Abstract

Nitric oxide (NO) is a highly reactive signalling molecule that has numerous targets in plants. Both enzymatic and non-enzymatic synthesis of NO has been detected in several plant species, and NO functions have been characterized during diverse physiological processes such as plant growth, development, and resistance to biotic and abiotic stresses. This wide variety of effects reflects the basic signalling mechanisms that are utilized by virtually all mammalian and plant cells and suggests the necessity of detoxification mechanisms to control the level and functions of NO. During the last two years an increasing number of reports have implicated non-symbiotic haemoglobins as the key enzymatic system for NO scavenging in plants, indicating that the primordial function of haemoglobins may well be to protect against nitrosative stress and to modulate NO signalling functions. The biological relevance of plant haemoglobins during specific conditions of plant growth and stress, and the existence of further enzymatic and non-enzymatic NO scavenging systems, suggest the existence of precise NO modulation mechanisms in plants, as observed for different NO sources.

Introduction

NO is a small reactive molecule that rapidly diffuses and permeates cell membranes. Its broad chemistry involves an array of interrelated redox forms with different reactivities (Delledonne, 2005). Because of its unique chemistry, which permits its stability and reactivity, NO and its redox-activated forms are intra- and intercellular signalling molecules (Durner et al., 1998).

In plants, NO has a role in several physiological processes including disease resistance and abiotic stress responses as well as growth and development (Neill et al., 2003; Romero-Puertas et al., 2004). The complexity of NO signalling involves various messenger molecules such as cGMP, cADP ribose, and Ca2+ (Durner et al., 1998; Wendehenne et al., 2001; Lamotte et al., 2004; Romero-Puertas et al., 2004), which both directly and indirectly modulate several physiological functions and alter the expression of specific genes (Polverari et al., 2003; Parani et al., 2004). Furthermore, the NO signalling pathways involve post-translational modification of target proteins such as NO-dependent tyrosine nitration and reversible cysteine S-nitrosylation, which can modulate the activity and function of different proteins (Sokolovski and Blatt, 2004; Feechan et al., 2005; Lindermayr et al., 2005). Although the existence of multiple mechanisms for NO action renders the dissection of specific pathways difficult, it may explain the incomplete inhibition observed when individual steps in specific NO-mediated pathways are blocked (Clarke et al., 2000).

Both cytotoxic and cyto-protecting/stimulating properties of NO have been described in plants (Beligni and Lamattina, 1999). Therefore, the wide variety of sources of NO and its effects suggests the necessity of detoxification mechanisms to control its level, reactivity, and signalling functions. In this review, recent publications that have provided new insights into NO regulation are presented that aid in the elucidation of the specific role of haemoglobin (Hb)-based control of NO under different conditions in plants.

NO functions in plants

NO is a widespread signalling molecule that plays a crucial role in the modulation of several physiological processes during the entire life of the plant (Crawford and Guo, 2005) from germination (Bethke et al., 2004b; Simontacchi et al., 2004; Zhang et al., 2005) to fruit maturation and senescence (Leshem et al., 1998; Beligni and Lamattina, 2001). In roots, NO operates in the auxin signalling pathway that leads to root organogenesis (Pagnussat et al., 2003; Correa-Aragunde et al., 2004) and it also plays an important role in modulation of the gravitropic response (Hu et al., 2005). In leaves, NO mediates abscisic acid-induced stomatal closure (Desikan et al., 2002, 2004; Garcia-Mata and Lamattina, 2002), modulates the rate of leaf expansion (Leshem and Haramaty, 1996), and may affect metabolic processes such as photosynthesis (Hill and Bennett, 1970) and respiration (Zottini et al., 2002). Furthermore, NO also seems to be involved in programmed cell death during xylem differentiation (Gabaldon et al., 2005) and is a key signal for the control of flowering timing (He et al., 2004) and for the orientation of pollen tube growth (Prado et al., 2004).

NO is also involved as a control signal during several abiotic stress responses, including salinity and osmotic stress, temperature, UV light stress, and anoxia (Rockel et al., 2002; An et al., 2005; Shimoda et al., 2005). In particular, NO increases resistance to different abiotic stress such as drought, salt, and oxidative stress (Zhao et al., 2004; Shi et al., 2005).

