RESEARCH PAPER |
Possible plant mitochondria involvement in cell adaptation to drought stress
A case study: durum wheat mitochondria
1Dipartimento di Scienze Agroambientali, Chimica e Difesa Vegetale, Facoltà di Agraria, Università di Foggia, Via Napoli, 25 – 71100 Foggia, Italy
2Centro di Ricerca Interdipartimentale BIOAGROMED, Università di Foggia, Via Napoli, 6/B – 71100 Foggia, Italy
3Istituto Sperimentale per la Cerealicoltura – C.R.A., S.S. 16, Km 675 – 71100 Foggia, Italy
* To whom correspondence should be addressed. E-mail: d.pastore{at}unifg.it
Received 23 December 2005; Accepted 14 November 2006
 |
Abstract |
|---|
 Top Abstract IntroductionDissipating systems in DWM...Effects of oxidative and...ConclusionsReferences |
|---|
Although plant cell bioenergetics is strongly affected by abiotic stresses, mitochondrial metabolism under stress is still largely unknown. Interestingly, plant mitochondria may control reactive oxygen species (ROS) generation by means of energy-dissipating systems. Therefore, mitochondria may play a central role in cell adaptation to abiotic stresses, which are known to induce oxidative stress at cellular level. With this in mind, in recent years, studies have been focused on mitochondria from durum wheat, a species well adapted to drought stress. Durum wheat mitochondria possess three energy-dissipating systems: the ATP-sensitive plant mitochondrial potassium channel (PmitoKATP); the plant uncoupling protein (PUCP); and the alternative oxidase (AOX). It has been shown that these systems are able to dampen mitochondrial ROS production; surprisingly, PmitoKATP and PUCP (but not AOX) are activated by ROS. This was found to occur in mitochondria from both control and hyperosmotic-stressed seedlings. Therefore, the hypothesis of a ‘feed-back’ mechanism operating under hyperosmotic/oxidative stress conditions was validated: stress conditions induce an increase in mitochondrial ROS production; ROS activate PmitoKATP and PUCP that, in turn, dissipate the mitochondrial membrane potential, thus inhibiting further large-scale ROS production. Another important aspect is the chloroplast/cytosol/mitochondrion co-operation in green tissues under stress conditions aimed at modulating cell redox homeostasis. Durum wheat mitochondria may act against chloroplast/cytosol over-reduction: the malate/oxaloacetate antiporter and the rotenone-insensitive external NAD(P)H dehydrogenases allow cytosolic NAD(P)H oxidation; under stress this may occur without high ROS production due to co-operation with AOX, which is activated by intermediates of the photorespiratory cycle.
Key words: Alternative oxidase, drought stress, durum wheat, oxidative stress, plant mitochondria, potassium channel, salt stress, uncoupling protein
|
Introduction |
|---|
|
TopAbstractIntroductionDissipating systems in DWM...Effects of oxidative and...ConclusionsReferences |
|---|
It is known that plant mitochondria are involved in some metabolic processes implicated in cell adaptation to abiotic stresses. Mitochondria interact with chloroplasts and peroxisomes in the photorespiratory cycle; this allows excess reducing equivalents produced during photosynthesis under conditions of restricted Calvin cycle to be eliminated, thus preventing an over-reduction of the carriers of photosynthetic electron transport (Krömer, 1995). Mitochondria are implicated in the metabolism of proline, which accumulates under hyperosmotic stress conditions as an osmoprotectant, being the first step of its oxidation catalysed by proline dehydrogenase, an inner mitochondrial membrane enzyme (Kiyosue et al., 1996, and references therein). Moreover, respiration controls synthesis of ascorbate, a powerful antioxidant playing a key role in reactive oxygen species (ROS) detoxification; this occurs by regulating the activity of L-galactono-
-lactone dehydrogenase, a mitochondrial enzyme which catalyses the last step of ascorbate synthesis (Millar et al., 2003). It has also been reported recently that leaf mitochondria may play a central role in counteracting environmental stresses by modulating cell redox homeostasis and by setting antioxidant capacity (Dutilleul et al., 2003). Plant mitochondria may also sense cellular stress early and regulate programmed cell death (Jones, 2000; Rhoads et al., 2006). Furthermore, mitochondria may play a major role in inter-organelle cross-talk under environmental/oxidative stresses by signalling with chloroplasts (Millar et al., 2001) and by inducing altered nuclear gene expression through mitochondria-to-nucleus signalling, which is referred to as mitochondrial retrograde regulation (Rhoads et al., 2006). A key role of mitochondria, that is receiving increasing interest, is their ability to defend themselves (and the cell) from an excess of ROS. In fact, in the plant cell, mitochondria represent a major source of ROS production and consequent oxidative damage, as indicated by proteomic studies (Sweetlove et al., 2002; Bartoli et al., 2004; Taylor et al., 2005). This occurs under abiotic stresses, drought and salinity in particular (Alscher et al., 1997), thus suggesting that high tolerance of plants to environmental stresses may be associated with efficient defence against oxidative stress at cellular and subcellular levels. To do this, plant mitochondria display three different strategies (Møller, 2001): the first line of defence is the avoidance of ROS production, achieved by keeping the electron transport chain adequately oxidized, while the second and the third ones are ROS detoxification and the repair of ROS-mediated damages, respectively. Since the last two lines of defence require continuous consumption and regeneration of small antioxidant molecules, such as ascorbate, glutathione, and NADPH, the avoidance of ROS production may appear more advantageous for mitochondria.
These topics have been investigated by many research groups through the classical biochemical techniques using isolated mitochondria, as well as by more sophisticated approaches (gene expression, proteomics, transgenic plants, isotope fractionation, ‘in vivo’ microscopy) applied to organelles and ‘in vivo’ systems from cultured cells to whole plants. Commonly studied species are Arabidopsis, a useful genetic model, together with tobacco, pea, potato, tomato, and cereals. In the last few years, studies have been focused on the first line of defence against oxidative stress, the avoidance of ROS production, which is still largely unknown. In particular, bioenergetics of mitochondria purified from durum wheat, a species widely cultivated in semi-arid regions of the Mediterranean area and well adapted to drought and thus representing a useful model system, have been studied (Flagella et al., 1998, and references therein). Durum wheat mitochondria (DWM) possess three active energy-dissipating systems, namely the ATP-sensitive plant mitochondrial potassium channel (PmitoKATP) (Pastore et al., 1999a), the plant uncoupling protein (PUCP) (Pastore et al., 2000), and the alternative oxidase (AOX) (Pastore et al., 2001), all three able to control ROS production. To date nothing is known about the possible existence in DWM of the cold shock protein, CSP 310, acting as a non-phosphorylating bypass of the respiratory chain in some cereals (Kolesnichenko et al., 2005, and references therein).
DWM also possess the rotenone-insensitive external NAD(P)H dehydrogenases [NAD(P)H DHext] and a very active malate/oxaloacetate (MAL/OAA) shuttle, both allowing cytosolic NAD(P)H oxidation (Pastore et al., 2003). They may co-operate with the AOX thus protecting the chloroplast/cytosol from over-reduction by oxidizing excess NAD(P)H without high ROS production (Pastore et al., 2001). The effect of oxidative/abiotic stresses on the activity of the three dissipating systems and on the electrical membrane potential (
) generation by DWM was checked. This was done by using ‘in vitro’ isolated mitochondria treated with ROS (Pastore et al., 1999a, 2000, 2001, 2002) and mitochondria purified from seedlings subjected to mannitol or NaCl stress (Trono et al., 2004; Flagella et al., 2006).
