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

Abstract

In plants, the existence of a mitochondrial potassium channel was firstly demonstrated about 15 years ago in durum wheat as an ATP-dependent potassium channel (PmitoKATP). Since then, both properties of the original PmitoKATP and occurrence of different mitochondrial potassium channels in a number of plant species (monocotyledonous and dicotyledonous) and tissues/organs (etiolated and green) have been shown. Here, an overview of the current knowledge is reported; in particular, the issue of PmitoKATP physiological modulation is addressed. Similarities and differences with other potassium channels, as well as possible cross-regulation with other mitochondrial proteins (Plant Uncoupling Protein, Alternative Oxidase, Plant Inner Membrane Anion Channel) are also described. PmitoKATP is inhibited by ATP and activated by superoxide anion, as well as by free fatty acids (FFAs) and acyl-CoAs. Interestingly, channel activation increases electrophoretic potassium uptake across the inner membrane toward the matrix, so collapsing membrane potential (ΔΨ), the main component of the protonmotive force (Δp) in plant mitochondria; moreover, cooperation between PmitoKATP and the K+/H+ antiporter allows a potassium cycle able to dissipate also ΔpH. Interestingly, ΔΨ collapse matches with an active control of mitochondrial reactive oxygen species (ROS) production. Fully open channel is able to lower superoxide anion up to 35-fold compared to a condition of ATP-inhibited channel. On the other hand, ΔΨ collapse by PmitoKATP was unexpectedly found to not affect ATP synthesis via oxidative phosphorylation. This may probably occur by means of a controlled collapse due to ATP inhibition of PmitoKATP; this brake to the channel activity may allow a loss of the bulk phase Δp, but may preserve a non-classically detectable localized driving force for ATP synthesis. This ability may become crucial under environmental/oxidative stress. In particular, under moderate hyperosmotic stress (mannitol or NaCl), PmitoKATP was found to be activated by ROS, so inhibiting further large-scale ROS production according to a feedback mechanism; moreover, a stress-activated phospholipase A2 may generate FFAs, further activating the channel. In conclusion, a main property of PmitoKATP is the ability to keep in balance the control of harmful ROS with the mitochondrial/cellular bioenergetics, thus preserving ATP for energetic needs of cell defense under stress.

MSL1 is a mechanosensitive ion channel that dissipates mitochondrial membrane potential and maintains redox homeostasis in mitochondria during abiotic stress

“…In chloroplasts, osmotic pressure and ion homeostasis are controlled not only by MSL2 and MSL3 (Veley et al, 2012), but also by a family of K + /H + antiporters (KEA) that work cooperatively with other cation channels (Kunz et al, 2014). A similar K + /H + antiporter (KHE) also exists in plant mitochondria, although its molecular identity remains unknown to date (Hensley and Hanson, 1975;Diolez and Moreau, 1985;Trono et al, 2015). Nevertheless, it is also notable that treatment of WT and msl1-1 roots with hyper-osmotic concentrations of mannitol did not cause a significant increase in oxidation of the mitochondrial glutathione pool (Figure 7c), suggesting that MSL1 is not a major part of the mechanism that maintains mitochondrial redox poise under this stress condition.…”

Properties of the Permeability Transition of Pea Stem Mitochondria

“…A common feature of the PT of pea stem mitochondria and the Ca 2+ -induced Ca 2+ -release channel of Drosophila is the lack of swelling, which is consistent with the absence of Cyt c release from mitochondria and suggests a low conductance of the PTP in these species. This mechanism for Ca 2+ release might act in synergy with K + channels, which are involved in the modulation of mitochondrial permeability during responses to environmental/oxidative stress and in the control of ROS production in plants (Vianello et al, 2012; Trono et al, 2015).…”

What is the role of putrescine accumulated under potassium deficiency?

“…Polyamines can have an impact on mitochondrial transmembrane potential (Δ Ψ ), perhaps mediated by their effect on mitochondrial ATP‐sensitive K + channels ( mito K ATP ). Both the molecular identity of mito K ATP and their structural similarity with plasma membrane K ATP channels (which are abundant in animal tissues but absent in plants) are still a matter of debate (Szabo & Zoratti, ; Trono, Laus, Soccio, Alfarano, & Pastore, ). Under the assumption that mito K ATP are structurally similar to K + inward rectifiers (as animal plasma membrane K ATP channels are), the K + current through the channel pore would be modulated in a voltage‐dependent manner by cytosolic polyamines.…”