Abstract
Optimization of photosynthetic performance and protection against abiotic stress are essential to sustain plant growth. Photorespiratory metabolism can help plants to adapt to abiotic stress. The beneficial role of photorespiration under abiotic stress is further strengthened by cyclic electron flow (CEF) and alternative oxidase (AOX) pathways. We have attempted to critically assess the literature on the responses of these three phenomena—photorespiration, CEF and AOX, to different stress situations. We emphasize that photorespiration is the key player to protect photosynthesis and upregulates CEF as well as AOX. Then these three processes work in coordination to protect the plants against photoinhibition and maintain an optimal redox state in the cell, while providing ATP for metabolism and protein repair. H2O2 generated during photorespiratory metabolism seems to be an important signal to upregulate CEF or AOX. Further experiments are necessary to identify the signals originating from CEF or AOX to modulate photorespiration. The mutants deficient in CEF or AOX or both could be useful in this regard. The mutual interactions between CEF and AOX, so as to keep their complementarity, are also to be examined further.
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Introduction
Plants are sessile and often exposed to stressful environments due to suboptimal or supraoptimal conditions like drought, high or low CO2, high or low light, high or low temperature, limiting N/P/K and heavy metal stress. The abiotic stress causes alterations in metabolism, nutrient uptake, growth and development. Severe stress results in damage and cell death (Wang et al. 2008; Verslues et al. 2006). The basal factor during most of the stresses is the excess production of reactive oxygen species (ROS) much more than its removal by scavenging (Miller et al. 2010; Suzuki et al. 2012). The ROS include radicals such as singlet oxygen, superoxide, hydrogen peroxide and hydroxyl radicals. Besides the accumulation of ROS, abiotic stress frequently causes an imbalance in the supply/demand of ATP/NADPH, changes in membrane structure and additional damage due to lipid peroxidation products (Mignolet-Spruyt et al. 2016). The production of ROS and the energy/redox imbalance occurs among different compartments of cell.
Plants have the ability to respond and acclimate to these adverse conditions. In order to protect themselves, plants employ adaptive mechanisms mainly to scavenge the excess ROS using antioxidants (e.g. ascorbate, glutathione, carotenoids, flavonoids) and/or antioxidant enzymes (e.g. catalase, superoxide dismutase) (Gratao et al. 2005; Scandalios 2005; Racchi 2013; Acosta-Motos et al. 2017). Additional protective mechanisms attempt to achieve an energy balance (ATP/NADPH). There are excellent reviews on the adaptive responses of plants to various stresses (to cite a few: Miller et al. 2010; Baxter et al. 2014; Golldack et al. 2014; Mignolet-Spruyt et al. 2016; Acosta-Motos et al. 2017; Szymanska et al. 2017; Zarattini and Forlani 2017).
Adaptations of photosynthesis to abiotic stress
Photosynthesis is one of the major metabolic pathways affected markedly by changing environmental conditions (Foyer et al. 2012). The abiotic stress slows down not only the biochemical reactions of carbon assimilation but also photochemical activities. Among the thylakoid components, PSII has a higher turnover rate in response to stress, while PSI is relatively stable except under cold stress. Under severe stress, all the components including the membranes get disrupted. Any disturbance of the balance between the production and utilization of ATP/NADPH can lead to the accumulation of ROS and subsequent photoinhibition or photodamage of photosystems (Walker et al. 2014). PSII photodamage and the inhibition of repair can be alleviated by different photoprotection mechanisms (Takahashi and Badger 2011).