Here, recent papers concerning mitochondria from durum wheat and the related literature are reviewed to infer the possible involvement of plant mitochondria in adaptation to drought-induced oxidative stress. Among the three energy-dissipating systems, the focus is particularly on the potassium channel; in fact, while the AOX and, more recently, the PUCP have been heavily studied by several groups using different plant systems, to date fewer than 10 papers in the literature deal with the potassium channel in plant mitochondria. So, this channel is certainly not well-known to many scientists in this field and, so far, it has very often been forgotten in the papers about plant mitochondria and stress.
|
Dissipating systems in DWM and their effect on and ROS production
|
|---|
|
TopAbstractIntroductionDissipating systems in DWM...Effects of oxidative and...ConclusionsReferences |
|---|
PmitoKATP
The existence of a potassium channel inhibited by ATP in plant mitochondria was first shown by using DWM (Pastore et al., 1999a). This channel was named PmitoKATP in analogy with the animal counterpart (mitoKATP; Paucek et al., 1992). The main characteristics of this channel are summarized in Table 1. Notably, ATP inhibits this channel with at least 10-fold lower efficiency than the mammalian counterpart (Garlid, 1996); moreover Mg2+, which inhibits the mammalian channel, is ineffective in DWM. Some variability of data reported in Table 1 may be observed depending on the stock of seeds and the conditions of seedling growth.
|
The plant species in which the existence of a potassium uniport has been reported to date are listed in Table 2. Only the channel of pea is well characterized and shows some analogies with durum wheat (DW)-mitoKATP, as, for example, the inhibition by ATP (Petrussa et al., 2001; Chiandussi et al., 2002; Casolo et al., 2003); on the contrary, potato, tomato, and maize mitochondria were found to show an ATP-insensitive potassium import pathway (Ruy et al., 2004).
|
In DWM, PmitoKATP catalyses the electrophoretic uniport of potassium through the inner mitochondrial membrane; the co-operation between PmitoKATP and the K+/H+ antiporter, very active in plant mitochondria (Diolez and Moreau, 1985), allows the operation of a potassium cycle. In the course of substrate oxidation, protons are ejected in the intermembrane space by complexes I, III, and IV of the respiratory chain, thus generating the protonmotive force, which drives ATP synthesis; the potassium cycle causes re-entry of protons in the mitochondrial matrix, thus potentially uncoupling mitochondria (Fig. 1A). While in mammalian mitochondria this uncoupling is negligible due to the low activity of the cycle (Garlid and Paucek, 2003), the capacity of the potassium cycle in DWM is so high as to completely collapse
(Pastore et al., 1999a), the main component of protonmotive force in plant mitochondria (Douce et al., 1987). This is clearly shown in Fig. 2A, in which of DWM was measured by using the fluorimetric probe safranin ‘O’ (Pastore et al., 1996). When succinate (5 mM), a respiratory substrate, was added to DWM, a rapid and large was generated; this was largely decreased by 25 mM KCl plus 10 µM diazoxide, a potassium channel opener (Table 1), while 0.2 mM ATP restored . Finally, the artificial uncoupler carbonyl cyanide p-trifluoromethoxyphenylhydrazone (FCCP) completely collapsed . In a previous set of experiments, the depolarization induced by KCl was even faster, although obtained without diazoxide (Pastore et al., 1999a), thus showing that the channel is able to depolarize DWM at different rates in different mitochondrial preparations. Here is shown an experiment where the channel is less active in order to highlight the sensitivity to diazoxide and ATP better and unambiguously to identify the operation of the PmitoKATP as uncoupling mode. It should be reported that pH, the other component of protonmotive force, is negligible in succinate-respiring DWM (about 0.03 units), as expected in the light of the high activity of the K+/H+ antiporter (D Pastore, D Trono, MN Laus, unpublished data). Therefore, PmitoKATP is able to completely collapse (and protonmotive force) in ‘in vitro’ isolated DWM, whereas the degree of decrease ‘in vivo’ should be dependent on the balance of modulators under different physiological conditions, as proposed later.
|
|
PUCP
The existence of an uncoupling protein in plant mitochondria was described for the first time in potato (Vercesi et al., 1995) and it is now demonstrated in a variety of organs and tissues of higher plant species including monocots and dicots, and C3, C4, and CAM plants (Je
ek et al., 2000). cDNAs for uncoupling proteins were obtained from potato, Arabidopsis, bread wheat, and skunk cabbage (references given in Hanák and Jeek, 2001), and from rice (Watanabe and Hirai, 2002). Current knowledge of PUCPs including biochemical properties, distribution, and regulation of gene expression, as well as gene family and evolutionary aspects, have been reviewed recently by Vercesi et al. (2006). It has been shown that DWM possess a very active PUCP (Pastore et al., 2000). With the notable exception of UCP1 in brown adipose tissue (Klingenberg and Echtay, 2001), the PUCP in DWM is probably the most active uncoupling protein so far described among animal and plant mitochondria. In Table 3 the main characteristics of DW-UCP are summarized. ATP is the main inhibitor, while GDP and GTP are less effective.
|
In the presence of free fatty acids (FFAs), PUCP catalyses re-entry of protons in the course of substrate oxidation, so allowing
to decrease in plant mitochondria (Fig. 1B). The mechanism of activation of UCPs by FFAs has been one of the most debated issues over the years, but it is beyond the scope of this paper (for further elucidation see the following reviews: Skulachev, 1998; Klingenberg and Echtay, 2001; Vercesi et al., 2006). In particular, as shown in Fig. 2B, DW-UCP is so active it quickly and completely collapses of succinate-respiring mitochondria, even at low FFA concentration (8 µM linoleic acid in this experiment). ATP (0.5 mM) induced a large recoupling. FCCP (1 µM) completely collapsed at high rate. It should be mentioned that the ATP/ADP antiporter may also significantly uncouple mitochondria in the presence of FFAs (Skulachev, 1998, and references therein), but its contribution was inhibited by including atractyloside in the reaction medium (Trono et al., 2006). Also in this case, even though PUCP is able to completely collapse of DWM ‘in vitro’, the activity ‘in vivo’ should be dependent on physiological conditions (see below).
AOX
Plant mitochondria possess an AOX showing a quinol-oxidizing activity; it branches from the respiratory chain at the level of ubiquinone and it is known to be insensitive to cyanide and antimycin A, inhibitors of cytochrome c oxidase. The AOX bypasses the last two sites of energy conservation associated with the cytochrome pathway (complexes III and IV; compare A and B with C in Fig. 1), showing a non-phosphorylating and, consequently, an energy-dissipating character (for excellent reviews, Moore and Siedow, 1991; Vanlerberghe and McIntosh, 1997). In this case, non-coupled rather than uncoupled respiration takes place (Skulachev, 1998).
At present, the physiological role of the AOX has been well established only in specialized thermogenic plant tissues (Meeuse, 1975). The AOX function in non-thermogenic plants has not been completely understood, but it is commonly accepted that the AOX energy-dissipating character can play a protective role under biotic and abiotic stress by lowering mitochondrial ROS generation in isolated mitochondria, cultured cells (Vanlerberghe and McIntosh, 1997; Maxwell et al., 1999, and references therein), and the whole plant (Umbach et al., 2005). The analysis of extensive mRNA expression data in Arabidopsis indicates that five Aox genes are expressed, but organ and development regulation are evident, suggesting regulatory specialization of Aox gene members (Clifton et al., 2006). Interestingly, a microarray study using an Arabidopsis AtAOX1a anti-sense line shows AOX influences outside mitochondria, particularly in chloroplasts and on several carbon metabolism pathways (Umbach et al., 2005). Also, analysis of genes co-expressed with Aoxs from studies of responses to various treatments altering mitochondrial functions and/or from plants with altered AOX levels reveals that this gene set encodes more functions outside the mitochondrion than functions in mitochondria, thus showing a role in re-programming cellular metabolism in response to the ever-changing environment encountered by plants (Clifton et al., 2006).
