Nitrate–Nitrite–Nitric Oxide Pathway in Plants: Comparison
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Oxygen (O2) is the most crucial substrate for numerous biochemical processes in plants. Its deprivation is a critical factor that affects plant growth and may lead to death if it lasts for a long time. However, various biotic and abiotic factors cause O2 deprivation, leading to hypoxia and anoxia in plant tissues. To survive under hypoxia and/or anoxia, plants deploy various mechanisms such as fermentation paths, reactive oxygen species (ROS), reactive nitrogen species (RNS), antioxidant enzymes, aerenchyma, and adventitious root formation, while nitrate (NO3−), nitrite (NO2−), and nitric oxide (NO) have shown numerous beneficial roles through modulating these mechanisms. However, the end product of nitrate-nitrite-nitric oxide pathway, the NO is toxic if accumulated. Thus, its scavenging or inhibition is equally important for plant survival. Here, we point out NO reduction to nitrous oxide (N2O) could play an important role in reducing NO toxicity in plants, thus, reducing nitro-oxidative stress and helping plants to survive for longer period during O2-limited conditions

  • plants
  • hypoxia and anoxia
  • nitric oxide signaling
  • nitric oxide toxicity
  • nitrous oxide

1. Introduction

Oxygen (O2) deficiency hinders respiration and other biochemical processes essential for plants’ survival, but extreme events such as heavy precipitation and flooding cause waterlogging, which directly affects O2 supply and prevents their growth [1]. Moreover, several other conditions can also lead to hypoxic and anaerobic conditions in well-aerated tissues of plants. For example, pathogen attacks, tissue exposure to freezing, sulfur dioxide (SO2), ozone, and water deficiencies can cause anaerobic conditions, leading to anaerobic metabolisms in plant tissues [2][3]. Abiotic stress such as salt stress can disrupt the symplastic connections between cells, which decreases the permeability of cells to O2, resulting in hypoxia and anoxia [4][5]. Moreover, under normal conditions, an endogenously generated O2 gradient also exists, such that the O2 concentration may fall below 5% in plant tissues, such as in seeds, bulk tissues, shoot apical meristems, and roots [6].

Hypoxia and anoxia result in the modification of various normal metabolic paths [7]. Thus, they usually inhibit respiration, photosynthesis, nitrogen assimilation, biological nitrogen fixation, water and nutrient uptake, and stomata closure in plants [7][8][9][10][11] through a reduced adenosine triphosphate (ATP) concentration, nicotinamide adenine dinucleotide (NAD+) and nicotinamide adenine dinucleotide hydrogen (NADH) ratio (NAD+/NADH), and cell viability [12]. Meanwhile, the accumulation of reactive oxygen species (ROS) and reactive nitrogen species (RNS) is triggered, which severely damages the cell components [13]. Moreover, during hypoxia and anoxia, a drop in pH causes cytoplasmic acidosis which affects numerous metabolic activities that may even contribute to plant death [14]. Overall, hypoxia and anoxia have numerous deleterious effects on plant metabolism (Figure 1).

