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Polyamine Oxidases-Generated Hydrogen Peroxide in Plant Development: Comparison
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Metabolism and regulation of cellular polyamine levels are crucial for living cells to maintain their homeostasis and function. Polyamine oxidases (PAOs) terminally catabolize polyamines or catalyse the back-conversion reactions when spermine is converted to spermidine (Spd) and Spd to putrescine. Hydrogen peroxide (H2O2) is a by-product of both the catabolic and back-conversion processes. Pharmacological and genetic approaches have started to uncover the roles of PAO-generated H2O2 in various plant developmental and adaptation processes such as cell differentiation, senescence, programmed cell death, and abiotic and biotic stress responses.

  • polyamines
  • polyamine oxidase
  • polyamine catabolism
  • hydrogen peroxide
  • plant development
  • stress response

1. Introduction

Polyamines (PAs) are small, positively-charged organic molecules that are present in all living organisms. PAs show tissue- and organ-specific distribution patterns [1][2]. The most relevant PAs in plant cells are putrescine (Put), spermidine (Spd), and spermine (Spm). In plants, PA biosynthesis produces Put from arginine catalysed by the arginine decarboxylase enzyme (ADC), but in several plants, the ornithine decarboxylase (ODC) can also synthesise Put from ornithine [2][3][4]. Put can be converted to Spd by spermidine synthase (SPDS), which can be further converted to Spm by spermine synthase (SPMS). Thermospermine (t-Spm) is a specially modified polyamine synthesized by the thermospermine synthase (named ACAULIS5 or ACL5 in Arabidopsis) by transferring an aminopropyl residue to the N- terminal amino group of Spd [5]. Some species also have cadaverin (Cad) which is synthesized from lysine through a fully independent pathway by ornithine/lysine decarboxylases (O/LDCs) [6]. PAs can be found in plant cells in different forms, such as free, covalently conjugated, or non-covalently conjugated ones. The covalently conjugated PAs can be further classified as perchloric acid-soluble or insoluble [2].
PAs are involved in cell division, organ development, leaf senescence, fruit development and ripening, and abiotic stress responses, [2][7][8]. The involvement of PAs in stress tolerance has many aspects. They directly interact with and protect macromolecules and organelle membranes acting as compatible solutes. Further, they (in)directly scavenge oxygen and hydroxyl radicals, promote the production of hydrogen peroxide (H2O2) acting as a signal molecule, thereby contributing to the production of antioxidant enzymes and metabolites, contribute to nitric oxide (NO) production, regulate ion channels and metabolic activities, for example, limit ammonia toxicity [1][8]. Their cellular levels depend on the different phases of plant growth and development and the level and form of environmental stress experienced by the plant [1]. Exogenous applications of PAs often result in higher stress tolerance, but higher than optimal levels prove to be toxic [8]. It is clear, therefore, that the polyamine homeostasis of the cells must be tightly regulated to ensure their proper functioning and adaptation. Neither the direct relationship between increased levels of PAs and abiotic stress tolerance nor the mechanism by which PAs regulate plant growth and stress responses is still fully understood [2][9].
Plants, in response to different stress stimuli but also during normal metabolism, produce reactive oxygen species (ROS). These include oxygen radicals such as superoxide anion (O2•-), hydroperoxyl radical (HO2), alkoxy radical (RO•), and hydroxyl radical (HO•), as well as nonradicals such as hydrogen peroxide (H2O2) and singlet oxygen (1O2). At higher concentrations, ROS can damage cell content, which can lead to programmed cell death [10]. Therefore, their levels must be tightly controlled [11][12]. To avoid harmful ROS accumulation, plants have developed various ROS scavengers [11]. Plants deal with oxidative stress primarily by enzymatic and non-enzymatic antioxidants present in all cellular compartments [12][13].