NO is produced during biotic stress in both pathological and non-pathological plant–microbe interactions (Romero-Puertas et al., 2004; Wendehenne et al., 2004; Zeidler et al., 2004). Its accumulation under conditions that are concomitant with the avirulent gene-dependent oxidative burst has been linked to the induction of the hypersensitive cell death (Delledonne et al., 1998; de Pinto et al., 2002) and to cell-to-cell spread of apoptotic signals (Zhang et al., 2003; Tada et al., 2004). The NO produced during biotic stress is also involved in the activation of systemic acquired resistance (Durner et al., 1998) through the up-regulation of defence genes (Polverari et al., 2003). Furthermore, NO production was recently observed during the response to necrotrophic pathogens and insect herbivores (Jih et al., 2003; Huang et al., 2004; Van Baarlen et al., 2004) in addition to a beneficial plant–microbe interaction, as demonstrated in Lotus japonicus with the symbiotic rhizobium Mesorhizobium loti (Shimoda et al., 2005).

The above observations indicate that NO plays a key role in plant metabolism, signalling, defence, and development, suggesting that control of the level of NO in plants is required in order to activate proper signalling functions. As for animal systems, where different nitric oxide synthases (NOS) have been identified (Stuehr et al., 2004), different NO sources in plants also seem to be involved in NO production during specific processes (Neill et al., 2003; Romero-Puertas et al., 2004). Recently, the presence of a plant NOS gene has been shown in Arabidopsis (AtNOS1; Guo et al., 2003). AtNOS1 plays an important role in plant growth, fertility, and hormone signalling (Guo et al., 2003; He et al., 2004) and it is also involved in the plant–pathogen response (Zeidler et al., 2004).

Another enzymatic source of NO is nitrate reductase (NR), an enzyme with a fundamental role in nitrogen assimilation, which can produce NO from nitrite when photosynthetic activity is inhibited or when its substrate nitrite accumulates (Yamasaki and Sakihama, 2000; Rockel et al., 2002; Lamattina et al., 2003). NR is an important source of abscisic acid-induced NO synthesis in stomata guard cells (Desikan et al., 2002; García-Mata and Lamattina, 2003), although no significant effects of NR have been observed with regard to NO accumulation during pathogenic infection (Zhang et al., 2003) or during wounding stress (Garces et al., 2001).

Recent studies have shown other nitrite-mediated NO sources in plants, including the enzymatic production of NO in mitochondria under anoxia (Planchet et al., 2005) and the membrane associated nitrite-NO oxidoreductase in roots (Stöhr et al., 2001). Other potential enzymatic NO sources such as xanthine oxidoreductase, horseradish peroxidase, or cytochrome P450 should be also considered (Corpas and del Rio, 2004), as well as non-enzymatic mechanisms, including the spontaneous liberation of NO from nitrite in the presence of acid pH and reducing agents (Yamasaki and Sakihama, 2000; Bethke et al., 2004a) and the carotenoid-mediated NO production in the presence of nitrite and light (Cooney et al., 1994).

Therefore, different NO sources are most likely required to control the production of NO during specific processes, although the physiological significance of NO production in different instances and identification of the precise source of NO depending on the physiological process and its regulation or interrelation with other possible sources requires further investigation.

NO reactions

NO and its exchangeable redox-activated forms are well known as intra- and intercellular signalling molecules, since NO can rapidly diffuse across biological membranes and contribute to transient cell-to-cell signalling for brief periods of time (Beligni and Lamattina, 2001). As free NO is highly reactive, several reactions that are controlled by both the concentration and redox state of NO and the availability and reactivity of target groups can occur without enzyme catalysis (Crawford and Guo, 2005). These reactions regulate the signalling and toxicity of NO and may also modulate its levels. The free radical NO has a half-life of just a few seconds and rapidly reacts with O2 to form nitrogen dioxide (NO2), which degrades to nitrite and nitrate in aqueous solutions (Neill et al., 2003). NO can also react with the free radical superoxide

\((\mathrm{O}_{2}^{{-}})\)
to form the reactive molecule peroxynitrite (ONOO), which can lead to the formation of NO2 and the potent oxidant hydroxyl radical (OH·). OH· is a very strong oxidizing specie that can rapidly attack biological membranes and all types of biomolecules such as DNA and proteins leading to irreparable damage, metabolic dysfunction, and cell death (del Rio et al., 2003). By itself, ONOO is responsible for tyrosine nitration and oxidation of thiol residues to sulphenic and sulphonic acids (Lamattina et al., 2003) and it is considered the major toxic reactive nitrogen species in animal cells (Stamler et al., 1992), but not for plant cells (Delledonne et al., 2001).

