Plant Vacuoles
Year: 1999
Type: article
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-specific aquaporin α-TIP (Höfte et al., 1992; Paris et al., 1996; Swanson et al., 1998; see below). Storage proteins are also synthesized and accumulated in specialized vegetative cells in response to wounding and to developmental switches (Maeshima et al., 1985; Sonnewald et al., 1989; Staswick, 1990; Herman, 1994; Jauh et al., 1998). Distinctively, the membrane of the vegetative storage vacuoles contains the aquaporin ∂-TIP (Jauh et al., 1998; Neuhaus and Rogers, 1998). In the endosperm of cereal grains, proteins accumulate in endoplasmic reticulum (ER)–derived organelles of vacuole-like size (see below). A few recent studies show that distinct vacuoles may simultaneously function in the same cell. Two separate vacuolar compartments, defined by α-TIP and γ-TIP, occur together in the root tip cells of barley and pea seedlings, mature tobacco plants, as well as in the plumule cells of pea seedlings (Paris et al., 1996). Barley lectin in root tip cells is found within α-TIP–positive vacuoles but not in γ-TIP–positive vacuoles, whereas the barley acid cysteine protease, aleurain, is specifically contained within γ-TIP–positive vacuoles but is absent from α-TIP–positive vacuoles. Thus, α-TIP defines a storage vacuole in which proteins are protected against degradative enzymes, whereas γ-TIP defines a separate, acidic, lytic vacuole. As cells develop large vacuoles, these two compartments appear to merge because the marker membrane antigens, α-TIP and γ-TIP, colocalize to the same membrane, in of the vacuolar compartments (Paris et al., 1996). Two distinct vacuole are found in of barley et al., 1998). In to cells contain a of lytic as vacuoles by the of this study. Although and vacuoles are lytic organelles with acidic it was that the vacuoles, which have many of plant vacuoles, function as lysosomes and be involved in the of cells et al., 1998). of the of vacuoles from of the cells of the from et al., The vacuole that in the cell is located the contains large of and is to act as a The vacuole that is found in mature cells not contain is much than the vacuole, and occupies a central in mature cells. The in cell volume that are for leaf from the membrane of the vacuole, on which the γ-TIP aquaporin and the are (for a of membrane see et al., 1999, in this issue). vacuoles to cell The vacuole whereas the vacuole membrane In any the vacuole and the vacuole not merge but within the mature cell. because vacuoles are of in of both and function, of vacuole may be found within a given cell. In the cells of pea for two of vacuole are a vegetative and a storage vacuole (Hoh et al., in cells to protein is by vacuoles that are together with the more mature central vacuole et al., 1996; and 1996). of the vacuoles are into the central vacuole. However, intracellular digestion is vacuoles in the as from the large central vacuole. The of function and in the that the definition of vacuoles is to and distinct as be in the their is In that may be variously defined to and physical may not to distinct of the and of vacuoles was on morphological over the few have of vacuolar to a more detailed molecular vacuolar proteins as well as proteins destined for are delivered to the vacuole the secretory which the and endocytotic that are in The basic mechanisms that these in are (see Battey et al., 1999; Sanderfoot and Raikhel, 1999, in this issue). In plant as in animal cells and of synthesized soluble as well as membrane proteins through the vacuolar pathway the soluble proteins destined for the vacuole are synthesized as with a signal by The is to the their the membrane, the secretory proteins are and to early such as the binding protein et al., synthesized in their that to the are by a that not the to the vacuole. some proteins that are not in the are delivered to the by the et al., 1997; et al., 1998; see and 1999, in this issue). A for in the basic pathways are for the maintenance, and of vacuoles. and in the early secretory pathway to sorting of vacuolar proteins in the to a an early biosynthetic vacuolar pathway. from to vacuole the biosynthetic vacuolar pathway. from early secretory to pathway to the vacuole an with possible material from by the endocytotic pathway from the cell surface to the vacuole to vacuole through autophagy by degradative or biosynthetic of ions and the early endoplasmic proteins that are into or the membrane contain sorting for their targeting to in any of the compartments the secretory pathway. some the organelle is the and these proteins are not other proteins for the secretory pathway are to the a Indeed, have been to direct the and the occur in a than to the in a that from that assumed to in animal and cells. The has a in the secretory pathway. In plant it of a of by a in animal morphological in the plant cell a and a Marty, and 1995; and 1998). The of of and that be defined by their distinct and by their and biochemical and of synthesized secretory which in the are in the and As they are vacuolar proteins transit through the early stages of the secretory pathway together with proteins that are