TY - JOUR
AU - Lorenzo, Oscar
AB - Abstract Plants are aerobic organisms that have evolved to maintain specific requirements for oxygen (O2), leading to a correct respiratory energy supply during growth and development. There are certain plant developmental cues and biotic or abiotic stress responses where O2 is scarce. This O2 deprivation known as hypoxia may occur in hypoxic niches of plant-specific tissues and during adverse environmental cues such as pathogen attack and flooding. In general, plants respond to hypoxia through a complex reprogramming of their molecular activities with the aim of reducing the impact of stress on their physiological and cellular homeostasis. This review focuses on the fine-tuned regulation of hypoxia triggered by a network of gaseous compounds that includes O2, ethylene, and nitric oxide. In view of recent scientific advances, we summarize the molecular mechanisms mediated by phytoglobins and by the N-degron proteolytic pathway, focusing on embryogenesis, seed imbibition, and germination, and also specific structures, most notably root apical and shoot apical meristems. In addition, those biotic and abiotic stresses that comprise hypoxia are also highlighted. Developmental cues, hypoxic stress, N-degron pathway, nitric oxide, oxygen, phytoglobins Introduction Nitric oxide (NO) has important features as a key signaling molecule in plants since it is rapidly synthesized, induces defined effects within the cells, and is also scavenged quickly when no longer required. NO is an essential component of the gaseous network described to modulate pre-adaptation to hypoxic conditions, a system that also comprises O2, ethylene (ET), and carbon dioxide (CO2) (reviewed in Sasidharan et al., 2018). An optimal balance of controlled levels of reactive oxygen species (ROS) is required for plant survival. Therefore, a tightly dynamic circuit of flooding signals is essential for suitable plant responses. Diverse processes occur during this situation, such as metabolic adjustments and physiological changes, leading to plant survival. Hypoxia includes both developmental and stress-related conditions. It is important to differentiate between stress-induced hypoxia (stress hypoxia) and constitutively generated chronic hypoxia (physiological hypoxia) (Weits et al., 2020). During stress hypoxia, a prompt decrease in O2 concentration and an NO burst occur as a result of an environmental stress (e.g. flooding), among others changes in the cellular state. This hypoxia led to different adaptive responses, mainly controlled through Group VII of the ethylene response factors (ERFVIIs). Physiological hypoxia refers to specific tissues where O2 concentrations are constitutively low. This type of hypoxia is found in the so-called ‘hypoxic niches’ and does not constitute a stress. Hypoxic niches have specific attributes that keep the O2 concentration low, including high respiration rates and the inability to release O2 since they are heterotrophic tissues. Among them, various growth situations are governed by lower O2 levels, such as embryogenesis, seed imbibition and germination, and also specific structures, most notably the root apical (RAM) and shoot apical (SAM) meristems. In addition, some biotic and abiotic stresses such as pathogen attack and flooding can lead to hypoxia. To endure O2 deprivation, plants have developed sensing mechanisms, leading to transcriptional reprogramming to allow hypoxia responses. Here, we outline the influence of NO during the molecular crosstalk that underlies perception and acclimation processes. More than one source of NO is involved in the response during hypoxia, mainly nitrate reductase (NR) and plant mitochondrial activities (Gupta et al., 2005; Igamberdiev et al., 2005; Planchet et al., 2005). The NO burst that occurs during O2 deprivation is not an undesirable trait and there are some data from different plant species supporting the role of NO in the plant acclimation to hypoxia (reviewed in Sasidharan et al., 2018; Armstrong et al., 2019). Nitric oxide and hypoxic stress crosstalk As aerobic organisms, plants have evolved to maintain specific requirements for O2 that lead to a correct respiratory energy supply. A close relationship between both O2 and NO sensing is mediated by phytoglobins (PGBs), which are able to modulate the level of diatomic gases such carbon monoxide (CO), NO, and O2, and by the N-degron pathway, which perceives the fluctuations of these gases and activates a transcriptional response through N-terminal recognition that targets proteins for degradation (Fig. 1). Hypoxic conditions lead to an increase in NO levels, suggesting a key role for the NO/O2 balance during this stress (Dordas et al., 2003; Borisjuk et al., 2007; Ma et al., 2016). Fig. 1. Open in new tabDownload slide NO and O2 involvement in different steps of the N-degron pathway in plants and implication of PGBs. The stability of N-degron substrates is controlled by NO/O2 levels, whose balance is modulated by phytoglobins (PGBs). Under normoxia (1), these substrates are degraded by the action of different enzymes consecutively along the PCO branch. When plants suffer a hypoxic-related stress (2), this pathway becomes inhibited, triggering the transcriptional responses. During stress, PGBs play a key role, scavenging free NO (3), which in turn is able to modify PGBs post-translationally, to determine a finely tuned redox balance and energy status (created with BioRender.com). MAPs (methionine aminopeptidases); PCOs (plant cysteine oxidases); ATEs (arginyl-tRNA-transferases); PRT6 (PROTEOLYSIS 6); NR (nitrate reductase); ZPR2 (protein LITTLE ZIPPER 2); VRN2 (VERNALIZATION 2); ERFVII (Group VII ethylene response factors). Fig. 1. Open in new tabDownload slide NO and O2 involvement in different steps of the N-degron pathway in plants and implication of PGBs. The stability of N-degron substrates is controlled by NO/O2 levels, whose balance is modulated by phytoglobins (PGBs). Under normoxia (1), these substrates are degraded by the action of different enzymes consecutively along the PCO branch. When plants suffer a hypoxic-related stress (2), this pathway becomes inhibited, triggering the transcriptional responses. During stress, PGBs play a key role, scavenging free NO (3), which in turn is able to modify PGBs post-translationally, to determine a finely tuned redox balance and energy status (created with BioRender.com). MAPs (methionine aminopeptidases); PCOs (plant cysteine oxidases); ATEs (arginyl-tRNA-transferases); PRT6 (PROTEOLYSIS 6); NR (nitrate reductase); ZPR2 (protein LITTLE ZIPPER 2); VRN2 (VERNALIZATION 2); ERFVII (Group VII ethylene response factors). Phytoglobins modulate the balance between nitric oxide and oxygen Maintenance of correct spatiotemporal gradients in O2 and NO becomes a crucial factor to determine the cellular redox status, necessary for the regulation of plant developmental and stress processes. Non-symbiotic plant hemoglobins, recently renamed phytoglobins (PGBs) (Hill et al., 2016), are globular proteins able to bind small gaseous molecules such O2, NO, CO, and hydrogen sulfide (H2S). This huge binding capacity suggests an important role during sensing of gaseous molecules and regulatory mechanisms in diverse organisms from all living kingdoms, such as photosynthetic organisms, animals, fungi, or bacteria. Hemoglobins use heme as a cofactor (Hoy and Hargrove, 2008; reviewed in Gupta et al., 2011), which can bind the above-mentioned substrates, controlling their storage, transport, scavenging, and detoxification in the tissues (Arredondo-Peter et al., 1998). In plants, based on sequence cladistics, three classes of PGBs exist, symbiotic (SymPGB and Lb), non-symbiotic (PGB0, 1, and 2), and truncated (PGB3) (Hoy and Hargrove, 2008). Depending on the ligands, the expression pattern and their physiological functions are categorized as symbiotic and non-symbiotic (Table 1). During stress hypoxia, caused by flooding or pathogen attack, the presence of PGBs exerts a protective role, modulating NO levels (Hartman et al., 2019). Table 1. Overview of the phytoglobins described in plants Name (correlation between new and old nomenclature) . Tissue specificity . Expression pattern . Processes regulated . Binding capacity . Biophysical role . References . Symbiotic phytoglobin (SymPhytogb) Symbiotic hemoglobin (sHb) Root nodules Nodule-specific expression pattern O2 transport and release during N2 fixation to maintain the flux for respiration High affinity for O2 Facilitate O2 diffusion Appleby et al. (1983); Jacobsen-Lyon et al. (1995); Gopalasubramaniam et al. (2008) Phytoglobin0 (Phytogb0) Non-symbiotic hemoglobin (nsHb) Whole plant Higher expression in gametophytes; induction under hot and cold stresses, exposure to nitrate, and increased sucrose supply NO detoxification under hypoxia stress High affinity for O2 NO scavenging Garrocho-Villegas and Arredondo-Peter (2008) Phytoglobin1 (Phytogb1) Class/type 1 Non-symbiotic hemoglobin (nsHb-1) Embryonic and vegetative organs Induction under hypoxia, ethylene, exposure to nitrate, and increased sucrose supply in roots and rosette leaves, and upon NO and H2O2 treatments Maintenance of NO and O2 levels during cellular hypoxic conditions to modulate energy status Highest affinity for O2, low dissociation rate O2 and NO scavenging, NO dioxygenase activity Trevaskis et al. (1997); Wang et al. (2000); Hunt et al. 2001, 2002); Lira-Ruan et al. (2002); Dordas et al. (2003, 2004); Perazzolli et al. (2004); Cantrel et al. (2011); Thiel et al. (2011); Hartman et al. (2019) Phytoglobin2 (Phytogb2) Class/type 2 Non-symbiotic hemoglobin (nsHb-2) Embryonic and vegetative organs Induction under cytokinin treatment and low temperature Maintenance of NO and O2 levels during cellular hypoxic conditions and during embryogenesis; regulation of oil and sucrose accumulation in seeds Moderate O2 binding capacity, low dissociation rate O2 and NO scavenging, O2 carrier, sensing role Trevaskis et al. (1997); Hunt et al. (2001); Dordas et al. (2003, 2004); Spyrakis et al. (2011); Vigeolas et al. (2011); Elhiti et al. (2018) Phytoglobin3 (Phytogb3) Class/type 3 Non-symbiotic hemoglobin/ truncated hemoglobin (tHb) Whole plant, higher in roots Inhibition under hypoxia; induction upon auxin, NO, and H2O2 treatments and biotic stress Modulation of NO and ROS levels during biotic stress CO and O2 in a reversible manner, low O2 affinity O2 carrier, NO dioxygenase activity Watts et al. (2001); Mukhi et al. (2017) Leghemoglobin (Lb) Legume root nodules Nodule-specific expression pattern O2 transport and release during N2 fixation to maintain the flux for respiration High affinity for O2 Facilitate O2 diffusion Wittenberg et al. (1975); Hargrove et al. (1997); Ott et al. (2005) Name (correlation between new and old nomenclature) . Tissue specificity . Expression pattern . Processes regulated . Binding capacity . Biophysical role . References . Symbiotic phytoglobin (SymPhytogb) Symbiotic hemoglobin (sHb) Root nodules Nodule-specific expression pattern O2 transport and release during N2 fixation to maintain the flux for respiration High affinity for O2 Facilitate O2 diffusion Appleby et al. (1983); Jacobsen-Lyon et al. (1995); Gopalasubramaniam et al. (2008) Phytoglobin0 (Phytogb0) Non-symbiotic hemoglobin (nsHb) Whole plant Higher expression in gametophytes; induction under hot and cold stresses, exposure to nitrate, and increased sucrose supply NO detoxification under hypoxia stress High affinity for O2 NO scavenging Garrocho-Villegas and Arredondo-Peter (2008) Phytoglobin1 (Phytogb1) Class/type 1 Non-symbiotic hemoglobin (nsHb-1) Embryonic and vegetative organs Induction under hypoxia, ethylene, exposure to nitrate, and increased sucrose supply in roots and rosette leaves, and upon NO and H2O2 treatments Maintenance of NO and O2 levels during cellular hypoxic conditions to modulate energy status Highest affinity for O2, low dissociation rate O2 and NO scavenging, NO dioxygenase activity Trevaskis et al. (1997); Wang et al. (2000); Hunt et al. 2001, 2002); Lira-Ruan et al. (2002); Dordas et al. (2003, 2004); Perazzolli et al. (2004); Cantrel et al. (2011); Thiel et al. (2011); Hartman et al. (2019) Phytoglobin2 (Phytogb2) Class/type 2 Non-symbiotic hemoglobin (nsHb-2) Embryonic and vegetative organs Induction under cytokinin treatment and low temperature Maintenance of NO and O2 levels during cellular hypoxic conditions and during embryogenesis; regulation of oil and sucrose accumulation in seeds Moderate O2 binding capacity, low dissociation rate O2 and NO scavenging, O2 carrier, sensing role Trevaskis et al. (1997); Hunt et al. (2001); Dordas et al. (2003, 2004); Spyrakis et al. (2011); Vigeolas et al. (2011); Elhiti et al. (2018) Phytoglobin3 (Phytogb3) Class/type 3 Non-symbiotic hemoglobin/ truncated hemoglobin (tHb) Whole plant, higher in roots Inhibition under hypoxia; induction upon auxin, NO, and H2O2 treatments and biotic stress Modulation of NO and ROS levels during biotic stress CO and O2 in a reversible manner, low O2 affinity