As a consequence, the effect of NO on animal cells depends on many complex conditions, such as the rate of production and diffusion, the concentration of reactive oxygen species (ROS), and the level of enzymes involved in ROS scavenging, such as superoxide dismutase and catalase (Tamir et al., 1993). In plants, the accumulation of NO and H2O2 during the hypersensitive disease resistance response (HR) is responsible for the execution of the cell death program (Delledonne et al., 1998; Clarke et al., 2000; de Pinto et al., 2002). Since the independent increase of only one component of this binary system has little effect on the induction of cell death (Delledonne et al., 2001), the relative rates of production of NO and

\(\mathrm{O}_{2}^{{-}}\)
are critical in modulating the effects of NO. This can paradoxically offer protection against oxidative damage by intercepting reactive species and converting them to less damaging and/or more easily detoxified products. Thus, whereas H2O2 is the noxious partner of NO to induce cell death,
\(\mathrm{O}_{2}^{{-}}\)
may be considered as a chemical NO scavenger that controls the level of NO in plant cells through the formation of ONOO (Delledonne et al., 2001).

NO can also react rapidly with thiol- and transition metal-containing proteins, including a wide functional spectrum of proteins such as receptors, transcription factors and cellular messengers (Stamler et al., 2001). For example, the NO-dependent activation of guanylate cyclase by binding to the haem iron established a function for NO in signal transduction (Murad, 1986). NO can react with glutathione to form S-nitrosoglutathione (GSNO), which can function as a mobile reservoir of NO bioactivity (Feechan et al., 2005) or a S-nitrosylating agent. S-nitrosylation is represented by binding of a NO group to the thiol side chain of a cysteine residue. In animals, this modification is involved in a large part of the almost ubiquitous influence of NO on cellular signal transduction (Hess et al., 2005), and during the last few years over 100 proteins have been identified as targets of S-nitrosylation (Stamler et al., 2001). Temporal and spatial regulation of S-nitrosylation allows post-translational modification to function as a mechanism that conveys redox-based signalling (Hess et al., 2005). Very little is known about S-nitrosylation in plants, although numerous proteins have been obtained from the deduced Arabidopsis proteome that have a degenerate S-nitrosylation motif (Huber and Hardin, 2004). Recently, a proteomic approach using the biotin switch method (Jaffrey et al., 2001) identified 63 proteins from Arabidopsis cell culture extracts treated with GSNO and 52 proteins from NO-treated Arabidopsis leaves as putative targets for S-nitrosylation in plants (Lindermayr et al., 2005). The characterization of mechanisms regulating S-nitrosylation/de-nitrosylation will undoubtedly aid in an improved understanding of the functional consequences and relevance of S-nitrosylation in plants, and might identify possible mechanisms to control the levels of NO and NO-related species.

Haemoglobins detoxify NO

The wide variety of NO sources and biological effects suggests the requirement of detoxification mechanisms in plants to control the levels of NO as well as its reactivity and signalling functions. Haemoglobins (Hbs) are most commonly recognized for their ability to act either as O2 carriers or stores to facilitate O2 delivery, even though they are also well known regulators of NO homeostasis. In humans, Hbs regulate the activity of NO through either detoxification (Joshi et al., 2002) or delivery through S-nitrosylation reactions (Gow et al., 1999). Bacterial flavohaemoglobins (flavoHbs) consume NO enzymatically through a NO reductase/denitrosylase activity (Gardner et al., 1998; Hausladen et al., 1998) to protect bacterial cells from NO, as also observed for truncated Hbs (Quellet et al., 2002). Ascaris Hb has a NO consumption activity that involves the intermediacy of S-nitrosylated Hb (Minning et al., 1999). Thus, the primordial function of Hbs, present not only in erythrocytes but also in micro-organisms, invertebrates, and plants may well be to protect against nitrosative stress and modulate the signalling functions of NO.

In plants, there are at least three distinct types of Hbs that have been classified as symbiotic, non-symbiotic Hbs (nsHb), and truncated Hbs. The latter are the most recently discovered plant Hbs; they are characterized by a three-dimensional structure with a 2-on-2 arrangement of α-helices (Watts et al., 2001) and appear to be ubiquitous in the plant kingdom (Vieweg et al., 2005). Symbiotic Hbs are found specifically in symbiotic legume root nodules where they scavenge and transport O2 to protect Rhizobium nitrogenase from inactivation (Appleby, 1984). The nsHbs appear to be ubiquitous in the plant kingdom and are organized in two classes. Class-1 Hbs have an extremely high affinity for O2 and are induced in plants during hypoxic stress, whereas class-2 nsHbs have lower affinity for O2, are induced by low temperature, and are expressed during plant development (Trevaskis et al., 1997; Hunt et al., 2001).

