Alternative oxidase in higher plants, IM Juszczuk, AM Rychter

Tags: Vanlerberghe, gene expression, alternative oxidase, AOX, McIntosh, Robson & Vanlerberghe, plant respiration, Maxwell, gene transcripts, Vanlerberghe & McIntosh, expression
Content: Vol. 50 No. 4/2003 1257­1271 QUARTERLY
Review
Alternative oxidase in higher plants.
Izabela M. Juszczuk and Anna M. RychterЅ
Department of Plant Bioenergetics, Institute of Experimental Plant Biology, Warsaw University, Miecznikowa 1, 02-096 Warszawa, Poland Received: 10 August, 2003; 16 October, 2003; accepted: 14 November, 2003 Key words: alternative oxidase, mitochondrial respiratory chain, post-translational/post-transcriptional regulation, reactive oxygen species, respiration, ubiquinol Plant respiratory chain branches at the level of ubiquinone from where the electrons flow through the cytochrome pathway or to alternative oxidase. Transfer of electrons from ubiquinone to oxygen by alternative oxidase has a non-protonmotive character and, by bypassing two sites of H+ pumping in complexes III and IV, lowers the energy efficiency of respiration. In this paper we review theoretical and experimental studies about the structure and possible function of alternative oxidase. The evidence for specific gene expression dependent on the physiological, developmental and environmental conditions is also described. We underline the physiological role of alternative oxidase as a "survival" protein that allows plants to cope with the stressful environment.
Cyanide-resistant respiration was discovered at the beginning of the 20th century as a curiosity in thermogenic plants during anthesis and was later found to be a typical feature of plant respiration. The phenomenon of respiration resistant to cyanide is connected with the presence in the respiratory
chain of an additional terminal oxidase -- alternative oxidase (AOX). The presence of AOX in higher plant mitochondria poses an intriguing question regarding its regulation in vivo and the role in plant metabolism. The progress in AOX research was achieved by biochemical studies but also in a great part by
.Presented at the 39th Congress of the Polish Biochemical Society, Gdask, Poland, September 16­20, 2003. ЅAddress correspondence to Anna M. Rychter; tel.: (48 22) 554 3005; fax: (48 22) 554 2022; e-mail: [email protected] Abbreviations: AOX, alternative oxidase; HR, hypersensitive response; PCR, polymerase chain reaction; PCD, programmed cell death; Q, ubiquinone; Qr, reduced ubiquinone, ubiquinol; ROS, reactive oxygen species; SA, salicylic acid.
1258
I.M. Juszczuk and A.M. Rychter
2003
the identification of AOX gene families and the utilization of transgenic plants with altered levels of AOX to study the regulation of its expression. The progress included an increased understanding of the biochemical/metabolic mechanisms regulating AOX activity (McDonald et al., 2002; Millar et al., 1993; Umbach & Siedow, 1993; Vanlerberghe & McIntosh, 1997). Several excellent reviews in the last few years have covered the subject of structure, regulation and the possible role of AOX in plant mitochondria (Vanlerberghe & McIntosh, 1997; Berthold et al., 2000; Siedow & Umbach, 2000; Affourtit et al., 2002; Considine et al., 2002; McDonald et al., 2002; Berthold & Stenmark, 2003). For most species examined under particular stress influence and/or growth conditions AOX presence is indicated by combination of biochemical (oxygen isotope discrimination and maximum activity/capacity) and molecular assays (AOX transcript level, protein level) (McDonald et al., 2002, and references
therein). More often AOX is studied in details using transgenic plants or in vitro cell cultures. Most information on AOX genes and AOX regulation comes from experiments on Sauromatum guttatum, Arabidopsis thaliana, Glycine max, Pisum sativum and Nicotiana tabacum. Although we have learnt a lot about the molecular nature of the alternative oxidase its role in plant respiratory metabolism is still a matter of debate. The present review summarises our present knowledge and understanding of the regulation and role of alternative oxidase in higher plant respiration. STRUCTURE AND REGULATION OF ACTIVITY AOX branches from the main respiratory chain at the level of ubiquinone and catalyses the four-electron reduction of oxygen to water (Fig. 1). In contrast to electron transfer by the
Figure 1. Alternative oxidase in plant mitochondrial respiratory chain. Alternative oxidase catalyzes cyanide-resistant reduction of oxygen to water without translocation of protons across the inner mitochondrial membrane, and thus functions as a non-energy-conserving component of the respiratory electron transfer chain. I, NADH -- ubiquinone oxidoreductase; II, succinate -- ubiquinone oxidoreductase; III, ubiquinol -- cytochrome c oxidoreductase; IV, cytochrome c oxidase; V, ATP synthase; AOX, alternative oxidase; c, cytochrome c; QH2, ubiquinol (reduced ubiquinone); ND ex/in, NAD(P)H dehydrogenases, respectively external/internal.
