Nitric Oxide Biosynthesis in Plants – the Short Overview
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Plant Soil Environ. Vol. 60, 2014, No. 3: 129–134 Nitric oxide biosynthesis in plants – the short overview D. Procházková1, D. Haisel1, D. Pavlíková2 1Institute of Experimental Botany, Academy of Sciences of the Czech Republic, Prague, Czech Republic 2Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, Prague, Czech Republic ABSTRACT In the past two decades, many pathways of nitric oxide biosynthesis have been described. This review offers the general knowledge of mechanisms of plant nitric oxide biosynthesis. Keywords: nitrate reductase; NOS like enzyme With the finding of a number of roles of the gaseous On one hand the indisputable evidence of such free radical nitric oxide (NO) in animal cells, many enzyme in plant cells is missing but on the other studies have reported its presence in the plant king- hand many other pathways were suggested. This dom and its diverse function in plant cells. In plants, review tries to offer the general knowledge of NO first came to prominence within the context of mechanisms of plant NO biosynthesis. regulating defence during pathogen infection (Mur et al. 2013b). Afterwards, it was described that NO is involved in many plant physiological processes, Enzymatic production e.g. in stimulation of seed (Beligni and Lamattina 2000) and pollen (Šírová et al. 2011) germination, Nitrate reductase. The best-characterized floral regulation (He et al. 2004), senescence (Jasid production pathway for NO in plants is nitrate et al. 2009), stomatal closure (Neill et al. 2008), root reductase (NR, EC 1.7.1.1.) pathway. This en- development (Pagnussat et al. 2003, Correa-Aragunde zyme was found both as a cytosolic form and as et al. 2004) etc. a plasma membrane-bound form (Planchet and Unfortunately, NO studies in plants lag behind Kaiser 2006). In Arabidopsis, NR is encoded by the studies in animal kingdom. One of the ques- two homologous genes, Nia1 and Nia2 (Wilkinson tions, which was acceptably clarified in animal and Crawford 1993). cells but remains unclear in plants, is NO bio- NR normally reduces nitrate to nitrite at the synthesis. In animal organisms, it is nitric ox- expense of NAD(P)H but also catalyzes 1-elec- ide synthase (NOS) which converts l-arginine tron transfer from NAD(P)H to nitrite resulting to l-hydroxyarginine and subsequently to nitric in NO formation (Planchet and Kaiser 2006) via oxide and citrulline with participation of O2 and the reaction: NADPH. Three independent animal NOS types + – → + NAD(P)H + 3 H3O + 2 NO2 NAD(P) + 2 NO + 5 H2O are known: neuronal NOS, inducible NOS which The reduction efficiency is low – about 1% of was originally isolated from macrophages, and NR activity (Rockel et al. 2002) but the importance endothelial NOS. Supported by the Czech Science Foundation, Grant No. P501/11/1239. 129 Vol. 60, 2014, No. 3: 129–134 Plant Soil Environ. of NR as a NO source was demonstrated by using However, Lo et al. (2000) demonstrated that NR-deficient mutants which produced significantly these antibodies are rather unspecific. Likewise, lower levels of NO (Planchet et al. 2005). the response of NOS activity in barley root mito- NR is more pronounced in a low-oxygen envi- chondria to inhibitors, substrates and cofactors was ronment and requires nitrite levels to be in excess atypical when compared to iNOS, hence the exist- of the natural substrate nitrate. For example for ence of NOS root mitochondria was implausible maize NR, the Km for nitrite is 100 μmol, and ni- (Gupta and Kaiser 2010). Another point, calling trate is a competitive inhibitor with a Ki of 50 μmol the existence of NOS in plants into question, is (Rockel et al. 2002). The enzyme is activated by a the necessity of tetrahydrobiopterin in mamma- decrease in the cellular pH (Kaiser and Brendle- lian NOS. This molecule seems to promote and/ Behnisch 1995). or stabilize the active dimeric form of the enzyme Nitrite:NO reductase. A plasma membrane- (Alderton et al. 2001). The presence of tetrahy- bond nitrite:NO reductase (NiNOR), distinct from drobiopterin in cells of higher plants is unclear. the plasma membrane NR, was shown to convert Nevertheless, its function could be carried out nitrite to NO in tobacco (Stöhr and Stremlau 2006, by tetrahydrofolate, whose metabolism was de- Moreau et al. 2010). The Km (nitrite) for NiNOR scribed sufficiently in higher plants (Sahr et al. reaction is 175 μmol for plant mitochondria (Gupta 2005, Corpas et al. 2009). In addition, no gene or et al. 2005). It appears to use cytochrome c as an protein with sequence similar to the large animal electron donor in vitro, but it has yet to be cloned NOS proteins was found even in the sequenced and fully identified (Wilson et al. 2008). Arabidopsis genome (Crawford and Guo 2005). The plasma membrane-bound NR:NiNOR sys- Nevertheless, Arabidopsis has a gene with 16% tem was suggested to be involved in the sensing sequence similarity to the gene from snail Helix of nitrate availability in the soil (Meyer and Stöhr pomatia which is implicated in NO synthesis 2002). Furthermore, evidence has recently been and which, when expressed in Escherichia coli, provided that NiNOR mediated NO production increases NO synthesis in crude cytosolic frac- has a role in the regulation of root infection by tions from particular snail organs (Huang et al. mycorrhizal fungi (Moche et al. 2010). 