Despite their potentially harmful nature, ROS are involved in the regulation of various metabolic, physiological, and developmental processes [12][14][15][16]. To name a few, ROS are needed for the development of root and shoot apical meristems, the emergence of lateral roots, and the polar growth of root hair cells and pollen tubes. ROS can specifically alter gene expression [16][17] and transmit information about changing environmental conditions [12][15][16]. Nevertheless, it's hardly know about the perception of ROS and the immediate downstream elements of their signalling [11]. ROS can act locally but can also spread from the place of synthesis [18]. Among ROS, H2O2 has the longest half-life (ca. 1ms) and thus can signal from the longest distance, even between cells in the apoplast [19].
In plants, the NADPH oxidases (NOX), also called respiratory burst oxidase homologs (RBOHs), are located in the plasma membrane and contribute to apoplastic H2O2 accumulation. Their enzymatic activity catalyses the production of apoplastic O2•- by transferring electrons from cytosolic NADPH or NADH to apoplastic O2. O2•- is further converted to H2O2 by superoxide dismutases [20]. NADPH oxidases are involved in abiotic and biotic stress responses and various aspects of plant development [13][20]. In Arabidopsis thaliana, ten isoforms of the NADPH oxidase enzyme have been identified. They are named RBOH (A–J), of which RBOHD and RBOHF play crucial roles in both biotic and abiotic stress responses. Others, such as RBOHC, RBOHH, and RBOHJ, are rather related to plant developmental processes [21].
Along with other flavoenzymes, such as the NADPH oxidases and xanthine dehydrogenase/oxidases (XDH), the flavin adenine dinucleotide (FAD)-dependent polyamine oxidases (PAOs) and the copper amine oxidases (CuAOs), also called diamine oxidases (DAOs), generate ROS [22][23]. CuAOs oxidize Put and Cad at the primary amino groups, producing ammonia, H2O2, and an aminoaldehyde. The Arabidopsis thaliana genome contains 10 CuAO genes [22][24]. CuAOs show tissue-specific expression patterns and localize in different compartments of the cells, such as the apoplast, peroxisomes, or vacuoles [24].
Plant PAOs can be classified into two classes based on their functions in PA catabolism. The first class of PAOs is responsible for the terminal catabolism of PAs. The reaction they catalyse leads to the oxidation of Spd or Spm, which results in the production of H2O2, 1,3-diaminopropane (DAP), and 4-aminobutanal (in the case of Spd catabolism) or N-(3-aminopropyl)-4- aminobutanal (in case of Spm catabolism). The PAOs in the second class catalyse PAs back-conversion reactions, such as the conversion of Spm to Spd and Spd to Put. These PAOs also generate H2O2 as a product of their catalytic activity. The PA terminal catabolic pathway is specifically activated extracellularly, whereas the PA back-conversion pathway mainly occurs in the intracellular space in the cytoplasm and mostly in peroxisomes [25]. PAOs may have substrate specificities and tissue-dependent differences in their expression pattern [26][27]. Considering their cellular localization, apoplastic, cytosolic, and peroxisomal PAOs are distinguished [3][22]. Until recently, PAO genes were characterized in both monocots and dicots [4][28]. The best-studied and characterized PAO is an apoplastic PAO (ZmPAO) of maize [29][30]. In Arabidopsis thaliana, the PAO isoforms are coded by five PAO genes. AtPAO1 catalyses the oxidation of Spm, [31] while AtPAO3 prefers Spd as substrate [32]. AtPAO2 and AtPAO4 have similar affinity for both Spd and Spm [33]. Interestingly, AtPAO5 is a t-Spm oxidase, as it catalyses the back-conversion of t-Spm to Spd [27]. PAOs achieve different optimal pH values and operation temperatures upon catalysing different reactions [33][34]. Emerging evidence suggests that PAOs and PA catabolic products play a critical signalling role in a variety of cellular and developmental processes [2][4][25]. These roles are likely mediated via the regulation of PA homeostasis, as well as the generation of H2O2.

