Nitric oxide signalling in plants.
Nitrogen monoxide or nitric oxide (NO) is an important molecule that acts in many tissues to regulate a diverse range of physiological processes. Its role was first determined by several groups who were trying to identify the agent responsible for promoting blood vessel relaxation and regulating vascular tone. This agent was named endothelium-derived relaxing factor (EDRF) and was at first presumed to be a protein like most other signal molecules. The discovery that EDRF was in fact NO--a small gaseous molecule--has led to an attraction of interest in this field. NO has now been implicated to play a role in a variety of biological processes including neurotransmission, vascular smooth muscle relaxation, immune defense, and apoptosis in animals (Moncada et al., 1991; Jaffrey & Synder, 1995; Lloyd-Jones & Bloch, 1996; Wink & Mitchell, 1998; Ignarro, 2000).
Research on NO in plants has increased significant awareness in recent years and there is increasing indication on the role of this molecule in plant growth and development (Gouvea et al., 1997; Leshem et al., 1998). NO is a highly reactive molecule that rapidly diffuses and permeates cell membranes. It is becoming apparent that NO is also a ubiquitous signal in plants. Different studies have particularly demonstrated NO signalling in the induction of cell death, defense genes and interaction with reactive oxygen species (ROS) during plant defense against pathogen attack (van Camp et al., 1998; Delledonne et al., 1998, 2001; Durner et al., 1998; Durner & Klessig, 1999; Klessig et al., 2000; Wendehenne et al., 2001; Neill et al., 2003; Romero-Puertas & Delledonne, 2003).
In this review first we are going to review the different sources and biosynthesis of NO in plants, and then we will discuss biological processes involving NO signalling and also signalling mechanisms exerted by NO.
Nitric Oxide Biosynthesis in Plants
It is necessary to investigate the different NO-producing enzymes in plants to understand endogenous NO synthesis, detailed signalling mechanism and the chemical changes induced by this molecule. There are two main sources of NO production proposed in plants:
1. From nitrate by nitrate reductase enzymatically or non-enzymatically (Rio et al., 2004).
2. From arginine by NO synthase as in mammals.
The way in, which NO is produced in each of these sources depends on the species, the cells and tissues, plant growth condition. These sources and their responses to specific conditions are discussed below.
Nitric Oxide Synthase Activity in Plants
Most NO produced is due to the enzyme nitric oxide synthase (NOS; E.C. 126.96.36.199) in animal systems (Moncada et al., 1991; Ignarro, 2000). In mammals there are three well-described genes encoding NOS, endothelial NOS (eNOS), neuronal NOS, (nNOS) and an inducible form (iNOS). iNOS expression increases in the presence of interferon, nNOS has a 160 kDa molecular mass, which is the largest of three forms, eNOS is about 135 kDa and iNOS about 130 kDa (Furchgott, 1995). Tatoyan and Ginlivi (1998) also reported mitochondrial NOS (mtNOS).
NOS catalyzes the oxygen and NADPH-dependent oxidation to NO and citrulline in a complex reaction involving FAD, FMN, BH4, calcium and calmodulin (Knowles & Montada, 1994; Alderton et al., 2001). Nowadays there is increasing data demonstrating the presence of NOS activity in plants analogous to mammalian NOS. In Ninnemann and Maier (1996) showed the presence of NOS activity for the first time in plants (Fig. 1).
NOS Localization in the Cell
There is not enough information about the subcellular localization of NOS activity in plants. Researchers using antibodies revealed that NOS protein was located in the cytoplasm of the cells and then translocated into the nucleus growth phase dependently (Ribeiro et al., 1999). NOS activity also was estimated in the matrix of peroxisomes, in chloroplasts and but not in mitochondria in pea leaves (Barroso et al., 1999). NOS was later also detected in peroxisomes from oil leaves and sunflower hypocotyls (Corpas et al., 2001). These data contrast with mammals where NOS was found in mitochondria from the rat brain and liver (Bates et al., 1995). Recently the presence of iNOS in animal peroxisomes has been estimated in rat hepatocytes cells (Stolz et al., 2002). This reveals that NOS could be a constituent enzyme of peroxisomes from different origins.
[FIGURE 1 OMITTED]
NO Biosynthesis by Nitrate Reductase
Other enzymes excepting NOS can also produce NO. Until recently it was thought that the main origin of NO production in plants was by the action of NADH-dependent nitrate and nitrite reductases (NR; EC 188.8.131.52; Yamasaki et al., 1999; Lamattina et al., 2003). Molybdenum cofactor containing enzyme NR can generate NO from nitrite (N[O.sub.2.sup.-]) with NADH as electron donor (Yamasaki et al., 1999; Rockel et al., 2002). NR also creates peroxynitrite at the same time with NO (Yamasaki & Sakihama, 2000). In plant cells N[O.sub.2.sup.-] can be accumulated when the photosynthetic activity is inhibited or under anaerobic conditions (Rockel et al., 2002; Lamattina et al., 2003). On the other hand in potato tubers infected by the fungus Phytophthora infestans the induction of NR has been demonstrated (Yamamoto et al., 2003). This suggests the involvement of NR in pathogen-induced NO production. Thus the NR dependent generation of NO is expected to be enhanced under plant stress conditions (Rockel et al., 2002). Another nitrite reducing enzyme that generates NO was demonstrated in tobacco roots (Stohr et al., 2001). This plasma membrane enzyme was specified as nitrite: NO reductase (Ni-NOR), and its mass was determined to be 310 kDa. It is necessary to describe this enzyme and to establish its tissue distribution (Fig. 1).
NO Biosynthesis by Xanthine Oxidoreductase
Xanthine oxidoreductase (XOR; EC 184.108.40.206) otherwise referred to as xanthine oxidase, xanthine oxidoreductase (XO) or xanthine dehydrogenase (XDH) is also an enzyme shown to produce NO (Harrison, 2002). XOR occurs into interconvertible forms: The superoxide producing XO and XDH (Palma et al., 2002). A high level of XOR was obtained in pea leaf peroxisomes where the dominant form of enzyme is XO (Sandalio et al., 1988; Corpas et al., 1997). XOR can produce free radicals during a catalytic reaction, depending on the oxygen level in animals (Millar et al., 1998; Godber et al., 2000; Harrison, 2002). The important property of producing 02 and NO radicals confers XOR a key role as a source of signal molecules in plant cells (Corpas et al., 2001)
NO Biosynthesis by Peroxidase
The production of NO and citrulline by horseradish peroxidase from N-hydroxyarginine (NOHA) and [H.sub.2][O.sub.2] was described by Boucher et al. (1992a). Recently, horseradish peroxidase was also showed to produce NO from hydroxyurea and [H.sub.2][O.sub.2] (Huang et al., 2002b). This NO source reveals that peroxidases are prevalent enzymes concerned in significant physiological processes in plant cells (Veitch, 2004).