Although the presence of stress-induced nsHbs is widespread in the plant kingdom, their function has only been recently elucidated and their cellular localization is not clearly understood. In particular, alfalfa class-1 nsHb has been shown to localize in both the nucleus and cytosol (Seregélyes et al., 2000), although the main nsHbs activity involved in NO degradation was found to be localized in the soluble cytosolic fraction (Igamberdiev et al., 2004) in agreement with the previous protein sequence analysis of rice and Arabidopsis class-1 nsHb (Arredondo-Peter et al., 1997; Trevaskis et al., 1997). In contrast to symbiotic Hb, the nsHbs exhibit an iron hexacoordination in which the ligand binding site on the haem prosthetic group is occupied by a His residue similar to many Hbs (Kundu et al., 2003). For example, the human neuroglobins show a hexacoordinated structure, are up-regulated during hypoxia, and their expression is directly associated with protection against hypoxic challenge (Sun et al., 2001, 2003). Similarly, class-1 nsHbs are strongly expressed during hypoxia or similar stresses, and are required for survival of plants after a severe hypoxic challenge (Hunt et al., 2002; Dordas et al., 2003b). However, these nsHbs possess a high affinity for O2 and slow O2 dissociation rate constants and are, therefore, unlikely to function as O2 transporters (Kundu et al., 2003). On the other hand, hypoxia is a stress condition that generates copious amounts of NO (Dordas et al., 2003b) suggesting other possible Hb-based cell-protection mechanisms.

Class-1 nsHbs from Arabidopsis (Perazzolli et al., 2004), barley (Igamberdiev et al., 2004), and alfalfa (Seregélyes et al., 2004) are now known to detoxify NO to nitrate in an NAD(P)H-dependent manner. Biochemical evidence indicates that rapid nitrate accumulation is accompanied by NO-dependent oxidation of oxygenated to oxidized nsHb (Dordas et al., 2004; Perazzolli et al., 2004). Furthermore, this Fe(III) intermediate of haem can be directly reduced by NADPH, as for nsHb from Arabidopsis, which catalyses an enzymatic cycle for NO metabolism with continuous nitrate accumulation in the presence of excess NO and NADPH (Fig. 1A; Perazzolli et al., 2004). Otherwise, oxidized nsHb might be reduced by a mixture of NADH and FAD, as for alfalfa nsHb (Seregélyes et al., 2004), or by a methaemoglobin reductase, as for barley nsHb (Igamberdiev et al., 2004).

Fig. 1.

Haemoglobin-based NO-detoxification reactions. (A) Reaction cycle for NO metabolism by Arabidopsis class-1 nsHb: oxygenated Hb is oxidized by NO with nitrate production. The recovery of oxygenated Hb for another NO degradation cycle is ensured by regeneration by NADPH and subsequent association with O2. This reduction of nsHb may be augmented in vivo by specific interaction with a methaemoglobin reductase system. (B). Reaction cycle for GSNO metabolism by Arabidopsis class-1 nsHb: oxygenated Hb is oxidized by GSNO with nitrate production through the formation of an S-nirosoHb intermediate. The recovery of oxygenated Hb is ensured by regeneration by NADPH and subsequent association with O2. The reduction of nsHb may be augmented in vivo by specific interaction with a methaemoglobin reductase system as well.

Fig. 1.

Haemoglobin-based NO-detoxification reactions. (A) Reaction cycle for NO metabolism by Arabidopsis class-1 nsHb: oxygenated Hb is oxidized by NO with nitrate production. The recovery of oxygenated Hb for another NO degradation cycle is ensured by regeneration by NADPH and subsequent association with O2. This reduction of nsHb may be augmented in vivo by specific interaction with a methaemoglobin reductase system. (B). Reaction cycle for GSNO metabolism by Arabidopsis class-1 nsHb: oxygenated Hb is oxidized by GSNO with nitrate production through the formation of an S-nirosoHb intermediate. The recovery of oxygenated Hb is ensured by regeneration by NADPH and subsequent association with O2. The reduction of nsHb may be augmented in vivo by specific interaction with a methaemoglobin reductase system as well.