Under fluctuating light, plants can adapt their photosynthetic characteristics by changing their photosynthetic apparatus (Kono et al. 2014). These adaptations can be for several hours and extend to even a few weeks. There are several authoritative reviews on the protection of photosynthesis against abiotic stress (Rumeau et al. 2007; Foyer and Noctor 2009; Takahashi and Badger 2011; Dall’Osto et al. 2012; Foyer et al. 2012; Goh et al. 2012; Erickson et al. 2015; Feller 2016; Yamori and Shikanai 2016; Suo et al. 2017). Besides antioxidant-based systems, plants use additional mechanisms to protect the photosystems from over-excitation. These are as follows: chlororespiration, water–water cycle (WWC), non-photochemical quenching and cyclic electron flow (CEF). Even mitochondrial metabolism, particularly oxidative electron transport, alternative oxidase (AOX) pathway and mitochondrial reactions of photorespiration can help to optimize and protect photosynthesis (Raghavendra and Padmasree 2003). Among these, activities of photorespiration, CEF and AOX appear to be quite crucial.
Photorespiration is one of the high-flux metabolic pathways associated with photosynthesis hosted in chloroplasts, peroxisomes, mitochondria and cytosol (Hodges et al. 2016). The process of photorespiration can dissipate excess ROS and energy either directly or indirectly (Voss et al. 2013). The reactions of photorespiration serve as direct sinks for photosynthetically generated ATP, NADPH and reduced ferredoxin. The peroxisomal catalase can directly scavenge H2O2. The indirect ways are the optimization of linear and CEF, promotion of AOX pathway and even the release of CO2 from glycine decarboxylation for intracellular recycling. Furthermore, glycine from photorespiratory metabolism is a source for glutathione, a major antioxidant in plant cells. A detailed description of the components of photorespiration, their regulation and the protective role can be found in some recent reviews (Kangasjarvi et al. 2012; Sorhagen et al. 2013; Voss et al. 2013; Araujo et al. 2014; Hodges et al. 2016; Zhang and Peng 2016).
The photochemical electron transport in chloroplasts operates in two modes, linear and cyclic. The linear electron transport leads to the generation of ATP as well as NADPH while the CEF, mediated by PSI accomplishes only the synthesis of ATP, but not NADPH. The equilibrium between ATP/NADPH production and their consumption gets disturbed and leads to photoinhibition or photodamage under conditions of abiotic stress. The balance can be adjusted back to equilibrium, by upregulation of CEF, which dissipates the excess energy in thylakoids via an enhanced energy-dependent non-photochemical quenching (qE-type NPQ). A few recent reviews summarize the extensive work on CEF (Chaux et al. 2015; Suorsa 2015; Ishikawa et al. 2016; Yamori and Shikanai 2016; Alric and Johnson 2017; Shikanai and Yamamoto 2017; Murata and Nishiyama 2018). The phenomenon of CEF is referred also as cyclic electron transport (CET) but we used the term CEF throughout this manuscript.
The AOX, localized in mitochondria, catalyses cyanide insensitive respiration. AOX is an important component of the members of mitochondrial energy dissipation pathway (MEDP), along with uncoupling proteins. The MEDPs play crucial roles in adaptation of plants to stresses. Regulation of MEDP members can occur at transcriptional, translational, post-translational and metabolic levels (Pu et al. 2015). AOX branches off from the cytochrome pathway of mitochondria at the level of ubiquinone (UQ). AOX bypasses complex III and IV of the cytochrome pathway, without ATP generation and hence the energy is dissipated as heat. AOX can limit excessive ROS/RNS generation in plants and helps in maintaining redox balance. The activity and levels of AOX increase under a variety of stresses (Moore et al. 2013; Wang et al. 2018). As a consequence, AOX optimizes photosynthesis under stress by modulating NADPH/ATP ratio, ATP/ADP ratio and carbon use efficiency. Further information on the AOX can be found in some recent reviews (Feng et al. 2013; Moore et al. 2013; Vanlerberghe 2013, Pu et al. 2015; Saha et al. 2016; Vanlerberghe et al. 2016; Wang et al. 2018).