In the past, it was reported that DWM do not show a cyanide-insensitive alternative pathway (Goldstein et al., 1980). This point was reinvestigated and it was shown that AOX activity may be elicited in DWM by using suitable activators (Pastore et al., 1999b, 2001). In particular, DW-AOX is mainly activated by glyoxylate and hydroxypyruvate, two intermediates of the photorespiratory cycle, while pyruvate, a typical activator of AOXs, is less effective (Table 4). Other intermediates of the photorespiratory cycle, such as glycine, glycolate, phosphoglycolate, and serine, as well as 2-oxoglutarate, activators of other AOXs (Millar et al., 1996), are ineffective on DW-AOX. The effect of AOX functioning on is shown in Fig. 2C. The reaction was started by treating DWM with 10 mM malate plus 1 mM NADH, thus inducing a high value. EGTA and EDTA were also present in the reaction medium to inhibit NADH oxidation via the Ca2+-dependent rotenone-insensitive external NADH dehydrogenase (NADH DHext). Since DWM cannot freely oxidize malate via the mitochondrial NADH-dependent malic enzyme (ME), malate dehydrogenase (MDH) was also added to the reaction medium in order to allow generation via the MAL/OAA shuttle (Pastore et al., 2001, 2003). The addition of cyanide caused an almost complete depolarization (Fig. 2C, trace a), which was not further enhanced by salicylhydroxamate (SHAM), an AOX inhibitor (Fig. 2C; Table 4). On the other hand, when the reaction medium also contained 1 mM pyruvate, the addition of cyanide depolarized DWM to a smaller extent compared with the control (Fig. 2C, trace b). In this case, SHAM addition induced obvious depolarization. These results are consistent with the oxidation of malate through the AOX pathway, which leads to the maintainance of some due to the complex I proton pumping activity (Vianello et al., 1997). Therefore, under conditions in which the cytochrome pathway is restricted, DW-AOX is unable to maintain a high . In the light of this, the non-coupled respiration due to AOX, although differing in its mechanism, is energy dissipating, the same as the uncoupled respiration due to PmitoKATP and PUCP.
|
Effect of the dissipating systems on mitochondrial ROS production in DWM
One of the major sources of oxygen radicals in cells are mitochondria, which basically convert to ROS about 2–6% of the total oxygen consumed (Boveris and Chance, 1973; Liu, 1997). In fact, some components of the initial (complex I) and middle part (Q-cycle, complex III) of the respiratory chain are the main reductants involved in one-electron reduction of oxygen to superoxide anion (
); among them, semiquinone (CoQH•) is apparently employed especially often (Skulachev, 1998). In plants, the oxygen concentration in the photosynthesizing cell is very high (Scandalios, 1993), thus plant mitochondria are potentially exposed to high ROS production causing an even greater oxidative damage than the animal counterpart.
Harmful ROS production is enhanced when is high and the intermediates of the respiratory chain are kept in a more reduced state; also Skulachev (1994, 1998) proposed that ‘mild’ uncoupling, by lowering , may protect mitochondria from high ROS production. Therefore, the ability of DWM dissipating systems to control mitochondrial production of was checked (Table 5). Activation of PmitoKATP by KCl, of PUCP by linoleic acid, and of AOX by pyruvate, reduced the rate of generation by half; moreover, if the dissipating systems were inhibited, the rate came back to control levels. Notably, if the PmitoKATP was activated by KCl plus mersalyl (Table 1), generation was reduced to zero. It was concluded that dissipating systems may strongly control ROS production in purified DWM. This result is not unique (Skulachev, 1997; Braidot et al., 1999; Casolo et al., 2000, and references therein). In order to compare DWM with other plant mitochondria also see Møller (2001). It should be underlined that ROS production by ‘in vitro’ isolated mitochondria may be quite different from the physiological one; nevertheless, ‘in vitro’ experiments give useful indications that are confirmed ‘in vivo’. A recent paper confirms that AOX dampens ROS generation by using a whole plant model system (transformed lines of Arabidopsis) and an ‘in vivo’ microscopy technique (Umbach et al., 2005). Also, transgenic plant cells lacking AOX have increased susceptibility to oxidative stress and programmed cell death (Robson and Vanlerberghe, 2002). Moreover, overexpression of PUCP in transgenic tobacco increases tolerance to oxidative stress (Brandalise et al., 2003).
|
|
Effects of oxidative and abiotic stresses on dissipating systems in DWM |
|---|
|
TopAbstractIntroductionDissipating systems in DWM...Effects of oxidative and...ConclusionsReferences |
|---|
Effect of ROS on PmitoKATP, PUCP, and on the mechanism of
generationThe demonstration that the DWM dissipating systems reduce ROS production is not surprising, since most modes of uncoupling have this effect (Wagner and Krab, 1995; Zoratti and Szabò, 1995; Skulachev, 1996a, b, 1997; Negré-Salvayre et al., 1997; Kowaltowski et al., 1998). Of potentially greater interest is the novel finding, reported in Table 6, showing that ROS can quickly stimulate PmitoKATP (Pastore et al., 1999a) and PUCP in DWM, the latter being evaluated as ATP-sensitive FFA-mediated uncoupling (Pastore et al., 2000). Activation of the mitochondrial potassium channel by ROS in cardiomyocytes (Lebuffe et al., 2003), as well as by NO in ventricular myocytes (Sasaki et al., 2000) and pea seedlings (Chiandussi et al., 2002), was successively reported.
|
Sensitivity of UCPs to ROS also seems to be a general property: besides DW-UCP, it was successively reported that animal UCP1, UCP2, and UCP3 are also activated by
(Echtay et al., 2002b), with UCP2 activation occurring from the matrix side (Echtay et al., 2002a), probably through a mechanism involving lipid peroxidation breakdown products such as hydroxyl-nonenal (Murphy et al., 2003). As for plant mitochondria, PUCP of potato tubers (Considine et al., 2003) and topinambur tubers (Paventi et al., 2006) were also shown to be activated by ROS; in potato, this has been shown to occur via hydroxyl-nonenal (Smith et al., 2004). Interestingly, AOX activity was insensitive to quick regulation by ROS and little inhibited by H2O2 in minutes. On the other hand, it is known that in tobacco suspension cells, H2O2 increased Aox1 mRNA within 2 h (Vanlerberghe and McIntosh, 1996) and that, in Arabidopsis, Aox1a and Aox1d are amongst the most stress-responsive genes amongst the hundreds of genes known to encode mitochondrial proteins (Clifton et al., 2006).
In another set of experiments the effect of on generation in DWM respiring either succinate or externally added NADH was studied (Table 6; Pastore et al., 2002). In a few minutes inhibited succinate oxidation as a result of a mixed (competitive/non-competitive) inhibition exerted on succinate transport across the inner mitochondrial membrane. In addition, no effect was observed on the oxidation of NADH, which is oxidized by the NADH DHext without crossing the membrane; this also shows that, in a few minutes of treatment, no effect occurs on the common electron carriers of the respiratory chain. After prolonged treatment (tens of minutes), gross damage occurred with complete impairment of DWM capability to generate (for oxidative damages to plant mitochondria, Taylor et al., 2004).
From the above results, the following picture emerges: during oxidative stress ROS may very rapidly elicit PmitoKATP and PUCP activity, which in turn may control ROS production. This suggests a possible feed back mechanism to protect mitochondria against ROS (see below). On the contrary, AOX regulation by ROS probably involves new synthesis under oxidative stress (Vanlerberghe and McIntosh, 1996), chilling stress (Vanlerberghe and McIntosh, 1997), and pathogen attack (Simons et al., 1999), but probably not under water stress (Ribas-Carbo et al., 2005). As for damage to membrane proteins, substrate carriers may be a sensitive early target (Atlante et al., 1992; Yang and Yang, 1997; Yan and Sohal, 1998; Valenti et al., 2002), thus possibly preventing further substrate oxidation and ROS production, while the respiratory chain is more resistant to ROS.
The time-course and the opposite effects induced by ROS confirm that they should be considered not only highly harmful reactive species, but also key factors for regulation and signalling (for recent reviews, Laloi et al., 2004; Rhoads et al., 2006).
