Role of the Plasma Membrane H+-ATPase in K+ Transport

Briskin, Donald P.; Gawienowski, Margaret

doi:10.1104/pp.111.4.1199

Cited by 29 publications

(14 citation statements)

References 39 publications

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“…Similar mechanisms of cytosolic ATP in control of K 1 efflux have been reported in other plant cells, in which the outwardrectified K 1 channels were activated or completely abolished within 15 min in the presence or absence of cytosolic ATP (Spalding and Goldsmith, 1993;Briskin and Gawienowski, 1996;Goh et al, 2004). This response period is similar to that observed for changes in nodule permeability to oxygen diffusion, providing further support for the suggestion that cytosolic ATP-coupled K 1 movement is involved in the control of oxygen diffusion in legume nodules.…”

Section: The 10% O 2 Treatmentsupporting

confidence: 68%

Adenylate-Coupled Ion Movement. A Mechanism for the Control of Nodule Permeability to O2 Diffusion

Wei

Layzell

2006

Plant Physiology

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In response to changes in phloem supply, adenylate demand, and oxygen status, legume nodules are known to exercise rapid (seconds to hours) physiological control over their permeability to oxygen diffusion. Diffusion models have attributed this permeability control to the reversible flow of water into or out of intercellular spaces. To test hypotheses on the mechanism of diffusion barrier control, nodulated soybean (Glycine max L. Merr.) plants were exposed to a range of treatments known to alter nodule O 2 permeability (i.e. 10% O 2 , 30% O 2 , Ar:O 2 exposure, and stem girdling) before the nodules were rapidly frozen, freeze dried, and dissected into cortex and central zone (CZ) fractions that were assayed for K, Mg, and Ca ion concentrations. Treatments known to decrease nodule permeability (30% O 2 , Ar:O 2 exposure, and stem girdling) were consistently associated with an increase in the ratio of [K 1 ] in cortex to [K 1 ] in the CZ tissue, whereas the 10% O 2 treatment, known to increase nodule permeability, was associated with a decrease in the [When these findings were considered in the light of previous results, a proposed mechanism was developed for the adenylate-coupled movement of ions and water into and out of infected cells as a possible mechanism for diffusion barrier control in legume nodules.

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Section: The 10% O 2 Treatmentsupporting

confidence: 68%

Adenylate-Coupled Ion Movement. A Mechanism for the Control of Nodule Permeability to O2 Diffusion

Wei

Layzell

2006

Plant Physiology

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“…Taken together, the data suggest that lightdriven photosynthesis is not directly involved in the activation of K out channel current in the plasma membrane, although the possibility of direct K ϩ transport by other ATPases (i.e. K ϩ -ATPases) cannot be ruled out (17). Mitochondrial respiration therefore provides the source of cytosolic ATP.…”

Section: Discussionmentioning

confidence: 76%

Mitochondria Provide the Main Source of Cytosolic ATP for Activation of Outward-rectifying K+ Channels in Mesophyll Protoplast of Chlorophyll-deficient Mutant Rice (OsCHLH) Seedlings

Goh

Jung

Roberts

et al. 2004

Journal of Biological Chemistry

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The role of mitochondria in providing intracellular ATP that controls the activity of plasma membrane outward-rectifying K ؉ channels was evaluated. The Os-CHLH rice mutant, which lacks chlorophyll in the thy- The OsCHLH mutant is unable to fix CO 2 and exhibits reduced growth. Wild type and mutant plants exhibit similar rates of respiratory O 2 uptake in the dark, whereas the rate of photosynthetic O 2 evolution by the mutant was negligible during illumination. During dark respiration the wild type and mutant exhibited similar levels of cytoplasmic ATP. In the mutant oligomycin treatment (an inhibitor of mitochondrial F 1 F 0 -ATPase) drastically reduced ATP production. The fact that this was reversed by the addition of glucose suggested that the mutant produced ATP exclusively from mitochondria but not from chloroplasts. In whole cell patch clamp experiments, the activity of outward-rectifying K ؉ channels of rice mesophyll cells showed ATPdependent currents, which were 1.5-fold greater in wild type than in mutant cells. Channels in both wild type and mutant cells were deactivated by the removal of cytosolic ATP, whereas in the presence of ATP the channels remained active. We conclude that mesophyll cells in the OsCHLH rice mutant derive ATP from mitochondrial respiration, and that this is critical for the normal function of plasma membrane outward-rectifying K ؉ channels.Mitochondrial metabolism not only impacts on other cellular biosynthetic and catabolic processes, but also plays an important role in providing the overall cellular energy supply. Dark respiration and photosynthesis are metabolic pathways that produce redox equivalents and ATP to meet the energy requirements to support cell growth and maintenance (2). The central role of mitochondria in plants is reflected by the array of mitochondrial transporters and shuttles that transfer metabolites and reducing equivalents back and forth between mitochondria and the cytosol. Oxidative phosphorylation provides the cytosol with ATP, which is required for sucrose synthesis and other cytosolic processes. Studies with specific respiratory inhibitors have shown that oxidative phosphorylation occurs both in darkness and in light (2-4). However, very little is known about the regulation of mitochondrial respiration in photosynthetic mesophyll cells, and the role of mitochondrial ATP production as a source of cytosolic ATP in this process is not fully understood.Many biochemical reactions in plant and mammalian cells depend on a tightly controlled ratio of ATP to ADP. In mammalian mitochondria, this ratio is preserved by regulatory mechanisms that couple the rate of cellular ATP consumption to the rate of ATP production by oxidative phosphorylation (5-8). Hence, efficient communication between cellular energy stores and membrane metabolic sensors is necessary for regulation of membrane excitability and associated functions. In most mammalian cells, there is a class of K ϩ channels whose activity is closely coupled to metabolism by ATP (9, 10). Recent studies have...

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“…The high-affinity transport system (HATS) is a saturable system catalyzing the thermodynamically active uptake of K + at low concentrations (o1 mM). The active influx of K + is thought to be coupled to the passive influx of H + down its electrochemical gradient, which is maintained by proton-pumping ATPase complexes in the plasma membrane (Cheeseman et al, 1980;Rodríguez-Navarro et al, 1986;Kochian et al, 1989; Maathuis and Sanders, 1994;Briskin and Gawienowski, 1996). Despite some disagreement concerning the precise stoichiometry of H + /K + symport, it is generally accepted to be 1:1 ( Maathuis and Sanders, 1994;Maathuis et al 1997), as has also been demonstrated in bacterial ( Bakker and Harold, 1980) and fungal systems (Rodríguez-Navarro et al, 1986).…”

Section: High-affinity K + Transportmentioning

confidence: 99%