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Journal of Stress Physiology & Biochemistry, Vol. 21, No. 1, 2025, pp. 222-230 ISSN 1997-0838 Original Text Copyright © 2024 by Borovskii, Gorbyleva, Katyshev, Pyatrikas and Fedoseeva
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The Role of Alternative Respiratory Enzymes in Photosynthetic Plant Cells Under Stress
G.B. Borovskii*, E.L. Gorbyleva, A.I. Katyshev,
D.V. Pyatrikas and I.V. Fedoseeva
1 Siberian Institute of Plant Physiology and Biochemistry SB RAS, 664033, Irkutsk, Russia
*E-Mail: [email protected]
Received September 5, 2024
In recent years, it has become clear that for mitochondria in photosynthetic plant cells, the main role of buffer capacity is becoming, allowing to keep under control the balance of ATP production, regulation of the level of pyridine nucleotide reduction, generation of ROS and RNS, as well as optimize the main metabolic flows, which is especially important under stress. Nonconjugated respiration is an important mechanism for achieving stable operation and maximum efficiency of photosynthetic cells. It is actively used in the light and becomes even more important under stress in lighting conditions. The most important part of these non-canonical mitochondrial functions is provided by alternative mitochondrial respiratory enzymes.
Key words: plant mitochondria, photosynthetic cells, uncoupled respiration, alternative respiratory enzymes, reactive oxygen species
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Plants have two interconnected systems of cellular energy generation - respiratory and photosynthetic. And if in heterotrophic cells the most important role in the energy supply of metabolic processes belongs to mitochondrial respiration, then in photosynthetic plant cells this function is assumed by photosynthesis and chloroplasts. However, this does not mean that mitochondria in autotrophic cells are reduced, inactive in light, or their functions are not important for cellular energy metabolism. The role of mitochondria remains paramount, but is being transformed for other tasks. In recent years, it has become clear that the main function for mitochondria in photosynthetic plant cells is the buffer function, which is expressed in maintaining the balance of ATP production, the level of pyridine nucleotide reduction, limiting the generation of ROS and RNS, as well as optimizing the main metabolic fluxes, which is especially important under stress (Popov et al., 2021; Igamberdiev, Bykova, 2023).
An important part of these non-canonical mitochondrial functions is provided by alternative mitochondrial respiratory enzymes. A significant number of enzymes of alternative electron transport pathways are present in plant mitochondria, many of which are active under stress (M0ller et al., 2021). In Arabidopsis thaliana, these enzymes encode seven NAD(P)H dehydrogenase genes (NDA1-2, NDB1-4, NDC1), five alternative oxidase genes (AOX1a-d, AOX2) and three uncoupling protein genes (UCP1-3) (Michalecka et al., 2003; M0ller etal., 2021; Lima etal., 2022).
Alternative NAD(P)H dehydrogenases (ND II)
The work and functions in photosynthetic cells and under stressful conditions of alternative NAD(P)H dehydrogenases were initially discovered using rotenone, an inhibitor of respiratory complex I. It turned out that part of the dehydrogenase activity of mitochondria is not suppressed by this inhibitor, and in order to distinguish these enzymes from those already known, they were called type II dehydrogenases (ND II). It was found that in this case NAD(P)H is oxidized by several enzymes localized on the intermembrane and
matrix surfaces of the inner membrane of mitochondria. As mentioned above, three groups of genes encoding these enzymes were found in Arabidopsis, some of these enzymes turned out to be sensitive to Ca2+ ions (Michalecka et al., 2003; M0ller et al., 2021), the amount of which increases in cells under various stresses. The localization of these enzymes has been established: NDB1-NDB4 are external (located on the outer side of the inner membrane of the mitochondria), and NDA1, NDA2 and NDC1 are internal (facing the mitochondrial matrix, Elhafez et al., 2006). NDA and NDB2 oxidize NADH, NADPH is used as a substrate by NDB1 and NDC1 (M0ller et al., 2021). It turned out that the expression of ND II genes increases under stressful conditions or under other influences in a coordinated manner with the expression of genes encoding AOX (Clifton et al., 2005; Wanniarachchi et al., 2018).
