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

Trono D, Laus MN, Soccio M, Alfarano M, Pastore D - Front Plant Sci (2015)

Bottom Line: PmitoKATP is inhibited by ATP and activated by superoxide anion, as well as by free fatty acids (FFAs) and acyl-CoAs.Fully open channel is able to lower superoxide anion up to 35-fold compared to a condition of ATP-inhibited channel.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.

View Article: PubMed Central - PubMed

Affiliation: Consiglio per la Ricerca in Agricoltura e l'Analisi dell'Economia Agraria, Centro di Ricerca per la Cerealicoltura , Foggia, Italy.

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.

No MeSH data available.


Related in: MedlinePlus

Effect of PmitoKATP activity on the electrical membrane potential (ΔΨ) and ATP synthesis. (A) In the absence of KCl, PmitoKATP is inactive and the proton re-entry into the matrix via the ATP synthase (ATPase) drives the ATP synthesis according to the classical chemiosmotic scheme. (B) In the presence of KCl, PmitoKATP is active and the concurrent K+ cycle (see Figure 1) competes with ATPase for protons. Since PmitoKATP represents the rate-limiting step of the cycle, its inhibition by ATP may carefully regulate the rate of the cycle, so that the bulk phase measurable ΔΨ is strongly lowered, but a latent ΔΨ remains feeding the ATPase pathway to regularly accomplish ATP synthesis. (C) On the contrary, in the presence of the K+ ionophore valinomycin (val), PmitoKATP and its modulation by ATP are bypassed, so the K+ cycle monopolizes protons and uncouples mitochondria collapsing both ΔΨ and ATP synthesis. The reducing equivalent flux through the respiratory chain to molecular oxygen, the coupled proton ejection into the intermembrane space, the ADP/ATP antiport via Adenine Nucleotide Translocator (ANT) and the ATP synthesis via ATPase are indicated; + and – signs refer to ΔΨ. The continuous or dotted arrows refer to a more or less active pathway, respectively. SH2, reduced substrates; S, oxidized substrates; i.m.m., inner mitochondrial membrane.
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Figure 3: Effect of PmitoKATP activity on the electrical membrane potential (ΔΨ) and ATP synthesis. (A) In the absence of KCl, PmitoKATP is inactive and the proton re-entry into the matrix via the ATP synthase (ATPase) drives the ATP synthesis according to the classical chemiosmotic scheme. (B) In the presence of KCl, PmitoKATP is active and the concurrent K+ cycle (see Figure 1) competes with ATPase for protons. Since PmitoKATP represents the rate-limiting step of the cycle, its inhibition by ATP may carefully regulate the rate of the cycle, so that the bulk phase measurable ΔΨ is strongly lowered, but a latent ΔΨ remains feeding the ATPase pathway to regularly accomplish ATP synthesis. (C) On the contrary, in the presence of the K+ ionophore valinomycin (val), PmitoKATP and its modulation by ATP are bypassed, so the K+ cycle monopolizes protons and uncouples mitochondria collapsing both ΔΨ and ATP synthesis. The reducing equivalent flux through the respiratory chain to molecular oxygen, the coupled proton ejection into the intermembrane space, the ADP/ATP antiport via Adenine Nucleotide Translocator (ANT) and the ATP synthesis via ATPase are indicated; + and – signs refer to ΔΨ. The continuous or dotted arrows refer to a more or less active pathway, respectively. SH2, reduced substrates; S, oxidized substrates; i.m.m., inner mitochondrial membrane.

Mentions: In this context, the behavior of PmitoKATP-depolarized DWM represents the first evidence of isolated plant mitochondria that lack measurable ΔΨ and ΔpH, but, at the same time, are fully coupled and regularly accomplish ATP synthesis via OXPHOS. A possible explanation of this finding may reside in the PmitoKATP inhibition by ATP; a mechanistic model of this coupling in the absence of measurable bulk phase ΔΨ and ΔpH is represented in Figure 3. In DWM suspended in a KCl-free medium the PmitoKATP is inactive and mitochondria accomplish ATP synthesis according to classical chemiosmosis (Figure 3A). On the other hand, in the presence of KCl and ATP, a PmitoKATP 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 PmitoKATP 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 PmitoKATP activity is overcome, so exacerbating K+ cycle; under this condition, complete uncoupling occurs, preventing ATP synthesis (Figure 3C). In practice, while the classical uncouplers are unable to distinguish among different proton pools, somehow the PmitoKATP/ATP system appears to be able to distinguish the bulk phase Δp from a non-classically detectable driving force for ATP synthesis.