Effect of hyperosmotic stress on PmitoKATP and PUCP in DWM
Modulation by ROS and ATP:
It is well known that cellular ROS production can be increased as a result of plant exposure to various environmental stresses, thus inducing oxidative stress (Scandalios, 1993; Foyer et al., 1994; Møller, 2001). Mitochondria, which are a major source of ROS in the plant cell, were reported to increase ROS production, in particular under drought and salt stress (Alscher et al., 1997). Therefore, it is feasible that PmitoKATP and PUCP, which are quickly activated by ROS, serve as defence mechanisms under these conditions. Also, both dissipating systems were found to be activated in potato cells adapted to hyperosmotic stress (Fratianni et al., 2001) and in early etiolated seedlings of durum wheat submitted to moderate and severe osmotic and salt stress (Trono et al., 2004). In the latter case, durum wheat was chosen because it is a crop well adapted to semi-arid regions, where it undergoes water and salt stress, and etiolated early seedlings were used because of the central role mitochondria play in cellular bioenergetics at this stage. Main results regarding DWM are reported in Table 7. Both dissipating systems were strongly activated under all stress conditions; in particular, PmitoKATP showed a higher response to osmotic stress, and PUCP to the salt stress. The remarkable activation even under moderate stress is very interesting. In fact, the moderate stress imposed is unable to affect mitochondrial integrity or oxygen uptake rate and efficiency of phosphorylation of succinate-respiring mitochondria (Trono et al., 2004; Flagella et al., 2006). So, activation of PmitoKATP and PUCP precedes the occurrence of frank mitochondrial damage and may be considered an early response to stress. Moreover, under the severe stress imposed, which significantly damages mitochondrial integrity and functionality (Trono et al., 2004; Flagella et al., 2006), PmitoKATP and PUCP were further activated rather than inhibited, thus suggesting that both proteins can withstand high-stress conditions and that they are involved in a prolonged response to stress. As for the mechanism of PmitoKATP and PUCP activation, an increase of production by DWM purified from stressed seedlings was measured; in the case of severe salt stress, this was even double with respect to the control. It was also observed that inclusion in the reaction medium of superoxide dismutase plus catalase, which scavenge ROS, resulted in a strong reversion of PmitoKATP and PUCP activation. These results show that both systems are activated by ROS in DWM from hyperosmotic-stressed seedlings, the same as in control DWM (Trono et al., 2004). Finally, a strong inhibition of ATP synthesis under severe stress was measured (Flagella et al., 2006). These data are consistent with the hypothetical mechanism of PmitoKATP and PUCP activation reported in Fig. 3. Under control conditions, ATP inhibition prevails over ROS activation. Under stress, as ROS production is increased and ATP synthesis is inhibited, the balance between modulators changes; therefore, ROS activate PmitoKATP and PUCP that, in turn, dissipate , thus inhibiting further large-scale ROS production according to a feedback mechanism.
|
|
As for PUCP, a possible increase in FFAs may contribute to activation; in line with this hypothesis, PUCP-dependent uncoupling in tomatoes at different stages of ripening was found to change as a result of the availability of endogenous FFAs (Costa et al., 1999). Further studies are necessary to check this possibility.
Are new syntheses involved?:
To date, new synthesis of PmitoKATP and PUCP cannot be excluded. Anyway, the observation that ROS may largely account for the activation, strongly suggests that this mechanism may function to quickly switch on the decrease of and, as a consequence, of ROS production without waiting for protein expression. Also, it was observed that the transcript levels of two mitochondrial uncoupling protein-related genes (WhUCP1 and TC265881) are not affected under the experimental conditions of the study (Trono et al., 2006). This hypothesis is in agreement with results from other plant systems: Arabidopsis suspension cells subjected to a broad range of abiotic stresses showed no changes in the transcript levels of the two UCP genes under the majority of treatments (Clifton, 2005). Moreover, in dehydrated slices of topinambur tubers, PUCP was found to acquire ROS sensitivity without increasing protein content, as shown by western blot analysis (Paventi et al., 2006).
Results are quite different when using other plant/stress systems, probably due to a different plant model and kind of stress as well as its intensity, duration, and mode of imposition. Analysis of tobacco leaves acclimated to oxidative stress shows an increase in the expression of a gene encoding for a putative PUCP (Vranová et al., 2002); on the other hand, differential impact of environmental stresses on the pea mitochondrial proteome has been observed recently, with an increase of the PUCP as a result of drought, but not chilling or oxidative stress imposition (Taylor et al., 2005). Contrasting results were also obtained when the expression of PUCP was investigated under cold stress, in view of its possible thermogenic role: expression was enhanced in potato (Laloi et al., 1997; Nantes et al., 1999; Calegario et al., 2003) and in the case of AtUCP1 of Arabidopsis (Maia et al., 1998), but was unaffected in the case of AtUCP2 (Watanabe et al., 1999) and WhUCP1 of bread wheat (Murayama and Handa, 2000).
The cold-induced increase of PUCP expression is consistent both with the protein's thermogenic effect (Jarmuszkiewicz et al., 2001, and references therein) and with the control of ROS production under abiotic stress proposed herein, whereas the lack of increased expression appears to be in contrast to these effects. The hypothesis reported in Fig. 3 may help to reconcile these apparently conflicting findings. It is suggested that, as a result of ROS activation (and possibly of the increased availability of endogenous FFAs), PUCP-dependent uncoupling can be enhanced, even though protein content is unchanged.
Possible effect of drought stress on the oxidation of cytosolic NADH and the AOX activity in DWM
In green tissues, an important aspect is the chloroplast/cytosol/mitochondrion co-operation under stress to modulate cell redox homeostasis (Krömer, 1995; Raghavendra and Padmasree, 2003, and references therein). Under restriction of the Calvin cycle due to suboptimal CO2 availability (for example, under drought), chloroplasts may defend themselves from over-reduction and photoinhibition by releasing excess reducing power and energy via photorespiration, triose phosphate export, and the so-called ‘malate valve’ (Backhausen et al., 1998; Backhausen and Scheibe, 1999).
As for mitochondrial help, excess chloroplastic NAD(P)H exported in the cytosol is thought to be directly oxidized by mitochondria via NAD(P)H DHext. On the contrary, the MAL/OAA shuttle was reported to export reducing equivalents from the matrix towards the cytosol (Raghavendra and Padmasree, 2003, and references therein); in fact, plant cells are generally thought to be more aligned energetically to export NADH from mitochondria than to import it.
Surprisingly, in DWM and potato cell mitochondria, results quite different from the expected ones were observed (Pastore et al., 2003); they are summarized in Fig. 4. The systems involved in cytosolic NAD(P)H oxidation are shown and kinetic parameters of the enzymes implicated are reported in the legend. Cytosolic NADH can be oxidized by the MAL/OAA shuttle, which is highly active in DWM. In particular, a novel MAL/OAA antiporter representing the rate-limiting step of the shuttle has been described, thus determining the rate of NADH oxidation. On the basis of the kinetic analysis, at low physiological NADH concentrations (about 1 µM; Heineke et al., 1991), oxidation via the MAL/OAA shuttle occurs in DWM with about 100-fold higher efficiency than that due to the NADH DHext (10-fold in potato mitochondria). On the other hand, the contribution of the NADH DHext to NADH oxidation is expected to increase under stress conditions, when an increase of NADH cytosolic concentration and, possibly, in the NADH DHext content (Clifton et al., 2005) and of the activator Ca2+ (Krömer, 1995, and references therein) may occur.
|
As for NADPH, it is oxidized by the NADPH DHext, but not by the MAL/OAA shuttle. In Fig. 4 the possible link between NAD(P)H oxidation and the AOX pathway is also shown. In plant mitochondria, malate metabolism and AOX activity are generally linked to each other; in fact, malate or malate-generating substrates produce pyruvate, an AOX activator, via ME (Millar et al., 1993, 1996). Anyway, this does not occur in DWM (Pastore et al., 1999b, 2001). Really, pyruvate can activate DW-AOX (Table 4), but it cannot be generated from malate inside DWM because of the very low activity of ME and very high activity of mitochondrial MDH (see the legend to Fig. 4). Also, in the course of malate oxidation, DWM from both etiolated shoots and green leaves release oxaloacetate but not pyruvate via the MAL/OAA antiporter reported above (Pastore et al., 2001). On the other hand, as stated above, DW-AOX is efficiently activated by hydroxypyruvate and glyoxylate, thus showing a metabolic link between the AOX pathway and the photorespiratory cycle in durum wheat.