NO Biosynthesis via Cytochromes P450
Another enzymatic generation for NO is cytochrome P450. These proteins have been demonstrated to catalyze the oxidation of NOHA by NADPH and [O.sub.2] with generation of NO in plants (Boucher et al., 1992b; Mansuy & Boucher, 2002). Hemoglobin and other nitrogen oxides were also estimated to synthesize NO and other nitrogen oxides by catalyzing the oxidation of NOHA (Boucher et al., 1992a). This information underlines the significance of hemoproteins in NO generation enzymatically.
Non-Enzymatic NO Formation
In plants NO can also be produced by non-enzymatic mechanisms. Nitrification/ denitrification cycles supply NO as a by-product of [N.sub.2]O oxidation into the atmosphere (Wojtaszek, 2000). It is well known that non-enzymatic reduction of nitrate can cause the formation of NO. This reaction is favored at an acidic environment when nitrite can dismutate to NO and nitrite (Stohr & Ullrich, 2002). Nitrite can also reduce by ascorbic acid to yield NO and dehydroascorbic acid (Henry et al., 1997). Recently it has been found that barley aleurone cells can generate an acidic apoplastic environment to help nitrite to NO conversion using ascorbate as reductant (Bethke & Jones, 2001).
Plants are more susceptible to the toxic effects of N[O.sub.2] when exposure takes place in the dark. Beta-carotene and other common carotenoids react with N[O.sub.2] in the dark to yield intermediate nitrosating agents consistent with the formation of nitrate esters. Simultaneous exposure of carotenoids to N[O.sub.2] and light significantly reduced formation of nitrosating intermediates and resulted in the release of NO into the gas phase. Light-mediated reduction of N[O.sub.2] to NO by carotenoids may be an important mechanism for preventing damage in plants exposed to N[O.sub.2]. The formation of nitrosating agents from the reaction of carotenoids with N[O.sub.2] suggests that their ability to prevent nitrosative damage associated with N[O.sub.2] exposure in both plants and animals may be limited in the absence of light (Cooney et al., 1994). N[O.sub.2]was also shown to be absorbed by rush, grass and ginkgo leaves were found to adsorb N[O.sub.2] and release NO; they established that at steady state the conversion of adsorbed N[O.sub.2] to NO reached 70% (Nishimura et al., 1986).
Roles of Nitric Oxide in Plant Growth and Development
NO radically affects plant metabolism and consequently studies have concentrated on NO effects in plant physiology. It has been also known for a long time that plants release NO under normal growing conditions and NO can accumulate in the atmosphere from a variety of sources such as industrial pollution (Wildt et al., 1997). The effects of NO on plant growth and development were established as being concentration dependent (Anderson & Mansfield, 1979); high concentrations (4080 pphm) inhibited tomato growth, while low concentrations (0-20 pphm) enhanced it (Hufton et al., 1996), these findings were also found in lettuce and pea plants (Leshem & Haramaty, 1996).
The effects of NO on hypocotyl and internode elongation have also been demonstrated. NO donors inhibited hypocotyls growth and stimulated de-etiolation in Arabidopsis (Beligni & Lamattina, 2000). NO also increased chlorophyll content in pea leaves, mainly in guard cells (Leshem et al., 1997), and retarded chlorophyll loss in Phytophthora infestans-infected potato leaves (Laxalt et al. 1997; Graziano et al., 2002). The positive effects of NO on chlorophyll maintenance may reflect NO effects on iron availability. Graziano et al. (2002) have shown that iron availability is increased in the presence of NO. Iron deficiency results in chlorosis reasoned by reduced chloroplast development, and NO treatment of wild type maize inhibited such chlorosis. In addition, iron deficiency in yellow stripe mutants was reversed by NO treatment. NO also increase chlorophyll content of wheat seedlings grown in the dark. Short white or red light treatments caused a three-fold increase in the chlorophyll level in NO-treated seedlings compared to the control plants (Bewley & Black, 1982), these findings reveal the supposed role of NO in de-etiolation.
Leshem and Haramaty (1996) showed that NO have senescence-retarding properties and later Leshem (2001) established that this result is the consequence of the inhibition of ethylene biosynthesis. On the contrary, some reports revealed that treatment of Arabidopsis plants with NO raised the ethylene level and inhibition of NO biosynthesis did not affect the ethylene increment (Magalhaes et al., 2000). Fruit ripening is an ethylene-promoted physiological process that can be delayed by NO. During fruit ripening ethylene formation increases and this occurs together with reduced NO release (Leshem & Pinchasov, 2000; Leshem, 2001). Moreover, treatment of fruits with NO also delayed the senescence and prolonged their postharvest period.
NO have also been reported as stimulators of seed germination in different plant species. Seeds of Paulownia tomentosa need a long period of light to germinate, bur if seeds were treated with KN[O.sub.3] as a NO donor, a single red light application would be sufficient to trigger germination (Grubisic & Konjevic, 1992). These researchers established that some organic and inorganic nitrates between 1 and 10 mM also stimulate seed germination. Likewise, dormant seeds of California chaparral plant were also induced to germinate by smoke containing NO (Keeley & Fotheringham,. 1997). Organic material combustion or post-fire biogenic nitrification manufactures a considerable amount of NO and these processes stimulate seed germination. Lettuce seeds need light to germinate at 26-32[degrees]C (Bewley & Black, 1982). In these experiments NO donors, like gibberellic acid ([GA.sub.3]), could break dark-required dormancy. NO was determined to be more effective than [GA.sub.3]. It is possible that the same signal transducers are concerned with both NO and GA-mediated stimulation of germination. Some researchers also reported that seed germination was nitrite-stimulated in different plant species (Hendricks & Taylorson, 1975; Cohn et al., 1983). Giba et al. (1998) found that phytochrome-mediated seed germination was controlled by NO; at pH 2.5-3 nitrite-stimulated seed germination and acidic condition minus nitrite did not stimulate seed germination. These effects of nitrite and NO on seed germination reveal that the level of soil nitrite is one factor controlling seed germination.
Root segments of maize were incubated in different solutions containing substances that non-enzymatically release NO, such as sodium nitrite, sodium nitroprusside (SNP), nitrosoglutathione and nitrosocysteine by Gouvea et al. (1997). They found that all of these substances induced root tip expansion in a dose-dependent manner. NO scavenger such as methylene blue prevented elongation induced by NO-releasing substances such as sodium nitrite (SN), sodium nitroprusside (SNP), nitrosoglutathione (NGLU) and nitrosocysteine (NCYS), but had no effect on IAA-induced cell expansion. Their results suggest that NO is the putative elongation inducer and that IAA- and NO-releasing substances conceivably share common steps in the signal transduction pathway, since both elicited the same plant response. Recently, Pagnussat et al. (2002) demonstrated that NO mediates the auxin response leading to adventitious root formation. A transient increase in NO concentration was shown to be required and to be part of the molecular events involved in adventitious root development induced by IAA.