destined to be into the or delivered to the plasma The is a major in the secretory pathway and is the of sorting that separate proteins destined for from those to the vacuole. The in size to the specific function of the cell. the that biogenetic and processes are in response to specific cell morphological studies have been in cells. The processes involved in the of vacuoles and their for are in the cells of the root the of into cells. In cells in which new vacuoles are the of a of from a central the a single be by and be observed the and from the the of to the vacuole. of the of in cells from the root of The vacuolar apparatus was by the (see Marty, The was with a very were are in in and and in The on the vacuolar pathway an the sorting and the vacuole. have been referred to as because they act ontogenetically as the of the vacuole. They also the and the vacuole and functional in the to the vacuole. of this they be to act as a for proteins to the vacuole from of the have an than the of the the into the same as the from which they is with that are from of their membranes Marty, The in cells may be an of the in cells and yeast et al., The membrane from a that occur either membrane of the were or the membrane from the the endocytotic were the be a in which the endocytotic and vacuolar biogenetic pathways As by microscopy, the of vacuoles with a of that to of cytoplasmic material this of that as to of of the in a and, through a and the of through these are as early (i.e., a cytoplasmic by a by and studies show that the and are acidic and contain lysosomal acid The in the is after it has been is that the enzymes are from the as the membrane of the a vacuole is The membrane, which to hydrolytic enzymes, within the vacuole and the vacuoles together to a few large vacuoles. Ultimately, of through the tonoplast, by γ-TIP in vacuole et al., 1992; of stages of cytoplasmic by involved in cellular and to of of a cell from the root of of the to a and of were as in the to In response to autophagy is in cells that are The pathway is for after of cells et al., 1994; et al., 1996; and 1996). of are first in the and The vacuoles, in the are into the central vacuole. has been that the of cellular autophagy is by the of with and not by the in the of and et al., 1996). of vacuoles has been with an in the of intracellular and and a of membrane et al., 1996). As a degradative autophagy a central in protein and organelle has been in and cell and it is for such as also be for biosynthetic as a cytoplasm-to-vacuole targeting as in and with regard to (see below). cells in seeds and vegetative organs accumulate proteins that function as of The most common storage proteins are the which are found in and the which are to cereal storage including and some have been to be to vacuoles the and Larkins, see also Herman and Larkins, 1999, in this issue). However, studies on the and of storage proteins in and have that reserve proteins be diverse sites the vacuolar pathway. As a proteins are stored in a variety of compartments specific to the plant of cell and protein morphological and and biochemical analyses have evidence for a to the in and other Storage proteins are synthesized as that are into the of the and the apparatus into specialized vacuoles is to their protein storage are observed in the of the the early of the storage proteins are commonly in in in with the or of the et al., 1996). of are commonly found in to the that storage cell wall and The of two sites for vacuolar proteins the and the of secretory suggest to vacuole function and to storage proteins the and proteins processes as they progress through the to the they are to the storage vacuoles and Hinz, the were found to from the storage the but not the are involved in the of soluble storage proteins to the vacuole. A pathway has been in cells from seeds of and et al., 1998). In these and were to be from the to the large to in large are distinct from the but to the protein bodies in pea and Hinz, was that the of storage contained in these large from protein that are in the et al., they accumulate and proteins such as but not mature In the of storage proteins are not the the apparatus such that their is not by the In to seeds contain storage with in the The are into the the of the Storage together with other storage are by the mature as as the However, the of the pathway to the storage vacuole are was that the of the into occur by membrane or by of the into the vacuole. a system to both the of the and the intracellular of vacuolar reserve proteins In the cells of the very few large vegetative vacuoles become by studies that the vegetative vacuoles of cells are by a membrane system that contains storage proteins et al., However, the origin of this new membrane system is not The vegetative vacuoles as the storage vacuoles with storage proteins (Hoh et al., the the storage proteins as against the tonoplast and it to into the a the protein by the tonoplast, become storage vacuoles in the stages of the and the storage vacuole, which to accumulate reserve into a distinct of large storage vacuole. A of storage protein is in the cells the to stages of storage protein