Journal of Experimental Botany, Vol. 71, No. 2 pp. 465–469, 2020 doi:10.1093/jxb/erz428 Advance Access Publication September 27, 2019 This paper is available online free of all access charges (see http://jxb.oxfordjournals.org/open_access.html for further details) eXtra Botany Viewpoint Does the alternative respiratory pathway offer protection against the adverse effects resulting from climate change? Igor Florez-Sarasa1, Alisdair R. Fernie2 and Kapuganti Jagadis Gupta3,* 1 Centre for Research in Agricultural Genomics (CRAG) CSIC-IRTA-UAB-UB, Campus UAB Bellaterra, Barcelona, Spain 2 Max-Planck-Institute of Molecular Plant Physiology, Potsdam-Golm, Germany 3 National Institute for Plant Genome Research, Aruna Asaf Ali Marg, New Delhi, India * Correspondence: jgk@nipgr.ac.in Elevated greenhouse gases (GHGs) induce adverse con- to adopt new strategies for developing more climate-resilient ditions directly and indirectly, causing decreases in plant crops with high yield and productivity in order to meet the productivity. To deal with climate change effects, plants enhanced global population food demand (Dhankher and have developed various mechanisms including the fine- Foyer, 2018). Considering that respiration and photosynthesis tuning of metabolism. Plant respiratory metabolism is are the main components of plant carbon balance, alterations highly flexible due to the presence of various alternative in respiration can potentially affect plant growth and prod- pathways. The mitochondrial alternative oxidase (AOX) uctivity (Zhang et al., 2018; Amthor et al., 2019). In particular, respiratory pathway is responsive to these changes, and the AOX pathway has been demonstrated to improve plant several lines of evidence suggest it plays a role in redu- performance under different physiological conditions—mainly cing excesses of reactive oxygen species (ROS) and re- due to its roles both in providing metabolic flexibility and in active nitrogen species (RNS) while providing metabolic lowering the level of mitochondrial reactive oxygen species flexibility under stress. Here we discuss the importance of (ROS) (Vanlerberghe, 2013; Selinski et al., 2018; Del-Saz et al., the AOX pathway in dealing with elevated carbon dioxide 2018a). As such, it probably functions to protect plants against (CO2), nitrogen oxides (NOx), ozone (O3), and the main abi- the adverse effects of climate change (Fig. 1). otic stresses induced by climate change. Susceptibility of plants to various abiotic and biotic stresses can be aggravated by climate change-induced ROS including Recent advances in our understanding concerning the in vivo the superoxide anion (O2–), hydrogen peroxide (H2O2), and the regulation of alternative oxidase (AOX) and its structural prop- hydroxyl radical (·OH–) (Cassia et al., 2018). These ROS ori- erties suggest that novel AOXs with altered regulatory proper- ginate from various sources such as the mitochondria, chloro- ties could be used in future gene editing strategies. We suggest plast, peroxisome, and the plasma membrane NADPH oxidase that fine-tuning modulation of the regulatory properties of (Mittler, 2017).Various stresses additionally induce nitric oxide AOX and targeting its expression in different plant tissues could (NO), which in turn reacts with ROS, leading to the produc- improve plant growth and productivity under climate change tion of reactive nitrogen species (RNS) such as peroxynitrite conditions promoted by elevated greenhouse gasses (GHGs). (ONOO–), nitric dioxide (NO2), nitrosyl anion (NO–), di- Moreover, we also emphasize the need for extensive study on nitrogen trioxide (N2O3), dinitrogen tetroxide (N2O4), and ni- the interactive effects of major global change factors on AOX trous acid (HNO2). Low levels of these free radicals trigger respiration and the importance of studies differentiating be- important signals; however, if they are produced in higher tween the roles of AOX in sink versus source tissues under field levels, they can cause adverse effects such as damage to lipids, conditions in order to improve plant productivity in response proteins, and DNA, and consequently impact on plant growth to elevated GHGs. and development. Plants have accordingly evolved various ma- Climate change is associated with an elevation of the green- chineries that can deal with elevated ROS, including ascorbate house gases such as (CO2), nitrogen oxides (NOx), ozone peroxidase (APX), catalase (CAT), superoxide dismutase (SOD), (O3), and methane (CH4), and with increased events of adverse and other enzymes involved in the ascorbate–glutathione cycle conditions for plants including drought and high temperature (Choudhury et al., 2017). Among mitochondrial proteins, the stress as well as flooding (Min et al., 2011; Pall et al., 2011). AOX controls mitochondrial ROS production and plays a Such abiotic stress conditions in combination with increasing role in adaptive plasticity. Briefly, AOX protein is inserted in biotic stresses are challenging plant and agricultural research the inner membrane of plant mitochondria and branches the © The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Experimental Biology. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/ by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com 466 | Florez-Sarasa et al. Fig. 1. The role of the alternative oxidase (AOX) pathway in mitigating the effects of climate change and improving plant growth. Environmental, human, and microbial activities lead to increased greenhouse gases (GHGs). These GHGs can elevate ROS and RNS directly or directly via inducing various stresses. AOX can reduce excess ROS and RNS while maintaining energy and carbon balance to improve plant growth. In the inset, a schematic representation of the plant mitochondrial electron transport chain (mETC) is shown. The mETC contains the classical components involved in oxidative phosphorylation [I, II, III, IV (or cytochrome oxidase, COX), and V], which yields ATP. Complexes I, III, III, and IV are also sources of superoxide (O2–) and nitric oxide (NO), which can be transformed into other ROS and RNS. The AOX is inserted at the inner mitochondrial membrane (IMM) and diverts electrons from the ubiquinone (UQ) pool by reducing O2 to H2O without proton (H+) translocation into the intermembrane space (IMS). In this way, the AOX can stabilize the reduction level of the UQ pool and other mETC components, thus preventing the formation of O2– and NO. At the same time, the AOX activity renders respiration independent of adenylate control, thus allowing the reoxidation of matrix and extramitochondrial NAD(P)H under high- energy charge or COX restriction. Several physiological situations can require the action of AOX to maintain or enhance the activities of the TCA cycle and other cellular metabolic processes under energy and carbon imbalance. Yellow and red boxes indicate induced and reduced molecule levels or processes by the action of AOX, respectively. cytochrome c oxidase (COX) pathway at the level of the ubi- transcription, translation, and metabolism, resulting in de- quinone (UQ) pool bypassing two sites of proton translocation creases in plant productivity of up to 15% (Wilkinson et al., associated with ATP production (Fig. 1). In this manner, the 2012). In addition, increased formation of numerous free rad- AOX pathway can stabilize the UQ reduction level and pre- icals has been reported in plants after O3 exposure (Fiscus et al., vent the production of excessive ROS. Furthermore, the ac- 2005). These radicals can disrupt various organelles, causing tivity of the AOX pathway renders respiration independent of programmed cell death and reducing yield in various crops adenylate control, thus allowing the continuation of respiratory (Mills et al., 2011). AOX can protect plants against damage im- metabolism, which is crucial for plants to cope with different posed by ozone. stress conditions (Del-Saz et al., 2018a) such as those promoted Intriguingly, Ederli et al. (2006) reported that exposure of to- by climate change. bacco plants to 300 ppb O3 strongly induced AOX expression. Moreover,Tosti et al. (2006) reported that O3 exposure resulted in the induction of AOX protein promoted by a crosstalk be- The AOX pathway in modulating ROS and tween ethylene and NO signalling. Furthermore, induction of RNS induced by greenhouse gases AOX occurs via the inhibition of the cytochrome c pathway by O3, and at the same time the inhibition of the cytochrome Different studies have reported that AOX expression is respon- pathway by O3 leads to production of H2O2. Consequently, the sive to a variety of greenhouse gases such as O3, NO, and CO2. H2O2 produced causes further induction of AOX1a via retro- O3 is an important component of the stratosphere. It aids in grade signalling (Tosti et al., 2006).While the extent of the effect filtering dangerous UV. In contrast, in the troposphere, O3 is of O3 on in vivo AOX activity has not yet been determined, it deleterious to plant performance. O3 in the stratosphere is made follows that the overexpression of AOX in crop plants may offer by reaction between NOx, CO2, CH4, and volatile organic plant resistance to O3 injury by reducing the levels of ROS. compounds (VOCs) in the presence of sunlight (Hickman, Excess NOx (such as NO and NO2), which occur within 2010). Increased O3 can cause adverse effects on plants. For the natural atmosphere, can be problematic since they are both instance, exposure of plants to O3 causes massive changes in components of GHGs as well as being inducers of other GHGs