Vacuoles and prevacuolar compartments

doi:10.1016/S1369-5266(00)00115-1

Current Opinion in Plant Biology

Volume 3, Issue 6, 1 December 2000, Pages 469-475

https://doi.org/10.1016/S1369-5266(00)00115-1 Get rights and content

Abstract

Plant vacuoles are complex and dynamic organelles. Important advances have been made in our understanding of the transporters present in the tonoplast and of the molecular interactions that allow targeting to vacuoles. Despite these advances, markers that permit vacuoles to be defined unambiguously have not yet been identified.

Introduction

Plant vacuoles are morphologically and functionally diverse organelles, and recent reports have emphasized that there are different kinds of plant vacuoles. Some function primarily as storage organelles, others as lytic compartments. More than one kind of vacuole has been observed in cells undergoing differentiation [1], maturation [2], and autophagy [3], and in fully differentiated cells [4], [5]. Vacuole function depends on a suite of soluble and membrane-bound proteins. These are specifically tailored for each cell type at every developmental stage, and the import and destruction of vacuolar proteins is carefully orchestrated.

A major impediment to our understanding of plant vacuoles is the lack of specific markers for these organelles and other endomembrane components. Different kinds of vacuoles may be morphologically similar, and prevacuolar compartments may be indistinguishable from other single- membrane-bound organelles. Yet, an accurate interpretation of many kinds of data requires precise identification of endomembrane compartments. Our view of plant vacuoles and prevacuolar compartments is clouded because dependable markers are not available and agreed upon. Markers for these compartments have been proposed, but have not been shown to be unambiguous. Indeed, a unique marker may not exist for some compartments.

In this review, we consider recent developments in our understanding of plant vacuoles and prevacuolar compartments. Particular attention is focused on integral membrane transporters in the tonoplast and vesicle trafficking of proteins to the vacuole. This review is limited to literature published in 1999 to mid-2000 that has particular relevance to these topics.

Section snippets

Aquaporins are abundant constituents of all vacuoles

The tonoplast-intrinsic proteins (TIPs) are often the most abundant vacuolar transporters (for review see [6 radical dot ]). Many of these proteins function as water channels (i.e. aquaporins) when expressed in Xenopus laevis oocytes. Individual plant species typically have several TIP genes, with representatives in evolutionarily conserved classes (e.g. see [7]). TIP genes within species are differentially regulated, suggesting that different TIPs may be utilized under specific conditions. Two recent

Routes for protein transport to the vacuole

Proteins destined for the vacuole are synthesized on the ER and delivered by vesicles to the vacuole (for reviews see [29], [30], [31], [32]). Most soluble proteins transported to the vacuole pass through the Golgi apparatus, where they are sorted into vesicles. These vesicles may then fuse with a prevacuolar compartment or directly with the tonoplast. Alternative routes that bypass the Golgi or begin as endocytotic vesicles are likely to exist.

Morphologically distinct transport vesicles carry proteins to the vacuole

Three classes of morphologically distinct vesicles

Vacuolar sorting signals

The orderly sorting of proteins into transport vesicles requires recognition of vacuolar sorting signals by vesicle-associated receptors. Three classes of vacuolar signals have been characterized in plants: first, short sequences within an amino-terminal propeptide containing a consensus sequence of NPIR or NPIXL (using the single-letter code for amino acids); second, short sequences with no identified consensus sequence at the carboxyl terminus of a carboxy-terminal propeptide; and third,

The uncertain nature of prevacuolar compartments

Although there is agreement that plant cells might contain a prevacuolar compartment, the nature of this organelle remains unclear. Prevacuoles are defined as organelles that receive cargo from transport vesicles and subsequently deliver that cargo to the vacuole by fusion with the tonoplast. Alternatively, a prevacuole can be defined as an organelle that contains t-SNAREs and v-SNAREs, which bind to v-SNAREs on transport vesicles and t-SNAREs on vacuoles, respectively. To date, a prevacuolar

Conclusions

Plant vacuoles and prevacuolar compartments are part of a continuum of endomembrane compartments. All of these compartments are specialized for individual functions. Most of them are dynamic and can change morphologically and functionally to suit the needs of the cell. Although our understanding of plant vacuoles remains rudimentary, we are beginning to appreciate the plasticity of this organelle. Rapid progress is being made in the areas of tonoplast transport and the regulation and import of

Acknowledgements

The authors thank Masayoshi Maeshima and Christophe Maurel for critical review of this manuscript. Eleanor Crump assisted in editing the manuscript and her help is gratefully acknowledged.