O2 carrier, NO dioxygenase activity Watts et al. (2001); Mukhi et al. (2017) Leghemoglobin (Lb) Legume root nodules Nodule-specific expression pattern O2 transport and release during N2 fixation to maintain the flux for respiration High affinity for O2 Facilitate O2 diffusion Wittenberg et al. (1975); Hargrove et al. (1997); Ott et al. (2005) Open in new tab Table 1. Overview of the phytoglobins described in plants Name (correlation between new and old nomenclature) . Tissue specificity . Expression pattern . Processes regulated . Binding capacity . Biophysical role . References . Symbiotic phytoglobin (SymPhytogb) Symbiotic hemoglobin (sHb) Root nodules Nodule-specific expression pattern O2 transport and release during N2 fixation to maintain the flux for respiration High affinity for O2 Facilitate O2 diffusion Appleby et al. (1983); Jacobsen-Lyon et al. (1995); Gopalasubramaniam et al. (2008) Phytoglobin0 (Phytogb0) Non-symbiotic hemoglobin (nsHb) Whole plant Higher expression in gametophytes; induction under hot and cold stresses, exposure to nitrate, and increased sucrose supply NO detoxification under hypoxia stress High affinity for O2 NO scavenging Garrocho-Villegas and Arredondo-Peter (2008) Phytoglobin1 (Phytogb1) Class/type 1 Non-symbiotic hemoglobin (nsHb-1) Embryonic and vegetative organs Induction under hypoxia, ethylene, exposure to nitrate, and increased sucrose supply in roots and rosette leaves, and upon NO and H2O2 treatments Maintenance of NO and O2 levels during cellular hypoxic conditions to modulate energy status Highest affinity for O2, low dissociation rate O2 and NO scavenging, NO dioxygenase activity Trevaskis et al. (1997); Wang et al. (2000); Hunt et al. 2001, 2002); Lira-Ruan et al. (2002); Dordas et al. (2003, 2004); Perazzolli et al. (2004); Cantrel et al. (2011); Thiel et al. (2011); Hartman et al. (2019) Phytoglobin2 (Phytogb2) Class/type 2 Non-symbiotic hemoglobin (nsHb-2) Embryonic and vegetative organs Induction under cytokinin treatment and low temperature Maintenance of NO and O2 levels during cellular hypoxic conditions and during embryogenesis; regulation of oil and sucrose accumulation in seeds Moderate O2 binding capacity, low dissociation rate O2 and NO scavenging, O2 carrier, sensing role Trevaskis et al. (1997); Hunt et al. (2001); Dordas et al. (2003, 2004); Spyrakis et al. (2011); Vigeolas et al. (2011); Elhiti et al. (2018) Phytoglobin3 (Phytogb3) Class/type 3 Non-symbiotic hemoglobin/ truncated hemoglobin (tHb) Whole plant, higher in roots Inhibition under hypoxia; induction upon auxin, NO, and H2O2 treatments and biotic stress Modulation of NO and ROS levels during biotic stress CO and O2 in a reversible manner, low O2 affinity O2 carrier, NO dioxygenase activity Watts et al. (2001); Mukhi et al. (2017) Leghemoglobin (Lb) Legume root nodules Nodule-specific expression pattern O2 transport and release during N2 fixation to maintain the flux for respiration High affinity for O2 Facilitate O2 diffusion Wittenberg et al. (1975); Hargrove et al. (1997); Ott et al. (2005) Name (correlation between new and old nomenclature) . Tissue specificity . Expression pattern . Processes regulated . Binding capacity . Biophysical role . References . Symbiotic phytoglobin (SymPhytogb) Symbiotic hemoglobin (sHb) Root nodules Nodule-specific expression pattern O2 transport and release during N2 fixation to maintain the flux for respiration High affinity for O2 Facilitate O2 diffusion Appleby et al. (1983); Jacobsen-Lyon et al. (1995); Gopalasubramaniam et al. (2008) Phytoglobin0 (Phytogb0) Non-symbiotic hemoglobin (nsHb) Whole plant Higher expression in gametophytes; induction under hot and cold stresses, exposure to nitrate, and increased sucrose supply NO detoxification under hypoxia stress High affinity for O2 NO scavenging Garrocho-Villegas and Arredondo-Peter (2008) Phytoglobin1 (Phytogb1) Class/type 1 Non-symbiotic hemoglobin (nsHb-1) Embryonic and vegetative organs Induction under hypoxia, ethylene, exposure to nitrate, and increased sucrose supply in roots and rosette leaves, and upon NO and H2O2 treatments Maintenance of NO and O2 levels during cellular hypoxic conditions to modulate energy status Highest affinity for O2, low dissociation rate O2 and NO scavenging, NO dioxygenase activity Trevaskis et al. (1997); Wang et al. (2000); Hunt et al. 2001, 2002); Lira-Ruan et al. (2002); Dordas et al. (2003, 2004); Perazzolli et al. (2004); Cantrel et al. (2011); Thiel et al. (2011); Hartman et al. (2019) Phytoglobin2 (Phytogb2) Class/type 2 Non-symbiotic hemoglobin (nsHb-2) Embryonic and vegetative organs Induction under cytokinin treatment and low temperature Maintenance of NO and O2 levels during cellular hypoxic conditions and during embryogenesis; regulation of oil and sucrose accumulation in seeds Moderate O2 binding capacity, low dissociation rate O2 and NO scavenging, O2 carrier, sensing role Trevaskis et al. (1997); Hunt et al. (2001); Dordas et al. (2003, 2004); Spyrakis et al. (2011); Vigeolas et al. (2011); Elhiti et al. (2018) Phytoglobin3 (Phytogb3) Class/type 3 Non-symbiotic hemoglobin/ truncated hemoglobin (tHb) Whole plant, higher in roots Inhibition under hypoxia; induction upon auxin, NO, and H2O2 treatments and biotic stress Modulation of NO and ROS levels during biotic stress CO and O2 in a reversible manner, low O2 affinity O2 carrier, NO dioxygenase activity Watts et al. (2001); Mukhi et al. (2017) Leghemoglobin (Lb) Legume root nodules Nodule-specific expression pattern O2 transport and release during N2 fixation to maintain the flux for respiration High affinity for O2 Facilitate O2 diffusion Wittenberg et al. (1975); Hargrove et al. (1997); Ott et al. (2005) Open in new tab Specifically, PGBs from Class 1 and 2 are key players at the crossroads between O2 and NO, since the former regulates NO turnover and the latter controls O2 delivery and buffering in the tissues in greater depth. These proteins are also involved in the hemoglobin–NO cycle under hypoxia, which has been proposed to relieve the inhibition of the mitochondrial transport chain by O2 deficiency (Dordas et al., 2004; Perazzolli et al., 2004; Igamberdiev et al., 2005; Hebelstrup et al., 2006). This cycle increases the energy status by oxidizing NAD(P)H to enhance the proton flow, resulting in ATP production. Protection against the severe effects of hypoxia depends on the binding capacity for ligands such as O2 or NO, since plants that overexpress a PGB1 mutated with lower O2 affinity are as susceptible to hypoxia as the wild