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

Trono D, Laus MN, Soccio M, Alfarano M, Pastore D - Front Plant Sci (2015)

Effect of PmitoKATP activity on the electrical membrane potential (ΔΨ) and ATP synthesis. (A) In the absence of KCl, PmitoKATP is inactive and the proton re-entry into the matrix via the ATP synthase (ATPase) drives the ATP synthesis according to the classical chemiosmotic scheme. (B) In the presence of KCl, PmitoKATP is active and the concurrent K+ cycle (see Figure 1) competes with ATPase for protons. Since PmitoKATP represents the rate-limiting step of the cycle, its inhibition by ATP may carefully regulate the rate of the cycle, so that the bulk phase measurable ΔΨ is strongly lowered, but a latent ΔΨ remains feeding the ATPase pathway to regularly accomplish ATP synthesis. (C) On the contrary, in the presence of the K+ ionophore valinomycin (val), PmitoKATP and its modulation by ATP are bypassed, so the K+ cycle monopolizes protons and uncouples mitochondria collapsing both ΔΨ and ATP synthesis. The reducing equivalent flux through the respiratory chain to molecular oxygen, the coupled proton ejection into the intermembrane space, the ADP/ATP antiport via Adenine Nucleotide Translocator (ANT) and the ATP synthesis via ATPase are indicated; + and – signs refer to ΔΨ. The continuous or dotted arrows refer to a more or less active pathway, respectively. SH2, reduced substrates; S, oxidized substrates; i.m.m., inner mitochondrial membrane.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4664611&req=5

Figure 3: Effect of PmitoKATP activity on the electrical membrane potential (ΔΨ) and ATP synthesis. (A) In the absence of KCl, PmitoKATP is inactive and the proton re-entry into the matrix via the ATP synthase (ATPase) drives the ATP synthesis according to the classical chemiosmotic scheme. (B) In the presence of KCl, PmitoKATP is active and the concurrent K+ cycle (see Figure 1) competes with ATPase for protons. Since PmitoKATP represents the rate-limiting step of the cycle, its inhibition by ATP may carefully regulate the rate of the cycle, so that the bulk phase measurable ΔΨ is strongly lowered, but a latent ΔΨ remains feeding the ATPase pathway to regularly accomplish ATP synthesis. (C) On the contrary, in the presence of the K+ ionophore valinomycin (val), PmitoKATP and its modulation by ATP are bypassed, so the K+ cycle monopolizes protons and uncouples mitochondria collapsing both ΔΨ and ATP synthesis. The reducing equivalent flux through the respiratory chain to molecular oxygen, the coupled proton ejection into the intermembrane space, the ADP/ATP antiport via Adenine Nucleotide Translocator (ANT) and the ATP synthesis via ATPase are indicated; + and – signs refer to ΔΨ. The continuous or dotted arrows refer to a more or less active pathway, respectively. SH2, reduced substrates; S, oxidized substrates; i.m.m., inner mitochondrial membrane.
Mentions: In this context, the behavior of PmitoKATP-depolarized DWM represents the first evidence of isolated plant mitochondria that lack measurable ΔΨ and ΔpH, but, at the same time, are fully coupled and regularly accomplish ATP synthesis via OXPHOS. A possible explanation of this finding may reside in the PmitoKATP inhibition by ATP; a mechanistic model of this coupling in the absence of measurable bulk phase ΔΨ and ΔpH is represented in Figure 3. In DWM suspended in a KCl-free medium the PmitoKATP is inactive and mitochondria accomplish ATP synthesis according to classical chemiosmosis (Figure 3A). On the other hand, in the presence of KCl and ATP, a PmitoKATP 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 PmitoKATP 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 PmitoKATP activity is overcome, so exacerbating K+ cycle; under this condition, complete uncoupling occurs, preventing ATP synthesis (Figure 3C). In practice, while the classical uncouplers are unable to distinguish among different proton pools, somehow the PmitoKATP/ATP system appears to be able to distinguish the bulk phase Δp from a non-classically detectable driving force for ATP synthesis.

Bottom Line: PmitoKATP is inhibited by ATP and activated by superoxide anion, as well as by free fatty acids (FFAs) and acyl-CoAs.Fully open channel is able to lower superoxide anion up to 35-fold compared to a condition of ATP-inhibited channel.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.

View Article: PubMed Central - PubMed

Affiliation: Consiglio per la Ricerca in Agricoltura e l'Analisi dell'Economia Agraria, Centro di Ricerca per la Cerealicoltura , Foggia, Italy.

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.

No MeSH data available.


Related in: MedlinePlus