Storage proteins accumulate in and with terminal may and become bodies in seedlings, are by a vegetative vacuole through of sequestration and of of the tonoplast and of cytoplasmic in the have been et al., and Herman, from seeds by the as storage proteins in endosperm cells et al., are into the of the In many including and which are within the of the and, as in the of the et al., et al., In endosperm become as synthesized are and with the of protein and molecular such as and Larkins, 1989; et al., and Larkins, 1996). of other including and on the other accumulate in vacuoles together with and Larkins, et al., are the pathway the to the vacuolar whereas are into the vacuole by an et al., have that mechanisms storage proteins from are in vegetative tobacco cells et al., 1996; et al., 1997; et al., 1998). The in the as in many storage cells in but the are by an and delivered to the vegetative vacuole, they are be the of storage proteins to storage vacuoles by large in cells et al., 1992; et al., 1998; see suggest that the cellular of autophagy be for proteins and early to the vacuole, a biosynthetic cytoplasm-to-vacuole targeting pathway as in The of the compartments specialized in protein storage is and not all are all belong to the vacuolar apparatus of plant cells. a more detailed of see Herman and in this is defined as the of and plasma membrane materials from the cell surface into the cell. has been in plant cells in which both and have been in and 1994; Marty, 1997; see also Battey et al., 1999, in this issue). Two distinct of by endocytosis have been to in plant (1) from the plasma membrane to an including the and the and (2) from the plasma membrane to the and the vacuoles and from plasma membrane have also been as of a in cells and of plasma membrane to the cell together with a of in cells et al., Barrieu et al., studies of cells by suggest that the endocytotic and biosynthetic vacuolar pathways the vacuoles are Marty, The these pathways in cells is but it to that the be the and belong to the vacuolar but their direct to the of the vacuole the of plasma membrane has been in plant the involved to be by A is a protein functionally to the (see localized on a early in soluble proteins and membrane proteins through the early stages of the secretory pathway. they are away from proteins destined for to the cell surface the of the Sanderfoot and Raikhel, 1999, in this issue). proteins a sorting signal to for vacuolar after their from the in the of such they are to the of vacuolar targeting have been and Raikhel, vacuolar proteins (e.g., and contain an as a targeting (e.g., barley tobacco and contain a whereas some vacuolar proteins (e.g., and contain a targeting signal in an of the mature The targeting in from the barley cysteine et al., and from et al., contain a acid in the is and for the sorting of the to the vacuole et al., et al., is delivered to the vacuole in cells from the of the (Maeshima et al., whereas is to a lytic distinct from the (Paris et al., 1996). to a vacuolar sorting has not been in targeting the was to be and for the targeting of barley lectin to the vacuole and Raikhel, et al., The of the in barley lectin is not for it the of of the in the are for the targeting of barley lectin et al., analyses have been to characterize the targeting signal of tobacco et al., from vacuolar proteins in and it was that a from contains information for with the vacuolar sorting in a et al., 1998). The barley and accumulate in whereas tobacco is delivered to vacuoles of vegetative cells. that more than one sorting the targeting signal and that of proteins from the to the vacuoles more than one pathway et al., 1995; et al., 1998). and vacuolar also and and were found to be functionally in proteins to the vacuole et al., plant vacuolar proteins are synthesized a on from et al., and from et al., have targeting information in of the mature which are in the of the reserve cells of soluble such as and which are have been in the that the vacuolar targeting not be in all cells et al., recent on cells that some vacuolar be into the The pathway for these proteins from either the vacuole or the of the last et al., 1998). Although acid of plant vacuolar proteins are to proteins to the vacuole in yeast et al., plant proteins are to the yeast vacuole by from those by plants, that the is yeast and plants and Raikhel, membrane and soluble proteins are to vacuoles by and studies on from tobacco plants suggest that soluble proteins such as and membrane proteins such as α-TIP the same by through and pathways for membrane proteins of the tonoplast have been (Höfte and 1992; and Rogers, 1998). The vacuolar membrane α-TIP and γ-TIP are membrane with and both and located in the In an early of the targeting information contained in it was found that a the and the cytoplasmic of α-TIP is to a protein to the In the cytoplasmic was not found for the targeting of α-TIP in the same tobacco cells (Höfte and the of a membrane protein was in tobacco and Rogers, 1998). was found that the of the plant vacuolar sorting (see the protein the to the and the cytoplasmic of γ-TIP not this contrast, the cytoplasmic of α-TIP of the