type (Hunt et al., 2002). It is also proposed that PGBs 1 and 2 might function as NRs under certain conditions of extreme hypoxia (Tiso et al., 2012). NO also controls PGBs post-translationally to determine a finely tuned redox balance and energy status, as will be discussed later in this review. The N-degron pathway operates as a nitric oxide and oxygen sensor The plant N-degron pathway is a proteolytic system that recognizes proteins containing certain N-terminal degradation signals, called ‘N-degrons’, and polyubiquitinates them for their degradation through the 26S proteasome (Bachmair et al., 1986; Varshavsky, 2011). This proteolytic pathway exists in prokaryotes and eukaryotes, and the enzyme system responsible for substrate degradation in plants is conserved with higher animals (Graciet et al., 2010). In plants, there are, so far, two different N-degron pathways based on the E3 ligase, PROTEOLYSIS1 and 6 (PRT1 and PRT6), that recognize non-overlapping sets of N-terminal residues. The PCO branch of the PRT6 N-degron pathway functions as both an O2 and NO sensor, as these two gases are required for the degradation of PRT6 substrates (Gibbs et al., 2011, 2014; Licausi et al., 2011) (Fig. 1). Methionine-cysteine (Met-Cys-) initiating substrates undergo four enzymatic reactions prior to their degradation through the proteasome, namely Met excision (carried out by methionine aminopeptidases, MAPs), Cys oxidation (by plant cysteine oxidases, PCOs), arginylation (by arginyl-tRNA-transferases, ATEs), and polyubiquitination (by PRT6). The O2 sensors in plants are thought to be the PCOs (Weits et al., 2014), since these iron-dependent dioxygenases use molecular oxygen to catalyze the Cys oxidation and their Kmapp (O2) values are within a physiologically relevant range for response to both external and internal O2 deficit that enables them to react sensitively to changes in O2 availability (White et al., 2018). Similarly, in mammals, the ADO enzyme is required for O2-dependent degradation of N-degron substrates in human cells (Masson et al., 2019). This enzyme, which was previously assigned as cysteamine dioxygenase, is a thiol oxidase that is functionally identical to PCOs in plants, catalyzing the conversion of the N-terminal Cys to Cys sulfinic acid. Remarkably, when human ADO is expressed under control of the PCO1 promoter, it is able to complement the pco1/2/3/4 Arabidopsis mutant and plants can develop normally. It therefore remains to be explained how NO positively influences the substrate degradation of the PCO branch of the PRT6 N-degron pathway. NO itself could affect the activities of enzymatic components of the pathway (Zarban et al., 2019) or alter the cellular energy balance in an indirect manner (Armstrong et al., 2019). ERFVII group was the first substrate of the PCO branch of the PRT6 N-degron pathway described in plants (Gibbs et al., 2011; Licausi et al., 2011) followed by the transcriptional regulators polycomb repressive complex 2 subunit VERNALIZATION 2 (VRN2) (Gibbs et al., 2018) and LITTLE ZIPPER 2 (ZPR2) (Weits et al., 2019). N-degron pathway substrates regulate important aspects of plant development such as seed storage mobilization (Zhang et al., 2018a, b), germination (Holman et al., 2009; Gibbs et al., 2014), photomorphogenesis (Abbas et al., 2015), stomatal closure (Gibbs et al., 2014), shoot and leaf development (Graciet et al., 2009), root architecture (Shukla et al., 2019), SAM function (Weits et al., 2019), vernalization (Gibbs et al., 2018; Labandera et al., 2020), flowering (Vicente et al., 2017), or leaf senescence (Yoshida et al., 2002), and also regulates stress responses such as flooding (Hartman et al., 2019) or pathogen attack (de Marchi et al., 2016; Vicente et al., 2019; Till et al., 2019). In the case of VRN2 and ZPR2, these transcriptional regulators are located in hypoxic niches. ZPR2 is found in the SAM where it controls the meristem maintenance; VRN2, besides the SAM, is also located in young leaf primordia and root meristematic zones, and has a role in vernalization and root architecture (Weits et al., 2019; Labandera et al., 2020). The physiological hypoxia that exists in these zones prevents these proteins from degradation through the N-degron pathway. A different regulation occurs in the case of the ERFVII group during normoxia or non-stressed growth conditions, where these transcription factors (TFs) are attached to the plasma membrane, avoiding their degradation (Licausi et al., 2011). When hypoxia stress occurs (e.g. flooding), stable ERFVIIs migrate to the nucleus and activate different hypoxia response genes. When flooded, plants rapidly accumulate ET and increase the levels of the NO-scavenger PGB1. This ET-mediated NO depletion, besides hypoxia, promotes ERFVII accumulation and pre-adapts plants to survive subsequent hypoxia (Hartman et al., 2019). These results confirm the key function of the N-degron pathway in the regulation of genetic and molecular networks through NO/O2 balance sensing. Nitric oxide post-translational modifications of key hypoxia molecular players A landmark in NO biology is the ability to modulate protein function and/or stability through three post-translational mechanisms, the nitration of Tyr residues, the S-nitrosation of Cys residues, and the nitrosylation of transition metals (reviewed in Sanz et al., 2015; Sánchez-Vicente et al., 2019b). A higher accumulation of S-nitrosothiols under hypoxic conditions points to this modification as a key feature by which NO exerts its responses (Hebelstrup et al., 2012). S-Nitrosoglutathione reductase (GSNOR) is a master modulator of the intracellular levels of NO and, consequently, controls the concentration of S-nitrosothiols in the cell (Liu et al., 2001). Autophagy constitutes an important recycling process for normal growth and also under stress conditions, including hypoxia (Chen et al., 2015). It has been recently reported that NO is also coupled to hypoxia-related autophagy events through selective S-nitrosation of GSNOR (Zhan et al., 2018). Several key molecular players during the hypoxia adaptive response are described to be controlled by NO. Previous reports indicate that this gasotransmitter inhibits cytochrome c oxidase (COX) (Millar and Day, 1996), aconitase (Gupta et al., 2012), and ascorbate peroxidase 1 (APX1) (Begara-Morales et al., 2014). Consequently, the altered enzymatic activity is reorganized to modulate O2 consumption, optimizing energy usage and supply. The phytohormone ET, NO, and PGB1 are all associated