This result suggests that under environmental stress, for example, drought, when photorespiration is really active, AOX is activated to oppose oxidative stress. In addition, Ribas-Carbo et al. (2005) reported recently that in soybean leaves severe water stress caused a significant shift of electrons from the cytochrome to the alternative pathway, due to a biochemical regulation other than protein synthesis. So, although it is clear that photorespiration increases relative to net CO2 uptake during drought, it is less evident whether flux through the photorespiratory pathway increases in absolute terms or not (Noctor et al., 2002, and references therein). On the other hand, studies of several barley mutants with decreased amounts of enzymes involved in the photorespiratory pathway suggest that flux does increase to some extent during drought stress (Wingler et al., 1999).
As a whole, it is proposed that, in green tissues under drought stress, the mitochondrial oxidation of cytosolic NADH may occur via the MAL/OAA shuttle and, probably, to a less extent via the NAD(P)H DHext. Concurrently, the photorespiratory cycle intermediates, glyoxylate and hydroxypyruvate, activate AOX, which works as an energy-dissipating system. Therefore, DWM may prevent chloroplast/cytosol over-reduction by discharging reducing equivalents without high ROS production by the respiratory chain. It should be noted that endogenous NADH produced via the shuttle may be oxidized via the rotenone-insensitive internal NADH dehydrogenase (NADH DHin) (Fig. 4). This would provide the mitochondria with a pathway for re-oxidation via ubiquinone to the AOX and oxygen, where no protons are pumped because all three sites of proton pumping are bypassed (Fig. 1). In this way, over-reduction and the accompanying production of ROS at complexes I and III is minimized (Møller, 2002). The hypothesis that there is co-operation among the MAL/OAA shuttle, NADH DHin, and AOX in green tissues is also in agreement with the diurnal regulation of the NDA1 gene and with the co-ordinated up-regulation of NDA2 and Aox1a genes under various treatments in Arabidopsis (Elhafez et al., 2006).
|
Conclusions |
|---|
|
TopAbstractIntroductionDissipating systems in DWM...Effects of oxidative and...ConclusionsReferences |
|---|
It is well known that plant mitochondria participate in some metabolic processes involved in response to drought stress (photorespiration, proline oxidation, and ascorbate synthesis). Here it is proposed that mitochondria may also play a key role in adaptation to drought by acting against drought-induced oxidative stress. In addition, durum wheat that is used as a model species is well adapted to drought and even possesses three mitochondrial dissipating systems acting against oxidative stress. PmitoKATP and PUCP are very active and are modulated by ROS in such a way to warrant a quick control of mitochondrial ROS production. On the other hand, AOX is ROS-insensitive, while it appears to be regulated by photorespiratory metabolism.
This meets the expectation that the three systems should be subjected to cross-regulation under different metabolic conditions and/or developmental stages. In line with this hypothesis, an opposite regulation of PUCP and AOX by FFAs was reported (Sluse et al., 1998); moreover, hydroxyl-nonenal, a lipid peroxidation breakdown product, which activates PUCP (Smith et al., 2004), was reported recently to inhibit AOX (Winger et al., 2005). Interestingly, it has been suggested that, while both AOX and PUCP may act to forestall mitochondrial ROS production, only PUCP may be able to operate when ROS levels become increased (Rhoads et al., 2006).
Differences also exist in gene expression profiles. AOX and PUCP were differently expressed and regulated during off-vine ripening in tomato (Almeida et al., 1999), but not in mango (Considine et al., 2001) or during on-vine ripening in tomato (Holtzapffel et al., 2002). Very recently, the expression profiles of the gene families of PUCP and AOX in a monocot (sugarcane) and a dicot (Arabidopsis) have been studied (Boreck
et al., 2006). Uncoupling protein genes were expressed more ubiquitously than the AOX genes. Distinct expression patterns among gene family members were observed between species and during chilling stress, thus showing a variation in cell or tissue/organ transcriptional regulation (Boreck et al., 2006).
In DWM, the picture emerging from the results is that the AOX may act as an antioxidant defence system when green tissues are exposed to drought stress by working in combination with the photorespiratory cycle, while, in etiolated tissues, this role is questionable in the light of the high PmitoKATP and PUCP functioning under stress.
Further investigations will be necessary to understand the significance and regulation of the three energy-dissipating systems under different stress conditions and plant species.
|
Abbreviations |
|---|
, electrical membrane potential; AOX, alternative oxidase; DWM, durum wheat mitochondria; FCCP, carbonyl cyanide p-trifluoromethoxyphenylhydrazone; FFAs, free fatty acids; MAL/OAA, malate/oxaloacetate; MDH, malate dehydrogenase; ME, malic enzyme; NAD(P)H DHext, rotenone-insensitive external NAD(P)H dehydrogenases; NAD(P)H DHin, rotenone-insensitive internal NAD(P)H dehydrogenases; , superoxide anion; PmitoKATP, ATP-sensitive plant mitochondrial potassium channel; PUCP, plant uncoupling protein; ROS, reactive oxygen species; SHAM, salicylhydroxamate. |
References |
|---|
|
TopAbstractIntroductionDissipating systems in DWM...Effects of oxidative and...ConclusionsReferences |
|---|
Almeida AM, Jarmuszkiewicz W, Khomsi H, Arruda P, Vercesi AE, Sluse FE. (1999) Cyanide-resistant, ATP-synthesis-sustained, and uncoupling-protein-sustained respiration during postharvest ripening of tomato fruit. Plant Physiology 119 1323–1330.
Alscher RG, Donahue JL, Cramer CL. (1997) Reactive oxygen species and antioxidants: relationships in green cells. Physiologia Plantarum 100 224–233.[CrossRef]
Atlante A, Passarella S, Moreno G, Salet C. (1992) Effects of rhodamine 123 in the dark and after irradiation on mitochondrial energy metabolism. Photochemistry and Photobiology 56 471–478.[Web of Science][Medline]
Backhausen JE, Emmerlich A, Holtgrefe S, Horton P, Nast G, Rogers JJM, Müller-Röber B, Scheibe R. (1998) Transgenic potato plants with altered expression levels of chloroplast NADP-malate dehydrogenase: interactions between photosynthetic electron transport and malate metabolism in leaves and in isolated intact chloroplasts. Planta 207 105–114.[CrossRef]
Backhausen JE and Scheibe R. (1999) Adaptation of tobacco plants to elevated CO2: influence of leaf age on changes in physiology, redox states and NADP-malate dehydrogenase activity. Journal of Experimental Botany 50 665–675.
Bartoli CG, Gómez F, Martínez DE, Guiamet JJ. (2004) Mitochondria are the main target for oxidative damage in leaves of wheat (Triticum aestivum L.). Journal of Experimental Botany 55 1663–1669.
Boreck J, Nogueira FTS, de Oliveira KAP, Maia IG, Vercesi AE, Arruda P. (2006) The plant energy-dissipating mitochondrial systems: depicting the genomic structure and the expression profiles of the gene families of uncoupling protein and alternative oxidase in monocots and dicots. Journal of Experimental Botany 57 849–864.
Boveris A and Chance B. (1973) The mitochondrial generation of hydrogen peroxide: general properties and effect of hyperbaric oxygen. Biochemical Journal 134 707–716.[Web of Science][Medline]
Braidot E, Petrussa E, Vianello A, Macrì F. (1999) Hydrogen peroxide generation by higher plant mitochondria oxidizing complex I or complex II substrates. FEBS Letters 451 347–350.[CrossRef][Web of Science][Medline]
Brandalise M, Maia GI, Boreck J, Vercesi AE, Arruda P. (2003) Overexpression of plant uncoupling mitochondrial protein in transgenic tobacco increases tolerance to oxidative stress. Journal of Bioenergetics and Biomembranes 35 203–209.[CrossRef][Web of Science][Medline]
Calegario FF, Cosso RG, Fagian MM, Almeida FV, Jardim WF, Jezek P, Arruda P, Vercesi AE. (2003) Stimulation of potato tuber respiration by cold stress is associated with an increased capacity of both plant uncoupling mitochondrial protein (PUMP) and alternative oxidase. Journal of Bioenergetics and Biomembranes 35 211–220.[CrossRef][Web of Science][Medline]
Casolo V, Braidot E, Chiandussi E, Macrì F, Vianello A. (2000) The role of mild uncoupling and non-coupled respiration in the regulation of hydrogen peroxide generation by plant mitochondria. FEBS Letters 474 53–57.[CrossRef][Web of Science][Medline]
Casolo V, Braidot E, Chiandussi E, Vianello A, Macrì F. (2003) 
channel opening prevents succinate-dependent H2O2 generation by plant mitochondria. Physiologia Plantarum 118 313–318.[CrossRef]
Casolo V, Petrussa E, Kraj
áková J, Macrì F, Vianello A. (2005) Involvement of the mitochondrial channel in H2O2- or NO-induced programmed death of soybean suspension cultures. Journal of Experimental Botany 56 997–1006.