The demonstration that class-1 nsHb from Arabidopsis can also metabolize GSNO through production of S-nitrosohaemoglobin (Fig. 1B; Perazzolli et al., 2004) suggests a conserved role of haemoglobin S-nitrosothiols in processing NO and S-nitroso compounds across humans, nematodes, and plants. Hexacoordinate plant Hbs appear to operate as Ascaris Hb (Minning et al., 1999), although they are structurally very different. Both Arabidopsis class-1 and Ascaris Hbs have evolved distal cysteine residues in the haem pocket, not present in human and bacterial Hbs, which are implicated in NO/SNO detoxification. Arabidopsis class-1 nsHb seem to retain the primitive function in NO/SNO detoxification by positioning cysteine residues in the distal haem pocket similar to Ascaris Hb, whereas NO delivery function in human haemoglobin is accomplished through the use of a proximal cysteine residue (Jia et al., 1996).

A role of nsHbs in NO modulation has been largely demonstrated in vitro and in vivo only for the high O2 affinity class-1. Conversely, the function of the strongly different class-2 nsHbs has not been investigated. Class-2 nsHbs seem to be exclusive to dicots (Hunt et al., 2001), are induced by cold stress (Trevaskis et al., 1997), and are expressed in specific tissues of mature flowering plants (Hunt et al., 2001). The Arabidopsis class-2 nsHb show lower O2 affinity than class-1 nsHbs and might be involved in O2 storage or transport (Trevaskis et al., 1997). A possible interaction with NO, particularly in NO biosynthesis from nitrite at low O2 levels, has recently been proposed (Crawford and Guo, 2005).

Haemoglobin-based NO modulation during hypoxic stress

The main physiological function for the NO scavenging activity of nsHb appears to be protection against nitrosative stress associated with hypoxia (Dordas et al., 2003b, 2004; Perazzolli et al., 2004). Overexpression of class-1 nsHb results in a greater cell viability and stronger plant growth under hypoxia in Arabidopsis (Hunt et al., 2002; Perazzolli et al., 2004) and in alfalfa cultures expressing the barley nsHb (Dordas et al., 2003b), whereas the suppression of nsHb expression reduces organ growth under hypoxic stress (Dordas et al., 2003b; Perazzolli et al., 2004). This nsHb-mediated hypoxia tolerance depends on the high O2 affinity of nsHbs and NO detoxification (Dordas et al., 2003b; Perazzolli et al., 2004), but it is not due to O2 delivery (Hunt et al., 2002).

Hypoxic stress activates NR leading to copious amounts of NO synthesis and elevated NO emission from plant tissues that are measurable by chemiluminescence (Rockel et al., 2002; Perazzolli et al., 2004) and electron paramagnetic resonance (Dordas et al., 2003b, 2004). Hypoxia stimulated NO accumulation is dramatically suppressed in Arabidopsis plants expressing Arabidopsis class-1 nsHb (Fig. 2; Perazzolli et al., 2004), in alfalfa root cultures overexpressing barley class-1 nsHb (Dordas et al., 2003b) and in maize cell lines expressing the same barley nsHb (Dordas et al., 2004); whereas the transgenic lines suppressed for nsHbs expression have enhanced levels of NO (Fig. 2; Dordas et al., 2003b, 2004; Perazzolli et al., 2004).

Fig. 2.

Gas phase NO emission pattern of Arabidopsis wild-type plants (black bars) and transgenic Arabidopsis lines expressing the Arabidopsis class-1 nsHb gene in sense (grey bars) or antisense (white bars) orientation, 30 min after light exposure (light), after transfer of light-adapted plants to darkness (light-off), 30 min after dark adaptation (dark), and 20 min or 60 min after hypoxic stress by flushing with N2 in the dark (dark N2 20 min and 60 min; Perazzolli et al., 2004).

Fig. 2.

Gas phase NO emission pattern of Arabidopsis wild-type plants (black bars) and transgenic Arabidopsis lines expressing the Arabidopsis class-1 nsHb gene in sense (grey bars) or antisense (white bars) orientation, 30 min after light exposure (light), after transfer of light-adapted plants to darkness (light-off), 30 min after dark adaptation (dark), and 20 min or 60 min after hypoxic stress by flushing with N2 in the dark (dark N2 20 min and 60 min; Perazzolli et al., 2004).