In summary, NO affects plant growth and differentiation, hypocotyl elongation, senescence, seed germination, root growth and de-etiolation by interacting with plant growth regulators in different plant species (Table 1).
Nitric Oxide Interaction with Plant Regulators
NO is a non-traditional regulator of plant growth. Several studies have reported that NO can regulate processes related to plant growth and development as stated before. NO is mainly formed in actively growing tissue such as embryonic axes and cotyledons and the levels decrease in mature and senesced organs (Leshem et al., 1998; Caro & Puntarulo, 1999). The small size and high diffusion rate of NO through membranes mean that NO fits the basis that hormones are easily transported. NO also acts at low concentrations and most of its functions are dependent on its amount (Beligni & Lamattina, 2001), in this framework, NO could be considered to be a plant growth regulator.
Recent studies suggested that NO mediates some cytokinin effects. Cytokinin has been demonstrated to induce NO synthesis in tobacco, parsley and Arabidopsis cell cultures (Tun et al., 2001). NO can imitate some cytokinin effects; NO donors induced betalaine accumulation in Amaranthus seedlings and NOS inhibitor inhibited cytokinin-induced betalaine accumulation (Scherer & Holk, 2000). Carimi et al. (2002) proposed the role of cytokinins in programmed cell death. This topic is going to be handled in the cell death section below in detail.
Moreover NO has been identified as a mediator of guard cell ABA signalling. ABA induces the synthesis of NO in guard cells; NO induces stomatal closure and either scavenging of NO or inhibition of NO synthesis reduces ABA-induced stomatal closure. These data indicate that NO synthesis is critical for ABA-induced stomatal closure (Neill et al., 2002a). This finding has been confirmed in Vicia faba (Garcia-Mata & Lamattina, 2002) and Arabidopsis (Desikan et al., 2002). Tun et al. (2001) indicated the tissue specificity of ABA to induce NO synthesis in Arabidopsis suspension cultures. NOS as a source of NO, as ABA-induced stomatal closure and NO synthesis were both inhibited by NO synthase inhibitor, NG-nitro-L-arginine methyl ester (L-NAME) but not by tungstate, a potential NR inhibitor. ABA-induced NO synthesis is also required for ABA-induced stomatal closure in Arabidopsis (Desikan et al., 2002), therefore the basis of NO appears to be NR, but not NOS. Moreover, guard cells in NR-deficient Arabidopsis nia1, nia2 mutant (Wilkinson & Crawford, 1993) do not synthesize NO and they do not close also in response to nitrate or ABA (Desikan et al., 2002). Therefore, it is possible to conclude that there is a species difference in NO synthesis, at least in terms of guard cell response to ABA.
Additionally, NO biosynthesis also been established to be induced by auxin in cucumber roots (Pagnussat et al., 2002; Guo et al., 2003). NO was needed for root growth and the formation of lateral roots. Recently, it has been indicated that NO can stimulate cell division and embryogenic cell formation in leaf protoplast-derived cells of alfalfa in the presence of auxin (Otvos et al., 2005). It was found that various NO-releasing compounds promoted auxin-dependent division of leaf protoplast-derived alfalfa cells. In contrast, application of NO scavenger or NO synthesis inhibitor inhibited the same process. Furthermore, Hu et al. (2005) investigated the auxin and gravity signal transduction by demonstrating that the NO and cGMP mediate responses to gravistimulation in primary roots of soybean. Horizontal orientation of soybean roots caused the accumulation of both NO and cGMP in the primary root tip. These results indicated that auxin-induced NO and cGMP mediate gravitropic curvature in soybean roots.
It has also been shown that the NO donor's sodium nitroprusside (SNP) and S-nitroso-N-acetylpenicillamine delayed GA-induced programmed cell death in Hordeum vulgare aleurone layers (Beligni et al., 2002). In these cells, death is promoted by ROS (Bethke & Jones, 2001; Fath et al., 2001), and NO delays death by acting as ah antioxidant (Beligni et al., 2002). When aleurone layers were treated with GA, 70% of cells were dead 48 h after hormone treatment, but almost no cells were dead when layers were treated with ABA. These data reveal that NO is an effective modulator of the cell death program in Hordeum vulgare aleurone cells. Beligni et al. (2002) also suggested that aleurone layers produce NO and that endogenous NO plays a role in GA-induced programmed cell death. The role of GA related with NO in seed germination it has been underlined before also.
In addition, researchers also investigated the NO relation with the plant stress hormone ethylene. Low concentrations of NO either endogenously-produced or exogenously-applied in the [10.sup.-6] M range exert significant growth promoting and ethylene inhibiting effects, which are reversed by higher NO concentrations or equimolar applications of NOS inhibitor [N.sup.6]-methyl-arginine or NO releasing compounds (Leshem, 1996). Recently, Li et al. (2005) showed that 1-aminocyclopropane-1-carboxylic acid (ACC), the immediate precursor of ethylene, nitrite, GA4 and benzyladenine improved seed germination in the presence of salt in Suaeda salsa. The alternative oxidase 1 a gene (AOX1a) was used as a molecular probe to investigate its regulation by signal molecules such as [H.sub.2][O.sub.2], NO, ethylene, salicylic acid (SA) and jasmonic acid (JA) all of them reported to be involved in the ozone response. Ozone fumigation leads to accumulation of [H.sub.2][O.sub.2] in mitochondria and early accumulation of NO in leaf tissues (Ederly et al., 2006).
Polyamines (PAs) are multifunctional and interact with polyanionic macromolecules like DNA or protein. But in spite of their potential importance, the PA-dependent signal transduction system has not been revealed yet. Tun et al. (2006) have lately reported a possible linkage between PA and NO, another ubiquitous signalling molecule. These researchers present pharmacological indication that, in addition to [H.sub.2][O.sub.2], PAs induce the production of NO in various tissues within seedlings of Arabidopsis thaliana.
It is well known that supplemental PA provides an anti-senescence effect in many plant species. The antisenescence effect of PAs can be partially mimicked by NO (Leshem et al., 1998). Tun et al. (2001) had previously presented similar pharmacological evidence for cytokinin-induced NO generation in various plant cell cultures, a result that might present the clue needed to understand the functional overlap between NO and cytokinin and PAs.
Nitrie Oxide in Stress
NO as a key signalling molecule has been involved in mediation of a variety of biotic and abiotic stress-induced physiological responses in plants. Avariety of stresses for example drought, low and high temperature, UV and ozone exposure induce the generation of ROS (Neill et al., 2002b; Vranova et al., 2002; Arasimovic and Floryszak-Wieczorek 2007). ROS initiate various signalling pathways. Therefore, preservation of suitable ROS levels might correspond to survival response. NO interacts with ROS in different ways and serve as an antioxidant during various stresses.