Vol. 50
Regulation and role of alternative oxidase in higher plant respiration
1259
cytochrome chain (complex III and IV), AOX does not pump H+, so the transfer of electrons by AOX does not generate a transmembrane potential and the drop in free energy between ubiquinol and oxygen is dissipated, or `wasted', as heat (Vanlerberghe & McIntosh, 1997). The enzyme remains difficult to purify to homogeneity in a stable, active form (Berthold & Siedow, 1993; Bonner et al., 1986; Elthon & McIntosh, 1987; Huq & Palmer, 1978; Zhang et al., 1996). However, a few models of AOX structure delivered from complete cDNA sequences encoding the alternative oxidase protein have been presented during the last decade. It was proposed (Umbach & Siedow, 1993; Siedow et al., 1995) that AOX is an approximately 32-kDa homodimeric integral mitochondrial inner membrane protein with a non-haem di-iron centre and two membranespanning helices connected by a single a-helix at the inter-membrane space. Subsequently, in 1999, it was pointed out by Andersson and Nordlund that this model was not in agreement with the structure of other well-characterized di-iron proteins. The revised model considered AOX not as a trans-membrane protein but rather an interfacial protein peripherally associated with the matrix side of the inner membrane (Andersson & Nordlund, 1999; Siedow & Umbach, 2000). Such a location is generally supported by site-directed mutagenesis experiments (Albury et al., 2002). However, the question is, to what extent is the structure of AOX as a di-iron centre interfacial mitochondrial protein conserved? (Affourtit et al., 2002; Moore et al., 2002; Berthold and Stenmark, 2003). Studies in vitro showed that the activity of AOX increased considerably upon reduction of the intersubunit disulfide bridge, yielding a non-covalently linked homodimeric protein (Umbach & Siedow, 1993; Umbach et al., 1994). The reduced enzyme is further activated by a-keto acids, particularly pyruvate, which forms a thiohemiacetal with a protein-derived sulfhydryl moiety (Umbach &
Siedow, 1996; Rhoads et al., 1998; Umbach et al., 2002). The suggested catalytic site of AOX activation by a-keto acids involves at least one cysteine residue, highly, but not universally, conserved in the known plant AOX sequences (Affourtit et al., 2002; Umbach et al., 2002). The structure of the ubiquinone (Q) binding site(s) of AOX was proposed by Berthold et al. (1998; 2000). It is based on the similarity in structure and chemical catalysis between AOX and the R2-type di-iron proteins (Berthold & Stenmark, 2003). The two electrons needed to reduce the diferric centre of AOX would be delivered from reduced ubiquinone (Berthold et al., 2000). A similar model of the AOX catalytic cycle was presented by Affourtit et al. (2002) and contained the analogues of the hydroxylase component of methane monooxygenase (MMOH) and AOX binuclear centre. Analysis of site-directed mutant proteins in combination with the recent development of more efficient bacterial over-expression systems should help test the structural and functional hypotheses. GENE EXPRESSION AOX in higher plants is encoded by the nuclear genome (Elthon et al., 1989). The first AOX antibody was raised against the protein isolated from Sauromatum guttatum and gene (AOX1) was cloned (Elthon et al., 1989; Rhoads & McIntosh, 1991). By the use of techniques such as cDNA library screening, PCR (polymerase chain reaction) with primers designed from highly conserved regions or complementation methods, AOX was found to be encoded by a small family of nuclear genes (subfamilies AOX1, AOX2a and AOX2b, formerly named AOX3) among a wide variety of nonthermogenic monocotyledon and eudicotyledon plants (Considine et al., 2002, and references therein). Differential expression of the soybean (G. max) genes in response to developmental cues, environmental perturba-
1260
I.M. Juszczuk and A.M. Rychter
2003
tions or site-directed mutagenesis was studied (Millar & Day, 1997; Finnegan et al., 1997; 1998; McCabe et al., 1998; Karpova et al., 2002). During soybean development two AOX2-type isoenzymes, AOX2-a and AOX2-b, have been described (Finnegan et al., 1997; McCabe et al., 1998). The AOX1 gene is most widely known for its expression by stress stimuli in many tissues and is present in both monocotyledon and eudicotyledon Plant species. On the other hand, the AOX2 gene is usually constitutively or developmentally expressed in eudicotyledon species but is absent from the genomes of all monocotyledon species examined to date (Considine et al., 2002, and references therein). There is a need to investigate the apparent absence of the AOX2 gene from monocotyledon plants. It has been proposed that AOX1 gene expression constitutes the plant's adaptation to stress factors whereas AOX2 expression depends on the tissue and developmental stage and is required for a "housekeeping" function in respiratory metabolism but does not respond to stress (Vanlerberghe & McIntosh, 1997; Considine et al., 2002). Among other species the soybean and A. thaliana gene expression is best characterised and fits this model. In these plants AOX1 gene expression is limited to conditions of extreme environmental stress, whereas AOX2 is not induced by stress but is expressed during normal seed development (Finnegan et al., 1997; McCabe et al., 1998; Millar et al., 1997; Saisho et al., 1997; 2001a; 2001b; Simons et al., 1999; Tanudji et al., 1998; 1999). The background of the studies of AOX genes and their expression were recently summarised in details (Vanlerberghe & McIntosh, 1997; Simons & Lambers, 1999; McDonald et al., 2002). Alternative oxidase gene expression under a variety of biotic and/or abiotic stress conditions indicates that AOX belongs to the stress-induced plant proteins but its constitutive presence in some tissues determines its potential role in integrated plant