NO is an effective inhibitor of cytochrome oxidase in the mitochondrial electron transport chain (Zottini et al., 2002) and may further reduce cell respiration and energy production. Under hypoxia, nsHbs scavenge NO and may also help in maintaining the energy status of plant cells by an alternative mechanism to the classic fermentation pathways (Igamberdiev and Hill, 2004; Igamberdiev et al., 2005). The NR-dependent production of NO and its subsequent oxidation by nsHb seems to be a NAD(P)H-consuming mechanism. The overall system oxidizes 2.5 moles of NADH per 1 mol of nitrate recycled, leading to the maintenance of redox status during hypoxia (Dordas et al., 2003a; Igamberdiev and Hill, 2004). The lower NADH/NAD+ and NADPH/NADP+ ratios in alfalfa root cultures expressing barley nsHb compared with control cells, and the higher ratios in nsHb silenced lines upon low O2 and antimycin treatment, support the existence of this alternative fermentation mechanism (Igamberdiev et al., 2004). Since alfalfa root cultures expressing barley nsHb (Dordas et al., 2003a) and maize-cultured cells expressing barley nsHb (Sowa et al., 1998) have lower alcohol dehydrogenase activity than control cultures under hypoxia, alternative fermentation based on nsHb could substitute alcohol dehydrogenase for recycling NADH. Furthermore, this nsHb cycle sustains glycolysis and the energy status of plant cells, maintaining a higher level of ATP in nsHb overexpressing lines under hypoxia (Sowa et al., 1998; Dordas et al., 2003a; Igamberdiev et al., 2005).

Haemoglobin-based NO modulation during plant growth conditions

NO accumulates under normal growth conditions as it is produced from nitrite either through light-mediated non-enzymatic conversion by carotenoids or by the action of NR (Klepper, 1990). In Arabidopsis lines overexpressing the class-1 nsHb, the NR–mediated emission of NO resulting from the accumulation of nitrite on transfer of light-adapted plants to darkness (Kaiser et al., 2002) is significantly lower compared with control plants (Fig. 2; Perazzolli et al., 2004), suggesting a function of nsHbs in the constant control of NO accumulation.

Arabidopsis class-1 nsHb is induced by nitrate (Wang et al., 2000), a class-1 nsHb of the Lotus japonicus is strongly induced by NO (Shimoda et al., 2005), and both rice class-1 nsHbs are strongly up-regulated by nitrite, nitrate, and NO (Ohwaki et al., 2005). Furthermore, treatment with nitrate and nitrite failed to induce nsHbs in rice mutants defective in NR expression (Ohwaki et al., 2005) indicating that the induction of nsHb is closely associated with NR-dependent NO production. Since NR-derived NO is potentially dangerous, these data indicate that nsHbs may well protect against NO generated following nitrogen fertilization (Klepper, 1990) and during normal growth condition (Ohwaki et al., 2005). The effect of nsHbs in defence against nitrosative stress is observed during treatment with NO donors (Dordas et al., 2003a; Seregélyes et al., 2003). NO treatment causes a decline in the ATP levels and ATP/ADP ratios in transgenic alfalfa cultures underexpressing the nsHbs, whereas lines overexpressing the class-1 barley nsHb show protection against this nitrosative stress (Dordas et al., 2003a). Similarly, tobacco seedlings and leaves of transgenic lines overexpressing the alfalfa class-1 nsHb are less sensitive to NO than wild-type plants (Seregélyes et al., 2003).

Transient NO generation observed after symbiotic bacteria inoculation in Lotus japonicus roots indicates that NO also accumulates during beneficial plant–microbe interactions (Shimoda et al., 2005). NO could be produced in the infected cells of root nodules due to their high metabolic activity during the infection process, or in the release of NO by nitrogen-fixing bacteroids (Vieweg et al., 2005). Thus, NO may be involved in symbiotic interactions, either as a messenger molecule or as a by-product of the altered metabolism in root nodules (Herouart et al., 2002). Symbiotic rhizobium infection causes the up-regulation of a class-1 nsHb in Lotus japonicus (Shimoda et al., 2005) and the induction of the two truncated Hbs in root nodules and in roots of Medicago truncatula colonized by arbuscular mycorrhizal fungi (Vieweg et al., 2005). It is assumed that these Hbs could be involved in NO detoxification in specific root tissues during symbiosis (Shimoda et al., 2005; Vieweg et al., 2005), since it can inactivate nitrogenase (Cueto et al., 1996).