Scope of present mini-review
One of our research interests has been the beneficial role of photorespiration and mitochondrial oxidative metabolism for photosynthetic carbon assimilation (Voss et al. 2013; Raghavendra and Padmasree 2003). We therefore focused this mini-review on the modulation by abiotic stress of photorespiratory components and associated phenomena of CEF and AOX. We describe how the three components of photorespiration, CEF and AOX exhibit adaptive responses to different stresses. In view of the large number of articles on this subject, we limited our discussion to a few selected stresses: drought, low CO2, high light, low N, low temperature and heavy metal stress. Our review attempts to high light the cross-talk between photorespiration, CEF and AOX. We propose that photorespiration is not only a major driving force but also upregulates CEF as well as AOX to provide additional protection of photosynthesis. A scheme is proposed to emphasize how photorespiration, CEF and AOX pathways act in tandem to protect plants under stress. Thus, the protective role of photorespiration is well complemented by CEF as well as AOX.
Modulation of photorespiration by abiotic stress
Upregulation of photorespiration is an important factor in optimizing photosynthesis and protecting against oxidative damage under high light or other abiotic stresses, such as drought, salinity and even heavy metals (Raghavendra and Padmasree 2003; Voss et al. 2013; Dellero et al. 2016; Hagemann et al. 2016; Hodges et al. 2016). Most of these studies were conducted with leaves of higher plants and some examples are presented and described below (Table 1).
It is not necessary that photorespiration always gets upregulated under drought or dissipates excess energy. The absolute rate of photorespiration can vary depending on the plant species and the intensity of drought itself. Noctor et al. (2002) provided evidence for an increase in the photorespiratory flux in leaves of two C3 plants: wheat and barley, at lower than ambient CO2 and drought. However, the contribution of photorespiration towards the oxidative load was minimal during severe stress in Pancratium maritimum (Abogadallah 2011). Similarly, photorespiration may not be the only energy sink and other processes of energy dissipation may be important to protect photosynthesis against photoinhibition under water stress (Guan and Gu 2009). Under conditions of extreme water deficit, the marked decrease in overall metabolism decreases photorespiration too. Under such conditions, metabolic components such as mitochondrial respiration and resultant ATP might become more important than photorespiration (Lawlor and Tezara 2009).
Drought and low CO2
Drought stress causes stomatal closure, creates low internal CO2 and increases the ROS levels in plant tissues. In leaves of Jatropha curcas and Ricinus communis, water deficit reduced the rates of photosynthesis, while photorespiration rate was increased by twofold (Neto et al. 2017). When exposed to drought, there was a sharp increase in the activities of several photorespiratory enzymes in tomato leaves e.g. phosphoglycolate phosphatase (PLGP), glycolate oxidase (GOX), catalase (CAT) and glycine decarboxylase (GDC) confirming the role of photorespiration in the adaptation to drought stress (Yuan et al. 2016). Under water stress, the rate of photorespiration increased in leaves of Holm oak (Quercus ilex) and J. curcas (Tsonev et al. 2014; Silva et al. 2015).
Overproduction of cytokinin in transgenic tobacco plants induced photorespiration to sustain photosynthetic processes (Rivero et al. 2009). When leaves of GS-overexpressing transgenic poplar were exposed to water stress, photorespiration was enhanced and the levels of serine and glycine increased, suggesting a key role of photorespiration during drought (Molina-Rueda and Kirby 2015). During acclimation to short-term ambient CO2, photorespiratory mutants of Arabidopsis exhibited an increase in pools of key metabolites e.g. glycolate, glycine, serine and glycerate. Thus, photorespiratory metabolite flux may protect photosynthesis during acclimation to low CO2 (Eisenhut et al. 2017).
High light and low N
When coffee leaves were exposed to high light, the rate of photorespiration increased significantly along with marked increase in the antioxidant systems, indicating the ability of photorespiration to consume excess reductants (Martins et al. 2014). In tobacco plants, photorespiration increased by twofold under high light, along with activation of WWC in tobacco plants (Huang et al. 2016a). Thus, photorespiration along with WWC played an important role in energy balancing when plants are exposed to high light.
