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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

Regulation of ROS production and ATP synthesis by PmitoKATP under control and hyperosmotic stress conditions. (A) Under control conditions, a basal production of activators occurs, whereas ATP is produced at high level; as a consequence, in the balance of modulators, ATP inhibition of the PmitoKATP activity prevails, thus allowing only a basal channel activity. (B) Under moderate stress conditions, an increase in the mitochondrial generation of ROS occurs that activates PmitoKATP, which, in turn, according to a feedback mechanism, may dampen excess ROS production. Moreover, an activation of the mitochondrial PLA2 also occurs, that may increase the in vivo production of FFAs/acyl-CoAs, which further enhance channel activation. On the other hand, channel inhibition by ATP may represent a brake able to finely regulate the K+ cycle, so that ΔΨ is strongly decreased to control ROS, but the ATP synthesis is not impaired. In this manner, PmitoKATP meets the cell needs, i.e., to dampen harmful ROS production to curtail oxidative stress and, at the same time, to preserve energy to counteract stress. (C) Severe stress conditions determine a further increase in the ROS generation, as well as in the PLA2 activity, which, in turn, may increase the in vivo production of FFAs/acyl-CoAs. Under these conditions, the balance between channel modulators favors stronger channel activation by activators over inhibition by ATP. This further increased PmitoKATP activity determines a ΔΨ collapse able to counteract large-scale ROS production, but, in this case, it leads to a strong decrease in the ATP synthesis, although not complete impairment is observed. For details, see the text. The continuous or dotted arrows refer to a more or less active pathway, respectively.
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Figure 4: Regulation of ROS production and ATP synthesis by PmitoKATP under control and hyperosmotic stress conditions. (A) Under control conditions, a basal production of activators occurs, whereas ATP is produced at high level; as a consequence, in the balance of modulators, ATP inhibition of the PmitoKATP activity prevails, thus allowing only a basal channel activity. (B) Under moderate stress conditions, an increase in the mitochondrial generation of ROS occurs that activates PmitoKATP, which, in turn, according to a feedback mechanism, may dampen excess ROS production. Moreover, an activation of the mitochondrial PLA2 also occurs, that may increase the in vivo production of FFAs/acyl-CoAs, which further enhance channel activation. On the other hand, channel inhibition by ATP may represent a brake able to finely regulate the K+ cycle, so that ΔΨ is strongly decreased to control ROS, but the ATP synthesis is not impaired. In this manner, PmitoKATP meets the cell needs, i.e., to dampen harmful ROS production to curtail oxidative stress and, at the same time, to preserve energy to counteract stress. (C) Severe stress conditions determine a further increase in the ROS generation, as well as in the PLA2 activity, which, in turn, may increase the in vivo production of FFAs/acyl-CoAs. Under these conditions, the balance between channel modulators favors stronger channel activation by activators over inhibition by ATP. This further increased PmitoKATP activity determines a ΔΨ collapse able to counteract large-scale ROS production, but, in this case, it leads to a strong decrease in the ATP synthesis, although not complete impairment is observed. For details, see the text. The continuous or dotted arrows refer to a more or less active pathway, respectively.

Mentions: A possible physiological role of the PmitoKATP under environmental/oxidative stresses derives from its property to act as energy-dissipating system able to control ΔΨ, ATP synthesis and, above all, ROS production. It is well known that cellular ROS production can be increased as a result of plant exposure to various environmental stresses (Scandalios, 1993; Foyer et al., 1994; Møller, 2001); mitochondria, in particular, are known to increase ROS generation under drought and salt stress (Alscher et al., 1997). Consistently, in DWM purified from hyperosmotically (mannitol or NaCl) stressed seedlings, an increase in the rate of superoxide anion production of about 40% and 120% with respect to the control was found under moderate and severe stress conditions, respectively (Trono et al., 2004). In particular, stress was considered moderate when a starting oxidative stress was observed, without a concomitant damage on substrate oxidation, ATP synthesis and mitochondria intactness. On the other hand, it was considered as severe a stress that induced a drop of substrate oxidation (Trono et al., 2004; Soccio et al., 2010), ATP synthesis (Flagella et al., 2006) and, consequently, a remarkable ATP content decrease (Trono et al., 2011; Soccio et al., 2013), as well as some loss of outer membrane integrity (Trono et al., 2004; Soccio et al., 2010). All these findings were obtained on mitochondria isolated from stressed seedlings in which PmitoKATP was maintained essentially inactive by carrying out measurements in KCl-free or low-KCl media. On the other hand, when the channel was activated under stress, it was found to deeply affect ROS and ATP production (Figure 4).