metabolism. Several environmental as well as developmental conditions involve changes in AOX mRNA, protein, and/or cyanide-resistant respiration. These are, for example, pathogen infections (Simons et al., 1999; Maxwell et al., 2002; Ordog et al., 2002), freezing injury, cold (Vanlerberghe & McIntosh, 1992; Purvis & Shewfelt, 1993), phosphate deficiency (Parsons et al., 1999; Juszczuk et al., 2001), changes in oxygen concentration (Szal et al., 2003) and also flowering (Raskin et al., 1987), ageing (Hisher & McIntosh, 1990; Maxwell et al., 2002), and fruit ripening (Cruz-Hernandez & Gomez-Lim, 1995; Considine et al., 2001). However, in some stresses like cold, it has been reported that AOX is not always induced (Gonzales-Meler et al., 1999; Svensson et al., 2002). Based on a sophisticated molecular approach it has been shown how AOX gene expression may change in response to an experimental treatment in a developmental-specific, tissue-specific, and stress-specific manner. In S. guttatum, mRNA for AOX1 increased before thermogenesis and after application of salicylic acid to the immature appendix (Rhoads & McIntosh, 1992). In Arabidopsis the concentration of mRNA for AOX changed in response to inhibitors of electron transport or ATP synthesis (Saisho et al., 1997; 2001a; 2001b). In soybean (Finnegan et al., 1997; McCabe et al., 1998) the expression of three AOX genes in the roots and cotyledons differs in the amount of particular gene transcripts and protein levels. In soybean cotyledons the relative amount of both AOX2 transcripts and protein increase upon greening of dark-grown seedlings (McCabe et al., 1998). In potato, AOX mRNA and AOX protein accumulate during ageing (Hisher & McIntosh, 1990). Under phosphate deficiency in bean roots the level of AOX protein increased (Juszczuk et al., 2001). In contrast to the common reaction to stress factors of inducing AOX (see the references above), low oxygen conditions caused no change in AOX transcript but a large decrease in AOX protein
Vol. 50
Regulation and role of alternative oxidase in higher plant respiration
1261
level and AOX activity in barley roots (Szal et al., 2003). During the last decade, alternative oxidase gene(s) expression has been specifically altered through genetic transformations in both "sense" and "antisense" orientations. The most popular model system is the sense and antisense tobacco lines (Vanlerberghe et al., 1994; 1998; 2002; Parsons et al., 1999; Yip & Vanlerberghe, 2001; Robson & Vanlerberghe, 2002). Other transgenic plant systems have been also constructed with potato mutants (Hisher et al., 1996) and Arabidopsis mutants (Johnson-Potter et al., 2001). Comparison of plant phenotypes and changes in the respiratory metabolism between wild-type and AOX gene-mutated plants would be useful to provide insight into the physiological role of AOX. SIGNAL TRANSDUCTION FROM MITOCHONDRIA TO THE NUCLEUS AOX is induced not only in response to different environmental stress factors but also as a result of inhibition of the respiratory chain in vivo or in vitro (Vanlerberghe & McIntosh, 1997, and references therein). Experiments with respiratory-deficient mutants combined with inhibitors treatment indicate that the AOX gene expression pattern is specific for the type of mitochondrial respiratory chain modifications (Karpova et al., 2002). The NADH dehydrogenase-defective maize NCS2 mutant has high expression of AOX2a, whereas the cytochrome oxidase-defective NCS6 mutant predominantly expresses AOX2b (formerly named AOX3). Similarly, AOX2a and AOX2b (AOX3) can be induced differentially in normal maize seedlings by rotenone or KCN, specific inhibitors of these complexes (Karpova et al., 2002). There is increasing evidence suggesting signal transduction from stressed mitochondria to the nucleus for transcription of genes whose products (among them AOX) are
needed to cope with altered metabolic conditions. Partition of electrons between the cytochrome chain and alternative oxidase is highly regulated and influenced by stress conditions. This implies that the signal inducing the expression of AOX gene(s) is perceived in the mitochondrion and transmitted to the nucleus (McIntosh et al., 1998). While AOX protein concentration and AOX activity are generally low in unstressed plants, both increase when plants are subjected to suboptimal conditions such as, for example, chilling (Purvis & Shewfelt, 1993), pathogen attack (Simons et al., 1999), or phosphate deficiency (Parsons et al., 1999; Juszczuk et al., 2001). Most if not all stress conditions induce oxidative stress resulting in an increased formation of reactive oxygen species (ROS) by the mitochondrial respiratory chain. In non-photosynthetic tissues ROS are thought to arise mainly from mitochondria and function as second messengers (McIntosh et al., 1998; Maxwell et al., 1999; Mrller, 2001; Maxwell et al., 2002). Several experimental observations suggest a role of ROS in the increase of the alternative oxidase protein. Addition of 1 mM H2O2 to cultured Petunia hybrida cells resulted in a strong induction of the AOX protein (Wagner & Krab, 1995; Wagner & Wagner, 1995). In tobacco suspension cells addition of 5 mM H2O2 caused a considerable increase in AOX1 mRNA levels and AOX capacity (defined as salicylhydroxamic acid (SHAM)-sensitive O2 uptake in the presence of KCN) (Vanlerberghe & McIntosh, 1996). As shown earlier genetic alteration of the level of AOX protein in transgenic tobacco was sufficient to alter the capacity for AOX respiration (Vanlerberghe et al., 1994). It was demonstrated on intact plant cells that restriction of the cytochrome chain exacerbated mitochondrial ROS levels and that over-expression of AOX decreased ROS formation (Maxwell et al., 1999). Treatment of tobacco cells with mitochondrial electron transport inhibitor antimycin A (AA) caused a rapid AOX gene expression (Vanlerberghe et al.,
1262
I.M. Juszczuk and A.M. Rychter
2003
1994; 2002) probably mediated by increased ROS formation (Maxwell et al., 2002; Vanlerberghe et al., 2002). When cultured tobacco cells were treated with AA, or H2O2 or salicylic acid (SA) AOX1 gene was found to be induced. Antimycin A caused the fastest induction of AOX1 while H2O2 the slowest (Maxwell et al., 2002). There was no clear correlation between the intensity of ROS formation and accumulation of AOX1 transcript. However, addition of antioxidants lowered the intracellular ROS level and inhibited AOX1 gene expression (Maxwell et al., 2002). Since ROS generation is a by-product of aerobic metabolism and its increased production is a common feature in most stresses that induce AOX1, an increase in ROS alone may not be sufficient to activate the signal transduction pathway leading to changes in gene expression and the signal transduction pathway of AOX1 induction may be more complex. Maxwell et al. (2002) suggested that neither H2O2 nor SA alter the gene expression directly but lead to a rapid rise in the intracellular ROS concentration, which causes a non-specific disruption of mitochondrial function (similarly as AA treatment). Their findings support the notion that mitochondria may serve as an intermediary in intracellular stress signalling, the nature of which remains to be established. The respiratory-deficient as well as direct AOX-gene mutants could serve as model systems for the analysis of the mitochondrial-nuclear signalling pathways. It would be interesting to determine whether the communication between the mitochondria and nucleus is a common response to mitochondrial dysfunction (for example a decrease in the activity of the cytochrome pathway caused by stressful conditions) and to other conditions not involving any obvious mitochondrial dysfunction (Robson & Vanlerberghe, 2002; Vanlerberghe et al., 2002). Biochemical and genetic studies confirm that hydrogen peroxide is a signalling molecule in plants that mediates responses to biotic and/or abiotic stresses