Photorespiration helps to maintain adequate N levels in plants by promoting NH4+ production and assimilation (Bloom 2015). The photorespiratory rate, along with glycine levels, was enhanced and the activities of GO and GGAT increased markedly in Lactuca sativa and Brassica oleracea under Zn deficiency, indicating a need for photorespiration for NH4+ assimilation (Narvarro-Leon et al. 2016).
Low temperature and heavy metal stress
Low temperature limits photosynthesis due to reduction in stomatal conductance and enhanced uptake of O2, reflecting an increase in photorespiration (Flexas et al. 1999). When Quercus guyavifolia leaves were exposed to low temperature and high light, the rate of photorespiration increased by 50%, so as to protect the photosynthetic apparatus against photodamage (Huang et al. 2016b).
Exposure of plants to high concentrations of heavy metal results in the accumulation of ROS eliciting changes in the antioxidant components of cells (Gratão et al. 2005). Exposure of Brassica juncea to Cd stress, leads to reduction in stomatal conductance and decrease in internal CO2 concentration. The Cd stress increased phosphoglycolate levels, indicating that photorespiration could act as an electron sink to prevent over-reduction of photosynthetic components and photoinhibition (D’Alessandro et al. 2013).
Modulation of CEF by abiotic stress
Some of the stresses, known to affect CEF, are drought, low CO2, high light, low N, low temperature and heavy metal stress. The factor of elevated or high CO2 is unique that it can upregulate CEF (Satoh et al. 2002; Levitan et al. 2010), while not favouring photorespiration. Under severe stress, PSII becomes more sensitive to damage than PSI. The operation of CEF is crucial for protecting PSI by alleviating the over-reduction of the acceptor side of PSI and ATP production (Munekage et al. 2004). The PSI-dependent CEF is mediated by either proton gradient regulation 5 (PGR5) or PGRL1 (PGR5 like photosynthetic phenotype) proteins or a chloroplast NADH dehydrogenase-like (NDH) complex (Yamori and Shikanai 2016). The CEF is invariably upregulated under these conditions (Table 2).
Drought and low CO2
Water deficit triggers stomatal closure and results in low CO2 within leaves. As a result, drought stress inhibits photosynthetic carbon fixation due to both stomatal and non-stomatal limitation (Golding and Johnson 2003; Jia et al. 2008). Upregulation of CEF ensures survival under high light or drought stress (Lehtimaki et al. 2010). In resurrection plants of Parobea rufescens, CEF was stimulated by twofold not only under high light but also under low light in leaves subjected to drought (Huang et al. 2012). The ratio of CEF to ETR was stimulated up to twofold in two ferns: Microsorum punctatum and Paraleptochillus decurrens (Wang et al. 2013a). When J. curcas was exposed to drought, the dissipation of excess energy increased along with a threefold increase in CEF (Neto et al. 2017). Such associated increases in NPQ, photorespiration and CEF appear to be important to mitigate the effects of excess light, while preventing cellular damage, and maintain photochemical efficiency under limiting CO2.
In algal cells, a CO2 concentrating mechanism (CCM) is activated under low CO2 conditions. The CCM, involving a complex series of carbonic anhydrases and transporters, requires energy (Raven 2010; Wang et al. 2011). CEF can provide sufficient energy in the form of ATP to power the CCM. Under low CO2 conditions, CEF is activated and provides ATP for cellular needs as well as CCM in Chlamydomonas reinhardtii and Synechocystis PCC6803 (Deng et al. 2003). The rates of CEF increased up to fivefold in C. reinhardtii cells under severe depletion of inorganic carbon (Lucker and Kramer 2013). In higher plants, low CO2 availability induces higher photorespiratory flux. A similar situation of 2.5-fold increase was found in sunflower under photorespiratory conditions i.e. low CO2 and high O2 (Takagi et al. 2016).
High light and low N
Under high light conditions, the CEF is stimulated, proton gradient is dissipated and the non-photochemical quenching (NPQ) is increased. The upregulation of the thylakoidal NDH-complex seems to be the basis for such rise in CEF in Oat plant under photoinhibitory conditions (Quiles and Lopez 2004). The PSI-mediated CEF increased to almost fourfold in Synechococcus sp. PCC 7942 under high light (Herbert et al. 1995). Similarly, tobacco plants grown in high light had a fivefold higher activity of CEF compared with low light grown plants (Miyake et al. 2005).