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Figure 1. Possible causes of hypoxia and anoxia, their consequences, and defense mechanisms in response to O2 deficiency. Red arrows represent negative effects to plants, while green ones represent positive effects.
To survive O2 deficiency, plants use numerous strategies through biochemical, anatomical, and morphological changes (Figure 1). However, the accumulation of ethanol and lactic acid (major products of the fermentation process) are toxic [15]. Moreover, antioxidant defense systems could also be a limiting factor if the stress is present for a longer time or beyond the tolerance capacity. This suggests that if anaerobic processes proceed for a longer time, the ultimate fate of plants is death. Along with metabolic changes, plant adaptation mechanisms can improve tissue O2 status. A number of mechanisms have been reported to help plants to improve O2 status during soil waterlogging conditions.
Nitric oxide (NO), a widely recognized signaling molecule, plays an important role in hypoxia and anoxia tolerance in plants [16][17]. Not only NO but also nitrate (NO3−), nitrite (NO2−), and nitrate reductase (NR, EC 1.6.6.1) play a similar role in plants during O2 deficiency [18]. This suggests that tolerance to O2 deficiency is due to the reductive pathways of NO formation. However, numerous studies indicate that O2 deficiency, as well as other stresses, can trigger NO formation [17][18][19]. Meanwhile, a higher concentration of NO could be cytotoxic, leading to the accumulation of ROS and other RNS that would lead to nitro-oxidative stress [19][20]. Nitric oxide could promote [21] or inhibit [22] ethylene biosynthesis, a key phytohormone for plants’ survival during O2 limitation, while the latter case is mediated through the S-nitrosylation of methionine adenosyltransferase (MAT1) [22]. Phytohormones such as salicylic acid (SA), jasmonic acid, and abscisic acid (ABA) reduce oxidative stresses and enhance the activities of antioxidants during stress conditions [23][24]. However, NO is reported to inhibit the activities of antioxidants, as well as proteins involved in regulating phytohormones through S- nitrosylation [24][25], thus, again, increasing nitro-oxidative stress in plants.
Thus, there should be a fine regulation of these signaling molecules (NO, ROS, and other RNS) for beneficial roles. The key to surviving during hypoxia and anoxia depends upon mechanisms that could lessen the harmful effects of nitro-oxidative damages by increasing the activities of adaptation mechanisms. Therefore, understanding the reductive pathways of NO formation along with NO scavenging mechanisms would provide insight into the mechanisms involved in lessening the effects of O2 deprivation.

2. Pathways of NO Formation during Hypoxia and Anoxia

Various pathways of NO formation in plant cells have been documented, and they have been categorized into oxidative and reductive pathways. Oxidative pathways are oxygen-dependent, involving L-arginine, polyamine, and hydroxylamine [26]. The reductive pathways of NO formation occur during low O2 and are dependent on NO3−, NR, NO2−, plasma membrane NR, plasma membrane-bound nitrite reductase (PM NiNOR), xanthine oxidoreductase in plant peroxisomes, photosynthetic-electron-transport-chain-dependent NO2− reduction in chloroplasts, and mitochondrial electron transport chains (ETCs) such as cytochrome bc1 complex (complex III, EC 1.10.2.2), cytochrome c oxidase (CcO, EC 1.9.3.1), and alternative oxidase (AOX, EC 1.10.3.11) in mitochondria [26][27]. In Chlamydomonas reinhardtii, NR, together with nitric-oxide-forming nitrate reductase (NOFNiR), reduces NO2− to NO [28]. Moreover, NO2− can be reduced to NO in acidic pH without the involvement of any enzyme. NO production pathways during O2 deficiency and other stresses would be different. For example, salt stress can increase both oxidative pathways (l-arginine-dependent) [29] as well as the reductive pathways of NO production [30]. However, during O2 deficiency, NO is produced through the reductive pathways [26]. Interestingly, this occurs not only during O2 deficiency but many other biotic- and abiotic-stress-induced reductive pathways of NO formation. For example, salinity stress, water deficiency, UV radiation, freezing, pathogen attacks, and wounding can trigger NO production in plants [31][32][33][34][35][36], which could be due to the fact that these stresses could lead to hypoxia and anoxia in plant tissues, while its formation could be a defense strategy to survive harsh conditions. Nitric oxide is formed in various cell compartments such as the cytosol, apoplasts, chloroplasts, peroxisomes, and mitochondria of plants through enzymatic or non-enzymatic pathways [26]. Nitric oxide production in various compartments of plant cells has numerous functions. For example, NO formed in chloroplasts can prevent the oxidation of chloroplastic lipids and proteins, while NO-mediated peroxynitrite (ONOO−) production may result in its damage [37]. Similarly, NO formed in mitochondria can protect its components, while NO-mediated ONOO− production causes mitochondrial dysfunction [38]. Therefore, maintaining optimum level of NO is critical for its beneficial roles.

