The uniqueness of the plant mitochondrial potassium channel

Abstract

The ATP-inhibited Plant Mitochondrial K+ Channel (PmitoKATP) was discovered about fifteen years ago in Durum Wheat Mitochondria (DWM). PmitoKATP catalyses the electrophoretic K+ uniport through the inner mitochondrial membrane; moreover, the co-operation between PmitoKATP and +/H+ antiporter allows such a great operation of a K+ cycle to collapse mitochondrial membrane potential (ΔΨ) and ΔpH, thus impairing protonmotive force (Δp). A possible physiological role of such ΔΨ control is the restriction of harmful reactive oxygen species (ROS) production under environmental/oxidative stress conditions. Interestingly, DWM lacking Δp were found to be nevertheless fully coupled and able to regularly accomplish ATP synthesis; this unexpected behaviour makes necessary to recast in some way the classical chemiosmotic model. In the whole, PmitoKATP may oppose to large scale ROS production by lowering ΔΨ under environmental/oxidative stress, but, when stress is moderate, this occurs without impairing ATP synthesis in a crucial moment for cell and mitochondrial bioenergetics. [BMB Reports 2013; 46(8): 391-397]

The Enigmatic Metabolite Transport in Plant Mitochondria Lacking Proton Motive Force - news from Durum Wheat Mitochondria

“…As a consequence, passive anion transport across the inner mitochondrial membrane may shift from the energy-dependent anion carriers toward the electrophoretic flux through the PIMAC. Results from in vitro studies on DWM are in line with this picture [10,11,19], with the notable exception of AAC function. Both ADP and ATP are not transported by PIMAC, moreover, in de-energized DWMthe ADP/ATP exchange is inhibited by oligomycin, a powerful AAC inhibitor, thus suggesting AAC operation in the absence of measurableΔΨ, the driving force for AAC.…”

“…This occurs in a KCl medium able to activate the ATP-sensitive mitochondrial potassium channel (PmitoKATP); under this particular condition, the massive K+ uptake by DWM may strongly decreaseΔΨ without compensation due to ΔpH increase, thus collapsing pmf [9,10]. A possible mechanism explaining this unexpected ATP synthesis has been recently reported [11], but another point remains still unsolved regarding the transport of metabolites: to synthesize ATP via OXPHOS it is necessary to carry out uptake of succinate, Inorganic Phosphate (Pi) and ADP as well as to release the newly synthesized ATPoutside DWM. Since the force driving these transports should derive from ΔΨ and ΔpH, the question arises about how these movements of metabolites may be possiblein the absence of pmf in this in vitro model system.…”

“…In practice, a ROS-induced activation of PmitoK ATP and PUCP occurs under stress, able to dissipate ΔΨ and ΔpH up to a complete collapse; this strong pmf decrease induces in turn an inhibition of ROS production, according to a feed-back mechanism [13,15]. According to another pathway of regulation,under abiotic stress an increase of mitochondrial FFA content occurs in DWM, due to the activation of a mitochondrial Phospholipase A2 (PLA2) [16]; FFA increase activates both dissipative systems, moreover, the acylCoAs deriving from FFAs stimulate K+ transport via PmitoK ATP [17]; once again, activation of PmitoK ATP and PUCP may lowerROS production [11]. So, DWM may dissipate pmf in order to avoid ROS over production and cellular oxidative stress.…”

Transport, signaling, and homeostasis of potassium and sodium in plants

“…A mitochondria‐localized K + channel (mitoK ATP channel) has also been isolated as a K + uniporter (Pastore et al , , ). It has been indicated that K + concentrations in the mitochondrial matrix are regulated by the mitoK ATP channel and subsequent K + entry into the mitochondria results in depolarization of the membrane (Jarmuszkiewicz et al ).…”

Modulation of Potassium Channel Activity in the Balance of ROS and ATP Production by Durum Wheat Mitochondria—An Amazing Defense Tool Against Hyperosmotic Stress

“…On the other hand, in the presence of KCl and ATP, a PmitoK ATP activity exists, but it is inhibited, thus reducing the whole rate of the K + cycle; so, a “controlled collapse” is achieved that avoids complete uncoupling. In particular, this ATP-braked activity of PmitoK ATP may strongly reduce the classically detectable bulk phase Δp, but in such a manner to only partially subtract protons to ATP synthase and to retain a latent proton movement, able to sustain ATP synthesis and transport ( Pastore et al, 2013 ; Trono et al, 2014 ; Figure 3B ). Consistently, in the presence of valinomycin, the ATP brake of PmitoK ATP activity is overcome, so exacerbating K + cycle; under this condition, complete uncoupling occurs, preventing ATP synthesis (Figure 3C ).…”