The effect of high light is exerted even under limiting nitrogen. The CEF increased by twofold in Dunaliella salina under N deficiency and under high light, likely as the result of improved PSI quantum yields (Einali et al. 2013). Nitrogen limitation forces photosynthetic cells to readjust the balance between ATP/NADPH generation and their use for cellular metabolism. In C. reinhardtii, N deprivation led to the stimulation of type II NADPH dehydrogenase (NDA2)-dependent CEF by twofold, with little contribution from PGR5/PGRL1-dependent CEF. The H+ gradient which is generated by CEF was essential to sustain NPQ and ATP production for cell growth (Saroussi et al. 2016).
Low temperature and heavy metal stress
At low temperature, plants slow down their metabolism and create excess excitation energy, leading to ROS production and photoinhibition of PSII/PSI (Zhang and Scheller 2004). Furthermore, low-temperature stress decreases the levels of intracellular ATP and limits the repair of PSII and PSI (Murata et al. 2007). When cotton (Gossypium hirsutum L. var. Xinluzao 45) was grown under low temperature, there was a fivefold stimulation of CEF to prevent photoinhibition of photosynthesis (Fei et al. 2017). Similarly, low-temperature exposure increased CEF by tenfold in leaves of chilling sensitive Calotropis gigantea (Huang et al. 2017).
Heavy metals create oxidative stress by elevating ROS levels. The presence of heavy metals promotes CEF and helps in photoprotection of PSI while decreasing PSII-dependent electron flow. Generally, PSII is more sensitive than PSI to heavy metals (Atal et al. 1991; Siedlecka and Krupa 1996; Wang et al. 2013b). For e.g. when Microcystis aeruginosa, a cyanobacterial species was exposed to Sb(V), the CEF increased twofold (Wang et al. 2015).
Modulation of AOX by abiotic stress
The operation of AOX helps in maintaining a redox balance as well as metabolic homeostasis in plants (Vanlerberghe et al. 2016). Further, AOX is an important factor to switch between anabolic and catabolic modes of respiration and to maintain carbon, energy and redox balance in plant cells (Rasmusson et al. 2009; Vanlerberghe 2013). An increase in the capacity and activity of AOX is common during the response of plants to abiotic stress (Saha et al. 2016).
AOX is encoded by small family of nuclear genes, belonging to two types: AOX1 and AOX2. Among these genes, AOX1a is well studied and most responsive to variety of stress (drought, chilling, high light, high salt and low nitrogen) conditions. The over-expression of AOX1A in Arabidopsis plants conferred tolerance to different abiotic stresses (Feng et al. 2013; Wang et al. 2018). A few examples of stress modulated AOX components are given in Table 3.
Drought and low (ambient) CO2
In many monocot and dicot leaves, drought stress leads to an increase in the components of AOX: transcription of AOX gene(s), capacity and activity. For e.g. under drought conditions, 12-fold increase in AOX protein and 1.6-fold increase in AOX activity occurred in tobacco (Dahal and Vanlerberghe 2017; Vanlerberghe et al. 2016). Similarly, the expression of AOX increased fivefold under drought in barley (Wanniarachchi et al. 2018). Low CO2 or high O2 favours the photorespiratory pathway. Very few reports are available on the effect of low CO2 on respiration. In C. reinhardtii, slight decrease in AOX capacity was observed under ambient CO2 grown algae (Goyal and Tolbert 1989).
