ReviewVacuoles and prevacuolar compartments
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]). 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
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