Chiandussi E, Petrussa E, Macrì F, Vianello A. (2002) Modulation of a plant mitochondrial channel and its involvement in cytochrome c release. Journal of Bioenergetics and Biomembranes 34 177–184.[CrossRef][Web of Science][Medline]
Clifton R, Lister R, Parker KL, Sappl PG, Elhafez D, Harvey Millar AH, Day DA, Whelan J. (2005) Stress-induced co-expression of alternative respiratory chain components in Arabidopsis thaliana. Plant Molecular Biology 58 193–212.[CrossRef][Web of Science][Medline]
Clifton R, Millar AH, Whelan J. (2006) Alternative oxidases in Arabidopsis: a comparative analysis of differential expression in the gene family provides new insights into function of non-phosphorylating bypasses. Biochimica et Biophysica Acta 1757 730–741.[Medline]
Considine MJ, Daley DO, Whelan J. (2001) The expression of alternative oxidase and uncoupling protein during fruit ripening in mango. Plant Physiology 126 1619–1629.
Considine MJ, Goodman M, Echtay KS, Laloi M, Whelan J, Brand MD, Sweetlove LJ. (2003) Superoxide stimulates a proton leak in potato mitochondria that is related to the activity of uncoupling protein. Journal of Biological Chemistry 278 22298–22302.
Costa AD, Nantes IL, Jezek P, Leite A, Arruda P, Vercesi AE. (1999) Plant uncoupling mitochondrial protein activity in mitochondria isolated from tomatoes at different stages of ripening. Journal of Bioenergetics and Biomembranes 31 527–533.[CrossRef][Web of Science][Medline]
Diolez P and Moreau F. (1985) Correlations between ATP synthesis, membrane potential and oxidation rate in plant mitochondria. Biochimica et Biophysica Acta 806 56–63.[CrossRef]
Douce R, Bourguignon J, Brouquisse R, Neuburger M. (1987) Isolation of plant mitochondria: general principles and criteria of integrity. Methods in Enzymology 148 403–415.
Dutilleul C, Garmier M, Noctor G, Mathieu C, Chétrit P, Foyer CH, de Paepe R. (2003) Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulation. The Plant Cell 15 1212–1226.
Echtay KS, Murphy MP, Smith RA, Talbot DA, Brand MD. (2002a) Superoxide activates mitochondrial uncoupling protein 2 from the matrix side: studies using targeted antioxidants. Journal of Biological Chemistry 277 47129–47135.
Echtay KS, Roussel D, St-Pierre J, et al. (2002b) Superoxide activates mitochondrial uncoupling proteins. Nature 415 96–99.[CrossRef][Medline]
Elhafez D, Murcha MW, Clifton R, Soole KL, Day DA, Whelan J. (2006) Characterisation of mitochondrial alternative NAD(P)H dehydrogenases in Arabidopsis: intraorganelle location and expression. Plant and Cell Physiology 47 43–54.
Flagella Z, Campanile RG, Stoppelli MC, De Caro A, Di Fonzo N. (1998) Drought tolerance of photosynthetic electron transport under CO2-enriched and normal air in cereal species. Physiologia Plantarum 104 753–759.[CrossRef]
Flagella Z, Trono D, Pompa M, Di Fonzo N, Pastore D. (2006) Seawater stress applied at germination affects mitochondrial function in durum wheat (Triticum durum) early seedlings. Functional Plant Biology 33 357–366.[CrossRef]
Foyer CH, Lescure JC, Lefebvre C, Morot-Gaudry JF, Vincentz M, Vaucheret H. (1994) Adaptations of photosynthetic electron transport, carbon assimilation, and carbon partitioning in transgenic Nicotiana plumbaginifolia plants to changes in nitrate reductase activity. Plant Physiology 104 171–178.[Abstract]
Fratianni A, Pastore D, Pallotta ML, Chiatante D, Passarella S. (2001) Increase of membrane permeability of mitochondria isolated from water stress-adapted potato cells. Bioscience Reports 21 81–91.[CrossRef][Web of Science][Medline]
Garlid KD. (1996) Cation transport in mitochondria – the potassium cycle. Biochimica et Biophysica Acta 1275 123–126.[Medline]
Garlid KD and Paucek P. (2003) Mitochondrial potassium transport: the K+ cycle. Biochimica et Biophysica Acta 1606 23–41.[Medline]
Goldstein AH, Anderson JO, McDaniel RG. (1980) Cyanide-insensitive and cyanide-sensitive O2 uptake in wheat. Plant Physiology 66 488–493.
Hanák P and Jeek P. (2001) Mitochondrial uncoupling proteins and phylogenesis: UCP4 as the ancestral uncoupling protein. FEBS Letters 495 137–141.[CrossRef][Web of Science][Medline]
Heineke D, Riens B, Grosse H, Hoferichter P, Peter U, Flügge U-I, Heldt HW. (1991) Redox transfer across the inner chloroplast envelope membrane. Plant Physiology 95 1131–1137.
Holtzapffel RC, Finnegan PM, Millar AH, Badger MR, Day DA. (2002) Mitochondrial protein expression in tomato fruit during on-vine ripening and cold storage. Functional Plant Biology 29 827–834.[CrossRef]
Jarmuszkiewicz W, Sluse-Goffart CM, Vercesi AE, Sluse FE. (2001) Alternative oxidase and uncoupling protein: thermogenesis versus cell energy balance. Bioscience Reports 21 213–222.[CrossRef][Web of Science][Medline]
Jeek P, 
á
ková M, Ka
a
ová J, Rodrigues ETS, Madeira VMC, Vicente JAF. (2000) Occurrence of plant-uncoupling mitochondrial protein (PUMP) in diverse organs and tissues of several plants. Journal of Bioenergetics and Biomembranes 32 549–561.[CrossRef][Web of Science][Medline]
Jones A. (2000) Does the plant mitochondrion integrate cellular stress and regulate programmed cell death? Trends in Plant Science 5 225–230.[CrossRef][Web of Science][Medline]
Kiyosue T, Yoshiba Y, Yamaguchi-Shinozaki K, Shinozaki K. (1996) A nuclear gene encoding mitochondrial proline dehydrogenase, an enzyme involved in proline metabolism, is upregulated by proline but downregulated by dehydration in Arabidopsis. The Plant Cell 8 1323–1335.[Abstract]
Klingenberg M and Echtay KS. (2001) Uncoupling proteins: the issue from a biochemist point of view. Biochimica et Biophysica Acta 1504 128–143.[Medline]
Kolesnichenko V, Grabelnych OI, Pobezhimova TP, Voinikov VK. (2005) Non-phosphorylating bypass of the plant mitochondrial respiratory chain by stress protein CSP 310. Planta 221 113–122.[CrossRef][Web of Science][Medline]
Kowaltowski AJ, Costa ADT, Vercesi AE. (1998) Activation of the potato plant uncoupling mitochondrial protein inhibits reactive oxygen species generation by the respiratory chain. FEBS Letters 425 213–216.[CrossRef][Web of Science][Medline]
Krömer S. (1995) Respiration during photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 46 45–70.[CrossRef][Web of Science]
Laloi C, Apel K, Danon A. (2004) Reactive oxygen signalling: the latest news. Current Opinion in Plant Biology 7 323–328.[CrossRef][Web of Science][Medline]
Laloi M, Klein M, Riesmeier JW, Muller-Rober B, Fleury C, Bouillaud F, Ricquier D. (1997) A plant cold-induced uncoupling protein. Nature 389 135–136.[CrossRef][Medline]
Lebuffe G, Schumacker PT, Shao Z-H, Anderson T, Iwase H, Vanden Hoek TL. (2003) ROS and NO trigger early preconditioning: relationship to mitochondrial KATP channel. American Journal of Physiology, Heart and Circulatory Physiology 284 H299–308.