High light and low N
Under high light conditions, AOX protects chloroplasts from over-reduction, thereby decreasing photoinhibition (Xu et al. 2011; Florez-Sarasa et al. 2016a). This is because AOX is an effective sink for excess reducing equivalents generated in chloroplasts. The capacity as well as expression of AOX increases under high light conditions in several plants, including Arabidopsis thaliana and Cucumis sativus (Florez-Sarasa et al. 2016a; Zhang et al. 2017). Strong correlations between respiration rates and leaf N contents were found in various plant species. When the N is low, the respiration in leaves consumes more starch and the mitochondrial AOX capacity increases (Noguchi and Terashima 2006). The capacity and protein levels of AOX increased in tobacco cells cultured in a low-N medium (Watanabe et al. 2010).
Low temperature and heavy metals
The AOX pathway dissipates energy in the form of heat and this is quite crucial for plant adaptation to chilling. The protein abundance and the activity of AOX are low in plants under normal conditions, but are enhanced at low-temperature (Feng et al. 2008). Similarly, more than twofold increase in AOX capacity and expression of AOX under chilling conditions was reported in A. thaliana (Wang et al. 2012).
Exposure of plants to heavy metals leads to an increase in ROS. When exposed to Cd, Cr and Al, the AOX pathway is activated at both transcriptional and translational levels in A. thaliana (Keunen et al. 2015), Salvinia minima (Prado et al. 2010) and tobacco plants (Panda et al. 2013).
Interactions of photorespiration with CEF and AOX during abiotic stress
Photorespiration, CEF and mitochondrial AOX pathway are all important components of adaptations to abiotic stress of leaves. These three phenomena help in dissipating the excess reducing equivalents generated in the cell and protect against photoinhibition (Raghavendra and Padmasree 2003; Foyer et al. 2012). There are convincing reports that the elevated photorespiratory metabolism under stress can in turn stimulate both CEF and AOX.
The contribution of photorespiration or CEF in maintaining the redox poise of the chloroplast stroma was studied in several plants, such as sunflower, Arabidopsis, tobacco, rice, cotton, cyanobateria and even microalgae (Kramer and Evans 2011; Alric 2014; Kono et al. 2014; Huang et al. 2015; Takagi et al. 2016; Yamori and Shikanai 2016; Yi et al. 2018; Wada et al. 2018). The importance of AOX pathway in energy balance, involving photosynthesis and photorespiration, has been demonstrated using plants of Arabidopsis and tobacco with altered levels of either AOX1a (Vanlerberghe et al. 2016; Watanabe et al. 2016), or GDC (Igamberdiev et al. 2001; Bykova et al. 2005, 2014). There are several studies made on the modulation of either photorespiration (Table 1) or CEF (Table 2) or AOX (Table 3) in photosynthetic tissues under abiotic stress. However, only a few studies have monitored the modulation of CEF and/or AOX, in relation to photorespiration under a given stress (Tables 4, 5).
Photorespiration upregulates CEF
High light and low CO2 conditions increase the photosynthetic linear electron flow, causing an over-reduction of the electron transport chain and high ROS accumulation. Under such stressful conditions, plants increase the oxidation of P700 through CEF to suppress ROS production at PSI. The importance of photorespiration in maintaining the oxidation of P700 through CEF under limiting CO2 conditions was shown in sunflower leaves and transgenic rice with manipulated Rubisco content (Takagi et al. 2016; Wada et al. 2018). When Arabidopsis plants grown under high CO2 are transferred to ambient air, plants trigger photorespiratory responses due to the decreased CO2 availability. The enhanced expression of NDH-dependent CEF genes (NDF4 and NDF6) under such conditions suggests the activation of CEF to meet the increased ATP/NADPH demand of photorespiration (Foyer et al. 2012). In petioles of Calla lily (Zantedeschia aethiopica), high CEF around PS I was always accompanied by higher photorespiratory rates. In the absence of O2, the electron transport rate decreased dramatically in petioles and pedicels indicating the need for high photorespiration rates (Yiotis and Manetas 2010).