with flooding-induced hypoxia since all of them are induced under O2 deficiency (Hebelstrup et al., 2012; Hartman et al., 2019). Increased NO levels are associated with NR activity under nitrite accumulation (Planchet et al., 2005; Mugnai et al., 2012; reviewed in Gupta and Igamberdiev, 2016). PGB1, critical for plant survival during O2 depletion, is also post-translationally controlled by NO through Cys nitrosation (Perazzolli et al., 2004; Rubio et al., 2019), metal nitrosylation (Perazzolli et al., 2004), and Tyr nitration (Sainz et al., 2015). Interestingly, the binding of NO to the heme group of PGBs affects the scavenging of this molecule (Gupta et al., 2011). The interplay between NO and ET also impacts plant responses. Previous reports proved that both gases may affect each other, depending on the developmental stage and stress conditions studied (Magalhaes et al., 2000; Li et al., 2016; Liu et al., 2017; Singh and Bhatla, 2018). Recently, these molecules were linked to PGB1 during flooding events, establishing a complex cycle that involved the requirement of all of them for the correct plant adaptation (Hebelstrup et al., 2012; Hartman et al., 2019). This overview showed us the intricate network governing hypoxia dynamic responses, mainly directed by the connection and coordination among PGB1, ET, and NO to maintain the energy state. Abscisic acid (ABA) also participates in the response to hypoxic conditions, such as root flooding (Hsu et al., 2011) or the seed environment before germination (Benech-Arnold et al., 2006), and its exogenous application promotes hypoxia tolerance in roots (Ellis et al., 1999). In fact, ABA perception and signaling constitute a key hormonal network affected by the N-degron pathway (Holman et al., 2009; Vicente et al., 2017). Nitric oxide impact on somatic embryogenesis and seed germination under low oxygen conditions Somatic embryogenesis is the initiation of autonomous embryo development in somatic cells in response to exogenous and/or endogenous signals (Fehér, 2014), and is considered to be one of the most extreme examples of flexibility in plant development (Fehér et al., 2003). The phases of somatic embryogenesis as a morphogenic phenomenon are characterized by distinct biochemical and molecular events (Suprasanna and Bapat, 2005). The first phase is the induction stage in which differentiated somatic cells acquire embryogenic competence. This phase is followed by the expression or initiation of somatic embryogenesis in which competent cells or proembryos start developing. Finally, during maturation, somatic embryos anticipate germination by desiccation and accumulation of reserves (Jiménez, 2001). Two categories of inductive conditions which allow differentiated cells to develop into competent dedifferentiated cells are now recognized. These include plant growth regulators and stress factors (reviewed in Zavattieri et al., 2010). It has been described that this process is generally favored by mild hypoxia (Thorpe and Stasolla, 2001), which mimics the low O2 environment accompanying zygotic embryo development (Rolletschek et al., 2003) (Fig. 2). Fig. 2. Open in new tabDownload slide Network of NO and low oxygen interactions in a developmental stage-based context. Somatic embryogenesis, seed germination, RAM, and SAM. (A) The SAM displays a state of physiological hypoxia which prevents N-degron pathway activation, that is also influenced by low NO levels. VRN2 contributes to vernalization and hypoxia tolerance, while ZPR2 sustains leaf production in the SAM. (B) SE is generally favored by mild hypoxia, and oxidative stress-inducing compounds promote dedifferentiation by increasing endogenous auxin levels. NO stimulates the activation of cell division and embryogenic cell formation in some systems. Mutation of PGB2 increases the number of somatic embryos by suppressing the expression of MYC2 and induces the transcription of several IAA biosynthetic genes promoting SE. (C) NO is necessary for completion of germination; NO binds to ABI5, through Cys S-nitrosation of Cys153, and promotes the interaction with CULLIN4-based and KEEP ON GOING E3 ligases and consequently its degradation by the proteasome. ABI5 is modulated by NO and O2 through the N-degron pathway. Members of the ERFVII group have been identified as ABI5 transcriptional activators. (D) NO is necessary for normal RAM organization; however, high levels of NO reduce PIN1-dependent auxin transport, reducing RAM activity. NO influences meristem size and promotes PR root growth by preventing N-degron pathway activation. (E) NO donor treatments promote lateral root growth in a dose-dependent manner, NO could be promoting RAP2.12 degradation and thus reducing LRP stabilization and inhibiting LR density. Arrows and bars indicate positive and inhibitory effects, respectively. Dotted arrows and bars indicate putative regulations (created with BioRender.com). ZPR2 (protein LITTLE ZIPPER 2); VRN2 (VERNALIZATION 2); PGB2 (phytoglobin 2); MYC2 (basic helix–loop–helix protein 6); IAA (indole-3-acetic acid); ABA (abscisic acid); ABI5 (ABA INSENSITIVE 5); ERFVII (Group VII ethylene response factors); PRT6 (PROTEOLYSIS 6); PIN1 (PIN-FORMED 1); SAM (shoot apical meristem); SE (somatic embryogenesis); RAM (root apical meristem); PR (primary root); LR (lateral root). Fig. 2. Open in new tabDownload slide Network of NO and low oxygen interactions in a developmental stage-based context. Somatic embryogenesis, seed germination, RAM, and SAM. (A) The SAM displays a state of physiological hypoxia which prevents N-degron pathway activation, that is also influenced by low NO levels. VRN2 contributes to vernalization and hypoxia tolerance, while ZPR2 sustains leaf production in the SAM. (B) SE is generally favored by mild hypoxia, and oxidative stress-inducing compounds promote dedifferentiation by increasing endogenous auxin levels. NO stimulates the activation of cell division and embryogenic cell formation in some systems. Mutation of PGB2 increases the number of somatic embryos by suppressing the expression of MYC2 and induces the transcription of several IAA biosynthetic genes promoting SE. (C) NO is necessary for completion of germination; NO binds to ABI5, through Cys S-nitrosation of Cys153, and promotes the interaction with CULLIN4-based and KEEP ON GOING E3 ligases and consequently its degradation by the proteasome. ABI5 is modulated by NO and O2 through the N-degron pathway. Members of the ERFVII group have been identified as ABI5 transcriptional activators. (D) NO