(Neill et al., 2002a). H2O2 modulates the expression of various genes, mainly encoding antioxidant and programmed cell death-involved enzymes (Desikan et al., 2001; BaxterBurrell et al., 2002; Neill et al., 2002b). H2O2 specific-regulatory DNA sequences and their transcription factors have not yet been isolated and characterised (Neill et al., 2002a) but it is proposed that H2O2 may directly oxidise transcription factors or modulate phosphorylation processes (Neill et al., 2002a). The synthesis and action of hydrogen peroxide and other ROS appear to be linked to those of nitric oxide (NO) (Millar & Day, 1997; Neill et al., 2002b). Treatment of Arabidopsis cell cultures with NO strongly induced AOX1a transcription (Huang et al., 2002). NO-induced AOX expression might be an important part of the cell death mechanism (Huang et al., 2002). Besides the hypothesis that H2O2 and/or other ROS regulate AOX gene expression, there are some studies indicating that the carbon flux through the TCA cycle can effectively control AOX gene expression. The almost forgotten hypothesis of citrate-induced AOX1 expression (Vanlerberghe & McIntosh, 1996) may rise again as a result of considerations that the signals influencing AOX1 gene expression are connected with the carbon and redox status of mitochondria (Vanlerberghe et al., 2002). In spite of different experiments with wild-type and AOX-mutated plants or with in vitro-cultured cells, it still needs to be established whether ROS are indeed involved in the induction of AOX as a messenger in a specific signalling pathway, or alternatively, cause cell damage involving a more general change in the cellular metabolism. POSTTRANSLATIONAL CONTROL OF ACTIVITY In a given species or tissue under specific growth conditions the abundance of AOX pro-
Vol. 50
Regulation and role of alternative oxidase in higher plant respiration
1263
tein is one of the obvious factors. However, there is no direct correlation between AOX protein abundance and its activity or "engagement" in respiration (McDonald et al., 2002). This observation suggests that partitioning of electrons to AOX is primarily determined by posttranslational mechanisms. In vitro substrate level, ubiquinone (Q) concentration and its redox poise, the redox state of AOX itself and a-keto acids, (mainly pyruvate) are factors regulating AOX activity (Millar et al., 1996; Vanlerberghe & McIntosh, 1997; Siedow & Umbach, 2000; Affourtit et al., 2002; McDonald et al., 2002; Umbach et al., 2002). Since reduced ubiquinone (Qr, ubiquinol) is the common substrate of the cytochrome chain and alternative oxidase, the absolute concentration of Qr and/or the redox state of total Q are thought to be important factors regulating AOX activity. However, in the presence of pyruvate AOX becomes active at a much lower level of ubiquinone reduction than in the absence of pyruvate (Hoefnagel et al., 1995). Voltametric assays (Moore et al., 1988) as well as organic extraction and HPLC analysis (Ribas-Carbo et al., 1995; Wagner & Wagner, 1995; Millar et al., 1998; Millenaar et al., 2001) were performed to study the redox state of Q pool in isolated mitochondria and intact cells or tissues. The results indicate in general that Q redox state remains remarkably constant over a wide range of AOX engagement in respiration. A second biochemical regulatory mechanism of AOX activity concerns the fact that AOX exists as a homodimer, where the subunits are linked in a reversible manner by a disulphide bond (Umbach & Siedow, 1993; Umbach et al., 1994; Vanlerberghe et al., 1995). The relative amount of oxidized dimer appears to depend on the redox state of the mitochondrial pyridine nucleotide pool and may change quickly in response to mitochondrial metabolism (Vanlerberghe et al., 1995). The Cys-residue responsible for this redox regulation was determined using site-directed mutagenesis (Rhoads et al., 1997; 1998;
Vanlerberghe et al., 1998). The regulatory cysteine corresponds to the more N-terminal of the two highly, but not universally, conserved cysteines found among plant alternative oxidase sequences (Siedow & Umbach, 2000). When alternative oxidase is reduced, the enzyme can be activated by pyruvate (Millar et al., 1993; Day et al., 1994; Umbach et al., 1994; 2002; Vanlerberghe et al., 1999; Siedow & Umbach, 2000). The amino-acid residue at which this regulatory feature operates is that forming the covalent association of the two AOX subunits (Umbach & Siedow, 1996; Rhoads et al., 1997; 1998; Berthold et al., 2000; Affourtit et al., 2002). Pyruvate forms thiohemiacetal with cysteine sulfydryl. This results in the introduction of a negatively charged carboxylate (Umbach & Siedow, 1996; Umbach et al., 2002). The regulatory mechanisms in vitro suggest that pyruvate concentration in the mitochondrial matrix as well as matrix redox State control AOX engagement in respiration (Umbach & Siedow, 1996; Juszczuk et al., 1998; Djajanegara et al., 1999; Vanlerberghe et al., 1999; Umbach et al., 2002). However, the importance of this type of regulation for the functioning of alternative oxidase in vivo is still unclear (McDonald et al., 2002; Millar et al., 1998; Umbach et al., 2002). No experimental approaches to readily manipulate and measure these matrix parameters (and their effects on AOX engagement) in vivo have been reported (Millenaar et al., 2001; McDonald et al., 2002; Umbach et al., 2002). Future experiments to investigate the importance of the regulatory mechanisms in vivo must utilize transgenic plants expressing mutated AOX proteins with altered in organello regulatory properties (McDonald et al., 2002; Umbach et al., 2002). Obviously, the study of AOX posttranslational regulation would be aided by purification of the active enzyme as well as by improvements in the sophisticated systems for heterologous expression of plant AOX in bacteria and yeast systems (McDonald et al., 2002).
1264
I.M. Juszczuk and A.M. Rychter
2003