It is not possible to block the synthesis of all ND II in plants constitutively, since it is impossible to obtain viable seeds (Smith et al., 2011), however, several works on blocking individual ND II genes have been published. There are results showing that deletion of the NDB4 gene encoding the external NADH dehydrogenase of A. thaliana led to a decrease in the level of ROS generation. The authors believed that this effect could be caused by an increase in the activity of antioxidant enzymes and alternative oxidase (Smith et al., 2011). Other researchers (Wallstrom et al., 2014a; Wallstrom et al., 2014b) studied how suppression of the expression of NDA1, NDA2, and NDB1 genes encoding alternative internal and external NAD(P)H dehydrogenases of A. thaliana affects plant growth and metabolism, as well as changes in the expression of other genes. It has been shown that a decrease in the number of NDA1 and NDA2 proteins leads to a slowdown in growth and an increase in the lactate content in cells. However, no significant phenotypic differences were found between mutants and wild-type plants (Wallstrom et al., 2014a). A decrease in the amount of NDB1 protein disrupted plant growth, but had no effect on respiratory activity. At the same time, the lack of NDB1 significantly affected the expression of genes involved in protein synthesis, as well as in the functioning of plant signaling systems (Wallstrom et al.,
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2014b). It has been shown that the activity of the NDB2 gene plays a role in the resistance of Arabidopsis to drought in strong light (Sweetman et al., 2019), and the drought-resistant soybean variety shows significantly higher expression of NDB2 (as well as a number of other genes of alternative respiratory pathways) than plants sensitive to this stress factor (Alizadeh et al., 2023). Increased expression of the NDA1 and NDA2 genes encoding the internal alternative NADH dehydrogenase led to a decrease in ROS generation, restored the photosynthetic system and increased the survival of seedlings under conditions of anoxia-reoxygenation (Jethva et al., 2023). The effect of constitutive heterologous NDB2 expression on plant resistance to low temperature and the rate of ROS generation were studied on transgenic tobacco plants, into whose cells the A. thaliana NDB2 (AtNDB2) gene was introduced (Korotaeva et al., 2023). An assessment of the effect of low positive and negative temperatures in the range from +3° C to -3° C did not reveal differences in the survival rate of transgenic plants and wild-type plants (Borovskii et al., 2023). At the same time, the best characteristics of the photosystem of transgenic plants functioning under low-temperature stress were shown -a lower drop in non-photochemical quenching (NPQ) and maximum quantum yield of photosystem II (Fv/Fm) in comparison with wild-type plants, as well as lower generation of ROS in leaves (Borovskii et al., unpublished data). The activity of NDB1 depends on the content of free Ca2+ ions and low pH values (Rasmusson et al., 2008). Consequently, acidification of the cytosol stimulates the oxidation of external NAD(P)H (Hao et al., 2015), which logically fits into the definition of these enzymes as stressful.
It is important for plants that ND II enzymes are able to support the oxidation of NAD(P)H in conditions in which the activity of mitochondrial complex I is reduced, however, they do not create significant competition for complex I in other conditions, for example, at low concentrations of NAD(P)H. In model experiments, when ND II dehydrogenase genes were transferred to cells of species in which they are absent in the genome, the activity of external ND II arabidopsis contributed to a decrease in oxidative stress with inhibited activity of the
mitochondrial complex I (Catania et al., 2019). This allows us to conclude that ND II enzymes work effectively in mitochondria that are not adapted for the functioning of alternative ETC.
Alternative oxidase (АОХ)
The functional role and regulation of the activity of genes and proteins of alternative electron transport routes under stress has been studied in the most detail for AOX. AOX is a terminal oxidase of plants that branches off from the main mitochondrial respiratory chain at the ubiquinone level and, using electrons obtained from it, catalyzes the reduction of oxygen to water. It is resistant to cyanide and therefore its activity is quite simple to fix. The path of electronic transport through AOX bypasses two points of generation of an electrochemical proton gradient (complexes III and IV), and the energy of oxidation of ubiquinone by oxygen is released as heat. This reduces the energy efficiency of respiration, reduces the influence of respiratory control, which regulates the rate of formation of ATP and NADH, depending on the needs of the cell. AOX is found not only in higher plants, but also in representatives of all kingdoms (except archaebacteria): bacteria, algae, mosses, ferns, fungi, and even in sedentary or immobile animals (sponges, anemones, nematodes, mollusks, Vanlerberghe etal., 2020).