In other detrimental plant–microbe interactions, NO exerts a number of fundamental functions, such as those occurring during plant defence against pathogen attack, by contributing together with ROS to trigger hypersensitive cell death and induce defence genes (Delledonne et al., 1998). The observation that challenge of Arabidopsis plants overexpressing the Arabidopsis class-1 nsHb with an avirulent strain of the bacterial pathogen Pseudomonas syringae causes normal accumulation of NO and hypersensitive cell death, indicates that nsHbs do not interfere with NO bursts originated by acute responses when NO signalling functions through the hypersensitive resistance response are needed (Perazzolli et al., 2004). However, further experimentation is required to elucidate the role of nsHb during disease resistance, since the overexpression of alfalfa nsHb in tobacco results in fewer lesions in leaves when challenged with incompatible bacteria or tobacco necrosis virus compared with control plants (Serégelyes et al., 2003). Moreover, these lines have higher ROS, salicylic acid (SA), and pathogenesis-related protein 1 levels after pathogen infection (Serégelyes et al., 2003, 2004). The differences of nsHb expressing plants during plant–pathogen interactions might be explicable by the different rates of catalytic NO detoxification. The expression of Escherichia coli flavoHb, which possesses strong NO detoxification activity (Gardner et al., 1998), is able to attenuate the pathogen-induced NO burst when expressed in plants and reduces the development of hypersensitive cell death and the expression of defence genes (Zeier et al., 2004).

Further NO modulation mechanisms in plant

In addition to Hb-based NO detoxification and non-enzymatic NO scavenging by

\(\mathrm{O}_{2}^{{-}}\)
or through thiols, plants may possess additional NO metabolizing mechanisms to control the levels of NO under different conditions. For example, some enzymes such as xanthine oxidase, glutathione peroxidase, and GSNO reductase (GSNOR) are reported to break down NO-related species (Sies et al., 1997; Trujillo et al., 1998; Díaz et al., 2003). GSNO has been shown to induce systemic resistance against TMV infection in tobacco (Song and Goodman, 2001) and to be a powerful inducer of plant defence genes (Durner et al., 1998). An enzyme that metabolizes GSNO has been identified in E. coli (Liu et al., 2001a) and the characterization of GSNOR-deficient yeast showed enhanced susceptibility to nitrosative stress (Liu et al., 2001b). A similar gene has also been identified in both pea and Arabidopsis (Shafqat et al., 1996; Sakamoto et al., 2002), suggesting that plants may be able to modulate the bioactivity and signalling function of this stabilized form of NO. A recent study has shown that mutation in AtGSNOR1, an Arabidopsis thaliana GSNOR, modifies cellular levels of SNO under both physiological and pathophysiological conditions (Feechan et al., 2005) indicating the existence of cross-reactions between free NO and GSNO that could control the level of NO and its signalling capacity. In the absence of GSNOR activity, the cellular level of SNO is higher compared with control Arabidopsis lines and the plant resistance response against avirulent pathogens and virulent pathogens are compromised. This suggests that whereas a reduction of NO accumulation leads to pathogen susceptibility, a decrease in the concentration of SNO promotes protection against microbial infection (Feechan et al., 2005). AtGSNOR is also required to maintain the non-host resistance to the wheat powdery mildew pathogen in Arabidopsis and is a positive regulator of the SA signalling network since AtGSNOR is required for normal PR1 expression in pathogen-infiltrated and in SA-treated plants (Feechan et al., 2005). Arabidopsis plants overexpressing AtGSNOR show a reduced SNO level, accelerated kinetics of PR1 expression, and enhanced basal resistance against bacterial and oomycete pathogens (Feechan et al., 2005). These results confirm that an additional regulatory system depending on GSNO formation and AtGSNOR activity is involved in the control of NO signalling functions (Feechan et al., 2005). However, the physiological relevance of these enzymes in plant NO metabolism should be more thoroughly investigated under different stress conditions.