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)

Regulation of ROS production and ATP synthesis by PmitoKATP under control and hyperosmotic stress conditions. (A) Under control conditions, a basal production of activators occurs, whereas ATP is produced at high level; as a consequence, in the balance of modulators, ATP inhibition of the PmitoKATP activity prevails, thus allowing only a basal channel activity. (B) Under moderate stress conditions, an increase in the mitochondrial generation of ROS occurs that activates PmitoKATP, which, in turn, according to a feedback mechanism, may dampen excess ROS production. Moreover, an activation of the mitochondrial PLA2 also occurs, that may increase the in vivo production of FFAs/acyl-CoAs, which further enhance channel activation. On the other hand, channel inhibition by ATP may represent a brake able to finely regulate the K+ cycle, so that ΔΨ is strongly decreased to control ROS, but the ATP synthesis is not impaired. In this manner, PmitoKATP meets the cell needs, i.e., to dampen harmful ROS production to curtail oxidative stress and, at the same time, to preserve energy to counteract stress. (C) Severe stress conditions determine a further increase in the ROS generation, as well as in the PLA2 activity, which, in turn, may increase the in vivo production of FFAs/acyl-CoAs. Under these conditions, the balance between channel modulators favors stronger channel activation by activators over inhibition by ATP. This further increased PmitoKATP activity determines a ΔΨ collapse able to counteract large-scale ROS production, but, in this case, it leads to a strong decrease in the ATP synthesis, although not complete impairment is observed. For details, see the text. The continuous or dotted arrows refer to a more or less active pathway, respectively.
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Related In: Results  -  Collection

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Figure 4: Regulation of ROS production and ATP synthesis by PmitoKATP under control and hyperosmotic stress conditions. (A) Under control conditions, a basal production of activators occurs, whereas ATP is produced at high level; as a consequence, in the balance of modulators, ATP inhibition of the PmitoKATP activity prevails, thus allowing only a basal channel activity. (B) Under moderate stress conditions, an increase in the mitochondrial generation of ROS occurs that activates PmitoKATP, which, in turn, according to a feedback mechanism, may dampen excess ROS production. Moreover, an activation of the mitochondrial PLA2 also occurs, that may increase the in vivo production of FFAs/acyl-CoAs, which further enhance channel activation. On the other hand, channel inhibition by ATP may represent a brake able to finely regulate the K+ cycle, so that ΔΨ is strongly decreased to control ROS, but the ATP synthesis is not impaired. In this manner, PmitoKATP meets the cell needs, i.e., to dampen harmful ROS production to curtail oxidative stress and, at the same time, to preserve energy to counteract stress. (C) Severe stress conditions determine a further increase in the ROS generation, as well as in the PLA2 activity, which, in turn, may increase the in vivo production of FFAs/acyl-CoAs. Under these conditions, the balance between channel modulators favors stronger channel activation by activators over inhibition by ATP. This further increased PmitoKATP activity determines a ΔΨ collapse able to counteract large-scale ROS production, but, in this case, it leads to a strong decrease in the ATP synthesis, although not complete impairment is observed. For details, see the text. The continuous or dotted arrows refer to a more or less active pathway, respectively.
Mentions: A possible physiological role of the PmitoKATP under environmental/oxidative stresses derives from its property to act as energy-dissipating system able to control ΔΨ, ATP synthesis and, above all, ROS production. It is well known that cellular ROS production can be increased as a result of plant exposure to various environmental stresses (Scandalios, 1993; Foyer et al., 1994; Møller, 2001); mitochondria, in particular, are known to increase ROS generation under drought and salt stress (Alscher et al., 1997). Consistently, in DWM purified from hyperosmotically (mannitol or NaCl) stressed seedlings, an increase in the rate of superoxide anion production of about 40% and 120% with respect to the control was found under moderate and severe stress conditions, respectively (Trono et al., 2004). In particular, stress was considered moderate when a starting oxidative stress was observed, without a concomitant damage on substrate oxidation, ATP synthesis and mitochondria intactness. On the other hand, it was considered as severe a stress that induced a drop of substrate oxidation (Trono et al., 2004; Soccio et al., 2010), ATP synthesis (Flagella et al., 2006) and, consequently, a remarkable ATP content decrease (Trono et al., 2011; Soccio et al., 2013), as well as some loss of outer membrane integrity (Trono et al., 2004; Soccio et al., 2010). All these findings were obtained on mitochondria isolated from stressed seedlings in which PmitoKATP was maintained essentially inactive by carrying out measurements in KCl-free or low-KCl media. On the other hand, when the channel was activated under stress, it was found to deeply affect ROS and ATP production (Figure 4).

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