Liu S-S. (1997) Generating, partitioning, targeting and functioning of superoxide in mitochondria. Bioscience Reports 17 259–272.[CrossRef][Web of Science][Medline]
Maia IG, Benedetti CE, Leite A, Turcinelli SR, Vercesi AE, Arruda P. (1998) AtPUMP: an Arabidopsis gene encoding a plant uncoupling mitochondrial protein. FEBS Letters 429 403–406.[CrossRef][Web of Science][Medline]
Maxwell DP, Wang Y, McIntosh L. (1999) The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proceedings of the National Academy Sciences, USA 96 8271–8276.
Meeuse BJD. (1975) Thermogenic respiration in aroids. Annual Reviews of Plant Physiology and Plant Molecular Biology 26 117–126.[Web of Science]
Millar AH, Hoefnagel MHN, Day AD, Wiskich JT. (1996) Specificity of the organic acid activation of alternative oxidase in plant mitochodria. Plant Physiology 111 613–618.[Abstract]
Millar AH, Mittova V, Kiddle G, Heazlewood JL, Bartoli CG, Theodoulou FL, Foyer CH. (2003) Control of ascorbate synthesis by respiration and its implications for stress responses. Plant Physiology 133 443–447.
Millar AH, Wiskich JT, Whelan J, Day AD. (1993) Organic acid activation of the alternative oxidase of plant mitochondria. FEBS Letters 329 259–262.[CrossRef][Web of Science][Medline]
Millar H, Considine MJ, Day DA, Whelan J. (2001) Unraveling the role of mitochondria during oxidative stress in plants. IUBMB Life 51 201–205.[Web of Science][Medline]
Møller IM. (2001) Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annual Review of Plant Physiology and Plant Molecular Biology 52 561–591.[CrossRef][Web of Science][Medline]
Møller IM. (2002) A new dawn for plant mitochondrial NAD(P)H dehydrogenases. Trends in Plant Science 7 235–237.[CrossRef][Web of Science][Medline]
Moore AL and Siedow JN. (1991) The regulation and nature of the cyanide-resistant alternative oxidase of plant mitochondria. Biochimica et Biophysica Acta 1509 121–140.
Murayama S and Handa H. (2000) Isolation and characterization of cDNAs encoding mitochondrial uncoupling proteins in wheat: wheat UCP genes are not regulated by low temperature. Molecular and General Genetics 264 112–118.
Murphy MP, Echtay KS, Blaikie FH, et al. (2003) Superoxide activates uncoupling proteins by generating carbon-centered radicals and initiating lipid peroxidation. Journal of Biological Chemistry 278 48534–48545.
Nantes IL, Fagian MM, Catisti R, Arruda P, Maia IG, Vercesi AE. (1999) Low temperature and aging-promoted expression of PUMP in potato tuber mitochondria. FEBS Letters 457 103–106.[CrossRef][Web of Science][Medline]
Nègre-Salvayre A, Hirtz C, Carrera G, Cazenave R, Troly M, Salvayre R, Pénicaud L, Casteilla L. (1997) A role of uncoupling protein-2 as a regulator of mitochondrial hydrogen peroxide generation. FASEB Journal 11 809–815.[Abstract]
Noctor G, Veljovic-Javanovic S, Driscoll S, Novitskaya L, Foyer CH. (2002) Drought and oxidative load in the leaves of C3 plants: a predominant role for photorespiration? Annals of Botany 89 841–850.
Pastore D, Di Martino C, Bosco G, Passarella S. (1996) Stimulation of ATP synthesis via oxidative phosphorylation in wheat mitochondria irradiated with helium-neon laser. Biochemistry and Molecular Biology International 39 149–157.[Web of Science][Medline]
Pastore D, Di Pede S, Passarella S. (2003) Isolated durum wheat mitochondria and potato cell mitochondria oxidize externally added NADH mostly via the malate/oxaloacetate shuttle with a rate that depends on the carrier-mediated transport. Plant Physiology 133 2029–2039.
Pastore D, Fratianni A, Di Pede S, Passarella S. (2000) Effect of fatty acids, nucleotides and reactive oxygen species on durum wheat mitochondria. FEBS Letters 470 88–92.[CrossRef][Web of Science][Medline]
Pastore D, Laus MN, Di Fonzo N, Passarella S. (2002) Reactive oxygen species inhibit the succinate oxidation-supported generation of membrane potential in wheat mitochondria. FEBS Letters 516 15–19.[CrossRef][Web of Science][Medline]
Pastore D, Stoppelli MC, Di Fonzo N, Passarella S. (1999a) The existence of the K+ channel in plant mitochondria. Journal of Biological Chemistry 274 26683–26690.
Pastore D, Trono D, Laus MN, Di Fonzo N, Passarella S. (2001) Alternative oxidase in durum wheat mitochondria: activation by pyruvate, hydroxypyruvate and glyoxylate and physiological role. Plant and Cell Physiology 42 1373–1382.
Pastore D, Trono D, Passarella S. (1999b) Substrate oxidation and ADP/ATP exchange in coupled durum wheat (Triticum durum Desf.) mitochondria. Plant Biosystems 133 219–228.
Paucek P, Mironova G, Mahdi F, Beavis AD, Woldegiorgis G, Garlid KD. (1992) Reconstitution and partial purification of the glibenclamide-sensitive, ATP-dependent K+ channel from rat liver and beef heart mitochondria. Journal of Biological Chemistry 267 26062–26069.
Paventi G, Pastore D, Bobba A, Pizzuto R, Di Pede S, Passarella S. (2006) Plant uncoupling protein in mitochondria from aged-dehydrated slices of Jerusalem artichoke tubers becomes sensitive to superoxide and to hydrogen peroxide without increase in protein level. Biochimie 88 179–188.[Medline]
Petrussa E, Casolo V, Braidot E, Chiandussi E, Macrì F, Vianello A. (2001) Cyclosporin A induces the opening of a potassium-selective channel in higher plant mitochondria. Journal of Bioenergetics and Biomembranes 33 107–117.[CrossRef][Web of Science][Medline]
Petrussa E, Casolo V, Peresson C, Braidot E, Vianello A, Macrì F. (2004) The channel is involved in a low-amplitude permeability transition in plant mitochondria. Mitochondrion 3 297–307.[CrossRef][Web of Science][Medline]
Raghavendra AS and Padmasree K. (2003) Beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation. Trends in Plant Science 8 546–553.[CrossRef][Web of Science][Medline]
Rhoads DM, Umbach AL, Subbaiah CC, Siedow JN. (2006) Mitochondrial reactive oxygen species: contribution to oxidative stress and interorganellar signaling. Plant Physiology 141 357–366.
Ribas-Carbo M, Taylor NL, Giles L, Busquets S, Finnegan PM, Day DA, Lambers H, Medrano H, Berry JA, Flexas J. (2005) Effects of water stress on respiration in soybean leaves. Plant Physiology 139 466–473.
Robson CA and Vanlerberghe GC. (2002) Transgenic plant cells lacking mitochondrial alternative oxidase have increased susceptibility to mitochondria-dependent and -independent pathways of programmed cell death. Plant Physiology 129 1908–1920.
Ruy F, Vercesi AE, Andrade PBM, Bianconi ML, Chaimovich E, Kowaltowski AJ. (2004) A highly active ATP-insensitive K+ import pathway in plant mitochondria. Journal of Bioenergetics and Biomembranes 36 195–202.[CrossRef][Web of Science][Medline]
Sasaki N, Sato T, Ohler A, O'Rourke B, Marbán E. (2000) Activation of mitochondrial ATP-dependent potassium channels by nitric oxide. Circulation 101 439–445.