PHYSIOLOGICAL ROLE IN PLANT OXIDATIVE METABOLISM AOX has been recognized to act as an overflow mechanism (Lambers, 1985), also as a enzyme limiting mitochondrial ROS production (Mrller, 2001; Purvis & Shewfeld, 1993) and more recently the role AOX was described as part of a plant's ability to regulate energy balance in response to a changing environment (Hansen et al., 2002; Moore et al., 2002). The only confirmed function for respiration with AOX engagement is the thermogenesis in Araceae species where the heat produced during anthesis mobilises aromatic compounds to attract pollinators (Meeuse, 1975; Skubatz et al., 1993). In spite of very intensive studies on the structure and regulation of alternative oxidase (at the gene and protein level) its function in vivo in non-thermogenic tissues remains unclear. Considering the possible role of AOX in plant metabolism it is important to take into account the nonphosphorylating nature of AOX and its operation during periods of high rates of substrate oxidation (Simons & Lambers, 1999). Moreover, the results of a wide range of experiments indicate that AOX is a "stress-induced protein" because of its expression under several stressful treatments, such as chilling, wounding, drought, osmotic and nutrient stress and pathogen attack. It is also clear that any restriction (inhibition and/or decrease) of cytochrome c oxidase activity induces AOX (Moore et al., 2002; Vanlerberghe & McIntosh, 1997). The 20-year-old hypothesis of AOX as an "energy overflow" (Lambers, 1985) is still generally accepted with the one modification that AOX can compete for and share electrons with cytochrome c oxidase (Hoefnagel et al., 1995; Day et al., 1996; Simons & Lambers, 1999). Given the biochemical controls of the alternative oxidase enzyme, any metabolic condition that leads to accumulation of either reduced ubiquinone, mitochondrial pyridine
nucleotides, or pyruvate, citrate and other organic acids has the potential to increase electron flow to the alternative pathway. The function of AOX as an "overflow" may therefore be to balance carbon metabolism and electron transport (co-ordinated regulation between the upstream respiratory carbon metabolism and the downstream electron transport) (Vanlerberghe & McIntosh, 1997; Simons & Lambers, 1999; Moore et al., 2002, and references therein). Tightly connected with the "energy overflow" is the "energy overcharge" hypothesis (De Visser et al., 1986). The ability of the mitochondrial electron transport to adjust its capacity rapidly via activation of alternative pathway may have at least two important consequences for plant metabolism. First, if cells require a large amount of carbon skeletons, but do not have a high demand for ATP, AOX allows operation of tricarboxylic acid cycle with minimal ATP synthesis (Simons & Lambers, 1999). Second, AOX may prevent over-reduction of the respiratory chain components that might otherwise result in the formation of harmful ROS (Mrller, 2001; Vanlerberghe & McIntosh, 1997). It has been proposed that AOX plays a role in avoidance of damage to the cell by ROS (Maxwell et al., 1999; Mrller, 2001; Parsons et al., 1999; Purvis & Shewfelt, 1993; Robson & Vanlerberghe, 2002; Yip & Vanlerberghe, 2001). In the mitochondrial respiratory chain AOX effectively allows the interaction of molecular oxygen with reduced ubiquinone (ubiquinol). Such a mechanism of the prevention of "long life" of ubiquinol is one way to minimize ROS production (Mrller, 2001). In vitro experiments with tobacco AOX mutants showed that cells in which AOX had been overexpressed contained half as much ROS as control cells (Maxwell et al., 1999). In contrast, cells in which the expression of AOX had been reduced by antisensing contained five times more ROS than control cells. The AS8 antisense tobacco AOX mutant generates about twice as much ROS as wild
Vol. 50
Regulation and role of alternative oxidase in higher plant respiration
1265
wide-type cells during phosphate starvation as well as under control conditions (Parsons et al., 1999; Yip & Vanlerberghe, 2001). The authors suggest that induction of AOX respiration in cell culture is an important metabolic adaptation to phosphate limitation. Evidence of AOX involvement together with symptoms of oxidative stress during acclimation to phosphate deficiency were also observed for bean plants in vivo (Juszczuk et al., 2001). Generation of ROS and oxidative stress in plants have been implicated in biotic and abiotic stresses (Mrller, 2001; Tiwari et al., 2002). Very often the increased ROS formation results in the induction of programmed death of individual cells or groups of the cells in a tissue. The potential role of mitochondria in the integration of the cellular stress and regulation of programmed cell death (PCD) has been suggested (Sun et al., 1999; Jones, 2000; Lam et al., 2001). A few studies have implicated the role of AOX in plant PCD (Lacomme & Roby, 1999; Maxwell et al., 2002; Ordog et al., 2002; Robson & Vanlerberghe, 2002; Vanlerberghe et al., 2002). In Arabidopsis AOX genes are induced early in hypersensitive response (HR) (Lacomme & Roby, 1999). Transgenic tobacco lacking AOX showed increased susceptibility to three different death-inducing compounds (H2O2, salicylic acid and the protein phosphatase inhibitor cantharidin) in comparison with wild-type cells (Robson & Vanlerberghe, 2002). Ordog et al. (2002) found that overexpression of AOX in S24 tobacco mutants reduced the size of HR lesions. But, in the same tobacco cells with enhanced susceptibility to tobacco mosaic virus infection, the overexpression of AOX did not significantly increase viral resistance. Vanlerberghe et al. (2002) showed that loss of the cytochrome pathway induced by cysteine or antimycin treatment in AS8 cells unable to induce AOX (due to the presence of an antisense transgene) causes a complete loss of respiratory capacity and results in massive cell death. Higher levels of AOX pro-
tein after anoxic treatment of soybean cells correlated with increased resistance to H2O2-induced PCD (Amor et al., 2000). It has been suggested that the ability of AOX to attenuate cell death might relate to its ability to generate small amounts of ATP (during NADH oxidation by complex I) (Vanlerberghe et al., 2002). Moreover, AOX may dampen the excessive mitochondrial generation of ROS by preventing over-reduction of the respiratory chain complexes (Mrller 2001, Vanlerberghe et al., 2002). The hypothesis of the role of AOX in oxidative stress defence has an evolutionary background with the postulated early function of AOX in di-oxygen scavenging (Gomes et al., 2001). The primary structure of AOX suggests that it belongs to the di-iron carboxylate family and an evolutionary relationship with primitive members of that family (Moore et al., 2002). However, plant cell have a more efficient ROS-scavenging system consisting of haem-copper enzymes (catalases, peroxidases, dismutases). Moore et al. (2002) ask the question: "if the scavenging of di-oxygen is not the principle function of the alternative oxidase, what is its role?" Hansen et al. (2002) suggest that the present-day function of alternative oxidase is to allow flexible control of ATP synthesis to maintain growth rate homeostasis. This is in agreement with the hypothesis that AOX takes part in the plant stress-acclimation process as a "survival protein" (Robson & Vanlerberghe, 2002). AOX protein is induced during plant response to nutritional phosphate deprivation (Juszczuk et al., 2001), and in green pepper under cold stress (Purvis & Shewfelt, 1993), as a result of PCD occurring during plant development and in response to biotic stress (Beers & McDowell, 2001), for example the HR response (Alvarez, 2000). It appears that the non-protonmotive nature of AOX allows a flexible and rapid adaptation of mitochondria to maintain relatively stable energy charge and, consequently, to maintain the growth rate under variable environmental conditions (Moore et al., 2002).