Until recently, research on the effects of NO in plants focused on atmospheric pollution by the oxides of nitrogen, NO and N[O.sub.2]. Uptake of NO into foliage, as well as its subsequent metabolism and phytotoxicity are well documented (Wellburn, 1990; Hendricks & Taylorson, 1975; Clark et al., 2000). Afterward it became clear that plants not only respond to atmospheric NO, but they are also able to produce considerable amounts of NO (Wildt et al., 1997). Increasing evidence also suggests that NO is a novel effector of plant growth, development and defense (Durner & Klessig, 1999; Wendehenne et al., 2001).
NO is also a constituent of polluted air; ozone, oxidative stress and atmospheric pollutants reduce plant growth and contribute to the decline of trees and also other plants in urban as well as forest environments (Skelly & Innes, 1994; Hufton et al., 1996; Sandermann, 1998). While NO and N[O.sub.2] rarely cause visible injury, NO pollution can significantly reduce tree life (Wellburn, 1990; Wellburn & Wellburn, 1996; Takahashi & Yamasaki, 2002). The combined stresses of resisting cellular acidification, increased levels of nutrients and the direct interference of NO with critical metal-containing enzymes and reaction centers (Clark et al., 2000) are thought to be major reasons why nitrogen oxides, especially NO, show a damaging effect on plant growth and development. In the presence of other air pollutants such as S[O.sub.2], NO and N[O.sub.2] cause free radical-induced damage similar to that induced by ozone (Wellbum, 1990). On the other hand, atmospheric NO might play a role as mediator of plant resistance reactions just as stated for ROS (Sandermann, 1998).
NO also may also be involved in seed germination after forest fires. Many trees release seeds during fire then germinate in response to constituents of wood smoke. In some cases the germination-inducing component was identified as NO (Giba et al., 1998). Germination is dependent on nitrite or hydroxylamines in some plants whose chelation with iron of hemes is an endogenous source of NO (Hendricks & Taylorson, 1975; Clark et al., 2000). In these experiments breaking seed dormancy was caused by catalase inhibition, an effect that can be attributed to NO.
Salinity by NaCl is one of the major abiotic stresses affecting plant productivity due to alterations produced in photosynthesis and respiration and in the protein and nucleic acid metabolisms (Leshem & Haramaty, 1996; Hasegawa et al. 2000). Researches carried out by Valderrama et al. (2006) on the effect of salt stress in olive plants showed that salinity produced in leaves an imbalance between the ROS production and antioxidant defences with the induction of oxidative stress. Same scientists very recently showed that under NaCl stress, NO and other NO-derived products are overproduced, indicated that in plant cells nitrosative stress could participate, in the mechanism of damage produced by abiotic toxic conditions (Valderrama et al., 2007).
Recently the effects of NO in protecting Zea mays leaves against iron deficiency-induced oxidative stress were investigated by Suna et al. (2007).They suggested that NO can protect maize plants from iron deficiency induced oxidative stress by reacting with ROS directly or by changing activities of ROS-scavenging enzymes.
Drought stress is a most important environmental limitation on crop production. ABA is synthesized following turgor deficiency and stimulates NO synthesis in stomata guard cells. It was also reported that wilting increases the NO emission from pea plants (Leshem & Haramaty, 1996) but some researchers obtained contradictory results in Arabidopsis thaliana (Magalhaes et al., 2000). However, treatment with an NO donor reduced the stomatal apertures and in that way decreased transpiration (Garcia-Mata & Lamattina, 2001). Probably, NO acts on stomata closing with other signallling molecules like [H.sub.2][O.sub.2]. As stated above there is also some indication that ROS and NO interact to induce ABA biosynthesis (Zhao et al., 2001). In response to drought stress an increment in NOS-like activity was found in wheat seedlings and the ABA titer decreased by NOS inhibitors. Recently, the effects of NO and ROS on leaf water control and the roles of ABA were determined using Triticum aestivum seedlings. Osmotic stress reduced leaf water loss while it increased leaf ABA content as compared with the control. The effects of osmotic stress on leaf water loss and ABA contents were partially reversed by NO scavengers or NOS inhibitors (Xing et al., 2004).
NO also react with other stresses such as heat and chilling stresses. Short term heat stress caused an increase in NO production in alfalfa (Leshem, 2001). NO treatment mediates for chilling resistance in different plants (Lamattina et al., 2001); this effect probably reflects the antioxidant properties of NO by inhibiting ROS following chilling or heat stress (Neill et al., 2002b).
It is worth pointing that several forms of abiotic stress lead to increased PAs biosynthesis (Bouchereau et al., 1999). Recently Tun et al. (2006) showed that the PAs induce NO production in Arabidopsis thaliana seedlings and concluded that NO may be a relation between PA-mediated stress responses and other stress mediators using NO as an intermediate.
Plants respond to wounding and pathogen attack by synthesizing defense molecules that facilitate wound healing, cell death or provide protection against further pathogen attack. Researchers found that the accumulation of NO and [H.sub.2][O.sub.2] as a result of wounding and pathogen challenge. It has been determined that although wounding does not induce the generation of NO, treatment with NO donors inhibited [H.sub.2][O.sub.2] generation after wounding, and expression of specific wound-induced genes (Delledonne et al., 1998; Cardenas & Ryan, 2002). These results propose that NO generated during pathogenesis might inhibit [H.sub.2][O.sub.2] synthesis and the activation of specific wound-induced signalling pathways.
NO was also reported to function as a critical signal for disease resistance in plants (Delledonne et al., 1998; Durner et al., 1998; Dumer & Klessig, 1999). NO enhances the reactive oxygen intermediates (ROI)-mediated induction of hypersensitive cell death by avirulent bacterial pathogens in both soybean cell culture and in Arabidopsis (Delledonne et al., 1998). Inhibitors of NO synthesis not only blocked hypersensitive cell death but also caused increased susceptibility in incompatible interactions (Delledonne et al., 1998).NO involvement in plant-pathogen interactions are going to be discussing later in detail.