is necessary for normal RAM organization; however, high levels of NO reduce PIN1-dependent auxin transport, reducing RAM activity. NO influences meristem size and promotes PR root growth by preventing N-degron pathway activation. (E) NO donor treatments promote lateral root growth in a dose-dependent manner, NO could be promoting RAP2.12 degradation and thus reducing LRP stabilization and inhibiting LR density. Arrows and bars indicate positive and inhibitory effects, respectively. Dotted arrows and bars indicate putative regulations (created with BioRender.com). ZPR2 (protein LITTLE ZIPPER 2); VRN2 (VERNALIZATION 2); PGB2 (phytoglobin 2); MYC2 (basic helix–loop–helix protein 6); IAA (indole-3-acetic acid); ABA (abscisic acid); ABI5 (ABA INSENSITIVE 5); ERFVII (Group VII ethylene response factors); PRT6 (PROTEOLYSIS 6); PIN1 (PIN-FORMED 1); SAM (shoot apical meristem); SE (somatic embryogenesis); RAM (root apical meristem); PR (primary root); LR (lateral root). An increasing number of publications link ROS and somatic embryogenesis. Oxidative stress-inducing compounds increase the cell endogenous auxin levels and promote dedifferentiation (Pasternak et al., 2002; Correa-Aragunde et al., 2006). Ötvös et al. (2005), working with alfalfa cell cultures, showed that H2O2 and NO have a promoting effect on somatic embryogenesis. NO stimulates the activation of cell division and embryogenic cell formation in leaf protoplast cells of alfalfa in the presence of auxins. In Arabidopsis, PGB1 scavenges NO produced under severe hypoxia, thus fulfilling a protective role during stress conditions (Dordas et al., 2003, 2004; Perazzolli et al., 2004). Like PGB1, overexpression of PGB2 enhances survival under hypoxic conditions through removal of cellular NO (Hebelstrup et al., 2006, 2012; Hebelstrup and Jensen, 2008). Mutation of PGB2 increases the number of Arabidopsis somatic embryos by suppressing the expression of MYC2, a repressor of auxin synthesis, and inducing the transcription of several indole-3-acetic acid (IAA) biosynthetic genes (Elhiti et al., 2013). An experimental reduction of NO through pharmacological treatments reverses the effects of PGB2 suppression on somatic embryogenesis (Elhiti et al., 2013). This phenotype can be reversed by the re-introduction of PGB2 in the nucleus but not in the cytoplasm; this promotive effect can be attenuated by reducing the level of NO (Godee et al., 2017). Embryo production in Arabidopsis appears to be susceptible to NO levels, as it is increased in the presence of the NO donors sodium nitroprusside (SNP) and S-nitroso-N-acetylpenicillamine (SNAP) and is decreased after scavenging with 2-phenyl-4,4,5,5,-tetramethylimidazoline-1-oxyl 3-oxide (PTIO) and carboxy-PTIO (Elhiti et al., 2013). Hypoxia is also linked to non-stress conditions, but at specific developmental stages such as seed imbibition and germination. The outermost layers of seed restrict O2 diffusion, leading to hypoxic or even almost anoxic states of inner seed tissues (Borisjuk et al., 2007). NO accumulation in response to O2 deficiency was described, avoiding endogenous anoxia and fermentation (Borisjuk et al., 2007). This gasotransmitter mediates a reversible O2 balance through modulation of respiratory fluxes, facilitating energy supply for the synthesis of storage compounds. PGB1 and 2 overexpression also promotes the metabolic reprogramming and lower NO content in the seed (Thiel et al., 2011; Vigeolas et al., 2011), highlighting again the importance of the molecular team composed of O2, NO, and PGBs. NO burst was also described during early seed germination events (Simontacchi et al., 2004; Albertos et al., 2015). This NO free gas is absolutely necessary for completion of germination at different molecular levels, converging into the bZIP TF ABI5 (reviewed in Sánchez-Vicente et al., 2019a, b). This TF represents a molecular hub during germination repression mediated by ABA (Finkelstein and Lynch, 2000; Lopez-Molina et al., 2001). NO binds directly to ABI5, through Cys S-nitrosation of Cys153, promoting the interaction with CULLIN4-based and KEEP ON GOING E3 ligases and consequently its degradation by the proteasome (Albertos et al., 2015). Additional post-translational levels of ABI5 regulation by NO correspond to the SUMO E3 ligase SIZ1, which is considered a Tyr nitration target (Lozano-Juste et al., 2011), and to the SNF1-RELATED PROTEIN KINASE2 (SnRK2), whose activity is inhibited by S-nitrosation (Wang et al., 2015). At the transcriptional level, ABI5 is also modulated by NO and O2 through the N-degron pathway. Members of the ERFVII group were identified as ABI5 transcriptional activators (Gibbs et al., 2014). Additionally, the ERFVII group controls the ABI5 transcriptional repressor BRAHMA (Vicente et al., 2017). The network integrated by NO, O2, and PGBs tightly regulates ABI5, at both the transcriptional and post-translational levels, highlighting the fine-tuning mechanisms controlling early developmental stages, which are governed by low O2 abundance. Nitric oxide function in the RAM and SAM, locations with scarce oxygen concentration Meristems are populations of small, isodiametric cells with embryonic characteristics. Vegetative meristems are self-perpetuating; not only do they produce all tissues and organs, but they also retain their embryonic character indefinitely (Taiz et al., 2014). Previous studies have measured and defined the O2 concentration profile in the maize RAM (Gibbs et al., 1998; Darwent et al., 2003) and, more recently, Weits et al. (2019) shaped the O2 profile in the Arabidopsis SAM, using a micro-scale Clark-type oxygen sensor. Both meristems display a decrease in O2 concentration in the central zone, the area committed to the maintenance of the stem cells that sustain growth and development. Besides O2 levels, NO has an important role in the maintenance of the meristems, and alteration in NO homeostasis is sufficient to influence the fate of whole meristems. NO is necessary for normal RAM organization (Sanz et al., 2014); however, high levels of NO reduce auxin transport via a PIN1-dependent mechanism and RAM activity is reduced concomitantly (Fernández-Marcos et al., 2011; Sanz et al., 2014). Some substrates of the N-degron pathway are found in meristems, where they have important functions (Gibbs et al., 2018; Weits et al., 2019; Labandera et al., 2020). The physiological hypoxia that exists in the meristems prevents its degradation through the N-degron pathway. During hypoxia, NO levels must be also kept