In Arabidopsis plants, the contribution of CEF to energy balance was quite significant during high light under photorespiratory conditions (high O2 and low CO2) (Walker et al. 2014). Under high light, the rate of photorespiration is expected to be high, and can afford additional ATP synthesis. Tobacco leaves acclimated to high light exhibited high rates of CEF (Miyake et al. 2005; Huang et al. 2015). The attenuated response of Gly/Ser ratio to high light in Arabidopsis CEF mutants—single (pgr5) and double (pgr5 crr4-3)—suggests an impairment in photorespiration, denoting a tight link between CEF and photorespiration (Florez-Sarasa et al. 2016b).
It has long been suggested that H2O2 generated as a result of over-reduction of the electron transport chain in chloroplasts can promote CEF (Livingston et al. 2010). Strand et al. (2015) checked the possibility of CEF regulation by H2O2 using transgenic Arabidopsis plants that express glycolate oxidase (GO) in chloroplasts. When chloroplast GO expressing plants were shifted from non-photorespiratory conditions of high CO2 to ambient air (photorespiratory conditions), rapid increase in CEF was observed within 20 min. Even an external supply of H2O2 induced higher levels of NDH proteins, facilitating the activation of CEF (Strand et al. 2015).
Photorespiration upregulates AOX
There is a positive correlation between photorespiratory glycine decarboxylation and activity of the AOX pathway. Oxidation of glycine by GDC results in the increased concentrations of NADPH in mitochondria activating AOX (Vanlerberghe et al. 1995; Bykova et al. 2014). AOX pathway favours photorespiration and can alleviate photo-inhibition by maintaining a functional photorespiratory pathway, by effective utilization of NADH from glycine oxidation under high light conditions (Watanabe et al. 2016).
Most of the work on the relation between AOX and photorespiration is done with aox1a mutants. There were only two studies on mutants with decreased photorespiratory activity, as the photorespiration-deficient mutants cannot grow in normal air. Suppression of GDC, one of the rate limiting steps of photorespiration, in a barley mutant resulted in significant changes in redox state, leading to over-reduction of the cellular components. Then compensatory mechanisms like increased mitochondrial respiration by either AOX or cytochrome oxidase (COX) were initiated (Igamberdiev et al. 2001). In fact, under conditions favourable for photorespiration such as drought, the enhanced AOX activity may protect even COX (Dahal and Vanlerberghe 2017). In transgenic potato plants with antisense reduction in P-protein of GDC, decrease in photorespiratory decarboxylation is compensated by an increase in respiratory decarboxylation (Bykova et al. 2005).
The Arabidopsis mutant lacking AOX (aox1a) showed decreased photosynthetic efficiency, expected to be due to disturbed photorespiratory metabolism (Yoshida et al. 2011). Similarly, under severe light stress (chronic photoinhibition) the inactivation of AOX in the CEF double mutants (pgr5 crr4-3) resulted in impairment of photorespiration as evidenced by small or no response of Gly/Ser ratio (Florez-Sarasa et al. 2016b).
Watanabe et al. (2016) showed that under high light conditions, AOX pathway alleviates photo inhibition by maintaining a functional photorespiratory pathway, when the cytochrome pathway was suppressed. Disruption or inhibition of AOX pathway (by inhibitors or the use of mutants) significantly decreased the photorespiration in Arabidopsis and C. sativus (Zhang et al. 2017). Suppression of AOX1A does not affect plant metabolism in normal light, but under high light results in the activation of photorespiratory components. The aox1a mutants increased their capacity for photorespiration compared to wildtype plants when the cytochrome pathway was inhibited (Strodtkotter et al. 2009).
CEF and AOX can compensate each other
From our understanding of the current literature, it appears that both CEF in chloroplasts and AOX in mitochondria are upregulated by photorespiration (Tables 4, 5) and perform the same function of dissipating excess reducing equivalents and protecting photosynthesis against stress.
Tobacco, with the knockdown of AOX showed enhanced CEF, whereas the overexpressed lines showed decreased CEF, when compared to wildtype, particularly during drought and light stress (Vanlerberghe et al. 2016). The AOX deficiency in tobacco resulted in highly reduced PSI, highly reduced NAD(P)H pool in the stroma and enhanced CEF. When overexpressed, AOX maintained an oxidized stromal NAD(P)H pool and lowered CEF in tobacco plants (Dahal et al. 2014, 2015).