3. Role of Nitrate and Nitrate Reductase (NR) during Hypoxia and Anoxia Tolerance

Nitrate is not only an important form of nitrogen (N) source to plants but also a signaling molecule [39]. It is usually a major form of N in aerobic soil, and its uptake by plant roots is achieved through NO3− transporters [40]. After being uptaken by roots, NO3− is reduced to NO2− by an enzyme called NR in the cytosol or plasma membrane or stored in the vacuole or transported to shoots and leaves for subsequent reduction [15]. Under normoxia, NO2− is transported to plastids/chloroplasts and is reduced to ammonium (NH4+) by nitrite reductase (NiR, EC 1.7.7.1). Then, glutamine synthetase/glutamate-oxoglutarate aminotransferase (GS, EC 6.3.1.2)/GOGAT, EC 1.4.1.13) assimilates NH4+ into amino acids. However, during hypoxia and anoxia, the NO3− or NH4+ assimilation path to amino acid as well as NO3− transport to the aerial parts is greatly reduced [41]. For example, O2 deficiency decreases NO3− and NH4+ assimilation and N incorporation into amino acids in various plant species as compared to normoxia [42][43]. Although N incorporation into amino acids is inhibited during O2 deficiency, several pieces of research have shown that NR is highly activated and NO3− is reduced to NO2− [44]. 

Several previous studies have shown that NO3− and NR are beneficial for hypoxia and anoxia tolerance. Germinating seeds generally experience hypoxic and anoxic conditions [45][46][47] due to the compaction and hindrance of O2 diffusion by the outermost layers of seeds [48]. Studies have reported that NO3− is beneficial during seed germination. For example, supplementation or priming with NO3− increases the viability of germination in seeds of various plants [49][50][51]. Light and temperature influence seed germination, while NO3− can reduce the dependency on environmental factors such as light [52] and temperature [53] during germination. Moreover, NO3− can promote germination in seeds during salt, metal, and heat stresses [54][55][56]. The mechanisms of seed germination by NO3− might be due to NO production in cytosol and mitochondria through the reductive pathways [47]. Similarly, NO3− has been shown to increase activities of antioxidant enzymes such as catalase (CAT, EC 1.11.1.6) and superoxide dismutase (SOD, EC 1.15.1.1) during the germination process [57], which could scavenge ROS, thus preventing oxidative damage and promoting germination. 

Waterlogging reduces several nutrients in plants, affecting plant metabolism [58], while the supplementation of NO3− increases the uptake of nutrients such as N, P, Fe, and Mn [59]. Nitrate can improve cytoplasmic acidification caused by anoxia in plants [60][61] while decreasing fermentative enzymes such as lactate dehydrogenase (LDH, EC 1.1.1.27), pyruvate decarboxylase (PDC, EC 4.1.1.1), and alcohol dehydrogenase (ADH, EC 1.1.1.1) [62]. Lower levels of lactate and ethanol in plant roots [10][62] and an increase in the ATP level were observed in NO3−-treated plants during waterlogging [62], which suggest that NO3− is highly beneficial to reducing toxic metabolites while increasing the energy status of waterlogged plants. Antioxidants such as SOD, CAT, ascorbate peroxidase (APX, EC 1.11.1.11), and guaiacol peroxidase (POD, EC 1.11.1.7) remove O2− and H2O2 [63][64]. 

Hypoxia and anoxia in roots caused by flooding decrease chlorophyll content in the leaves of plants, thus decreasing the plant biomass and photosynthesis rate [11]. Nitrate is more beneficial in terms of biomass, net photosynthesis rate, chlorophyll, and protein content as compared to NH4+ and glycine [65][66]. Moreover, the concentration of metabolites such as sucrose, γ-aminobutyrate, succinate, and nucleoside triphosphate are reduced significantly in the absence of NO3− during hypoxia in maize root [60]. Alanine aminotransferase (AlaAT, EC 2.6.1.2), via the reversible conversion of pyruvate and glutamate to alanine and 2-oxoglutarate, is involved in carbon and nitrogen metabolism [67]. The foliar spraying of NO3− during waterlogging increases AlaAT and GOGAT activities along with an increase in amino acid in plants [68], suggesting that NO3− is involved in regulating both glycolysis and the TCA cycle during O2 deficiency. Redox imbalance during hypoxia and anoxia directly affects cellular metabolisms [69]. Various studies have reported that NO3− supplementation to hypoxic and anoxic plant tissues can improve the redox state [15][70][71]. For example, NO3− and NR maintain redox balance during hypoxia in cucumber (Cucumis sativus L.) [12]. 