1266
I.M. Juszczuk and A.M. Rychter
2003
The potential role of AOX is obviously even more complicated in green tissues because of the evident interaction between mitochondria and chloroplasts in ATP and reducing power utilisation. Igamberdiev et al. (1997) proposed that AOX could participate in photorespiratory glycine oxidation helping to maintain the ATP/ADP ratio and oxidizing NADH. In potato AOX showed induction in mature leaves and light dependence indicating its role in photosynthetically associated mitochondrial metabolism (Svensson & Rasmusson, 2001). Most hypotheses for the role of AOX in plant metabolism are based on in vitro experiments of using cell cultures. future studies should verify whether the mechanisms of AOX regulation in vivo are the same. Transgenic plants with altered AOX expression and in vivo examination of the interactions between the organelles will help to understand the role of AOX in plant metabolism. Moreover, in addition to alternative oxidase, plant mitochondria contain uncoupling proteins (Vercesi et al., 1995) which also dissipate energy. The functioning of the two systems of modification of plant cell energy status also remains to be studied. REFERENCES Affourtit C, Albury MS, Crichton PG, Moore AL. (2002) Exploring the molecular nature of alternative oxidase regulation and catalysis. FEBS Lett.; 510: 121­6. Albury MS, Affourtit C, Crichton PG, Moore AL. (2002) Structure of the plant alternative oxidase -- site-directed mutagenesis provides new information on the active site and membrane topology. J Biol Chem.; 277: 1190­4. Alvarez ME. (2000) Salicylic acid in the machinery of hypersensitive cell death and disease resistance. Plant Mol Biol.; 44: 429­42. Amor Y, Chevion M, Levine A. (2000) Anoxia pre-treatment protects soybean cells against H2O2-induced cell death: possible involve-
ment of peroxidases and of alternative oxidase. FEBS Lett.; 477: 175­80. Andersson ME, Nordlund P. (1999) A revised model of the active site of alternative oxidase. FEBS Lett.; 449: 17­22. Baxter-Burrell A, Yang Z, Springer PS, Bailley-Serres J. (2002) RopGAP4-dependent Rop GTPase rheostat control of Arabidopsis oxygen deprivation tolerance. Science.; 296: 2026­8. Beers EP, McDowell JM. (2001) Regulation and execution of programmed cell death in response to pathogens, stress and developmental cues. Curr Opin Plant Biol.; 4: 561­7. Berthold DA. (1998) Isolation of mutants of the Arabidopsis thaliana alternative oxidase (ubiquinol:oxygen oxidoreductase) resistant to salicylhydroxamic acid. Biochim Biophys Acta.; 1364: 73­83. Berthold DA, Siedow JN. (1993) Partial purification of the cyanide-resistant alternative oxidase of skunk cabbage (Symplocarpus foetidus) mitochondria. Plant Physiol.; 101: 113­9. Berthold DA, Stenmark P. (2003) Membrane-bound di-iron carboxylate proteins. Annu Rev Plant Biol.; 54: 497­517. Berthold DA, Andersson ME, Nordlund P. (2000) New insight into the structure and function of the alternative oxidase. Biochim Biophys Acta.; 1460: 241­54. Bonner WD, Clarke SD, Rich PR. (1986) Partial purification and characterization of the quinol oxidase activity of Arum maculatum mitochondria. Plant Physiol.; 80: 838­42. Considine MJ, Daley DO, Whelan J. (2001) The expression of alternative oxidase and uncoupling protein during fruit ripening in mango. Plant Physiol.; 126: 1619­29. Considine MJ, Holtzapffel RC, Day DA, Whelan J, Millar AH. (2002) Molecular distinction between alternative oxidase from monocots and dicots. Plant Physiol.; 129: 949­53. Cruz-Hernandez A, Gomez-Lim MA. (1995) Alternative oxidase from mango (Magnifera in-
Vol. 50
Regulation and role of alternative oxidase in higher plant respiration
1267
dica L.) is differentially regulated during fruit ripening. Planta.; 197: 569­76. Day DA, Millar AH, Wiskich JT, Whelan J. (1994) Regulation of alternative oxidase activity by pyruvate in soybean mitochondria. Plant Physiol.; 106: 1421­7. Day DA, Krab K, Lambers H, Moore AL, Siedow JN, Wagner AM, Wiskich JT. (1996) The cyanide-resistant oxidase: to inhibit or not to inhibit, that is the question. Plant Physiol.; 110: 1­2. De Visser R, Spreen Brouwer K, Posthumus F. (1986) Alternative path mediated ATP synthesis in roots of Pisum sativum upon nitrogen supply. Plant Physiol.; 80: 295­300. Desikan R, Mackerness AH, Hancock JT, Neill SJ. (2001) Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol.; 127: 159­72. Djajanegara I, Holtzapffel R, Finnegan PM, Hoefnagel MHN, Berthold DA, Wiskich JT, Day DA. (1999) A single amino acid change in the plant alternative oxidase alters the specificity of organic acid activation. FEBS Lett.; 454: 220­4. Elthon TE, McIntosh L. (1987) Identification of the alternative terminal oxidase of higher plant mitochondria. Proc Natl Acad Sci U S A.; 84: 8399­403. Elthon TE, Nickels RL, McIntosh L. (1989) Monoclonal antibodies to the alternative oxidase of higher plant mitochondria. Plant Physiol.; 89: 1311­7. Finnegan PM, Whelan J, Millar AH, Zhang Q, Smith MK, Wiskich JT, Day DA. (1997) Differential expression of the multigene family encoding the soybean mitochondrial alternative oxidase. Plant Physiol.; 114: 455­66. Finnegan PM, Djajanegara IN, Schuller LJ, Smith MK, Whelan J, Day DA. (1998) Analysis of the antimycin A-inducible promoter region of soybean GmAOX1. In Plant mitochondria: from gene to function. Mцller IM, Gardestrцm P, Glimelius K, Glaser E, eds, pp 449­53. Backhuys Publishers, Leiden, The Netherlands.