protein through the but it to be localized to vacuoles. was that are two separate pathways to vacuoles for membrane a direct pathway by α-TIP from the to and a separate pathway by γ-TIP the and to the vegetative lytic vacuole and Rogers, 1998). vacuolar proteins are away from the pathway through a that to their to the vacuole. Two in the of plant vacuolar sorting et al., 1994; et al., was that the in the of and two was to be by a sorting et al., Indeed, a protein of has been from a of from all the of a vacuolar sorting is a membrane protein that is localized in the and in vacuolar vacuolar are distinct from both α-TIP and γ-TIP vacuoles but are analogous to have been and the appear to be in and plants (Paris et al., to the of an protein (for epidermal was on the use of functional in many of the proteins involved in intracellular protein sorting in and yeast cells et al., many common with and yeast is of in with the proteins of the from is located the in and on the in the root cells of is to that it also may a in targeting proteins to the vacuole et al., 1998; see also Sanderfoot and Raikhel, 1999, in this issue). the or vacuolar sorting of soluble proteins have not been and the of pathways for membrane proteins is in and Raikhel, In to sorting other components of the vacuolar targeting are in is a with the distinct from that of the tonoplast and which is for the targeting of soluble proteins to the vacuole et al., 1997; see et al., 1999, in this issue). of soluble and membrane proteins in the secretory pathway is to be by the and of and, in cell or by and direct compartments 1998). As an early in proteins that from the and and have been in plant cells et al., 1998; see Sanderfoot and Raikhel, 1999, in this issue). that a proteins in plant, and animal cells of the molecular of in and are to be by membrane (for soluble protein (see Sanderfoot and Raikhel, 1999, in this issue). to the on with on the membranes The soluble proteins (for and (for soluble the and a by ATP membrane The and of with the of which include and components of the of suggest that the mechanisms of and are and A of proteins functionally to the in yeast and cells is in plant cells and Raikhel, 1999, in this issue). show that the sorting for soluble proteins to the plant vacuole well with the The plant vacuolar (see is to the the As a the to be in the vacuolar together with to the the and the et al., are et al., 1998). The vacuolar is in the vacuolar pathway. However, function in or or in autophagy is evidence is also of compartments of the vacuolar pathway in cell or Indeed, the and the from the same from the and the and and vacuoles have been (see Marty, are with an intracellular by and and it be are not The vacuole an in the of the plant cell. is involved in the of cell volume and cell the of cytoplasmic ions and the storage of and and the sequestration of ions and are by specific proteins in the tonoplast and indicated in functions have been and et al., 1992; and and 1996; 1997; 1997; 1997; et al., 1998; see also et al., 1999; et al., 1999, in this issue). to the for the force by either the or the be to of ions and their is by specific and The and the vacuolar membrane are crucial to the diverse functions of the vacuole in plant such as cell and plant signal protoplasmic homeostasis, and of metabolic pathways et al., of and in a and is by an and an the vacuole. The force for and of (i.e., and or the tonoplast through transporters and the of Recent studies have the of a of to the that are by (Rea et al., 1998). are in the of a of including and to the the proteins in plants are to in the of and and compounds from the to the vacuole. They function in cell storage of and of A for plant is also in and of vacuoles a central in the strategies of plants in their In the of cells from the plant body, vacuoles the They are for the cell volume for of material and information cells and their In with the cell they turgor, which is basic to cell hydraulic stiffness and plant growth. In specialized and vacuoles serve as of and In vacuoles proteins to be for growth. The of vacuolar functions a in biochemistry, and A of intracellular pathways have been and a for concepts in vacuole The are many and but are which suggests that the vacuolar processes serve specific they are all any one of the compartments from a given pathway may function as to and is to characterize vacuoles and their more by molecular and to recent molecular findings to a Plant be to and characterize vacuolar functions. both in the degradative and biosynthetic as a in the and of the vacuolar the of vegetative vacuoles cells it the vacuolar apparatus switches from vegetative to storage and it is by are protein by membranes all have the same the and of the has also to be the of the in of and vacuoles and their are the mechanisms involved cells vacuoles from cells The is to and of and to for their contributions to the in this The is by from the et the the and the et
Source: The Plant Cell
DOI: 10.2307/3870886
Author: Francis Marty
Institution: Université de Bourgogne
Language: English
Subfield: Cell Biology
Domain: Life Sciences
Open Access status: green
OpenAlex ID: W4242491965