It was found that although plants have several alternative oxidase genes, these genes and the enzymes encoded by them do not duplicate and cannot fully compensate for the absence of each other (Selinski et al., 2018b). At the same time, different isoforms of AOX have different levels of sensitivity to pyruvate (Sweetman et al., 2022), and are also activated differently by intermediates of the tricarboxylic acid cycle (Selinski et al., 2018b). Posttranslational activation of AOX proteins is carried out in several ways, fine regulation is performed, among other things, by intermediates of the tricarboxylic acid (TCA) cycle, and the activity of AOX also depends on the redox status of the cell (Selinski et al., 2017). Regulation of the activity of AOX enzymes is carried out with the participation of two conserved cysteine residues - CysI and CysII. The formation of a disulfide bridge between the CysI of two
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AOX monomers under oxidized conditions leads to inactivation of the enzyme, their reduction in the dimer of non-covalently bound monomers converts the enzyme to the active form, and the interaction of both reduced Cys residues with pyruvate or other TCA cycle products to form thiohemiacetal leads to an even greater increase in enzyme activity (Selinski et al., 2018a). Thus, fine regulation of AOX by intermediates of mitochondrial metabolism can be achieved, and activation of AOX by intermediates of photorespiration - glyoxylate and hydroxypyruvate reveals the metabolic relationship of AOX with this process, which requires the oxidation of large amounts of NADH without conjugation with ATP synthesis (Igamberdiev, Bykova, 2023). The protective role of AOX in stress conditions of photosynthetic cells is well known. For example, in cucumber, AOX2 expression increases under cold stress, and this is associated with maintaining photosynthetic productivity (Ikkonen et al., 2020). It has been shown that the functioning of this enzyme prevents an uncontrolled increase in the amount of ROS and RNS when the respiratory chain is inhibited under stress or "overflow" of the reduced pool of ubiquinones. It is known that AOX is involved in retrograde signaling, which leads to changes in the expression of many other genes under stress (Saha et al., 2016; Garmash, 2021).
Interestingly, plants have another alternative terminal oxidase, similar in function to AOX. It is a plastid terminal oxidase (PTOX) that is found in chloroplasts. PTOX is a key factor for maintaining the redox balance of the plastoquinone pool (PQ) and functions as a "safety valve" to protect photosynthesis, obviously echoing the functions of mitochondrial AOX (Wang et al., 2016). It is a stress-sensitive protein that can protect plants from various types of stress (Stepien, Johnson, 2018). In this review, we will not consider this enzyme, but its presence and functions well illustrate the idea that evolution tends to invent the same solutions to similar problems repeatedly.
Uncoupling plant proteins (UCPs)
The respiration rate of mitochondria depends on the transmembrane potential on the inner membrane of organelles. Its increase to 180 mV significantly inhibits
the flow of electrons through complexes I, III and IV of the electron transfer chain generating ДцН+, which leads to a decrease in the consumption of NAD(P)H and other mitochondrial substrates. One way to avoid this is to increase the activity of non-conjugated electron transport pathways (Popov et al., 2021). Another way is to dissipate the potential with the help of specific proteins originally found in brown fat tissues in animals, where they participate in thermogenesis (Ricquier et al., 1983). Later, uncoupling proteins (UCPs) and the uncoupling effect were discovered in plants (Vercesi et al., 2006; Popov et al., 2021). The uncoupling proteins of A. thaliana are represented by a small family of genes (UCP1-3), their products are integral proteins of the inner mitochondrial membrane with molecular weights of about 33 kDa. Proteins are activated by free fatty acids and ROS, and are inhibited by purine nucleotides. UCPs activity leads to a decrease in the membrane potential of the inner mitochondrial membrane (Vercesi et al., 2006). The results of studies with double knockdown of various UCP genes show that UCP2 and UCP3 have a complementary function with UCP1 in plant reproductive and vegetative organs/tissues, as well as in adaptation to stress. The partial redundancy between UCP isoforms suggests that functionally they can act both separately and jointly (Lima et al., 2022). The mechanism by which UCP transports free fatty acids through the inner membrane of mitochondria has been the subject of debate (Jezek etal., 2018). The crystal structure of UCP suggests a model of protein activity known as the mechanism of cyclic fatty acid turnover, in which, instead of transporting a soluble substrate, UCP catalyzes the inversion of ionized fatty acids distributed in the membrane, which allows the proton to be moved by fatty acids from one side of the membrane to the other (Barreto et al., 2020).
The most studied function of UCPs is plant protection under such stresses as cold, hyperthermia, excessive illumination, drought, and exposure to pathogens. A probable defense mechanism is associated with a decrease in respiratory control and a decrease in ROS formation in mitochondria, since the formation of superoxide radicals depends on a high value of the transmembrane potential and increases
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exponentially with its increase (Liu, Huang, 1996; Popov et al., 2021). The absence of UCP1 leads to oxidative stress, although it does not impair the plant's ability to withstand a wide range of abiotic stresses. More importantly, in such plants, there is a significant restriction of photorespiration activity with a decrease in the rate of glycine oxidation in mitochondria, which leads to a related decrease in the rate of photosynthetic carbon assimilation (Sweetlove et al., 2006). Overexpression of UCP in plants correlates not only with adaptation to oxidative stress. It increases the productivity of photosynthesis and stimulates mitochondrial biogenesis, which correlates with changes in the expression of genes involved in energy metabolism and redox homeostasis (Laitz et al., 2015). Although the physiological role of UCPs in plants is still being discussed, it is clear that thermogenesis is not the most important function of these proteins. At the same time, it is obvious that they are important for plant adaptation to stressful conditions by regulating membrane potential and reducing ROS, as well as for balancing energy flows in photosynthetic cells (Barreto et al., 2020; Popov et al., 2021; Igamberdiev, Bykova, 2023).