Gomes CM, Le Gall J, Xavier AV, Teixeira M. (2001) Could a diiron-containing four-helix bundle protein have been a primitive oxygen reductase? Chem Biochem.; 7­8: 583­7. Gonzalez-Meler MA, Ribas-Carbo M, Giles L, Siedow JN. (1999) The effect of growth and measurment temperature on the activity of the alternative respiratory pathway. Plant Physiol.; 120: 765­72. Hansen LD, Church JN, Matheson S, McCarlie VW, Thygerson T, Criddle RS, Smith BN. (2002) Kinetics of plant growth and metabolism. Thermochim Acta.; 388: 415­25. Hisher C, McIntosh L. (1990) Alternative oxidase of potato is an integral membrane protein synthesized de novo during ageing of tuber slices. Plant Physiol.; 93: 312­8. Hisher C, Kapranov P, McIntosh L. (1996) genetic modification of respiratory capacity in potato. Plant Physiol.; 110: 277­86. Hoefnagel MHN, Millar AH, Wiskich JT, Day DA. (1995) Cytochrome and alternative respiratory pathways compete for electrons in the presence of pyruvate in soybean mitochondria. Archiv Biochem Biophys.; 318: 394­400 Huang X, von Rad U, Durner J. (2002) Nitric oxide induces transcriptional activation of the nitric oxide-tolerant alternative oxidase in Arabidopsis suspension cells. Planta.; 215: 914­23. Huq S, Palmer JM. (1978) Isolation of a cyanide-resistant duroquinol oxidase from Arum maculatum mitochondria. FEBS Lett.; 95: 217­20. Igamberdiev AU, Bykova NU, Gardestrцm P. (1997) Involvement of cyanide-resistant and rotenone-insensitive pathways of mitochondrial electron transport during oxidation of glycine in higher plants. FEBS Lett.; 412: 265­9. Johnson-Potter F, Wiskich JT, Dry IB. (2001) The production of an inducible antisense alternative oxidase (Aox1a) plant. Planta.; 212: 215­21. Jones A. (2000) Does the plant mitochondrion integrate cellular stress and regulate pro-
1268
I.M. Juszczuk and A.M. Rychter
2003
grammed cell death? Trends Plant Sci.; 5: 225­30. Juszczuk IM, Malusa E, Rychter AM. (1998) Alternative oxidase from phosphate-deficient bean roots. In Plant mitochondria: from gene to function. Mrller IM, Gardestrцm P, Glimelius K, Glaser E, eds, pp 481­5. Backhuys Publishers, Leiden, the Netherlands. Juszczuk IM, Wagner AM, Rychter AM. (2001) Regulation of alternative oxidase activity during phosphate deficiency in bean roots (Phaseolus vulgaris). Physiol Plant.; 113: 185­92. Karpova OV, Kuzmin EV, Elthon TE, Newton KJ. (2002) Differential expression of alternative oxidase genes in maize mitochondrial mutants. Plant Cell.; 14: 3271­84. Kearns A, Whelan J, Young S, Elthon TE, Day DA. (1992) Tissue-specific expression of the alternative oxidase in soybean and sirato. Plant Physiol.; 99: 712­7. Lacomme C, Roby D. (1999) Identification of new early markers of the hypersensitive response of Arabidopsis thaliana. FEBS Lett.; 459: 149­53. Lam E, Kato N, Lawton M. (2001) Programmed cell death, mitochondria and the plant hypersensitive response. Nature.; 411: 848­53. Lambers H. (1985) Respiration in intact plants and tissues: its regulation and dependence on environmental factors, metabolism and invited organisms. In Encyclopedia of Plant Physiology, new series 18. Douce CR, Day DA, eds, pp 444­8. Springer Verlag, Berlin. Maxwell DP, Wang Y, McIntosh L. (1999) The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc Natl Acad Sci U S A.; 96: 8271­6. Maxwell DP, Nickels R, McIntosh L. (2002) Evidence of mitochondrial involvement in the transduction of signals required for the induction of genes associated with pathogen attack and senescence. Plant J.; 29: 269­79. McCabe TC, Finnegan PM, Millar AH, Day DA, Whelan J. (1998) Differential expression of
alternative oxidase genes in soybean cotyledons during postgerminative development. Plant Physiol.; 118: 675­82. McDonald AE, Sieger SM, Vanlerberghe GC. (2002) Methods and approaches to study plant mitochondrial alternative oxidase. Physiol Plant.; 116: 135­43. McIntosh L, Eichler G, Gray G, Maxwell D, Nickels R, Wang Y. (1998) Biochemical and genetic controls exerted by plant mitochondria. Biochim Biophys Acta.; 1365: 278­84. Meeuse BDJ. (1975) Thermogenic respiration in aroids. Annu Rev Plant Physiol.; 26: 117­26. Millar AH, Day DA. (1997) Alternative solutions to radical problems. Trends Plant Sci.; 2: 155­8. Millar AH, Hoefnagel MHN, Day DA, Wiskich JT. (1996) Specificity of the organic acid activation of alternative oxidase in plant mitochondria. Plant Physiol.; 111: 613­8. Millar AH, Wiskich JT, Whelan J, Day DA. (1993) Organic acid activation of the alternative oxidase of plant mitochondria. FEBS Lett.; 329: 259­62. Millar AH, Finnegan PM, Whelan J, Drevon JJ, Day DA. (1997) Expression and kinetics of the mitochondrial alternative oxidase in nitrogen-fixing nodules of soybean roots. Plant Cell Environ.; 20: 1273­82. Millar AH, Atkin OK, Menz RI, Henry B, Farquhar G, Day DA. (1998) Analysis of respiratory chain regulation in roots of soybean seedlings. Plant Physiol.; 117: 1083­93. Millenaar FF, GonzBlez-Meler MA, Fiorani F, Welschen R, Ribas-Carbo M, Siedow JN, Wagner AM, Lambers H. (2001) Regulation of alternative oxidase activity in six wild monocotyledonous species. An in vivo study at the whole root level. Plant Physiol.; 126: 376­87. Mrller IM. (2001) Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu Rev Plant Physiol Plant Mol Biol.; 52: 561-91.
Vol. 50
Regulation and role of alternative oxidase in higher plant respiration
1269
Moore AL, Dry IB, Wiskich JT. (1988) Measurement of the redox state of the ubiquinone pool in plant mitochondria. FEBS Lett.; 235: 76­80. Moore AL, Albury MS, Crichton PG, Affourtit C. (2002) Function of the alternative oxidase: is it still a scavenger? Trends Plant Sci.; 7: 478­81. Neill S, Desikan R, Hancock J. (2002a) Hydrogen peroxide signalling. Curr Opin Plant Biol.; 5: 388­95. Neill SJ, Desikan R, Clarke A, Hurst RD, Hancock JT. (2002b) Hydrogen peroxide and nitric oxide as signalling molecules in plants. J Exp Bot.; 53: 1237­47. Ordog SH, Higgins VJ, Vanlerberghe GC. (2002) Mitochondrial alternative oxidase is not a critical component of plant viral resistance but may play a role in the hypersensitive response. Plant Physiol.; 129: 1858­65. Parsons HL, Yip JYH, Vanlerberghe GC. (1999) Increased respiratory restriction during phosphate-limited growth in transgenic tobacco cells lacking alternative oxidase. Plant Physiol.; 121: 1309­20. Purvis AC, Shewfelt RJ. (1993) Does the alternative pathway ameliorate chilling injury in sensitive plant tissues? Physiol Plant.; 88: 712­8. Raskin I, Ehmann A, Melander WR, Meeuse BJD. (1987) Salicylic acid: a natural inducer of heat production in Arum lilies. Science.; 237: 1601­2. Rhoads DM, McIntosh L. (1991) Isolation and characterization of a cDNA clone encoding an alternative oxidase protein of Sauromatum guttatum (Schott). Proc Natl Acad Sci U S A.; 88: 2122­6. Rhoads DM, McIntosh L. (1992) Salicylic acid regulation of respiration in higher plants: alternative oxidase expression. Plant Cell.; 4: 1131­9. Rhoads DM, Umbach AL, Siedow JN. (1997) Identification of the alternative oxidase cysteine residue involved in regulatory disulfide bond formation. Plant Physiol.; 114: 1016.