Nitrate reduction via NR can delay cell death during hypoxia and delay the anoxic symptoms in plants [72], while its inhibition can significantly disturb the growth [71]. Tobacco (Nicotiana tabacum) mutant plants lacking NR reductase are more sensitive to O2 deprivation as compared to wild types by showing symptoms of rapid wilting, more ethanol and lactate production, and less ATP generation [70], suggesting the role of NO3− is due to its reduction to NO2−. NR plays a role in the maintenance of energy status for nitrogen fixation under O2-limited conditions in Medicago truncatula nodules [73]. The use of NR inhibitors in the root system of nodulated alfalfa (Medicago sativa L.) results in a significant decrease in the ATP/ADP ratio under flooding and salinity stresses [5]. Waterlogging significantly degrades membrane lipids [74], while NO3− and NR activity can delay the anoxia-induced degradation of membrane lipids in plant cells [75]. Higher expression of NR in cucumber (Cucumis sativus) than tomato (Lycopersicon esculentum) was associated with a high tolerance of hypoxia in the roots [76]. During hypoxia and anoxia, NR plays an important role in plant biology by regulating NO production by supplying electrons to NOFNiR and truncated hemoglobin [77]. The regulation of NO is critical, as it is a signaling and also toxic molecule if it is accumulated in a higher amount in a cell [78]. Overall, both NO3−and NR are involved in hypoxia and anoxia tolerance with numerous benefits, which suggests that NO2− is also involved in the mechanisms. However, long-term O2 limitation would affect the NR acclivity, thus, again, questioning plants’ survival during O2-limitation conditions. For example, the NR level increases during O2 limitation conditions, while NR-mRNA remains constant during the early hours of O2 limitation and decreases after 48 h [72], suggesting long-term O2 limitation affects its activity. Moreover, NO, which is produced by NR itself, also decreases the level of NR protein through posttranslational modifications and ubiquitylation by affecting amino acids involved in binding the essential flavin adenine dinucleotide (FAD) and molybdenum cofactors [28][79]. Therefore, O2 limitation and a higher level of NO formation would affect NR activity after long-term hypoxia and anoxia, thus, again, affecting plants’ survival. Moreover, a higher concentration of NO3− is reported to affect plant growth through the increased production of NO, thus increasing lipid peroxidation and the H2O2 level [80]. 

4. Role of Nitrite during Hypoxia and Anoxia Tolerance

A well-known pathway of NO2− metabolism in plants is its assimilation to amino acids through reduction to NH4+. However, during O2 deprivation, the assimilatory pathway is inhibited, and NO2− is either accumulated in the cytoplasm [42] or reduced to NO by the NR in the cytoplasm or transported to mitochondria for reduction [81]. This is further supported by the fact that NiR is inhibited during O2-limited conditions [42]. Although NO2− assimilation to amino acids is significantly reduced during hypoxia and anoxia, NR is activated, and the NO2− level increases [15]. Similar to NO3−, NO2− can promote seed germination in plants [47][49][82]. Moreover, thermo-dependency during seed germination was lowered in the presence of NO2− [52]. During low O2 levels in mitochondria, NO2− can regulate the surrounding O2 concentration through the production of NO [83]. Exogenous NO2− can also reduce both ethanol and lactate production [84] and can minimize the acidification of cytoplasm in plants during hypoxia and anoxia [61]. Similarly, the role of NO2− in the protection of mitochondrial structures and functions has been well documented. NO2− supplementation during O2-limited conditions to the mitochondria isolated from roots of pea (Pisum sativum) shows better mitochondrial integrity, the energization of the inner mitochondrial membrane, increased ATP synthesis, and decreased production of ROS and also decreased lipid peroxidation [85]. Hypoxia and anoxia can degrade the activities of complex I [86], while NO2− supplementation can result in its higher levels and activities [85]. The role of NO2− in hypoxia tolerance in humans and animals has been well documented [87][88]. It could be through its reduction to NO, as hypoxia and anoxia trigger NO2− reduction to NO. However, a higher concentration of NO2− can lead to membrane damage, lipid peroxidation, protein oxidation, mutation, DNA damage, and cell death [89], which could be through a higher level of NO production. So, for its beneficial role, its concentration should be regulated.

