs), whose contents are less acidic and dominated by storage proteins, primarily serve a depot function.
  • Bounded by membranes rich in water channels (aquaporins) that enable rapid osmotic equilibration between the vacuole lumen and cytosol, vacuoles are crucial for establishing and maintaining cell turgor and for ensuring adequate hydration of the cytosol.
  • Plant vacuoles are vital for the temporary storage of both organic and inorganic nutrients and for maintaining their levels within the ranges compatible with metabolism in the cytosol and other intracellular organelles.
  • The plant vacuolar membrane (tonoplast) is unusual in containing two distinct categories of proton pumps – V‐type H+‐ATPases (V‐ATPases) and vacuolar H+‐pyrophosphatases (V‐PPases) – that are capable of contributing to vacuolar acidification and to the establishment of the transmembrane H+‐electrochemical gradient (proton motive force, PMF) required for secondary active solute transport into and out of the vacuole.
  • As the sole enzyme in plant cells capable of catalysing the direct hydrolysis of cytosolic inorganic pyrophosphate (PPi) to inorganic phosphate (Pi), the hydrolytic activity of the V‐PPase is critical if cytosolic biosynthetic reactions that generate PPi are to be sustained.
  • Vacuoles enable plant cells to accumulate both endogenous and exogenous toxins, for instance secondary metabolites and heavy metals, to levels that would be lethal if the same substances were to accumulate to similar levels in the cytosol or other intracellular compartments.
  • Multidrug and toxin efflux (MATE) transporters and ATP‐binding cassette (ABC) transporters mediate the vacuolar uptake of many secondary metabolites and xenobiotics.

Keywords: ATP‐binding cassette (ABC) transporters; vacuolar biogenesis and protein sorting; heavy metal detoxification; multidrug and toxin efflux (MATE) transporters; nutrient storage; secondary metabolites; storage excretion; vacuolar membrane (tonoplast); V‐ATPase; V‐PPase

Figure 1. Vacuole biogenesis and vacuolar protein sorting in plants. (a) Assembly of protein storage vacuoles (PSVs). Proteins synthesised on the ER that are destined for the PSV undergo sorting through Golgi‐dependent or Golgi‐independent pathways. In the Golgi‐dependent pathway, storage proteins are packaged into dense vesicles (DVs) which either directly fuse with the PSV or undergo transfer to multivesicular bodies (MVBs) before fusion with the PSV. In the Golgi‐independent pathway, storage proteins are relayed directly from the ER to the PSV via precursor‐accumulating compartments (PACs) in a process in which BP80 homologues and RMR family members contribute to cargo recognition. (b) Assembly of lytic vacuoles (LVs). Proteins synthesised on the ER that are destined for the LV undergo sorting through Golgi‐dependent or Golgi‐independent pathways. In the Golgi‐dependent pathway, there are two options. In the first, the proteins, after recognition by BP80/VSR vacuolar sorting receptors and adaptor protein AP1, are incorporated into clathrin‐coated vesicles (CCVs) which are then transported to the prevacuolar compartment (PVC) for fusion with the LV. In the second Golgi‐dependent pathway, proteins are transported to the LV in an AP3‐dependent manner. In the Golgi‐independent pathway, protein transfer to the LV is mediated by ER bodies. All of the Golgi‐dependent pathways regardless of whether PSVs or LVs are the final destination demand the participation of coat protein complexes (COPs) by means of which proteins are relayed to and from the ER to the Golgi. Reproduced by permission of Sara Jarret, CMI.
Figure 2. Vacuolar proton pumps. (a) V‐type H+‐ATPase (V‐ATPase). The V‐ATPase complex consists of a peripheral V1 sector responsible for ATP hydrolysis and an integral V0 sector responsible for H+ translocation across the membrane. ATP hydrolysis in the V1 sector induces rotation of the V0 sector and the relay of 2H+s from the cytosolic side to luminal side of the vacuolar membrane for each molecule of ATP hydrolysed to establish a pH difference (ΔpH) and an electrical potential difference (ΔΨ). (b) Vacuolar H+‐translocating inorganic pyrophosphatase (V‐PPase). The V‐PPase is a dimeric protein consisting of two identical integral subunits, each of which contains 16 transmembrane helices. PPi hydrolysis drives the translocation of 1H+ from the cytosolic to luminal side of the vacuolar membrane for each molecule of PPi hydrolysed. While the V‐ATPase is only one of many enzymes that hydrolyse cytosolic ATP derived from catabolic processes such as glycolysis and oxidative phosphorylation to ADP + Pi, the V‐PPase appears to be the only enzyme capable of catalysing the direct hydrolysis of cytosolic PPi to 2Pi. An implication of the importance of the V‐PPase for the hydrolysis of cytosolic PPi generated in biosynthetic reactions in which nucleotide triphosphates undergo hydrolysis to monophosphates + PPi is that this enzyme is crucial for cytosolic PPi stasis such that when the enzyme is inactive, the accumulation of PPi in the cytosol has a stalling action on various cytosolic biosynthetic reactions as exemplified by the synthesis of sucrose (glucose‐1‐P + UTP ⇌ UDP‐glucose + PPi; UDP‐glucose + D‐fructose ⇌ sucrose + UDP). Reproduced by permission of Sara Jarret, CMI.
Figure 3. Examples of transporters involved in the movement of sugars, organic acids, inorganic anions and inorganic cations across the vacuolar membrane. This is not intended as an exhaustive treatment of the pathways known but rather to provide an indication of the various modes of transport involved. The modes of transport shown are those mediated by primary pumps (red spheres, cylinders and/or ellipses), H+‐antiporters (brown ellipses), uniporters (grey ellipses) and channels (blue cylinders). Refer to main text for acronym definitions. Reproduced by permission of Sara Jarret, CMI.
Figure 4. Detoxification of arsenic through the combined action of phytochelatin synthase and vacuolar ABC transporters (Briat, ; Song et al., ). Arsenate (As(V); AsO34), a phosphate analogue (PO43), is taken up by plant roots by plasma membrane phosphate transporters. Once in the cytosol, As(V) is reduced by the enzyme arsenate reductase that utilises reduced glutathione (GSH) as a source of reducing equivalents to yield As(III) and oxidised glutathione (GSSG). The As(III) generated promotes the activity of phytochelatin synthase (AtPCS) which utilises GSH (γ‐Glu‐Cys‐Gly) for the synthesis of PCs ((γ‐Glu‐Cys)nGly polymers) that bind As(III) with high affinity to yield PC‐As(III) complexes. The PC‐As(III) complexes generated undergo ATP‐energised transport across the vacuolar membrane by two members of the ABCC subclass, ABCC1 (AtMRP1) and ABCC2 (AtMRP2). Protection from the toxic action of arsenic is exerted at two levels: at the level of detoxification by chelation and at the level of detoxification by sequestration (storage excretion). Inset: A characteristic feature of ABCC1 and ABCC2, and most other members of the ABCC subfamily of ABC transporters (Rea, ), is that in addition to the two NBDs (NBD1 and NBD2) and two TMDs (TMD1 and TMD2), they each have an additional N‐terminal TMD (TMD0) consisting of five transmembrane spans. Reproduced by permission of Sara Jarret, CMI.
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Further Reading

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Rea, Philip A() Plant Vacuoles. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0001675.pub3]