Energization of Plant Cell Membranes by H 1 -Pumping
ATPases: Regulation and Biosynthesis
Heven Sze, a,1 Xuhang Li, a and Michael G. Palmgren ba
Department of Cell Biology and Molecular Genetics, H.J. Patterson Hall, University of Maryland, College Park, Maryland 20742 b
Departmentof Plant Biology, Royal Veterinary and Agricultural University, Thorvaldsensvej 40, DK-1871 Frederiksberg C, Denmark
The circulation of ions across biological membranes is a fundamental process of cellular energetics (Harold, 1986).
Indeed, ion currents play the key role in energy capture during respiration and photosynthesis. They mediate the interconversion
of chemical, osmotic,and electrical forms of biological energy, and they support a range of physiological functions, including active transport and motility. Unlike animals, which use Na 1 ions, plants use protons almost exclusively as the coupling ion (Figure 1).
Regardless of the coupling ion used by an organism, the central theme of ion transport, which is based on Mitchell’s chemiosmotic theory, is conserved(Harold, 1986). A transport system generates an ion gradient whose electrochemical potential represents stored energy. Return of that ion across the membrane down its electrochemical gradient is mediated by a second transport system so as to link the “downhill” flux of the ion to the performance of some useful work, such as the “uphill” transport of another solute. The rate of work depends on therate of current flow, and its capacity depends on the potential gradient established by the primary transport system. Coupling ions usually carry a positive charge. Unlike uncharged , cations offer the advantage of contributing both an electrical and concentration gradient to the driving force. Furthermore, electrical imbalances can be rapidly transmitted over long distances along the surface ofmembranes
and are thus effective in both energy transduction and communicating information. Currents of protons in plants predominantly couple metabolism to work. In addition, H 1 as well as Ca 2 1 ions are used for transducing chemical and environmental signals. In addition to mitochondria (see Mackenzie and McIntosh, 1999, in this issue) and chloroplasts, there are three distinct pumps in plantsthat genergenerate proton electrochemical gradients (Figure 1). The plasma membrane H1-ATPase (PM H1-ATPase) extrudes H 1from the cell to generate a proton motive force with a membrane potential of 120 to 160 mV (negative inside) and a pH gradient of 1.5 to 2 units (acid outside). The vacuolar-typeH1 -ATPase (V-ATPase) and the vacuolar H1 -pumping pyrophosphatase (H1-PPase) acidify the vacuolarlumen and other endomembrane compartments. This review highlights the similarities and differences between the structures and modes of regulation of the two H1 -pumping ATPases and points out future challenges in the functional analysis of these proteins. The H1 -PPase is briefly discussed for comparative purposes.
SIMILAR YET DISTINCT ROLES FOR THE PM H1 -ATPase AND V-ATPase
PM H1 -ATPase
A keyfunction of the PM H 1-ATPase is to generate a proton electrochemical gradient, thereby providing the driving force for the uptake and efflux of ions and metabolites across the plasma membrane. Essential nutrients, such as nitrate and sulfate, are taken into cells against concentration and electrical gradients by H 1 -coupled anion symporters (Figure 1; Tanner and Caspari, 1996). The translocationof organic compounds from source tissues to sink tissues similarly involves energy-dependent steps, and various H 1 –coupled symporters for amino acids and sucrose have been identified and characterized (see Lalonde et al., 1999, in this issue).
The electrical gradient across the plasma membrane also determines the direction and extent of passive ion flow through ion-specific channels. In...