5. Role of Nitric Oxide during Hypoxia and Anoxia Tolerance

The role of NO in plant physiology has been described by numerous researchers. The reductive pathway of NO formation in plants is reported to be beneficial in plants as it promotes seed germination, increases biomass and root formation, increases energy status during O2 limitation, promotes tolerance to various biotic and abiotic stresses, and promotes the induction of different defense-related genes, and many others.

Similar to NO3− and NO2−, NO also stimulates germination in various plants species in a dose-dependent manner, i.e., low to medium NO has a positive effect, while a higher concentration inhibits germination [90][91]. The mechanism involved in seed germination by NO could be due to its capacity to reduce respiration rates and ROS levels while increasing carbohydrate metabolism and the level of amino acids and organic acids in germinating seeds [47]. The α-amylase (EC 3.2.1.1) activities of rice seed germination in the flooded condition are directly linked to seedling survival [92], while NO and GA can induce the activity of α-amylase [93]. However, the increase in activities of α-amylase by NO is time-dependent, such that at an early hour, it increases the activities, while prolonged NO exposure strongly reduces the activities [47]. This time-dependent role of NO could be due to the fact that prolonged exposure to NO could accumulate RNS which inhibit its activity. NO is involved in controlling seed dormancy through inducing the degradation of the ABI5 protein, thus enhancing ABA catabolism [94] while also increasing antioxidant enzymes [95]. However, a high level of NO can be toxic to cells, as it can inhibit mitochondrial respiration irreversibly [78] as well as inhibit antioxidants enzymes [96], which could explain the mechanisms of inhibiting germination by a higher level of NO. NO production in plant cells during hypoxia enhances the survival rate [97]. During waterlogging conditions, the application of NO donor increases leaf area, plant biomass, harvest index, lint yield, and boll number in the cotton plant [98]. Similarly, the net photosynthetic rate and chlorophyll content increase, and MDA, H2O2, ADH, and PDC content decrease [98]. The role of NO in increasing the net photosynthetic rate and chlorophyll content could be due to its role in inhibiting the transcriptional activation of chlorophyll breakdown pathway genes such as SRG, NYC1, PPH, and PAO [99]. Similarly, during waterlogging conditions, NO influences both the morphological and physiological characteristics of maize seedlings such that it increases height, dry weight, and antioxidant activities while decreasing MDA content and the ion leakage ratio [100]. The reductive pathway of NO production is involved in maintaining leaf shape and size in plants by increasing the cell size, chlorophyll a/b contents, antioxidant enzymatic activity, homeostasis of ROS  [101], and root elongation [102]. The mechanisms of hypoxia tolerance by NO are several. For example, NO improves H2S accumulation in maize seedling roots, which increases antioxidant defense, leading to the removal of excess ROS [97]. Moreover, during hypoxia and anoxia, NO is involved in ATP production through mitochondrial ETCs and the phytoglobin-NO cycle [15], thus increasing energy status. During hypoxia, NO production and the fine regulation of ROS and NO can slow down the respiration rate while preventing tissues from anoxia [103]. Nitric oxide could induce the expression of alternative oxidase (AOX) during various stress conditions  [104], while its expression is associated with less superoxide generation and lipid peroxidation during O2 limitation conditions, while AOX also prevents nitro-oxidative stress during reoxygenation [105]. During plant–microbial symbiosis, the enzyme of nitrogen fixation, i.e., nitrogenase, is only stable and functional in O2-limited conditions [106]. In such symbiotic interaction, plant NR and mitochondrial ETCs are involved in NO production, while excess and low NO inhibit the nodule establishment [107], suggesting that NO should be regulated in the symbiotic relationship between plants and microbes. The nitrate-NO respiration process in root nodules of Medicago truncatula plays a role in the maintenance of the energy status required for nitrogen fixation [73]. Calcium ion reduces the level of ROS and increases the antioxidant enzymes in mitochondria during hypoxia by improving metabolism and ion transport in plants, thereby increasing hypoxia tolerance [108]. Similarly, exogenous calcium application can increase the biomass, net photosynthesis, stomatal conductance, and efficiency of photosystem II during hypoxia stress in plants [109]. NO can regulate Ca2+ in plant cells [110]. For example, plant cells treated with NO donors are reported to have a fast increase in cytosolic Ca2+ concentration, which was strongly reduced when treated with NO scavengers [111]. The mechanism involved in this regulation of Ca2+ could be that NO can increase the free cytosolic Ca2+ concentration by activating plasma membrane Ca2+ channels and inducing plasma membrane depolarization  [111]. However, a higher concentration of NO is also reported to inhibit the cytosolic Ca2+ in human cells [112], suggesting NO should be regulated for its beneficial role. If a plant is exposed to O2 deficiency for a prolonged period, the ultimate fate of the plant will be death. So, the mechanisms that could improve the O2 status of waterlogged plants would only benefit the plant to survive, while NO formation is also highly beneficial for improving O2 status through various mechanisms. For example, adventitious root formation increases plant resistance to waterlogging by increasing the inward diffusion of O2 [113] or even participating in photosynthesis, thus improving O2 status [114], while NO is reported to play a role on its formation during waterlogging [113]. Aerenchyma formation allows O2 diffusion from aerated to waterlogged parts of plants, while NO also plays a role in aerenchyma formation in plants [21] , thus improving the O2 status. Nitric oxide as well as ethylene are involved in programmed cell death and aerenchyma formation during O2-limitation conditions [21][115]. Nitric oxide formed through reductive pathways induces the expression of aminocyclopropane-1-carboxylic acid (ACC) synthase (ACS) and ACC oxidase (ACO) genes responsible for ethylene synthesis [21] .