Coordination of the expression of genes of alternative ETC among themselves and with the state of the photosynthetic apparatus
With simultaneous operation of external and (or) internal ND II and AOX, the cell freely oxidizes part of NAD(P)H, converting chemical energy into thermal energy, which allows regulating the redox state of the pool of NAD(P)H, components of ETC mitochondria in a plant cell and shunting ROS generation sites in mitochondria (Popov et al., 2021). Since ND II is connected to the respiratory chain through ubiquinol, then in order for the potential not to be generated in the ETC, further AOX activity is needed. In the light of these data, it is clear why the expression of the NDB, NDA and AOX genes in plants are interrelated. The expression of these genes also occurs synchronously in response to various abiotic stresses, which implies joint regulation by common promoter elements. Thus, the expression level of AOX1a in A. thaliana determines the expression level
of the NDB2 gene under control conditions and under UV irradiation (Garmash et al., 2020). Under many stresses, such as drought, almost all genes encoding proteins of alternative mitochondrial electron transport pathways are involved in plant stress response and adaptation (Yerlikaya et al., 2022). In transgenic tobacco plants, N. sylvestris with overexpression of the potato StNDB1 gene (Solanum tuberosum L.) observed an increase in the activity of tobacco's own AOX (Liu et al., 2008). A similar effect of activation of the expression of different genes of alternative mitochondrial ETC in tobacco plants with increased expression of the AtNDB2 gene was observed in our work (Borovskii et al., 2021). During the operation of UCPs, mitochondria dissipate the potential accumulated during the operation of the cytochrome pathway (Vercesi et al., 2006), which reduces respiratory control in these organelles, and such activity can serve as an alternative to the functioning of AOX, which is especially important in conditions of anoxia and hypoxia.
The expression of genes of alternative ETC is related both to each other and to the functioning of the photosynthetic apparatus. This occurs in various ways and through various metabolites. Thus, citrate, a product of the tricarboxylic acid cycle, is an activator at the transcriptional level not only for AOX, but also for NDA (Igamberdiev, Bykova, 2023). One of the possible ways combining the expression of genes of alternative ETC is retrograde signaling, when mitochondrial redox signals induce the expression of NDA2, NDB2 and UCP1b together with genes of antioxidant systems (Garmash, 2021). Through the redox status of photosynthetic ETC, the regulation of genes of alternative mitochondrial ETC can also occur. The signal received from it coordinates the amount of AOX and the protein of the LHCB2 lightharvesting complex, and both proteins then contribute to maintaining the energy balance of chloroplasts, especially under stress (Chadee et al., 2021; Alber, Vanlerberghe, 2021; Igamberdiev, Bykova, 2023). Light stimulates the expression of NDA and NDC (Escobar et al., 2004). Strong light-activated gene expression is also observed in external NDB dehydrogenases (Michalecka et al., 2003).
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Coordination is necessary for photosynthetic cells, probably because in conditions where ATP and redox energy are intensively produced by light-dependent photosynthetic reactions, chloroplasts have insufficient ability to supply ATP to the cytosol. In the form of citrate, energy enters the mitochondria, where at this moment it is important to switch to the non-conjugated pathways of mitochondrial electron transport, which balances the ATP/ADP and NAD(P)H/NAD(P)+ in mitochondria, cytosol and other cellular compartments. Thus, uncoupled respiration is an important mechanism for achieving stable operation and maximum efficiency of photosynthetic plant cells (Igamberdiev, Bykova, 2023). In the light, mitochondria coordinate the phosphorylation of adenylates and the reduction of pyridine nucleotides in the cytosol and other cellular compartments in order to avoid excessive energization and optimize the main metabolic flows. This function, which can be defined as thermodynamic buffering, is largely realized due to the flexibility of the mitochondrial ETS, the presence of alternative pathways in it and the possibility of uncoupled respiration. It is actively used in the light and becomes even more important under stress in the lighting conditions of the cell.
ACKNOWLEDGEM ENT
The study was supported by grant No. 23-24-00097 from the Russian Science Foundation (https://rscf.ru/project/23-24-00097/).
CONFLICTS OF INTEREST
The authors declare no conflict of interest.
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