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Energization of Transport Processes in Plants. Roles of the Plasma Membrane H -Atpase

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Energization of Transport Processes in Plants. Roles of the Plasma Membrane H -Atpase Update on Energization of Nutrient Transport Energization of Transport Processes in Plants. Roles of the Plasma Membrane H1-ATPase1 Teis E. Sondergaard, Alexander Schulz, and Michael G. Palmgren* Department of Plant Biology, The Royal Veterinary and Agricultural University, DK–1871, Copenhagen, Denmark Much has been learned about the energization of proteins. Specialized cells throughout the plant body nutrient transport since Hoagland in 1944 gave his serve as transport interfaces between symplast and famous series of lectures on plant nutrition. Already at apoplast, and intense transport occurs across the that time it was speculated that energy for transport of plasma membrane of these cells. solutes into cells was provided by compounds con- taining energy-rich phosphate bonds (Hoagland, 1944). We now know that ATP-consuming proton COMMON CHARACTERISTICS OF CELLS pumps drive nutrient transport at several entry points SPECIALIZED TO ACCOMMODATE MASSIVE in the plant body. In this Update, we will focus on SOLUTE TRANSPORT those entry points within the plant body where nutri- ent transport is intense, and we will discuss their Cells with large fluxes of solutes across the plasma energization and regulation by proton pumps. membrane share a number of important characteristics in common. With regard to structure, cells specialized for transport are often characterized by (1) exposing a large surface area toward the uptake interface, e.g. TRANSPORT BARRIERS SEPARATE THE the plasma membrane exhibits many protrusions (e.g. SYMPLAST FROM THE APOPLAST epidermal cells) or invaginations (e.g. transfer cells); Any nutrient taken up by any cell must, at some and (2) having a great number of mitochondria, the stage, pass the plasma membrane (Fig. 1). The plasma role of which is to supply ATP for active transport. membrane is a lipid bilayer structure that surrounds Biophysically, transport competent cells are character- the cell and, in principle, is impermeable to solutes, istic by exhibiting (1) a large membrane potential such as ions and polar molecules. It is quite obvious difference between the internal and external face of why the membrane must be tight for nutrients. A root the membrane, typically ranging from 2150 mV to is always enriched in nutrients compared to the 2200 mV, negative on the inside; and (2) an acidic ex- surrounding soil and without a tight wrapping most terior, where apoplastic pH is typically between pH 4 of its contents would leak out of the plant and back and 5. Thus, across the plasma membrane of these into the growth medium. Thus, there is only one way cells, we observe a gradient of electric charge and that solutes can be transported from the outside chemical matter, which is termed the electrochemical medium, the apoplast, into a cell, and this is by gradient (Fisher, 2000). specific transport proteins that span the plasma mem- Although uphill transport of solutes into cells is an brane. As cells tend to accumulate nutrients, this energy-consuming process, it is rarely or never driven transport is most often uphill, i.e. against a concentra- directly by metabolic energy, i.e. ATP hydrolysis. tion gradient and/or an electrical gradient, and needs Rather, nutrient uptake systems are energized indi- to be energized. rectly. Thus, ATP is primarily consumed by pumps, 1 Once inside a plant cell, a given solute can diffuse which export H in order to generate an electrochem- from cell to cell via cellular bridges called plasmodes- ical proton gradient across the plasma membrane. This mata, forming a cellular continuum, the symplast. electrochemical gradient of protons in turn energizes Plasmodesmal transport by diffusion is not very nutrient uptake by channel proteins and carriers. effective, and for long-distance transport the nutrient Accordingly, transport-competent cells have at the in question might have to leave the symplast to enter molecular level (1) a large number of channel proteins a new from the apoplast in a neighboring cell or in and carriers (symporters, if nutrients get cotrans- 1 another part of the plant. Here again, uptake needs to ported with H in the same direction; antiporters, if 1 be energized and occurs through specialized transport nutrients and H are cotransported in opposite direc- tions; and uniporters, if nutrients are transported as 1 1 This work was supported by the European Union Framework 6 such without being accompanied by H ) and (2) large amounts of the plasma membrane H1-ATPase, a pro- program. 