Nitric Oxide Signal Transduction
NO Signalling Relation with cGMP
NO signalling in mammalian cells generally concerns cyclic guanosine monophosphate (cGMP) as a second messenger (Mayer & Hemmmens, 1997; Bogdan, 2001). The signalling pathways show increases in cytosolic [Ca.sup.2+] either by a release from intracellular sources or by influx from the extracellular environment. The other main procedure in signalling pathway is reversible protein phosphorylation.
cGMP concentrations change rapidly in response to an external stimulus. Typically, cGMP concentrations are increased by accelerated guanylyl cyclase (GC) activity that synthesizes cGMP from guanosine tri-phosphate (GTP). Concentrations are returned to original values by the activity of phosphodiesterases (PDE). There are many cellular effects of NO-mediated cGMP in mammalian cells. NO activates cGMP formation by interacting with a soluble form of GC. Therefore the cellular effects of NO are relatively short-lived as cGMP is rapidly degraded by PDE (Fig. 2).
cGMP was first detected and quantified by mass spectroscopy and radio-immunoassay methods in Zea mays (Janistyn, 1983) and Phaseolus vulgaris (Newton et al., 1999). Several data indicate the necessity for cGMP synthesis and action for plant responses to NO. Treatment of spruce needles with NO for 10 min caused cGMP to activate (Pfeiffer et al., 1994). Injection of recombinant rat NOS into tobacco leaves or treatment of tobacco suspension cultures with the NO donor S-nitrosoglutathione (GSNO), induced an increase in cGMP content. Furthermore, GC inhibitors LY 83583 and ODQ inhibited the induction of PAL and PR-1 gene expression by GSNO in tobacco suspension cultures (Hausladen & Stamler, 1998; Feelisch et al., 1999). Moreover, the treatment with a cell-penneable analogue of cGMP, 8-bromo-cGMP (8-Br-cGMP) induced the expression of both PR-1 and PAL. NO-induced programmed cell death was inhibited by ODQ and relieved together with 8-Br-cGMP, bur 8-Br-cGMP alone did not induce programmed cell death revealing that cGMP was required bur not enough for NO-initiated cell death (Clarke et al., 2000). Similarly cGMP's necessity for ABA- and NO-induced stomatal closure has been identified in pea and Arabidopsis (Neill et al., 2002a). In the same way, treatment with 8-Br-cGMP alone was not able to mimic the effects of ABA and NO. Therefore, it appears that cGMP is an intracellular mediator for some signalling pathways but for others additional signals are necessary.
[FIGURE 2 OMITTED]
cGMP-Independent NO Signalling
NO can complex with iron in other haem and iron containing proteins. Thus NO inhibits tobacco aconitase and iron-sulphur-containing enzyme that catalyzes the isomerisation of citrate to isocitrate (Navarre et al., 2000). In addition, NO converts the cytosolic forms of aconitase into iron-regulatory protein (IRP1), a protein that is involved in cellular iron homeostasis. In animal cells IRP1 inhibits the translation of mRNA encoding ferritin an iron binding protein (Wendehenne et al., 2001; Murgia et al., 2002). This would cause a decrease in cellular ferritin, resulting in an increase in free iron that leads to the production of ROS with resulting cell death. Murgia et al. (2002) also found that NO induced the accumulation of both ferritin mRNA and protein in Arabidopsis acting through the iron-dependent regulatory sequence present in the femtin promoter. NO inhibits the haem-containing enzymes catalase and peroxidases as well (Ferrer & Barcelo, 1999; Clark et al., 2000; Barcelo et al., 2002).
NO can also act together with cysteine and tyrosine amino acids in proteins and with thiol groups present in other molecules ubiquitous regulatory tri-peptide glutathione (Jia et al., 1996; Wendehenne et al., 2001). Thiol modification by ROS such as [H.sub.2][O.sub.2] is known as a potential signalling mechanism in plants (Neill et al., 2002b).
NO Signalling in Relation with Calcium
Recent studies have shown that NO participates in the increase of cytosolic-free [Ca.sup.2+] induced by osmotic stress and by the elicitor cryptogein in tobacco cells (Gould et al., 2003; Lamotte et al., 2004). Similarly, it has been shown that cytosolic [Ca.sup.2+] mediates the effects of NO leading to stomatal closure (Garcia-Mata et al., 2003; Neill et al., 2002a, 2003). In addition, treatment of NO stimulates an increase of intracellular [Ca.sup.2+] in Vicia faba guard and tobacco cells (Garcia-Mata et al., 2003; Lamotte et al., 2004). These data reveal the ability for NO to function as a [Ca.sup.2+]-activating intracellular compound in plant cells. Associated processes have been found in animals; many researches have showed that [Ca.sup.2+]-permeable channels, including plasma membrane voltage-dependent [Ca.sup.2+] channels, cyclic-nucleotide-gated [Ca.sup.2+] channels and the intracellular channels inositol triphosphate receptor and ryanodine receptors (RYR) are primary targets of NO. NO changes their activities by nitrosylation or indirectly by signalling pathways involving cGMP and/or cyclic ADP ribose (cADPR), which is an activator of RYR (Stamler et al., 2001). A cADPR antagonist, RYR inhibitors and cGMP synthesis inhibitors have all been shown to suppress the [Ca.sup.2+]-mobilizing actions of NO in plants; this implies that NO might activate RYR through cGMP and/ or cADPR (Garcia-Mata et al., 2003; Lamotte et al., 2004). NO treatment has definitely been demonstrated to increase cGMP levels both in tobacco and Arabidopsis thaliana (Dumer et al., 1998; Clark et al., 2000). However, the induction of cADPR synthesis by NO has not yet been established in plants.
NO Signalling in Relation with Protein Kinases
A common downstream target of cGMP in mammalian cells is cGMP-activated protein kinase (Wendehenne et al., 2001). NO primary targets in plant cells might include mitogen-activated protein kinase (MAPK). In plants MAPKs can be activated in response to extracellular signals such as drought, cold, phytohormones, pathogen attack and osmotic stress that cause to the activation of signal transduction pathways resulting in nuclear gene expression (Hirt, 1997). It has been demonstrated that [H.sub.2][O.sub.2] stimulates the activation of a MAPK in Arabidopsis suspension cultures (Desikan et al., 1999) and [H.sub.2][O.sub.2] have been determined to activate two MAPKs in Arabidopsis plants, at least one of, which is activated independently of SA and jasmonic acid (JA) and ethylene signalling pathways (Grant et al., 2000). The [H.sub.2][O.sub.2]-activated MAPK identified as AtMPK6 and its activity was estimated in Arabidopsis leaves and protoplasts (Desikan et al., 2001). Kovtun et al. (2000) also estimated that [H.sub.2][O.sub.2] activates AtMPK6 and related AtMPK3 in Arabidopsis leaf protoplasts. AtMPK6 is also activated in response to elicitor challenge and cold stress (Nuhse et al., 2000; Ichimura et al., 2000; Desikan et al., 2001). In addition, ozone and [H.sub.2][O.sub.2] treatment induced the activation of the tobacco orthologue of AtMPK, SA-activated mitogen activated protein kinase (SIPK; Samuel et al., 2000; Fig. 3).
It was revealed that [H.sub.2][O.sub.2]-induced transcription was determined by the specific stress-responsive promoters, GST6 and HSP18.2 (Kovtun et al., 2000). It was also demonstrated that [H.sub.2][O.sub.2] activates AtMPK3/6 by ANP1, the MAPKKK (mitogen-activated protein kinase kinases) at the head of the cascade. In addition, constitutive expression of ANP1 also activated GST6 and HSP18.2 expression. It was shown that transgenic tobacco plants over-expressing a tobacco MAPKKKK orthologous to ANP1, had increased tolerance to heat shock, freezing and salt stress, thus demonstrating that manipulation of a key signalling component responsive to [H.sub.2][O.sub.2] can protect plants against various environmental stresses (Kovtun et al., 2000).