2. PAOs and H2O2 in Plant Development

There is accumulating evidence suggesting that PAs interfere with various biological processes through the generation of H2O2 during their catabolism [4][7]. In agreement, the participation of PAOs has been reported in many developmental processes where ROS are involved.

2.1. PAOs in Cell Differentiation

Overexpression of the maize (Zea mays) ZmPAO1 resulted in early xylem differentiation and strongly affected root development in transgenic tobacco plants in correlation with augmented H2O2 production and increased rate of cell death [35]. This PAO was shown to accumulate in the cell wall of xylem precursors parallel to secondary wall deposition [30]. The AtPAO5 enzyme that specifically accumulates in the vascular system has also been reported to participate in xylem differentiation [36][37]. Although most PAOs generate ROS as a by-product of their activity, AtPAO5 preliminary control PA, especially t-Spm, levels [27][36][37]. Since AtPAO5 acts rather as a dehydrogenase than oxidase, it does not produce excess H2O2 [36]. In this way, AtPAO5 indirectly controls xylem differentiation via maintaining t-Spm homeostasis required for normal growth [36][38]. AtPAO5, via controlling the t-Spm level, was hypothesized to contribute to the tightly controlled interplay between auxins and cytokinins during the xylem differentiation process [37]. Nevertheless, there is ample evidence suggesting that the production of H2O2 by PA catabolism contributes to the cross-linking of cell wall polysaccharides during cell wall maturation [30][35]. For example, the apoplastic maize ZmPAO enzyme was shown to provide ROS for peroxidase-mediated wall stiffening during wound healing [39][40]. Moreover, rice OsPAO7 was hypothesized to control lignin synthesis in anther cell walls [41]. The polar growth of pollen tubes correlates with ROS accumulation at their tip region, controlling hyperpolarization-activated Ca2+ channels and cell wall stiffening [42]. Exogenous polyamines modulate pollen tube growth dependent on ROS generation [43]. In agreement, Spd treatment was reported to promote the opening of Ca2+ channels in pollen tubes [44]. Mutations in the AtPAO3 gene blocked the effect of Spd on Ca2+ channels and pollen tube growth, indicating that the effect was dependent on AtPAO3-mediated Spd degradation. Untreated pollen tubes of the AtPAO3 mutant also exhibited retarded growth, supporting the view that AtPAO3-generated ROS contributes to pollen tube growth [44]. The observation that the Arabidopsis polyamine transporter ABCG28 is required for the apical accumulation of ROS in growing pollen tubes and root hairs [45] further strengthens this hypothesis. PAs and their catabolism play a role in the induction of Ca2+ and K+ fluxes also in roots during stress adaptation [46], supporting the general significance of the PA-PAO-ROS-Ca2+ signalling connection. PAs are well known to be required for and promote in vitro plant regeneration, although the mechanism is largely uncovered (reviewed by [47]). It was suggested that metabolic degradation products of PAs, such as t-Spm and/or H2O2, can at least be partly responsible for the observed effects [48]. The expression of AtPAO5, unlike other AtPAO-coding genes, increased in parallel with the conversion of lateral root primordia to shoot meristem during direct in vitro organogenesis [48]. Furthermore, the ectopic expression of AtPAO5 but not AtPAO2 promoted the process. It was hypothesized that AtPAO5 exerted its effect via the modulation of the t-Spm homeostasis rather than H2O2 production [48] since AtPAO5, unlike the other AtPAO enzymes, is known to have a stronger dehydrogenase than oxidase activity and has a high affinity for t-Spm as substrate [36]. Interestingly, AtPAO5 had been reported to have a negative effect on indirect (via auxin-induced callus formation) [49] and not direct (via cytokinin-induced meristem conversion) [48] shoot regeneration from Arabidopsis roots. This strengthens the view that maintaining t-Spm homeostasis is the primary function of AtPAO5 [27] since t-Spm was shown to suppress auxin signalling [50], which plays a different role in direct and indirect shoot regeneration from Arabidopsis roots [51]. Furthermore, H2O2 as the metabolic product of PAs was found to be essential for the maintenance and propagation of embryogenic calli and their conversion into somatic embryos in cotton [52], indicating a more general role of PA catabolism in plant regeneration in vitro.

2.2. PAOs in Senescence and Programmed Cell Death

The link among PAs, ROS, and leaf senescence has been long established (reviewed in [53]). Augmenting transcription and activity of PA catabolic enzymes has been demonstrated during dark-induced senescence of barley leaves [53][54]. Inhibiting the PAO activity delayed the senescence process in parallel with Spm accumulation and reduced ROS production. In agreement, the Arabidopsis atpao4 mutant exhibited delayed senescence in correlation with high Spm levels but reduced ROS accumulation [55]. Altogether, the observations indicate that PAO-generated H2O2 is involved in leaf senescence. PA catabolism has been also associated with fruit ripening, a senescence-like developmental process in grapes, tomatoes, and peaches [56][57][58]. Fruit ripening is associated with the increased expression of genes coding for apoplastic PAO enzymes, catalysing the terminal oxidation of PAs. Inhibition of PAO activity reduced ethylene production and flesh softening of peach fruits and the expression of ripening-related genes, while PA contents were dramatically increased. The role of PAO-generated H2O2 as a ripening-promoting signal molecule was hypothesised as one of the potential mechanisms [22]. PAO-generated H2O2 was shown to contribute to developmental PCD during xylem differentiation [35][59]. Polyamine oxidases were also found to be key elements in the oxidative burst, leading to programmed cell death in cryptogein-treated tobacco-cultured cells [60]. Moreover, tobacco plants overexpressing the transgene coding for the same maize PAO enzyme had high H2O2 levels, which in some cases led to programmed cell death (PCD) [61].