Similarly, the Arabidopsis aox1a mutant showed a decrease in operating efficiency of photosystem II and enhanced CEF, indicating the importance of AOX in preventing the over-reduction of photosynthetic electron transport in chloroplasts under light stress (Yoshida et al. 2011). The Arabidopsis double mutant with lowered levels of both aox1a and pgr5 showed growth impairment and severe photoinhibition under even moderate light conditions, suggesting the co-operative nature of CEF and AOX in plant growth under high light (Yoshida et al. 2011). Florez-Sarasa et al. (2016b) found that the chronic photoinhibition in double mutant of CEF (pgr5 crr4-3) resulted in inactivation of AOX, while upregulating cytochrome pathway as sink for excess electrons from chloroplasts.
Concluding remarks
The available reports indicate the stimulation of CEF as well as AOX by photorespiratory conditions (e.g. sub-optimal CO2 or high O2 or fluctuating light). In turn, the operation of CEF and/or AOX seems to favour photorespiration. Once upregulated, photorespiration, CEF and AOX act in tandem, to achieve the same goal of protection and optimization of photosynthetic machinery (Fig. 1). Although these three processes are upregulated by a variety of stresses, we consider photorespiration as the major player, while CEF and AOX can be considered as priming factors that pre-condition plant tissues to be ready for exposure and adaptability to abiotic stresses. We also emphasize that photorespiration is upregulated under conditions favourable for CEF or AOX. Further, CEF or AOX appear to be capable of compensating the deficiency of the other, so as to keep photorespiration operational.
A schematic diagram of the beneficial role of photorespiration and its complementation by CEF and AOX to protect plants against abiotic stress. Any abiotic stress increases the level of ROS. Parallely, due to the disturbance in metabolism, the cellular compartments become over-reduced and thylakoids over-excited. The cells would then need more ATP for metabolism as well as repair processes. Under abiotic stress, the photorespiratory pathway is activated. In turn, photorespiration upregulates CEF and AOX. All three phenomena of photorespiration, CEF and AOX work together to optimize redox state of the cell, protect against photoinhibition and supply ATP for repair mechanisms. While the stimulation of CEF and AOX by photorespiration is well established, it is not clear, if there is a feedback modulation. Similarly, the extent of cross-talk between CEF and AOX is also not completely known. Solid arrows represent information available in the literature. The dotted arrows represent suggestions, which need to be verified experimentally
Photorespiratory H2O2 can be a powerful signal to stimulate CEF (Strand et al. 2015) or AOX (Sewelam et al. 2014). It would be interesting to check if CEF or AOX can generate any signal to stimulate photorespiration directly. This can be done by using mutants lacking key components of photorespiration, but this is quite challenging as most of the photorespiratory mutants are hard to grow in ambient air. However, the heterozygous barley mutants with partially reduced GDC (Wingler et al. 2000), which can grow in normal air, seem to provide an excellent window for such experiments.
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Acknowledgements
This work was supported by grants to ASR from Science and Engineering Research Board (SERB No. EMR/2017/005171) and Council of Scientific and Industrial Research (No. 38(1404)/15/EMR-II). DS supported by research fellowship from Council for Scientific and Industrial Research. RBB and VA were supported by research fellowships from University Grants Commission, New Delhi, India. We also thank grants from DST-FIST, UGC-SAP-CAS and DBT-CREBB, from New Delhi, India for support of infrastructure in Department/School.
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Sunil, B., Saini, D., Bapatla, R.B. et al. Photorespiration is complemented by cyclic electron flow and the alternative oxidase pathway to optimize photosynthesis and protect against abiotic stress. Photosynth Res 139, 67–79 (2019). https://doi.org/10.1007/s11120-018-0577-x
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DOI: https://doi.org/10.1007/s11120-018-0577-x