Actually, NO-activated protein kinase in tobacco was identified as SIPK, and SA was necessary for NO activation of SIPK, as it was not activated in the NahG mutant that has a reduced SA content. In addition, NO induces increases in endogenous SA (Kumar & Klessig, 2000). The NO-activated protein kinase in Arabidopsis has not yet been identified, but has characteristics of a MAPK (Clarke et al., 2000).
As stated before, NO and cGMP are involved in the auxin response during the adventitious rooting process in cucumber (Pagnussat et al., 2002, 2003). However, not much is known about the complex molecular network operating during cell proliferation and morphogenesis triggered by auxins and NO in that process. In order to explain signal transduction mechanisms that operate during IAA- and NO-induced adventitious root formation, Pagnussat et al. (2004) investigated the involvement of a mitogen-activated protein MAPK cascade in this process. To assess these mechanisms, cucumber explants were treated with SNP or with SNP plus the specific NO-scavenger cPTIO. Their results suggest that a MAPK signalling cascade is activated during the adventitious rooting process induced by IAA in a NO-mediated but cGMP-independent pathway. The activation of MAPKs is discussed in relation to the cell responses modulating mitotic process.
[FIGURE 3 OMITTED]
NO synthesis and signalling also concern regulation through protein phosphates. Cantharidin, a protein phosphate 2A inhibitor, treatment caused an increase in NO synthesis (Delledonne et al., 1998). In contrast, NR-mediated NO synthesis in spinach was shown to be inhibited by cantharidin (Rockel et al., 2002). Recent advances on MAPK and the relationship between programmed cell death and NO will be discussed below.
NO and Programmed Cell Death
NO has been determined to work together with ROS to induce DNA fragmentation and cell lysis in animal cells. Cell death is distinguished by chromatin condensation, vacuolization of cytoplasm and damage of the mitochondrial membrane. Recently, Vianello et al. (2007) reviewed the involvement of mitochondria in the manifestation of programmed cell death in comparison to that described in animal programmed cell death. The main feature, connecting animal and plant programmed cell death via mitochondria, is represented by the release of cytochrome c and possibly other chemicals such as nucleases, which may be accomplished by different mechanisms, involving both swelling and nonswelling of the organelles.
Programmed cell death during hypersensitive response (HR) in plants has been well studied. Neill et al. (2003) focused on establishing a role for NO during pathogen-induced programmed cell death in Arabidopsis cell cultures. Arabidopsis cells with avirulent Pseudomonas syringae induced NO synthesis associated with the production of [H.sub.2][O.sub.2] (Clarke et al., 2000). NO-induced cell death also has the distinctiveness of programmed cell death like chromatin condensation, and caspase-like cascade activation. Even though there is no indication for the presence of caspase in plants, recent studies have shown the overexpression of a cysteine protease in Arabidopsis cells in NO-induced cell death (Neill et al., 2002a). This result proposes the differences in NO-mediated signalling pathways leading to programmed cell death.
The antioxidant role for NO acting during developmental programmed cell death by hormones was determined by Beligni et al. (2002) GA-induced programmed cell death was delayed in aleurone layers in the presence of NO in barley plants that associated with a loss of activity of catalase and superoxide dismutase (SOD). However, Beligni et al. (2002) suggests that NO acts as a specific endogenous modulator of programmed cell death in this biological system.
Programmed cell death is correlated with altered mitochondrial function and emergence of NO. NO inhibition of ATP synthesis in mitochondria by inhibition of cytochrome oxidase activity in plant cells has been determined (Yamasaki et al., 2001). Changed mitochondrial activity promotes programmed cell death in plant cells. NO-induced programmed cell death in Arabidopsis cells occurred by the inhibition of respiration and the release of cytochrome c (Zottini et al., 2002).
Mitochondrial respiratory shut down can be compensated by an alternative pathway using alternative oxidase (AOX) found in plants. Recently, Huang et al. (2002a) found that treatment with NO induced the expression of the AOX gene. Inhibition of the AOX pathway stimulated NO sensitivity and cell death, revealing a shunting of the respiration pathway by AOX. Pathogen challenge of Arabidopsis and tobacco also stimulate AOX activity (Simons et al., 1999).
Mechanical stress is another factor affecting programmed cell death and is also involved with NO. Centrifugation induces generation and DNA fragmentation and cell death in Kalanchoe daigremontiana leaf and callus (Pedroso et al., 2000). Additionally, mechanical stress in Arabidopsis also induces NO generation by a NOS-like enzyme (Garces et al., 2001).
A fundamental link between SIPK and WIPK and defense gene activation as well as programmed cell death was suggested by a gain-of function approach (Yang et al., 2001). The MAPKK, NtMEK2 was found to activate specifically both SIPK and WIPK. Interestingly, salicylate was not necessary for NtMEK2-mediated initiation of programmed cell death. Moreover, activation of SIPK and WIPK by a constitutively active NtMEK2 derivative was not associated with the generation of [H.sub.2][O.sub.2] (Yang et al., 2001), which in between with NO signals defense gene activation and programmed cell death in tobacco and Arabidopsis (Delledonne et al., 1998; Clarke et al., 2000). In tobacco, SIPK is activated by [H.sub.2][O.sub.2], whereas in Arabidopsis, AtMPK3 and AtMPK6, the orthologs of WIPK and SIPK, were activated by MAPKK kinase (MAPKKK), ANP1 (Kovtun et al., 2000). It seems that, pathogen-induced MAPK-independent production of [H.sub.2][O.sub.2] can activate pathogen-induced MAPK cascades and might in that way increase the efficiency of MAPK-regulated reactions.
Interestingly, regulation of different signalling pathways can be brought about by one specific MAPK cascade. Activation of oxidative stress responses upon expression of a constitutively active derivative of the MAPKKK, ANP1, caused a simultaneous inhibition of the auxin response pathway (Yang et al., 2001). Similarly, inactivation of AtMPK4 not only causes to activation of salicylate mediated defence responses, but also inhibits salicylate-independent jasmonate-responsive gene expression, revealing positive regulation by AtMPK4 of the salicylate-independent jasmonate-responsive pathway (Kovtun et al., 2000). It seems that MAPK cascades form central elements in signalling networks that regulate a plant's response to a large number of stimuli. This complication, together with the 20 MAPKs found in the Arabidopsis genome, present an enormous future challenge for plant molecular biologists with an interest in MAPK function.
NO Signalling in Plant Defense Response
A widespread feature of plant disease resistance is HR, which is characterized by the formation of necrotic lesions at the infection site and by the restriction of pathogen spread. Following this local resistance response the plant develops systemic acquired resistance (SAR) to the next infection by the same or different pathogens. A number of studies suggest that the death of the host cells during HR results from the activation of a suicide processes (Gilchrist, 1998; Heath, 1998). Actually, HR is thought to be a form of programmed cell death.