1997). This Arabidopsis gene was identified as a NOS like enzyme. As plants appear able to grow member of GTP-binding family, encoding NOS- and to complete their life cycle in the absence like protein AtNOS1 (Guo et al. 2003). AtNOS1 of nitrate and nitrite, e.g., with ammonium as protein cross-reacts with antibodies against nNOS the only source of nitrogen, they must possess (Guo et al. 2003). As AtNOS1 might indirectly nitrite-independent, oxidative pathways for NO affect NO synthesis, because it might serve as production (Rümer et al. 2009). Indeed, in analogy GTPase, Crawford et al. (2006) suggested that to animal NOS (EC 1.14.13.39), plants appear to AtNOS1 should be rename nitric oxide associated have an enzyme, which is completely independent 1 (AtNOA1). However, the relationship between of nitrite and whose function consists in deamina- AtNOA1 function and NO accumulation is rather tion of l-arginine into l-citrulline and NO using unclear (Moreau et al. 2010). 2+ NADPH and O2 and requiring Ca /calmodulin: So far, two locations for AtNOA1 were reported: chloroplasts (Flores-Pérez et al. 2008) and mito- l-arginine + NAD(P)H + O → l-citrulline + NAD(P)+ + 2 chondria (Guo and Crawford 2005). Apart from + H O + NO 2 its role in NO production, AtNOA1 might act in NOS activity was measured in pea by ozone binding RNA/ribosomes (Sudhamsu et al. 2008). chemiluminiscence, using commercial neuronal In algae, namely in Ostreococcus tauri and O. lu- NOS as a positive control (Corpas et al. 2006). cimarinus, two NOS sequences were found (Foresi This activity was also detected using electron et al. 2010). In the case of O. tauri it was found paramagnetic resonance spin-trapping technique that the amino acid sequence of the NOS is 45% in soybean chloroplasts (Simontacchi et al. 2004) similar to that of a human NOS. It is close to the and in sorghum seed embryonic axes (Jasid et al. mammalian inducible NOS isoform because (a) its 2006). In addition, immunological evidence for folding was likely to be similar to that of human NOS occurrence in pea and maize tissues was inducible NOS and (b) this algae enzyme lacks the obtained with antibodies against animal NOS autoregulatory control element indicating that it (Barroso et al. 1999, Ribiero et al. 1999). is close to the mammalian inducible NOS isoform. 130 Plant Soil Environ. Vol. 60, 2014, No. 3: 129–134 On the other hand, Ostreococcus genome has been series of reactions, two molecules of HNO2 inter- completely sequenced (Derelle et al. 2006) and act and give rise to NO and NO2, and NO2 can be it lacks the genes encoding for the enzymes that converted to NO and oxygen (Stöhr and Stremlau synthetize tetrahydrobiopterin, suggesting that 2006, Moreau et al. 2010): Ostreococcus NOS may bind another cofactor for 2 NO– + 2 H+ ↔ 2 HNO ↔ NO + NO + H O ↔ catalytic activity (Correa-Aragunde et al. 2013). 2 2 2 2 ↔ 2 NO + ½ O + H O However, it is still premature to declare that plant 2 2 NOS was found because this organism belongs to At acidic pH, an apoplastic non-enzymatic con- a primitive class within the green plant lineage, version of nitrite to NO occurring in the presence the Prasinophyceae (Chlorophyta), so we cannot of reductants such as ascorbic acid was described assume that higher plants have retained this gene (Bethke et al. 2004). In addition, simultaneous expo- (Hancock 2012). sure of carotenoids to NO2 and light resulted in the Xanthine oxidoreductase. In addition to O2 release of NO into the gas phase (Cooney et al. 1994). reduction, xanthine oxidase is also capable of NO production from hydroxylamine and sali- reducing organic nitrates as well as inorganic cylhydroxamate. Rümer et al. (2009) described nitrate and nitrite releasing NO (Godber et al. another form of oxidative NO formation: when 2000). Xanthine oxidoreductase, the ubiquitous hydroxylamine was applied to tobacco cell cul- molybdenum-containing enzyme, occurs in two ture which was deficient in NR, NO was emit- convertible forms: the superoxide-producing xan- ted. However, because the natural existence of thine oxidase (form O, EC 1.1.3.22) and xanthine hydroxylamines in plants was not confirmed, the dehydrogenase (form D, EC 1.1.1.204) (Palma et al.