low to prevent N-degron pathway activation. ZPR2 sustains leaf production in the SAM (Weits et al., 2019), and VRN2 is found in the SAM, RAM, and lateral root primordia (LRPs) where it contributes to vernalization (cold-induced flowering) and hypoxia tolerance (Gendall et al., 2001; Gibbs et al., 2018). In LRPs, stabilized RAP2.12 (a member of ERFVII group) induces expression of core hypoxia-responsive genes, promoting LRP stabilization by attenuating auxin signaling (Shukla et al., 2019). Remarkably, there is a differential gene regulation between LRPs and the RAM since these hypoxia-responsive genes are not expressed in the RAM. According to this, NO donor treatments promote lateral root growth in a dose-dependent manner, while primary root growth is arrested (Correa-Aragunde et al., 2004). In LRPs, NO could be promoting RAP2.12 degradation and thus reducing LRP stabilization. PGB gene expression patterns in meristems (Heckmann et al., 2006; Hebelstrup et al., 2007, 2012) may indicate that these proteins are facilitating, alongside hypoxia, the stabilization of N-degron pathway substrates by reducing NO levels. PGBs also have a central role in the protection of meristems during stress, specifically the RAM. This meristem is particularly susceptible to environmental perturbations (e.g. salinity, drought, and flooding) since it is directly exposed to the soil. NO overaccumulates at the root tip under stress (Fernández-Marcos et al., 2011; Liu et al., 2015), risking RAM functionality. High levels of NO increase ET production to inhibit meristematic cell proliferation and to induce cell death through ROS (Mira et al., 2016b). PGBs have been reported to protect meristems during polyethylene glycol (PEG)-induced water stress (Mira et al., 2017) and hypoxia (Mira et al., 2016b) (Fig. 3). Under these conditions, PGBs accumulate to reduce the programmed cell death (PCD) initiated by the high levels of NO and mediated by ET via ROS (Mira et al., 2016b, 2017). In addition, plants with jeopardized PGB1 gene expression show a number of shoot- and leaf-related phenotypes that include flowering delay, the tendency of the SAM to reverse from the bolting stage to the rosette stage (Hebelstrup and Jensen, 2008), and stunted leaves with enlarged hydathodes (Hebelstrup et al., 2006). These phenotypes are coincident with NO accumulation in the affected organs, which hints at a role for PGBs in modulation of NO signaling during plant development (Hebelstrup et al., 2007). Fig. 3. Open in new tabDownload slide Network of NO and low oxygen interactions in a stress-based context. Abiotic and biotic stresses. Left: abiotic stress such as flooding causes NO and ethylene (ET) accumulation. ET signaling promotes enhanced levels of the NO-scavenger phytoglobin 1 (PGB1), limiting Group VII ethylene response factor (ERFVII) degradation through inactivation of the PRT6 N-degron pathway. ERFVII members induce expression of core hypoxia response genes. In roots, PGBs also protect meristems during PEG-induced water stress and hypoxia, since they scavenge NO to prevent programmed cell death (PCD), a process initiated by the overaccumulation of NO and mediated by ET and ROS. Right: after certain pathogen attacks, the respiration rate increases in the plant, leading to local hypoxia that promotes accumulation of ERFVII members. The oxidative burst (ROS and NO) as a response to the infection can trigger PCD and promotes, along with ERVII members, activation of defense genes. In addition, flooded soils predispose root plants to infections by soilborne pathogens (created with BioRender.com). EIN2 (ETHYLENE INSENSITIVE 2); PGB1 (phytoglobin 1); ERFVII (Group VII ethylene response factors); ROS (reactive oxygen species); PCD (programmed cell death). Fig. 3. Open in new tabDownload slide Network of NO and low oxygen interactions in a stress-based context. Abiotic and biotic stresses. Left: abiotic stress such as flooding causes NO and ethylene (ET) accumulation. ET signaling promotes enhanced levels of the NO-scavenger phytoglobin 1 (PGB1), limiting Group VII ethylene response factor (ERFVII) degradation through inactivation of the PRT6 N-degron pathway. ERFVII members induce expression of core hypoxia response genes. In roots, PGBs also protect meristems during PEG-induced water stress and hypoxia, since they scavenge NO to prevent programmed cell death (PCD), a process initiated by the overaccumulation of NO and mediated by ET and ROS. Right: after certain pathogen attacks, the respiration rate increases in the plant, leading to local hypoxia that promotes accumulation of ERFVII members. The oxidative burst (ROS and NO) as a response to the infection can trigger PCD and promotes, along with ERVII members, activation of defense genes. In addition, flooded soils predispose root plants to infections by soilborne pathogens (created with BioRender.com). EIN2 (ETHYLENE INSENSITIVE 2); PGB1 (phytoglobin 1); ERFVII (Group VII ethylene response factors); ROS (reactive oxygen species); PCD (programmed cell death). Role of nitric oxide signaling between low oxygen and biotic stress Plants rely on a sophisticated network of signal transduction pathways to respond to pathogen attacks and unfavorable environmental conditions, which leads to metabolic and transcriptional reprogramming (Valeri et al., 2020). Several phytohormones have been related to plant defense, among them salicylic acid (SA) is predominantly associated with biotrophs, while jasmonic acid (JA) and ET are associated with necrotrophs (Wildermuth et al., 2001; Thaler et al. 2004; reviewed in Conrath, 2006; Halim et al.. 2006). Although NO in plants is being revealed to be involved in a great variety of cellular processes associated with growth and development (reviewed in Sanz et al., 2015), it was first described as a molecule involved in the plant immune response (Delledonne et al., 1998; Durner et al., 1998). Basal defenses and hypersensitive responses rely on NO (Mur et al., 2013). For instance, modulation of Pgb expression, which is naturally up-regulated by low oxygen tensions (Taylor et al., 1994; Hunt et al., 2002), has been shown to influence plant responses to a variety of pathogens, and suppression of Pgb resulted in elevated levels of NO, hydrogen peroxide, and JA in Arabidopsis plants infected with Botrytis cinerea (Mur et al., 2012; reviewed in Mira et al., 2016a). One of the earliest cellular responses following successful pathogen recognition is the so-called oxidative burst, which is a rapid, transient production of ROS