Scandalios JG. (1993) Oxygen stress and superoxide dismutases. Plant Physiology 101 7–12.[Web of Science][Medline]
Simons BH, Millenaar FF, Mulder L, Van Loon LC, Lambers H. (1999) Enhanced expression and activation of the alternative oxidase during infection of Arabidopsis with Pseudomonas syringae pv. tomato. Plant Physiology 120 529–538.
Skulachev VP. (1994) The latest news of the sodium world. Biochimica et Biophysica Acta 1187 216–221.[CrossRef]
Skulachev VP. (1996a) Role of uncoupled and non-coupled oxidations in maintenance of safely low levels of oxygen and its one-electron reductants. Quarterly Reviews of Biophysics 29 169–202.[Web of Science][Medline]
Skulachev VP. (1996b) Why are mitochondria involved in apoptosis? Permeability transition pores and apoptosis as selective mechanisms to eliminate superoxide-producing mitochondria and cell. FEBS Letters 397 7–10.[CrossRef][Web of Science][Medline]
Skulachev VP. (1997) Membrane-linked systems preventing superoxide formation. Bioscience Reports 17 347–366.[CrossRef][Web of Science][Medline]
Skulachev VP. (1998) Uncoupling: new approaches to an old problem of bioenergetics. Biochimica et Biophysica Acta 1363 100–124.[Medline]
Sluse FE, Almeida AM, Jarmuszkiewicz W, Vercesi AE. (1998) Free fatty acids regulate the uncoupling protein and alternative oxidase activities in plant mitochondria. FEBS Letters 433 237–240.[CrossRef][Web of Science][Medline]
Smith AMO, Ratcliffe RG, Sweetlove LJ. (2004) Activation and function of mitochondrial uncoupling protein in plants. Journal of Biological Chemistry 279 51944–51952.
Sweetlove LJ, Heazlewood JL, Herald V, Holtzapffel R, Day DA, Leaver CJ, Millar AH. (2002) The impact of oxidative stress on Arabidopsis mitochondria. The Plant Journal 32 891–904.[CrossRef][Web of Science][Medline]
Taylor NL, Day DA, Harvey Millar A. (2004) Targets of stress-induced oxidative damage in plant mitochondria and their impact on cell carbon/nitrogen metabolism. Journal of Experimental Botany 55 1–10.
Taylor NL, Heazlewood JL, Day DA, Millar AH. (2005) Differential impact of environmental stresses on the pea mitochondrial proteome. Molecular and Cellular Proteomics 4 1122–1123.
Trono D, Flagella Z, Laus MN, Di Fonzo N, Pastore D. (2004) The uncoupling protein and the potassium channel are activated by hyperosmotic stress in mitochondria from durum wheat seedlings. Plant, Cell and Environment 27 437–448.[CrossRef]
Trono D, Soccio M, Mastrangelo AM, De Simone V, Di Fonzo N, Pastore D. (2006) The transcript levels of two plant mitochondrial uncoupling protein (pUCP)-related genes are not affected by hyperosmotic stress in durum wheat seedlings showing an increased level of pUCP activity. Bioscience Reports 26 251–261.[CrossRef][Web of Science][Medline]
Umbach AL, Fiorani F, Siedow JN. (2005) Characterization of transformed Arabidopsis with altered alternative oxidase levels and analysis of effects on reactive oxygen species in tissue. Plant Physiology 139 1806–1820.
Valenti D, Atlante A, Barile M, Passarella S. (2002) Inhibition of phosphate transport in rat heart mitochondria by 3'-azido-3'-deoxythymidine due to stimulation of superoxide anion mitochondrial production. Biochemical Pharmacology 64 201–206.[CrossRef][Web of Science][Medline]
Vanlerberghe GC and McIntosh L. (1996) Signals regulating the expression of the nuclear gene encoding alternative oxidase of plant mitochondria. Plant Physiology 111 589–595.[Abstract]
Vanlerberghe GC and McIntosh L. (1997) Alternative oxidase: from gene to function. Annual Review of Plant Physiology and Plant Molecular Biology 48 703–734.[CrossRef][Web of Science][Medline]
Vercesi AE, Boreck J, Maia IG, Arruda P, Cuccovia IM, Chaimovich H. (2006) Plant uncoupling mitochondrial proteins. Annual Reviews of Plant Biology 57 383–404.
Vercesi AE, Martins IS, Silva MAP, Leite HMF, Cuccovia IM, Chaimovich H. (1995) PUMPing plants. Nature 375 24.[CrossRef]
Vianello A, Braidot E, Petrussa E, Macrì F. (1997) ATP synthesis driven by 
-keto acid-stimulated alternative oxidase in pea leaf mitochondria. Plant and Cell Physiology 38 1368–1374.
Vranová E, Atichartpongkul S, Villarroel R, Van Montagu M, Inzé D, Van Camp W. (2002) Comprehensive analysis of gene expression in Nicotiana tabacum leaves acclimated to oxidative stress. Proceedings of the National Academy of Sciences, USA 99 10870–10875.
Wagner AM and Krab K. (1995) The alternative respiration pathway in plants: role and regulation. Physiologia Plantarum 95 318–325.[CrossRef]
Watanabe A and Hirai A. (2002) Two uncoupling protein genes of rice (Oryza sativa L.): molecular study reveals the defects in the pre-mRNA processing for the heat-generating proteins of the subtropical cereal. Planta 215 90–100.[CrossRef][Web of Science][Medline]
Watanabe A, Nakazono M, Tsutsumi N, Hirai A. (1999) AtUCP2: a novel isoform of the mitochondrial uncoupling protein of Arabidopsis thaliana. Plant and Cell Physiology 40 1160–1166.
Winger AM, Harvey Millar A, Day DA. (2005) Sensitivity of plant mitochondrial terminal oxidases to the lipid peroxidation product 4-hydroxy-2-nonenal (HNE). Biochemical Journal 387 865–870.[CrossRef][Web of Science][Medline]
Wingler A, Quick WP, Bungard RA, Bailey KJ, Lea PJ, Leegood RC. (1999) The role of photorespiration during drought stress: an analysis utilizing barley mutants with reduced activities of photorespiratoy enzymes. Plant, Cell and Environment 22 361–373.[CrossRef]
Yan L-J and Sohal RS. (1998) Mitochondrial adenine nucleotide translocase is modified oxidatively during aging. Proceedings of the National Academy of Sciences, USA 95 12896–12901.
Yang Z-W and Yang F-Y. (1997) Sensitivity of Ca2+ transport of mitochodria to reactive oxygen species. Bioscience Reports 17 557–567.[CrossRef][Web of Science][Medline]
Zoratti M and Szabò I. (1995) The mitochondrial permeability transition. Biochimica et Biophysica Acta 1241 139–176.[Medline]
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  I. Strodtkotter, K. Padmasree, C. Dinakar, B. Speth, P. S. Niazi, J. Wojtera, I. Voss, P. T. Do, A. Nunes-Nesi, A. R. Fernie, et al. Induction of the AOX1D Isoform of Alternative Oxidase in A. thaliana T-DNA Insertion Lines Lacking Isoform AOX1A Is Insufficient to Optimize Photosynthesis when Treated with Antimycin A Mol Plant, March 1, 2009; 2(2): 284 - 297. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 O. K. Atkin and D. Macherel The crucial role of plant mitochondria in orchestrating drought tolerance Ann. Bot., February 1, 2009; 103(4): 581 - 597. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. Weigelt, H. Kuster, T. Rutten, A. Fait, A. R. Fernie, O. Miersch, C. Wasternack, R. J. N. Emery, C. Desel, F. Hosein, et al. ADP-Glucose Pyrophosphorylase-Deficient Pea Embryos Reveal Specific Transcriptional and Metabolic Changes of Carbon-Nitrogen Metabolism and Stress Responses Plant Physiology, January 1, 2009; 149(1): 395 - 411. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. N. Laus, M. Soccio, D. Trono, L. Cattivelli, and D. Pastore Plant Inner Membrane Anion Channel (PIMAC) Function in Plant Mitochondria Plant Cell Physiol., July 1, 2008; 49(7): 1039 - 1055. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||