6. Adverse Effects of Nitric Oxide and Role of Nitric Oxide Scavenging on Hypoxia and Anoxia Tolerance

It is clear that NO, as the end product of the NO3-NO2-NO pathway, plays numerous beneficial roles during hypoxia and anoxia tolerance in plants. However, to be beneficial, the concentration of NO plays a critical role, while hypoxia and anoxia trigger NO production, which can be lethal to cells [78]. Some of the adverse effects of NO are summarized in Table 1. Moreover, oxidative stress caused by O2 limitation and the overproduction of NO during various stresses could damage major components of mitochondria [86][116] and inhibit antioxidants systems, thus accumulating ROS and RNS. RNS, if accumulated more, could exacerbate more damage than ROS by triggering free radical peroxidation [117]. Increased RNS and ROS production could lead to retrograde signaling to the nucleus to regulate gene expressions [118]. Nitric oxide, through the formation of RNS, could lead to mutation, DNA damage, and cell death [116][119]. So, for the longer survival of a cell during hypoxia and anoxia, the NO produced RNS should be scavenged efficiently.

Table 1. Adverse effects of a higher level of NO in plants. The high level of NO was achieved through a higher dose of NO donor or using NO-overproducing mutants or hypoxia plus NO donors.
Effects of Higher Level of NO References
Decreases the root growth through DNA damage, induces cell cycle arrest and inhibits primary root growth by affecting root apical meristem activity and cell elongation. [120][121]
Delayed flowering, retarded root development, and reduced starch granule formation through S-nitrosylation modification. [122]
Cell death through increased electrolyte leakage, cell wall degradation, cytoplasmic streaming, and DNA fragmentation. [21]
Decreases the expression of cyclins (CYC) and Cyclin-Dependent Kinases (CDKs), resulting in the downregulation of cell cycle progression. [123]
NO can generate peroxynitrite, which is a mediator of cytochrome c loss, protein oxidation and nitration, lipid peroxidation, mitochondrial dysfunction, damage DNA, and cell death. [20][124]
NO can inhibit antioxidants such as catalase, glutathione peroxidase (GPX), and ascorbate peroxidase in a reversible way and peroxynitrite in an irreversible way. [96][125]
NO can change the redox state and promote cell death. [26]
Inhibits lateral and primary root growth through reduced cell division and the expression of the auxin reporter markers DR5pro:GUS/GFP. [121][126]
Inhibits growth of tobacco plants through peroxynitrite formation and tyrosine nitration. [127]
Inhibits seed germination, while the scavenging of NO alleviates the effect. [91]
Inhibits the shoot growth and decreases the chlorophyll contents of the plants. [128][129]