via consumption of O2, that can trigger hypersensitive cell death (Wojtaszek, 1997; Govrin and Levine, 2000; Torres et al., 2006). In this context, it is difficult to separate NO from ROS, considering that their signaling pathways in plant biotic interactions are closely connected (Scheler et al., 2013; reviewed in Sánchez-Vicente et al., 2019b). NO also plays a major role in the signaling pathways of phytopathogenic fungi. For instance, the expression of the B. cinerea flavohemoglobin gene (Bcfhg1), which is the main NO detoxification method in this fungus, is developmentally regulated, with peak expression levels during germination of conidia, and is enhanced very quickly upon exposure to NO of germinating conidia. It is believed that the production of NO by B. cinerea is probably modulated to promote fungal colonization of the plant tissue (Turrión-Gómez et al., 2010; Turrión Gómez and Benito, 2011). Furthermore, the application of external NO to Colletotrichum coccodes defers spore germination, whilst treatment with NO scavengers stimulates spore germination (Wang and Higgins, 2005). Moreover, low O2 predisposes plants to infection by soilborne pathogens (Fig. 3). For instance, oxygen-deficient soils stress plants and predispose them to infection by water molds such as Pythium and Phytophthora cinnamomi (Davison et al. 1993), and O2-deprived roots leak greater amounts of soluble metabolites and ethanol, attracting zoospores (Kozlowski, 1997; Badri and Vivanco, 2009). Thus, as an aerobic organism and in a water-saturated growing medium, P. cinnamomi zoospores will infect roots near the surface where there is enough O2. The inactivation of different components of the Arg/N-degron pathway results in greater susceptibility of Arabidopsis to necrotrophic pathogens. Thus, it has been shown that induction of components of the hypoxia response, controlled by the ERFVIIs, enhanced clubroot disease progress, indicating that the protist hijacks the N-end rule ERFVII regulation system to enhance infection (Gravot et al., 2016). Early studies indicate that RAP2.3, and maybe other ERFVII TFs, might be key regulators in both the low-oxygen and plant biotic stress responses (Valeri et al., 2020). The results of Kim et al. (2018) show that OCTADECANOID-RESPONSIVE ARABIDOPSIS 59 (ORA59), one of the best characterized ERF TFs involved in B. cinerea resistance, interacts with RAP2.3, and its expression is induced synergistically by JA and ET, confirming its importance in the JA and ET signaling pathway (Pré et al., 2008). In this regard, Arabidopsis plants overexpressing RAP2.2 and a mutant line showed higher resistance and more susceptibility, respectively, suggesting an important role for RAP2.2 against the infection by the necrotroph (Zhao et al., 2012). A recent study conducted by Valeri et al. (2020) indicates that infection by B. cinerea induces increased respiration, leading to a drastic drop in the O2 level in the leaf and that the establishment of this local hypoxic area results in stabilization and nuclear relocalization of RAP2.12. As a consequence, this nuclear relocalization activates the hypoxia-responsive gene network, implying that ERFVII proteins can become stabilized in infected tissue and have an influence in pathogen resistance, allowing RAP2.3 to form a complex with ORA59 to regulate plant defense genes (Kim et al., 2018) or influencing other proteins with a hypoxia-dependent stabilization. Concluding remarks Among the challenges imposed by global warming, the forecast of unexpected and increased floods will cause limitations in plant normal development and productivity for agricultural purposes. Therefore, the control of plant responses to this hypoxia scenario is a landmark aspect for future research, as it critically impacts on seed germination, plant development and establishment, and, consequently, on plant productivity. The identification of the elements and the molecular bases that participate in hypoxic stress responses is essential to understand their function in the plant, which is a prerequisite for its genetic improvement. Thus, advances in the study of plant priming using NO-related compounds to enhance hypoxia tolerance could be achieved in a similar way to ET and ABA pre-treatments (Ellis et al., 1999; Hartman et al., 2019). In parallel, this environmental modification can favor the development of new plant pests and pathogens or increase the incidence levels of those that exist today. Nowadays some controversy still surrounds the NO homeostasis in plant immunity, at the level of both production and turnover (reviewed in Vandelle et al., 2016), that needs to be solved for a better pest control. The N-degron pathway was identified as a new NO sensor that functions through its ability to destroy specific regulatory proteins bearing N-terminal Cys residues in mammals (Hu et al., 2005; Masson et al., 2019). In plants, apart from the evidence reported by Gibbs et al. (2014, 2018) on the proteolytic control of ERFVII group of TFs and polycomb repressive complex 2 subunit VRN2, respectively, no other target has been related to NO directly. Deciphering the mechanism of NO sensing, by direct binding of the molecule, and the post-translational regulation of molecular targets across the different components of the N-degron pathway will shed light on controlling hypoxia, which is detrimental for plant survival. Acknowledgements This work was financed by grants BIO2017-85758-R from the Ministerio de Ciencia, Innovación y Universidades (MICIU), SA313P18 from Junta de Castilla y León and Escalera de Excelencia CLU-2018-04 co-funded by the P.O. FEDER of Castilla y León 2014–2020 Spain (to OL), and FS/26-2017 and FS/16-2019 from Fundación Solórzano (to IS-V). IM-G is supported by a FPU grant from the Ministerio de Universidades. We thank the BIO2015-68957-REDT and RED2018-102397-T Spanish network for stimulating discussions. Author contributions All authors contributed equally to the conceptualization, writing of the original draft, review. and editing. 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Published by Oxford University Press on behalf of the Society for Experimental Biology.
TI - Nitric oxide function during oxygen deprivation in physiological and stress processes
JF - Journal of Experimental Botany
DO - 10.1093/jxb/eraa442
DA - 2021-02-11
UR - https://www.deepdyve.com/lp/oxford-university-press/nitric-oxide-function-during-oxygen-deprivation-in-physiological-and-o30NCpsJRU
SP - 904
EP - 916
VL - 72
IS - 3
DP - DeepDyve
ER -