In the same way to what is observed in the macrophage action during the immune response, one of the earliest results in HR is the increase of ROI and NO. Synthesis of these species occurs through the activation of enzyme systems similar to neutrophil NADPH oxidase and NOS (Lamb & Dixon, 1997; Keller et al., 1998). It was shown that [H.sub.2][0.sub.2] is necessary to trigger localized host cell death, but is not enough for an effective response (Delledonne et al., 1998). NO cooperates with ROI in the induction of hypersensitive cell death and functions independently of ROI in the induction of various defense genes including pathogenesis-related proteins and enzymes of the phenylpropanoid metabolism that are concerned in the synthesis of lignin, antibiotics and SA (Delledonne et al., 1998; Durner et al., 1998).
Delledonne et al. (2001) investigated the role of different ROI in modulating NO signalling through the cell death pathway by altering the levels of NO and ROI alone and in combination. In soybean suspension cells it was estimated that only H202 increases the killing potential of NO, whereas ONOO was generated by reaction of NO with [O.sub.2]-induced cell death.
It was also demonstrated that during HR, SOD triggers NO killing by scavenging [O.sub.2.sup.-] with subsequent [H.sub.2][O.sub.2] production, and thus minimizing NO/[O.sub.2.sup.-] interaction and maximizing [H.sub.2][O.sub.2] potential of NO-mediated cell death. Although [O.sub.2.sup.-] is not the ROI that synergizes with NO to promote cell death, it is the sensor in triggering cell death in the Arabidopsis lsd1 mutant (Jabs et al., 1996) and roles as modulator of NO signalling during HR. Therefore, [O.sub.2.sup.-] can either stimulate HR by providing [H.sub.2][O.sub.2], or suppress HR cell death by scavenging NO.
It has also been indicated that any increase in the level of one individual component of the NO/ROI system must be balanced by an increased level of the other, in order to maintain the same degree of cell death from a well defined NO/ROI equilibrium. This may reveal the fact that in different experimental systems NO has been observed to exert both toxic and protective effects (Delledonne, 2005).
In many biological systems, the cytotoxic effects of NO and ROI derive from the diffusion-limited reaction of NO with [0.sub.2], which then interacts with many cellular components (Koppenol et al., 1992; Fang, 1997). Although extreme synthesis of [ONOO.sup.-] can injure normal tissue, the reactive chemistry of ONOO can be considered helpful when the entire organism is considered, due to its cytotoxic effects on invading pathogens (Fang, 1997) and tumor cells (Montalbini & Buonaurio, 1986). In plants, it has been shown that the ROI and NO produced during the start of a pathogen-induced hypersensitive reaction are associated with the trigger hypersensitive cell death (Delledonne et al., 1998) Consequently, Delledonne et al. (2001) investigated whether this trigger occurs through mechanisms similar to those established in animals, by analyzing the effect of exogenous [ONOO.sup.-] in soybean suspension cultures. Exposure of animal cells to ONOO at 1-1,000 [micro]M range causes cell death (Lin et al., 1995; Cookson et al., 1998; Foresti et al., 1999). Treatment of soybean cell suspensions with [ONOO.sup.-] did not result in cell death at concentrations up to 1 mM (Delledonne et al., 2001).
It has been shown that pathogens induce changes in the antioxidant gradient of plant cells (Vanacker et al., 1998). The amount of SOD enzyme increases in tobacco infected with tobacco mosaic virus during the expression of the hypersensitivity (Montalbini & Buonaurio, 1986) and in Phaseolus vulgar& a Cu,Zn-SOD activity increases in the hypersensitive response of resistant leaves (Buonaurio et al., 1987). Soybean suspension cultured cells have increased SOD activity, which may provide to limit the oxidative stress reasoned by the continuous agitation (Yahraus et al., 1995). Purification of these enzymes causing the inactivation of the Fe- and MnSOD isoforms, but showed that Cu,Zn-SOD could explain most of this activity. Furthermore, the sharp reduction of total SOD activity in diethyldithiocarbamate (DDC)-treated cells reflected the complete inhibition of the Cu,Zn-SOD isoform. Although total and Cu,Zn-SOD activities stayed steady during the hypersensitive response, analysis of Cu,Zn-SOD transcript accumulation showed a strong and sustained induction within 1 h of the treatment of the avirulent pathogen. This reveals that protein income might play a role in the response of Cu,Zn-SOD to activate oxygen or nitrogen species (Williamson & Scandalios, 1992).
LSD1, a negative regulator of cell death, regulates SA induction of Cu,Zn-SOD (Kliebenstein et al., 1998) in an [O.sub.2.sup.-]-dependent signal (Jabs et al., 1996) and provisions the future role for SOD as a modulator of [O.sub.2.sup.-] function. In fact, the spreading lesion phenotype of lsd1 mutants is associated with a lack of up-regulation Cu,Zn-SOD that seems to be in charge of detoxification of accumulating [O.sub.2.sup.-] before lsd1 can induce cell death (Kliebenstein et al., 1999).
NO production and ROS activation in response to infection is associated with the avirulent gene-dependent oxidative burst that occurs immediately prior to the onset of hypersensitive cell death (Allan & Fluhr, 1997; Delledonne et al., 1998; Clarke et al., 2000; Foissner et al., 2000; Romero-Puertas & Delledonne, 2003). NO synthesis rapidly increases after challenge with avirulent bacteria in Arabidopsis thaliana and soybean (Delledonne et al., 1998; Clarke et al., 2000; Zhang et al., 2003). Furthermore, direct contact of crown rust fungus with oat plants induces the synthesis of NO in an early stage in the defense response (Tada et al., 2004). In addition, tobacco epidermis cells treated with the fungal elicitor cryptogein and potato tubers treated with an elicitor from Phytophthora infestans accumulate NO (Foissner et al., 2000; Lamotte et al., 2004; Yamamoto et al., 2003). Lipopolysaccharides isolated from plant and animal pathogens have also been estimated to elicit a strong and quick burst of NO in Arabidopsis thaliana plants (Zeidler et al., 2004).
The mobile and chemical nature of NO suggests that the downstream effects of NO may be directly induced by interaction of NO with ion channels or proteins that change gene expression, or indirectly following interaction of NO with signalling proteins (Neill et al., 2003). In plants it has been suggested that activation of GC results in an increased production of cGMP as in mammalian systems (Hancock, 2005). Inhibitors of NO-inducible GC are able to suppress induction of PAL in tobacco plants, suggesting the involvement of cGMP-dependent components in NO-dependent defense gene activation (Durner et al., 1998).