Rhoads DM, Umbach AL, Sweet CR, Lennon AM, Rauch GS, Siedow JN. (1998) Regulation of the cyanide-resistant alternative oxidase of plant mitochondria. J Biol Chem.; 273: 30750­6. Ribas-Carbo M, Aroca R, GonzBlez-Meler MA, Irigoyen JJ, Sбnchez-Dнaz M. (1995) The electron partitioning between the cytochrome and alternative respiratory pathways during chilling recovery in two cultivars of maize differing in chilling sensitivity. Plant Physiol.; 122: 199­204. Robson CA, Vanlerberghe GC. (2002) Transgenic plant cells lacking mitochondrial alternative oxidase have increased susceptibility to mitochondria-dependent and -independent pathways of programmed cell death. Plant Physiol.; 129: 1908­20. Saisho D, Nambara E, Naito S, Tsutsumi N, Hirai A, Nakazone M. (1997) Characterization of the gene family for alternative oxidase from Arabidopsis thaliana. Plant Mol Biol.; 35: 585­96. Saisho D, Nakazono M, Tsutsumi N, Hirai A. (2001a) ATP synthesis inhibitors as well as respiratory inhibitors increase steady-state level of alternative oxidase mRNA in Arabidopsis thaliana. J Plant Physiol.; 158: 241­5. Saisho D, Nakazono M, Lee KH, Tsutsumi N, Akita S, Hirai A. (2001b) The gene for alternative oxidase-2 (AOX-2) from Arabidopsis thaliana consists of five exons unlike other AOX genes and is transcribed at an early stage during germination. Genes Genet Systems.; 76: 89­97. Siedow JN, Umbach AL. (2000) The mitochondrial cyanide-resistant oxidase: structural conservation amid regulatory diversity. Biochim Biophys Acta.; 1459: 432­9. Siedow JN, Umbach AL, Moore AL. (1995) The active site of the cyanide-resistant oxidase from plant mitochondria contains a coupled binuclear iron center. FEBS Lett.; 362: 10­14. Simons BH, Lambers H. (1999) The alternative oxidase -- is it a respiratory pathway allowing a plant to cope with stress? In Plant Re-
1270
I.M. Juszczuk and A.M. Rychter
2003
sponses to environmental stresses from phytohormones to genome reorganization. Lerener HR, eds, pp 265­86. Marcel Decker Inc. 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 Physiol.; 120: 529­38. Skubatz H, Tang W, Meeuse BJD. (1993) Oscillatory heat-production in the male cones of cycads. J Exp Bot.; 44: 489­92. Svensson AS, Johansson FI, Mrller IM, Rasmusson AG. (2002) Cold stress decreases the capacity for respiratory NADH oxidation in potato leaves. FEBS Lett.; 517: 79­82. Svensson AS, Rasmusson AG. (2001) Light-dependent gene expression for proteins in the respiratory chain of potato leaves. Plant J.; 28: 73­82. Sun YL, Zhao Y, Hong X, Zhai ZH. (1999) Cytochrome c release and caspase activation during menadione-induced apoptosis in plants. FEBS Lett.; 462: 317­21. Szal B, Jolivet Y, Hasenfrantz-Sauder M, Dizengremel P, Rychter AM. (2003) Oxygen concentration regulates alternative oxidase expression in barley roots during hypoxia and post-hypoxia. Physiol Plant.; 119: 494­502. Tanudji M, Daley DO, McCabe TC, Finnegan PM, Djajanegara IN, Day DA, Whelan J. (1998) Alternative oxidase proteins of soybean mitochondria: identification of the multiple isoforms in soybean tissues. In plant mitochondria: from gene to function. Mrller IM, Gardestrцm P, Glimelius K, Glaser E, eds, pp 525­9. Backhuys Publishers, Leiden, The Netherlands. Tanudji M, Sjцling S, Glaser E, Ehelan J. (1999) Signals required for the import and processing of the alternative oxidase into mitochondria. J Biol Chem.; 274: 1286­93. Tiwari BS, Belenghi B, Levine A. (2002) Oxidative stress increased respiration and generation of reactive oxygen species, resulting in
ATP depletion, opening of mitochondrial permeability transition, and programmed cell death. Plant Physiol.; 128: 1271­81. Umbach AL, Siedow JN. (1993) Covalent and noncovalent dimers of the cyanide-resistant alternative oxidase protein in higher plant mitochondria and their relationship to enzyme activity. Plant Physiol.; 103: 845­54. Umbach AL, Siedow JN. (1996) The reaction of the soybean cotyledon mitochondrial cyanide-resistant oxidase with sulfhydryl reagents suggests that a-keto acid activation involves the formation of a thiohemiacetal. J Biol Chem.; 271: 25019­226. Umbach AL, Wiskich JT, Siedow JN. (1994) Regulation of alternative oxidase kinetics by pyruvate and intermolecular disulfide bond redox status in soybean seedling mitochondria. FEBS Lett.; 348: 181­4. Umbach AL, GonzBlez-Meler MA, Sweet CR, Siedow JN. (2002) Activation of plant mitochondrial alternative oxidase: insights from site-directed mutagenesis. Biochim Biophys Acta.; 1554: 118­28. Vanlerberghe GC, McIntosh L. (1992) Lower growth temperature increases alternative pathway capacity and alternative oxidase protein in tobacco. Plant Physiol.; 100: 115­9. Vanlerberghe GC, McIntosh L. (1996) Signals regulating the expression of the nuclear gene encoding alternative oxidase of plant mitochondria. Plant Physiol.; 111: 589­95. Vanlerberghe GC, McIntosh L. (1997) Alternative oxidase: from gene to function. Annu Rev Plant Physiol Plant Mol Biol.; 48: 703­34. Vanlerberghe GC, Vanlerberghe AE, McIntosh L. (1994) Molecular genetic alteration of plant respiration: silencing and over-expression of alternative oxidase in transgenic tobacco. Plant Physiol.; 106: 1503­10. Vanlerberghe GC, Day DA, Wiskich JT, Vanlerberghe AE, McIntosh L. (1995) Alternative oxidase activity in tobacco leaf mitochondria: dependence on tricarboxylic acid
Vol. 50
Regulation and role of alternative oxidase in higher plant respiration
1271
cycle-mediated redox regulation and pyruvate activation. Plant Physiol.; 109: 353­61. Vanlerberghe GC, McIntosh L, Yip JYH. (1998) Molecular localisation of a redox-modulated process regulating plant mitochondrial electron transport. Plant Cell.; 10: 1551­60. Vanlerberghe GC, Yip JYH, Parsons HL. (1999) In organello and in vivo evidence of the importance of the regulatory sulfhydryl/disulfide system and pyruvate for alternative oxidase activity in tobacco. Plant Physiol.; 121: 793­803. Vanlerberghe GC, Robson CA, Yip JYH. (2002) Induction of mitochondrial alternative oxidase in response to a cell signal pathway down-regulating the cytochrome pathway prevents programmed cell death. Plant Physiol.; 129: 1829­42. Vercesi AE, Martins IS, Silva MAP, Leite HMF. (1995) PUMPing plants. Nature.; 375: 24.
Wagner AM, Krab K. (1995) The alternative respiration pathway in plants: role and regulation. Physiol Plant.; 95: 318­25. Wagner AM, Wagner MJ. (1995) Changes in mitochondrial respiratory chain components of petunia cells during culture in the presence of antimycin A. Plant Physiol.; 115: 617­22. Yip JYH, Vanlerberghe GC. (2001) Mitochondrial alternative oxidase acts to dampen the generation of active oxygen species during a period of rapid respiration induced to support a high rate of nutrient uptake. Physiol Plant.; 112: 327­33. Zhang Q, Hoefnagel MHN, Wiskich JT. (1996) Alternative oxidase from Arum and soybean: its stabilization during purification. Physiol Plant.; 96: 551­8.

IM Juszczuk, AM Rychter

File: alternative-oxidase-in-higher-plants.pdf
Title: rychter-cor.vp
Author: IM Juszczuk, AM Rychter
Author: Gosia
Published: Tue Dec 30 13:39:15 2003
Pages: 15
File size: 0.52 Mb


Without a doubt, 16 pages, 0.09 Mb

Sport and the 1916 Rising, 9 pages, 0.43 Mb

Kurzweil 3000 Version 10, 54 pages, 0.62 Mb
Copyright © 2018 doc.uments.com