AOX role in protection of plants from greenhouse gases | 467 such as O3 (Hickman et al., 2010). NO, a free radical signal CO2 (Del-Saz et al., 2018a; Dahal and Vanlerberghe, 2018a, b), molecule, is a component of NOx. Excess NO can cause tyro- which represent the major abiotic stresses challenging current sine nitration of proteins, thus inhibiting their activities. Several agricultural productivity with regard to climate change. The free radicals and metabolites such as pyruvate and citrate are beneficial role of such metabolic flexibility probably compen- inducers of AOX (Vanlerberghe, 2013). Among them, NO is an sates the theoretical negative effects of AOX in reducing ATP inducer of the AOX at the transcript and protein level (Huang and reductant availability required for growth (Vanlerberghe, et al., 2002; Kumari et al., 2019). Treatment of cell suspensions 2013). In this context, Dahal and Vanlerberghe (2018b) import- with NO leads to an increased capacity of the AOX pathway, antly reported that plant growth was higher in tobacco plants and inhibition of AOX leads to increased NO sensitivity to cell overexpressing AOX as compared with wild-type plants after death, suggesting that NO is induced to protect cells from cell prolonged water deficit. The beneficial effect on growth has death (Kumari et al., 2019). Fu et al. (2010) has shown that been linked to the ability of AOX to maintain a higher respir- AOX is important in the prevention of cell death induced by ation in light, which improves chloroplast energy balance and Tobacco mosaic virus. Since O3 also causes cell death, the induced photosynthesis (Dahal and Vanlerberghe, 2018b). The role of AOX can help in the protection from cell death (Overmeyer the AOX in improving photosynthesis has also been reported et al., 2005). The AOX pathway prevents excess ROS and NO in other species under different conditions (reviewed by Del- production (Maxwell et al., 1999; Cvetkovska and Vanlerberghe, Saz et al., 2018a) and is probably among the main reasons 2012; Alber et al., 2017; Vishwakarma et al., 2018). NO reacts explaining the beneficial role of AOX in plant growth and with superoxide, leading to production of ONOO– which can productivity. Nevertheless, there is also evidence suggesting cause tyrosine nitration and reduces function of various en- that the in vivo AOX activity favours the synthesis of tricarb- zymes. In this context, the capacity of AOX to control both oxylic acid (TCA)-derived metabolites with specific roles in NO and ROS production makes it a very powerful machinery protecting against high light (Florez-Sarasa et al., 2016) and for the protection of plants against these molecules. Recently, salinity stress (Del-Saz et al., 2016). it was demonstrated that AOX not only scavenges NO under Adjustments to the partitioning of electrons between AOX normoxia induced by flg22 (flagellin) but also generates NO and COX pathways were associated with changes in tissue en- under hypoxia (Vishwakarma et al., 2018). In contrast to ergy demands of plants exposed to long-term elevated CO2 normoxia, hypoxia-induced NO does not react with superoxide, conditions (Gomez-Casanovas et al., 2007). In addition, changes but rather is scavenged by phytoglobin1 via metaphytoglobin in mitochondrial electron partitioning to AOX were related to reductase activity. The scavenged NO has a role in recycling the improvement of leaf carbon balance and respiratory ef- nitrate, maintenance of the redox status, and operation of the ficiency under different CO2 growth conditions (Gonzàlez- phytoglobin–NO cycle to generate ATP (Vishwakarma et al., Meler et al., 2009). Recently, AOX overexpression has been 2018). NOx emissions also contribute to increased temperature, shown to prevent both carbohydrate and energy imbalances which indirectly can increase flash floods with the consequent in leaves of tobacco plants grown at elevated CO2 (Dahal and hypoxic atmosphere in soil. Hence AOX can play a role under Vanlerberghe, 2018a). All these studies suggest that increased flooding conditions to improve energy efficiency and survival. AOX activity can be beneficial for plant growth under elevated Although CO2 is important for photosynthesis, elevated CO2 CO2 conditions. can have some negative impacts on plants.The study of Loladze (2014) based on >130 species and crop species found that ele- vated CO2 can reduce mineral content on average by 8% and Future perspectives increases the ratio of soluble carbohydrates to proteins. Several important elements such as zinc and iron diminished in several As discussed above, the use of AOX-transgenic plants has pro- food crops such as rice, wheat, and soybean in the presence of vided important insights into the role of AOX in photosynthetic high CO2 (Myers et al., 