References and recommended reading

Papers of particular interest, published within the annual period of review,have been highlighted as:

• of special interest
•• of outstanding interest

References (50)

N Paris et al.
Plant cells contain two functionally distinct vacuolar compartments
Cell
(1996)
DG Robinson et al.
One vacuole or two vacuoles: do protein storage vacuoles arise de novo during pea cotyledon development?
J Plant Physiol
(1995)
R Kaldenhoff et al.
Features and function of plant aquaporins
J Photochem Photobiol B Biol
(1999)
JM Davies et al.
Energetics of the plasma membrane pyrophosphatase
Trends Plant Sci
(1997)
C Kluge et al.
Subunit D of the vacuolar H⁺-ATPase of Arabidopsis thaliana
Biochem Biophys Acta
(1999)
N Tavakoli et al.
Subunit C of the vacuolar H⁺-ATPase of Hordeum vulgare
FEBS Lett
(1999)
L Jiang et al.
Sorting of membrane proteins to vacuoles in plant cells
Plant Sci
(1999)
CR Hawes et al.
Endomembranes and vesicle trafficking
Curr Opin Plant Biol
(1999)
EA Miller et al.
Uncoating the mechanisms of vacuolar protein transport
Trends Plant Sci
(1999)
S Aubert et al.
Ultrastructural and biochemical characterization of autophagy in higher plant cells subjected to carbon deprivation: control by the supply of mitochondria with respiratory substrates
J Cell Biol
(1996)

Cited by (49)

The rice RMR1 associates with a distinct prevacuolar compartment for the protein storage vacuole pathway
2011, Molecular Plant
Citation Excerpt :
Arabidopsis AtRMR2 (JR702) was found to specifically bind tobacco chitinase ctVSD in vivo and in vitro (Park et al., 2007). PVCs are membrane-bounded intermediate organelles that have dual functions, either mediating protein traffic from Golgi apparatus or TGN to vacuoles, or protein recycling from PVC to Golgi apparatus or TGN (Bethke and Jones, 2000; Jiang and Rogers, 2003). Several studies indicated that the lytic PVC is a multivesicular body (MVB) in plant cells that is defined by the vacuolar sorting receptor proteins (VSRs) or their GFP-tagged reporters (Paris et al., 1997; Tse et al., 2004; Miao et al., 2006).
Transport of vacuolar proteins from Golgi apparatus or trans-Golgi network (TGN) to vacuoles is a receptor-mediated process via an intermediate membrane-bound prevacuolar compartment (PVC) in plant cells. Both vacuolar sorting receptor (VSR) and receptor homology region-transmembrane domain-RING-H2 (RMR) proteins have been shown to function in transporting storage proteins to protein storage vacuole (PSV), but little is known about the nature of the PVC for the PSV pathway. Here, we use the rice RMR1 (OsRMR1) as a probe to study the PSV pathway in plants. Immunogold electron microscopy (EM) with specific OsRMR1 antibodies showed that OsRMR1 proteins were found in the Golgi apparatus, TGN, and a distinct organelle with characteristics of PVC in both rice culture cells and developing rice seeds, as well as the protein body type II (PBII) or PSV in developing rice seeds. This organelle, also found in both tobacco BY-2 and Arabidopsis suspension cultured cells, is morphologically distinct from the VSR-positive multivesicular lytic PVC or multivesicular body (MVB) and thus represent a PVC for the PSV pathway that we name storage PVC (sPVC). Further in vivo and in vitro interaction studies using truncated OsRMR1 proteins secreted into the culture media of transgenic BY-2 suspension cells demonstrated that OsRMR1 functions as a sorting receptor in transporting vicilin-like storage proteins.
Expression and characterization of two functional vacuolar sorting receptor (VSR) proteins, BP-80 and AtVSR4 from culture media of transgenic tobacco BY-2 cells
2010, Plant Science
Vacuolar sorting receptors (VSRs) are type I integral membrane family proteins that mediate protein transport from late Golgi or trans-Golgi network (TGN) to vacuole in plant cells. The N-terminus of VSR is believed to be important for cargo binding while its transmembrane domain (TMD) and cytoplasmic tail (CT) are essential for its correct subcellular localization. In this study, we have developed and tested an expression system using transgenic tobacco BY-2 cells to produce truncated VSR (VSRNT) proteins lacking the TMD/CT into the culture media. The expressed truncated VSRs (BP80NT and AtVSR4NT) are properly secreted into the culture media and bind specifically to the known vacuolar sorting determinants (VSDs) of various vacuolar proteins in a calcium-dependent manner in vitro. Therefore, since VSR cargo proteins are likely secreted into the culture media along with the truncated VSRs, potential applications of such expression system include identification of native VSR cargo proteins from the culture media of transgenic cells via LC–MS/MS analysis and large-scale purification of truncated VSR proteins for structural study to understand cargo–receptor interaction mechanisms in plants.
The C-terminal sequence from common bugle leaf galactan:galactan galactosyltransferase is a non-sequence-specific vacuolar sorting determinant
2007, FEBS Letters
The Ajuga reptans L. galactan:galactan galactosyltransferase (ArGGT) is a vacuolar enzyme that synthesizes long-chain raffinose family oligosaccharides (RFOs), the major storage carbohydrates of this plant. ArGGT is structurally and functionally related to acid plant α-galactosidases (α-Gals) of the glycosylhydrolase family 27, present in the apoplast or the vacuole. Sequence comparison of acid α-Gals with ArGGT revealed that they all contain an N-terminal signal sequence and a highly similar core sequence. Additionally, ArGGT and some acid α-Gals contain C-terminal extensions with low sequence similarities to each other. Here, we show that the C-terminal pentapeptide, SLQMS, is a non-sequence-specific vacuolar sorting determinant. Analogously, we demonstrate that the C-terminal extensions of selected acid α-Gals from Arabidopsis, barley, and rice, are also non-sequence-specific vacuolar sorting determinants, suggesting the presence of at least one vacuolar form of acid α-Gal in every plant species.
Response to Gomord et al.: Golgi-bypassing: delivery of biopharmaceutical proteins to protein storage vacuoles in plant bioreactors
2006, Trends in Biotechnology
Hordein accumulation in developing barley grains
2019, Frontiers in Plant Science
Seeds as Bioreactors
2018, Molecular Pharming: Applications, Challenges and Emerging Areas