It is clear that NO scavengers work differently in plants. For example, the use of NO scavengers during low NO production have negative effects on plant growth  [130], while during high NO production, the same NO scavengers have positive effects [121]. A similar role of NO has been reported in mammals [131]. Therefore, the optimum level of NO could be different during normal and stress conditions. As a higher amount of NO is formed through the reductive pathways during the O2 limitation condition, it would be beneficial that some amount of NO is scavenged from cells. For example, the scavenging of NO using NO scavengers during hypoxia preserves the function of mammals’ mitochondria [132]. There may be several pathways of NO scavenging mechanisms during O2-limited conditions, such as NO reduction to N2O [18][133] and the phytoglobin-NO cycle in plants [134].

NO formation in plants is always suspected to be underestimated [15], which could be due to that fact that NO is not simultaneously measured with N2O. The use of tungsten as an NR inhibitor was reported to inhibit N2O formation in plants [135], while NR inhibition challenged the plants’ survival, as described in the above section, which further supports the concept that N2O formation also could play a role in plants’ survival strategies. Both NO [136] and N2O [137] can increase the activities of phenylalanine ammonialyase, cinnamate-4-hydroxylase, and 4-coumaroyl-CoA ligase during pathogen attack in plants while increasing total phenolic, flavonoid, and lignin content. Similarly, both NO and N2O are reported to slow down fruit ripening by lowering ethylene synthesis during post-harvest storage [138][139]. Therefore, the similar roles of both NO and N2O observed in plants could be due to NO reduction to N2O, which need further research as, to date, there is no research measuring both NO and N2O simultaneously. This NO reduction could take place in mitochondria and chloroplast of plants cell [18][140][141]. Thus, reducing the toxicity of NO in plants and protecting the components of mitochondria and chloroplast.

As stated in the above sections, the expression of Pgbs is beneficial for plants during O2-limited conditions, which is due to the NO scavenging mechanism. For example, during the germination of barley seeds, the scavenging of NO through the overexpression of Pgbs resulted in a higher germination rate, protein content, and ATP/ADP ratios and a lower rate of fermentation, the S-nitrosylation of proteins and S-nitrosoglutathione (GSNO) [134][142].

 

7. Nitric-Oxide-Mediated Post-Translational Modifications and Their Roles during Hypoxia and Anoxia

Recent research suggests that NO-mediated post-translational modifications are less reported in plants during O2-limitation conditions [143], which could be due to the fact that NO is reduced to N2O and emitted to the atmosphere. This could be supported by the fact that plants emit very high N2O levels during waterlogging conditions, which are even more than those in soil [144], while it has been recently suggested that the N2O emitted from plants even in field conditions is produced in plant cells through NO reduction [140]. However, during complete anoxic conditions, this NO reduction to N2O would be inhibited [145]. Moreover, the NO-scavenging capacity of Pgbs would not operate during complete anoxia [146], while they contribute to produce NO [147], thus, again, increasing the level of NO, and thus promoting nitro-oxidative stress and inducing NO-mediated post-translational modification in plants (Figure 2).
/media/item_content/202210/6348ba2926146ijms-23-11522-g002.png
Figure 2. Proposed model on mechanisms of hypoxia and anoxia tolerance as well as cell death by NO3-NO2-NO pathway. The red arrows represent negative effects, while the green ones represent positive effects.
 

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