3. PAOs and H2O2 in Plant Adaptation

3.1. PAOs and Abiotic Stress Responses

There is overwhelming evidence that increasing the polyamine content contributes to cell protection under environmental stress conditions. PAs take part in osmoprotection, stabilisation of macromolecular complexes, maintenance of the ion homeostasis, scavenging ROS, and stress and hormone signalling [2][62]. Not only biosynthesis, but PA catabolism has also been shown to have a significant role in various abiotic stress responses [25][63]. These roles can at least partly be attributed to the products of PA catabolism catalysed by DAO and PAO enzymes, such as gamma-aminobutyric acid (GABA) and/or H2O2 [63]. GABA, which is mainly synthesized in PA-independent pathways but can also be produced from PA-derived 4-aminobutanal, is an important plant metabolite with various protective functions in stress tolerance [64]. Under hypoxic conditions, PA catabolism with CuAO and PAO enzymes contributed to the GABA content by approximately 30% in Vicia faba [65]. Exogenous GABA, however, was shown to inhibit the breakdown of PAs, indicating negative feedback [64]. Besides GABA, the significance of PAO-dependent H2O2 generation has also been described in drought adaptation, namely during ABA, as well as ethylene-mediated stomatal closure in Vitis vinifera and Arabidopsis thaliana, respectively [66][67]. Fine-tuning PA catabolism during stress conditions might be required to control H2O2 generation. ROS produced by PA decomposing enzymes can serve as important signalling molecules to boost antioxidative defence reactions, but above a certain level, they can augment the stress-associated cellular damage or even lead to PCD [25][68]. For example, tobacco cells were found to secrete Spd into the apoplast where it was oxidized by PAO, thereby generating H2O2 at a level that promoted PCD [32][61]. In citrus (Citrus sinensis), the apoplastic CsPAO4 was shown to produce H2O2 and cause oxidative damages under salt stress [69]. In tomato, PA catabolism (both DAO and PAO enzymes) responded stronger to sublethal than lethal doses of the stress hormone salicylic acid in salinity tolerance signalling [70]. Downregulated expression of PAO-coding genes increased the thermotolerance of tobacco likely due to reduced heat-induced H2O2 generation [71]. PAO activity was shown to contribute to aluminium- or selenium-induced oxidative stress, further strengthening its pro-oxidant role during severe stresses [72][73]. However, the significance of PA-catabolism in antioxidant defence signalling contributing to the salt tolerance of PA-overproducing transgenic tobacco plants was also demonstrated by different groups [61][74]. Furthermore, contrasting salt stress tolerance of maize genotypes was found to be correlated with PA catabolism-dependent H2O2 production during salt stress, but it was rather DAO than PAO activity-dependent [75]. In the leaf blade elongation zone of salinized maize plants, the PAO activity was found to be strongly increased (app. 20-fold) [76]. Together with increased apoplastic PA secretion, the PAO activity resulted in increased apoplastic ROS accumulation, contributing to leaf blade elongation under salt stress. Polyamine oxidase 5 loss-of-function atpao5 mutants of Arabidopsis are salt-stress tolerant; however, their salt tolerance did not show correlation with diminished ROS production but rather with the increased level of t-Spm [38]. However, in the salt-tolerant pao1 pao5 double mutant with no cytoplasmic PAOs, reduced ROS production was observed under NaCl stress [77]. Interestingly, simultaneous mutations in the pao2 and pao4 genes, both coding for peroxisomal PAO, were salt-sensitive, while the pao2 pao3 pao4 triple mutant with no peroxisomal PAO enzymes was not viable [77]. The above observations highlight the differential contribution of the various PAOs with different activities, by-products, and intracellular localisations, to stress tolerance.

3.2. PAOs in Host–Pathogen Interactions

PAO-generated H2O2 may also contribute to pathogen defence. It may directly act as an anti-microbial agent in the apoplast or serve as a signalling molecule inducing the activation of defence genes [78][79]. PA levels and the activity of PA metabolic enzymes were found to be induced by various (biotrophic, as well as necrotrophic) pathogens infecting plant tissues [80][81][82]. For example, in response to the biotrophic pathogen Pseudomonas syringae, PAO activity was found to be increased in tobacco [83]. The infection also induced Spm secretion that, together with the elevated PAO activity, resulted in strong H2O2 accumulation in the apoplast. The apoplastic Spm-mediated disease resistance could be compromised by PAO inhibitors [81][83]. Therefore, in biotrophic plant–pathogen interactions, PAO activity-related H2O2 generation might contribute to the hypersensitive response (HR), as described for tobacco mosaic virus or Pseudomonas chicorii-infected tobacco [84][85] and powdery mildew (Blumeria graminis)-infected barley [84]. The oomycete Phytophthora cryptogea secretes cryptogein, a 10-kD protein that induces HR in tobacco. Inhibiting the expression of the gene coding for apoplastic tobacco PAO prevented PA degradation, cryptogein-induced apoplastic H2O2 generation, and cell death [60]. The observation that, in these plants, cryptogein-induced kinase signalling was also compromised, highlighted that, besides its cytotoxic effect, PAO-generated H2O2 also has a signalling role in the HR. The signalling role of Spm degradation-derived H2O2 was also hypothesized in the transcriptional responses of Arabidopsis to the HR-inducing cucumber mosaic virus [86]. While PA degradation and H2O2 production might beneficially control the HR response in biotrophic host–pathogen interactions, it might be detrimental in the case of infection by necrotrophic pathogens. In agreement, increased polyamine levels were reported to promote leaf necrosis during fungal infection dependent on PAO activity [81].

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