View all citing articles on Scopus

View full text

ReviewVacuoles and prevacuolar compartments

Abstract

Introduction

Section snippets

Aquaporins are abundant constituents of all vacuoles

Routes for protein transport to the vacuole

Morphologically distinct transport vesicles carry proteins to the vacuole

Vacuolar sorting signals

The uncertain nature of prevacuolar compartments

Conclusions

Acknowledgements

References and recommended reading

Cell

J Plant Physiol

J Photochem Photobiol B Biol

Trends Plant Sci

Biochem Biophys Acta

FEBS Lett

Plant Sci

Curr Opin Plant Biol

Trends Plant Sci

Ultrastructural and biochemical characterization of autophagy in higher plant cells subjected to carbon deprivation: control by the supply of mitochondria with respiratory substrates

J Cell Biol

Barley aleurone cells contain two types of vacuoles: characterization of lytic organelles by use of fluorescent probes

Plant Cell

Specific accumulation of GFP in a non-acidic vacuolar compartment via a C-terminal propeptide-mediated sorting pathway

Plant J

An abundant TIP expressed in mature highly vacuolated cells

Plant J

Desiccation and osmotic stress increase the abundance of mRNA of the tonoplast aquaporin BobTIP26-1 in cauliflower cells

Planta

Characterization of closely related delta-TIP genes encoding aquaporins which are differentially expressed in sunflower roots upon water deprivation through exposure to air

Plant Mol Biol

Osmotic water permeability of isolated vacuoles

Planta

Aquaporin Nt-TIPa can account for the high permeability of tobacco cell vacuolar membrane to small neutral solutes

Plant J

Tonoplast intrinsic protein isoforms as markers for vacuolar functions

Plant Cell

Energization of plant cell membranes by H+-pumping ATPases: regulation and biosynthesis

Plant Cell

Localization of pyrophosphatase in membranes of cauliflower inflorescence cells

Planta

Functional complementation of yeast vma1DELTA cells by a plant subunit A homolog rescues the mutant phenotype and partially restores vacuolar H+-ATPase activity

Plant J

The Arabidopsis det3 mutant reveals a central role for the vacuolar H+-ATPase in plant growth and development

Genes Devel

CAX1, an H+/Ca2+ antiporter from Arabidopsis

Proc Natl Acad Sci USA

Properties and molecular cloning of Ca2+/H+ antiporter in the vacuolar membrane of mung bean

Eur J Biochem

Functional expression of mung bean Ca2+/H+ antiporter in yeast and its intracellular localization in the hypocotyl and tobacco cells

Eur J Biochem

Review
Vacuoles and prevacuolar compartments

Energization of plant cell membranes by H⁺-pumping ATPases: regulation and biosynthesis

Functional complementation of yeast vma1DELTA cells by a plant subunit A homolog rescues the mutant phenotype and partially restores vacuolar H⁺-ATPase activity

The Arabidopsis det3 mutant reveals a central role for the vacuolar H⁺-ATPase in plant growth and development

CAX1, an H⁺/Ca²⁺ antiporter from Arabidopsis

Properties and molecular cloning of Ca²⁺/H⁺ antiporter in the vacuolar membrane of mung bean

Functional expression of mung bean Ca²⁺/H⁺ antiporter in yeast and its intracellular localization in the hypocotyl and tobacco cells