2014). Elevated CO2 also induces ROS tissues and growth. However, the effects of AOX genetic modifi- (Cheeseman, 2006) and, in order to detoxify ROS, plants also cation on root growth and metabolism under stress have received induce various antioxidants (AbdElgawad et al., 2016). Several much less attention (Smith et al., 2009, Keunen et al., 2016). reports suggest that AOX protein is highly responsive to elevated Importantly, AOX has a role in the synthesis of carboxylates in CO2 (Yoshida and Noguchi, 2009; Dahal and Vanlerberghe, white lupin (Florez-Sarasa et al., 2014), tobacco (Del-Saz et al., 2018a). The relationships between yield, ROS production, and 2017), and tomato (Del-Saz et al., 2018b). The root exudation mineral nutrition in AOX-modified plants under elevated CO2 of carboxylates improves phosphate acquisition, which bene- (eCO2) remain to be investigated and could provide more in- fits photosynthesis and plant growth (Pang et al., 2018). On the sights into the protective role of AOX. other hand, information about the impact of the AOX pathway on the growth of other sink and reproductive tissues, such as tubers and fruits, is limited (Xu et al., 2012; Zidenga et al., 2012) The AOX pathway in providing metabolic and represents an important area for future research. Given the adaptations of plants to stresses evidence for tissue-specific roles for AOX, the use of more so- phisticated genetic approaches specifically targeting sink and/or aggravated by climate change source tissues (Sonnewald and Fernie, 2018) will be required for The AOX pathway provides flexibility in cellular energy and disentangling the roles of AOX and its impact on plant growth carbon metabolism under drought, elevated temperature, and and productivity. Genetic engineering of respiration involving 468 | Florez-Sarasa et al. spatio-temporal changes of the target genes has been proposed Dahal K, Vanlerberghe GC. 2018b. Improved chloroplast energy balance during water deficit enhances plant growth: more crop per drop. Journal of as a crucial strategy to improve crop productivity (Amthor et al., Experimental Botany 69, 1183–1197. 2019). Particularly, fine-tuning alterations of AOX have been Del-Saz NF, Florez-Sarasa I, Clemente-Moreno MJ, Mhadhbi H, predicted to be among the most efficient strategies to achieve Flexas J, Fernie AR, Ribas-Carbó M. 2016. Salinity tolerance is related high biomass gains (Amthor et al., 2019). In this respect, recent in to cyanide-resistant alternative respiration in Medicago truncatula under sudden severe stress. Plant, Cell & Environment 39, 2361–2369. vitro (Selinski et al., 2018) and in vivo (Florez-Sarasa et al., 2019) Del-Saz NF, Ribas-Carbo M, McDonald AE, Lambers H, Fernie AR, evidence on the predominant role of the TCA cycle intermedi- Florez-Sarasa I. 2018a. An in vivo perspective of the role(s) of the alterna- ates on AOX regulation, together with new structural insights tive oxidase pathway. Trends in Plant Science 23, 206–219. on its active site (May et al., 2017), is paving the way to de- Del-Saz NF, Romero-Munar A, Cawthray GR, Aroca R, Baraza E, sign new AOXs with altered and desirable regulatory properties. Flexas J, Lambers H, Ribas-Carbó M. 2017. Arbuscular mycorrhizal fungus colonization in Nicotiana tabacum decreases the rate of both carb- Finally, the interactive effects of major global change factors on oxylate exudation and root respiration and increases plant growth under AOX respiration remain to be determined. Some studies have phosphorus limitation. Plant and Soil 416, 97–106. highlighted the importance of (photo) respiratory metabolism Del-Saz NF, Romero-Munar A, Cawthray GR, Palma F, Aroca R, under stress combination (Obata et al., 2015; El Aou-Ouad et al., Baraza E, Florez-Sarasa I, Lambers H, Ribas-Carbó M. 2018b. 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Interaction between nitric oxide and abiotic stresses (reviewed in Vanlerberghe, 2013; Saha et al., and ethylene in the induction of alternative oxidase in ozone-treated to- 2016; Del-Saz et al., 2018a), we envisage that AOX will provide bacco plants. Plant Physiology 142, 595–608. a beneficial role for plants under combined stress conditions in- El Aou-Ouad H, Bota J, Obata T, Montero R, Fernie AR, Medrano H, duced by climate change. Pou A, Florez-Sarasa I. 2018. Combined drought and virus infection trigger aspects of respiratory metabolism related to grapevine physiological responses. Journal of Plant Physiology 231, 19–30. Acknowledgements Fiscus EL, Booker FL, Burkey KO. 2005. Crop responses to ozone: up- take, modes of action, carbon assimilation and partitioning. Plant, Cell & This work is supported by the DST-DAAD exchange program be- Environment 28, 997–1011. tween KJG and ARF. 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