Conclusions

During the last two years large advances have been made in the field of NO regulation and metabolism. Recent publications have reported a crucial involvement of nsHbs in NO modulation during different plant growth and stress conditions, indicating that, in plants as well, the primordial function of Hbs is the detoxification of NO catalysing an O2 and NAD(P)H-dependent nitrate-forming reaction. The in vivo results have demonstrated that the Hb-based NO detoxification plays a crucial role to protect plant cells against nitrosative stress and modulation of NO signalling functions. Furthermore, the existence of different NO modulation reactions indicates that specific NO detoxification mechanisms may be involved in specific plant conditions in the fine control of the level and functions of NO. However, the identification of the precise source of NO, depending on the physiological process and the associated NO modulation system that prevent unregulated NO accumulation, needs further investigation. In particular, the involvement of nsHb and truncated Hbs in NO modulation during pathogenic and symbiotic plant–microbe interactions needs clarification. Moreover, nsHb interactions with NO have been demonstrated only for the class-1 molecule and the function of the strongly different class-2 nsHb has not yet been investigated. While the low O2 affinity of the class-2 nsHbs suggests their involvement in O2 storage or transport, their possible activity in NO biosynthesis at low O2 levels has recently been hypothesized. Furthermore, the reaction of NO with thiols and the subsequent SNO interaction with nsHb and other target proteins demonstrated in plants are a promising starting point to characterize enzymatic and non-enzymatic NO control more fully and the possible signal cascade by which NO operates in plant cells through protein S-nitrosylation.

Future prospectives

NO participates in the regulation of several physiological processes, and the identification of mechanisms controlling its level in plant cells indicates a fine-tuning between NO synthesis and detoxification. Recent reports suggest a crucial role of plant Hbs in NO metabolism, and these findings now raise questions about their main physiological functions. Whereas the role of high oxygen affinity class-1 nsHbs has been largely demonstrated in NO detoxification during plant growth and hypoxic stress (Dordas et al., 2003b, 2004; Igamberdiev et al., 2004; Perazzolli et al., 2004), other studies suggest a function in H2O2 metabolism (Sakamoto et al., 2004; Yang et al., 2005). Since during hypoxia copious amounts of H2O2 are generated, it has been proposed that the nsHb-dependent protection to hypoxia may be a result of the decreased cellular level of H2O2 (Yang et al., 2005). However, other evidence suggests that class-1 nsHbs overexpressing plants produce increased levels of H2O2 upon bacterial infection (Serégelyes et al., 2003). Further investigation of the balance between NO and ROS during hypoxia, together with a detailed characterization of the interaction between nsHb with H2O2 is expected to lead to a better understanding of the activities of nsHbs in ROS homeostasis. In addition a better biochemical characterization of plant Hbs can be expected. The structural features of haem iron coordination recently reported for tomato nsHb (Ioanitescu et al., 2005), and the kinetic binding properties of rice class-1 nsHb (Hargrove, 2000) have the potential to provide further information about the enzymatic properties of nsHbs. In particular, the effect of hexacoordination in the increase of the rate of iron reduction, reported for human and rice hexacoordinated Hbs (Weiland et al., 2005), could deepen the biochemical knowledge regarding mechanisms of nsHbs reduction through direct NAD(P)H processes (Perazzolli et al., 2004; Seregélyes et al., 2004) and through mediation of a specific reductase (Igamberdiev et al., 2004).

The evidence that bacterial flavoHbs (Zeier et al., 2004) and alfalfa class-1 nsHb (Serégelyes et al., 2003) affect SA accumulation in pathogen-infected plants, and the recent demonstration that the barley class-1 nsHb affects ethylene accumulation in NO- and hypoxia-treated maize cells (Manac'h-Little et al., 2005) indicates a role of nsHbs in controlling NO-dependent hormone-mediated signalling that deserves further investigation. The recent identification of S-nitrosylation of Arabidopsis class-1 nsHb (Perazzolli et al., 2004) and other plant proteins (Sokolovski and Blatt, 2004; Lindermayr et al., 2005), together with the evidence that Arabidopsis class-1 nsHb can mediate tyrosine nitration of itself and other proteins (Sakamoto et al., 2004), are important starting points from which to characterize the signal cascade by which NO operates in plant cells.

Abbreviations: cADPR, cyclic ADP ribose; cGMP, cyclic GMP; flavoHbs, flavohaemoglobins; GSNO, S-nitroso-L-glutathione; GSNOR, GSNO reductase; H2O2, hydrogen peroxide; Hb, haemoglobin; HR, hypersensitive response; NO, nitric oxide; NO2, nitrogen dioxide;
\(\mathrm{NO}_{3}^{{-}},\)
nitrate; NOS, nitric oxide synthase; NR, nitrate reductase, nsHb, non-symbiotic haemoglobin; O2, oxygen;
\(\mathrm{O}_{2}^{{-}},\)
superoxide anion; OH·, hydroxyl radical; ONOO, peroxynitrite; ROS, reactive oxygen species; SA, salicylic acid; SAR, systemic acquired resistance; SOD, superoxide dismutase; SNO, S- S-nitroso thiol.

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