SAR is activated after pathogen infection and causes the initiation of a plant defense response in uninfected parts of the plant. Consequently the whole plant is more resistant to another infection. SA plays an important role during incompatible interactions for the amplifications of early signals originating from pathogen-plant recognition (Shirasu et al., 1997). Exogenous application of SA has been estimated to imitate SAR and induces the transcription of PR genes. Numerous investigations revealed the effect of NO in the modulation of signalling leading to SAR, while its effect is completely dependent on the function of SA. NO treatment has been found to cause the accumulation of SA in tobacco plant (Durner et al., 1998). PR-1 induction by NO is mediated by SA and it is inhibited in transgenic NahG plants, which are unable of accumulating SA. Besides, tobacco plants when treated with NOS donors the lesions caused by TMV on non-treated leaves are induced in wild type, but not in NahG plants (Song & Goodman, 2001). Whereas treatments with NOS inhibitors or NO scavengers reduce SA-induced SAR.
Another mobile signal that activates SAR is S-nitroso-l-glutathione (GSNO; Dumer & Klessig, 1999). GSNO acts as both an intracellular and intercellular NO carrier. In addition GSNO has been revealed to induce systemic resistance against tobacco mosaic virus infection and PAL expression in tobacco (Durner et al., 1998; Song & Goodman, 2001). After the estimation of GSNO-catabolizing enzyme (GSFDH) and its encoding gene, mutant yeasts obtained that lack this gene showed enhanced susceptibility to nitrosative challenge. The estimation of the GS-FDH gene in plants implies the ability of the plant to change GSNO activity and signalling function (Neill et al., 2003).
Lately, MAPK cascades that are different from those activated upon pathogen infection or elicitor treatment, were demonstrated to negatively control defense in plants. Transposon inactivation of the gene encoding Arabidopsis AtMPK4 resulted in dwarfed mutants that show elevated levels of salicylate, constitutive PR gene expression and increased resistance to virulent pathogens (Petersen et al., 2000). This resistance required salicylate, but was independent of NPR1. Another study showed that a mutation in a putative Arabidopsis MAPKKK resulted in a mutant (edr1, improved disease resistance) with increased resistance to powdery mildew and Pseudomonas syringae without any phenotypic changes (Frye et al., 2001). Because edr1-mediated resistance was salicylate- and NPR1/NIM1-dependent and did not lead to enhanced levels of salicylate and constitutive PR gene expression, EDR1 is unlikely to control the AtMPK4 MAPK cascade. EDRI is homologous to members of the Raf-like MAPKKK family, such as the negative regulator of the ethylene response, CTR1 (Johnson & Ecker, 1998). Interestingly, the Arabidopsis MAPKs, AtMPK3 and ATMPK6, are regulated by the MAPKKK, ANP1, which does not belong to the EDR1/CTR1 family of MAPKKK (Kovtun et al., 2000).
Interaction with Other Signalling Pathways
NO can cooperate with other signals either directly or with other signalling pathways to direct cellular processes. ROS generation such as [H.sub.2][O.sub.2] is a regular companion of NO production. Therefore both ROS and NO are produced in response to pathogen attack (Dumer & Klessig, 1999) and also in guard cells in response to ABA (Neill et al., 2002a). Similarly, [H.sub.2][O.sub.2] is produced in response too many biotic and abiotic stimuli and also to NO, this interaction was stated in the previous section. It is also important to point out that both [H.sub.2][O.sub.2] and NO activate MAPKs and changes in intercellular calcium. In summary, NO interacts with many signals but a deeper understanding of signalling pathways in plants needs to be achieved.
Significant progress on the description of NO signalling in plants has been made in recent years using a combination of pharmacological, biochemical and genetic approaches. It is necessary that the biosynthetic origins of NO, an endogenous metabolite, need to be completely described.
NO can be synthesized from nitrite by NR, but the occurrence of an enzyme similar to mammalian NOS has not yet been proved. Recognition and subsequent manipulation of NO biosynthetic enzymes and the encoding genes need to be investigated. NO can induce a variety of pathways in plants, like programmed cell death, stomatal movement and root growth, but different NO sources may release different molecular species of NO that could have separate effects. However, researchers have show that endogenous NO mediates numerous responses to developmental and external stimuli. Intracellular signalling responses to NO involve the biosynthesis of cGMP and cADPR and increase of cytosolic calcium, but the exact biochemical and cell biological character of these responses is to be specified. Likewise, protein kinases and protein phosphatases, transcription factors, ion channels and other signalling proteins activated or suppressed by NO need recognition and characterization.
Recent information about the function of NO in plants has come from pharmacological approaches with NO donors, NO scavengers and NOS inhibitors. As a result sometimes it is very complex to distinguish between the physiological effect and pharmacological artifact found by chemical treatment, therefore the treatment of NO to a plant in different forms and doses needs to be subjected to special confirmation criteria with the aim of ensure reliability and reproducibility of metabolic responses stimulated by NO-supporters. However the most important challenge is to gain donors with increased stability and longer half-life, with a controlled NO release rate and donors exhibiting high tissue or cell specificity.
Furthermore the NO relation with other signals also requires to be illuminated, especially the interaction between SA, JA and ethylene. It also should be taken into account that various stress factors existing, consequently they can activate very complicated responses of the plant cell as a result of amplification, synchronization or negative regulation of signalling pathways. Most of the studies on the NO function in defence signalling system were carried out on cell suspension cultures. In order to supply evidence long-distance transmission between different cells and neighbour tissues, future experiments should be done also in whole plants. Although there is for sure that NO is produced in plants in reaction to various stress conditions, it still a mysterious molecule. Another essential difficulty is the identification of NO targets in plants. New techniques that are suitable for the diagnostic analysis of nitrosylated proteins are now available and capable to reveal NO targets in plants.
ABA abscisic acid
cGMP cyclic guanosine monophosphate
GA gibberellic acid
HR hypersensitive response
MAPK mitogen activated kinase
NO nitric oxide
NOS nitric oxide synthase
NR nitrite reductase
ROS radical oxygen species
SAR systemic acquired resistance
Published online: 4 April 2009
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Narcin Palavan-Unsal (1,2) * Damla Arisan (1)
(1) Faculty of Science and Letters, Istanbul Kultur University, 34156, Bakirkoy, Istanbul, Turkey
(2) Author for Correspondence; e-mail: firstname.lastname@example.org
Table 1 Effects of NO in plant growth and development and interacting plant growth regulators Physiological Interacting plant process No effect growth regulator Leaf expansion Induction Auxins and cytokinins Root growth Induction Auxins and cytokinins Senescence Delay Ethylene Seed germination Stimulation Gibberellins De-etiolation Stimulation Gibberellins and cytokinins Hypocotyl elongation Inhibition Gibberellins Fruit ripening Inhibition Ethylene Stomata opening Stimulation/ Abscisic acid and closing inhibition
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|Author:||Palavan-Unsal, Narcin; Arisan, Damla|
|Publication:||The Botanical Review|
|Date:||Jun 1, 2009|
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