Plant Vacuoles

Abstract

The vacuoles of plant cells are multifunctional organelles that are central to cellular strategies of plant development. They share some of their basic properties with the vacuoles of algae and yeast and the lysosomes of animal cells. They are lytic compartments, function as reservoirs for ions and metabolites, including pigments, and are crucial to processes of detoxification and general cell homeostasis. They are involved in cellular responses to environmental and biotic factors that provoke stress. In the vegetative organs of the plant, they act in combination with the cell wall to generate turgor, the driving force for hydraulic stiffness and growth. In seeds and specialized storage tissues, they serve as sites for storing reserve proteins and soluble carbohydrates. In this way, vacuoles serve physical and metabolic functions that are essential to plant life. Plant cell vacuoles were discovered with the early microscope and, as indicated in the etymology of the word, originally defined as a cell space empty of cytoplasmic matter. Technical progress has variously altered the operating definition of the plant vacuole over time. Today, definitions continue to be colored by the tools and concepts brought to bear in any given study. Indeed, the combination of microscopy, biochemistry, genetics, and molecular biology is fundamental to research into the plant vacuole. In this review, vacuoles are provisionally defined as the intracellular compartments that arise as a terminal product of the secretory pathway in plant cells. They are ontogenetically and functionally linked with other components of the vacuolar apparatus (i.e., vacuoles and those membranous bodies that are either committed to becoming vacuolar or have immediately completed a vacuolar function). 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 biogenetic pathways include (1) sorting of proteins destined for the vacuole away from those to be delivered to the cell surface after transit through the early stages of the secretory pathway; (2) endocytosis of materials from the plasma membrane; (3) autophagy pathways for vacuole formation; and (4) direct cytoplasm-to-vacuole delivery. Ultimately, sorting and targeting mechanisms ensure that specific proteins are faithfully assigned to conduct the vacuolar functions. The reader is referred to other contributions to this issue (i.e., Battey et al., 1999; Sanderfoot and Raikhel, 1999) and to previous reviews (Herman, 1994; Okita and Rogers, 1996; Bassham and Raikhel, 1997; Marty, 1997; Robinson and Hinz, 1997; Neuhaus and Rogers, 1998; Herman and Larkins, 1999) for detailed information on specific aspects of vacuole biology. Plant cell vacuoles are widely diverse in form, size, content, and functional dynamics, and a single cell may contain more than one kind of vacuole. Although major morphological differences were recorded by the very first microscopists, it has been commonly assumed that all vacuoles have the same origin and belong to a common group. However, with improvements in cell fractionation and biochemical analyses as well as in the use of new molecular probes, it has become possible to characterize specialized vacuolar compartments in the cells from a variety of tissues (Hoh et al., 1995; Paris et al., 1996; Fleurat-Lessard et al., 1997; Swanson et al., 1998; Webb, 1999, in this issue). In most cells from the vegetative tissues of the plant body, the central vacuole occupies much of the volume and is essential for much of the physiology of the organism. Among the many functions of this organelle are turgor maintenance, protoplasmic homeostasis, storage of metabolic products, sequestration of xenobiotics, and digestion of cytoplasmic constituents. In regard to the latter function, vacuoles are acidic and contain hydrolytic enzymes analogous to the lysosomal enzymes of animal cells. The membrane, or tonoplast, of such vacuoles contains the vegetative-specific aquaporin γ-TIP (for tonoplast intrinsic protein; Höfte et al., 1992; Marty-Mazars et al., 1995; Paris et al., 1996; Barrieu et al., 1998; see below). In some cell types, defense or signal compounds are stored in the vacuole, particularly within specialized cells located in strategically favorable tissues such as the leaf epidermis. As early as last century, it was observed that many pigments (e.g., anthocyanins) are localized in the vacuoles of epidermal cells from flowers, leaves, and stems. Recent findings suggest that the membranes of such specialized vacuoles contain specific ATP binding cassette (ABC) transporters (Rea et al., 1998). In contrast, reserve tissues of seeds and fruit contain vacuoles specialized in the storage of proteins (Okita and Rogers, 1996; Müntz, 1998; see Herman and Larkins, 1999, in this issue). The membrane of the protein storage vacuoles (PSVs) contains the seed-specifi