1 * Corresponding author; e-mail [email protected]; fax 45– ton pump. The proton pump exports H from the 3528–3365. cytoplasm into the apoplast at the expense of ATP. It is www.plantphysiol.org/cgi/doi/10.1104/pp.104.048231. this pump that is responsible for formation of the Plant Physiology, September 2004, Vol. 136, pp. 2475–2482, www.plantphysiol.org Ó 2004 American Society of Plant Biologists 2475 Sondergaard et al. Figure 1. Overview of main transport barriers in the plant body and the energization of cellular nutrient uptake by plasma membrane H1-ATPase. trans-plasma membrane electrochemical gradient tissue- and developmental-specific expression pat- (Palmgren, 2001; Arango et al., 2002). Transfer cells terns and have slightly different biochemical and are considered to be the most specialized cell type for regulatory properties (Palmgren, 2001; Arango et al., membrane transport, and, therefore, it is not surpris- 2002). Thus, it is likely that duplication of pump genes ing that H1-ATPase is abundant in the various transfer has provided a means for assuring appropriate activ- cell types of these cells (Bouche-Pillon et al., 1994; ities of pump protein in any given cell at any given Harrington et al., 1997; Schikora and Schmidt, 2002). time of development. ThePlasmaMembraneH1-ATPase The major ion pumps in plants and fungi are plasma CELLS SPECIALIZED FOR NUTRIENT TRANSPORT 1 membrane H -ATPases. Similar pumps are not Nutrient Uptake into the Root found in animals, in which the equivalent enzyme is the Na1/K1-ATPase, which in turn is absent from plants. Any nutrient in the soil that is to enter into the plant However, both types of pumps are evolutionarily re- will need to make contact with the root. The periphery lated and belong to the superfamily of P-type ATPases of the root is therefore a crucial transport barrier (Axelsen and Palmgren, 1998; Kuhlbrandt, 2004). (Kochian and Lucas, 1983). Nutrients are transferred P-type pumps are characterized by forming a phos- from the surface of the roots toward the long-distance phorylated reaction-cycle intermediate during cataly- transport system for water, the xylem, either by apo- sis. In this way, plasma membrane H1-ATPases differ plastic or symplastic pathways (Fig. 2). Either way, the from all other proton pumps in the plant cell, including nutrients have to pass at least one plasma membrane the vacuolar membrane H1-ATPase, another major in order to be transported into the xylem. When proton pump which energizes the vacuolar membrane. transferred via the symplastic pathway, nutrients have The vacuolar membrane H1-ATPase has more than 10 to pass the plasma membrane of epidermal cells. different subunits, whereas, in contrast, the functional When transferred via the apoplastic pathway, nu- unit of plasma membrane H1-ATPase is a monomer, trients have to cross the plasma membrane of cortex although it might be organized in the membrane as or endodermis cells in order to pass the Casparian a dimer or in oligomers. strip, which is an ion permeability barrier surrounding The yeast Saccharomyces cerevisiae is equipped with the endodermal layer. Membrane transport is thus two plasma membrane H1-ATPase genes, of which a decisive tool for the selective uptake of nutrients and one, PMA1, is essential for growth (Serrano et al., rejection of toxic ions from the environment. Measure- 1986). In plants, there are many more isoforms. The ments by x-ray microanalysis of the ionic composition genomes of the dicot Arabidopsis and the monocot of cells in the cortex, the endodermis, and the stele rice (Oryza sativa) have been sequenced, resulting have shown that the endodermis is indeed an effective in identification of 11 and 10 plasma membrane barrier, e.g. to Na1 (Pitman et al., 1981; Karahara et al., H1-ATPase isoforms, respectively (Baxter et al., 2004). The key function of the endodermis in selective 2003). The high number of isoforms in plants might uptake of nutrients is indicated by the presence of high indicate that some pumps have redundant functions. amounts of plasma membrane H1-ATPase as detected Isoform diversity may also be related to the multicel- by immunological methods (Parets-Soler et al., 1990). lular nature of plants. Individual isoforms exhibit At least one H1-ATPase isoform is specific for these 2476 Plant Physiol. Vol. 136, 2004 Update on Energization of Nutrient Transport Figure 2. Overview of cells and organs in the plant body where intense nutrient transport takes place. Plasma membrane H1-ATPase is always active at interfaces between the living symplast and the dead apoplast. Nutrient transporters can be either channel proteins or carrier proteins. Plant Physiol. Vol. 136, 2004 2477 Sondergaard et al. cells as shown by promoter-GUS (b-glucuronidase) by a transferred DNA results in strongly decreased K1 reporter expression of the plasma membrane translocation toward the shoots. The Arabidopsis H1-ATPase isoform AHA4 (Vitart et al., 2001). BOR1 gene encodes a boron transporter that, when fused to the fluorescent reporter green fluorescent pro- The Role of Root Hairs for Nutrient Uptake tein, can be detected in the pericycle and at the inner side of the endodermis (Takano et al., 2002). Mutant The epidermis constitutes the outermost layer of plants deficient in BOR1 have a strongly changed root- root cells, and the individual cells are equipped with to-shoot ratio of boron.
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