NO Production in Plants Exposed to Cadmium

Nitric oxide is a simple gaseous signaling molecule which, in many plant tissues, regulates a wide range of physiological and biochemical processes as well as plant responses to biotic and abiotic stresses (del Rio 2011; Delledonne 2005; Siddiqui et al. 2010). An increasing number of studies have reported the role played by NO in plant response to heavy metals including cadmium, although the source of NO and its role in metal toxicity and plant responses are not yet clearly established (Xiong et al. 2010). NO can be generated enzymatically by nitrate reductase and nitric oxide synthase (NOS)-like activities and can also be produced nonenzymatically by reduction of apoplastic nitrite under acid conditions and by reduction of nitrite to NO in the mitochondria (Neill et al. 2008; del Rio 2011).

There is still some uncertainty concerning NOS in plants. Although there is strong evidence to show the presence of L-arginine-dependent NOS activity in plants (Barroso et al. 1999; del Río 2011), the only NOS from the plant kingdom to be fully characterized so far is the enzyme from the Ostreococcus tauri green alga (Foresi et al.

2010). NOS activity has been shown to be present in peroxisomes from pea leaves (Barroso et al. 1999). This enzyme uses L-arginine as substrate and requires NADPH, Ca2+/calmodu-lin, BH4, FAD, and FMN, although its gene has not yet been characterized (Corpas et al. 2004; del Río 2011). The generation of NO in peroxi-somes by this NOS activity has also been reported by Corpas et al. (2004). In addition, chloroplasts have recently been identified as a source of NO via arginine and nitrite, although the enzyme involved has not been characterized yet (Jasid et al. 2006; del Río 2011). A nitrite-NO oxidoreductase enzyme (Ni-NOR) associated with root plasma membrane may also contribute to NO production (Stohr and Stremlau 2006). However, there are other potential enzymatic sources of NO in plants (del Río et al. 2004; del Río 2011) such as xanthine oxidase which can produce NO under hypoxic conditions (Millar et al. 1998; Harrison 2002). Regardless of the source of NO involved, the mechanisms determining the effects of NO are far from being fully understood, while a number of downstream signaling pathways involving Ca2+, cyclic GMP, and cyclic ADP-Rib have been described (Besson-Bard et al. 2008). NO is able to react with oxygen radicals such as O.-, generating peroxynitrite (ONOO(), and also to control ROS levels in cells and vice versa (Delledonne et al. 2001). NO can also react with GSH to produce S-nitrosoglutathione (GSNO), which is regarded as a long-distance-signaling molecule and a natural reservoir of NO (del Río

2011). NO directly or indirectly can regulate gene expression and protein functions. It therefore reacts very rapidly with heme groups and thiols, thus regulating enzymatic activities (Moreau et al. 2010). The protein S-nitrosylation of cystein residues has been demonstrated to be very important in regulating the enzymatic activity of certain proteins (Lindermayr et al. 2006; Lindermayr and Durner 2009; Romero-Puertas et al. 2007b, 2008). Some studies of NO production during the exposure of plants to heavy metals have reached controversial conclusions. The cell cultures of soybean (Kopyra et al. 2006) and Arabidopsis (De Michele et al. 2009) exposed to Cd showed an increase in NO and was dependent on NOS-like activity (De Michele et al. 2009); whereas, in pea leaves and roots, prolonged exposure to 50 mM Cd reduced NO accumulation (Rodríguez-Serrano et al. 2006, 2009). Bartha et al. (2005) reported increased NO in the roots of Brassica juncea and Pisum sativum exposed to 100 mM Cd, Cu, and Zn. Besson-Bard et al. (2009) have shown that NO production in Cd-treated roots is related to Cd-induced Fe deficiency. The discrepancies observed in these results could be because of differences in Cd exposure duration, with NO increasing after a short period of Cd treatment and decreasing after a prolonged treatment (Fig 9.2). The metal concentrations, plant ages, and plant tissues used could also explain these discrepancies (Rodríguez-Serrano et al. 2009). Exogenously supplied NO has been demonstrated to alleviate heavy metal toxicity (Kopyra and Gwózdz 2003; Hsu and Kao 2004; Yu et al. 2005; Wang and Yang 2005; Laspina et al. 2005; Xiong et al. 2010) possibly because of its ability to act as an ROS-scavenging antioxidant such as SOD and CAT (Wang and Yang 2005; Rodríguez-Serrano et al. 2006; Singh et al. 2008; Siddiqui et al. 2010). Exogenous NO application also affects root cell walls and helps in metal accumulation. NO cause increases in cytosolic Ca2+ concentrations by regulating Ca(+ channels and transporters, which may be involved in the signaling cascade that regulates gene expression under stress conditions (Besson-Bard et al. 2008( . Recently, cross-talk between Cd, Ca(+, ROS, and NO has been detected in pea leaves (Rodríguez-Serrano et al. 2009). The supply of exogenous Ca2+ to pea plants exposed to Cd reduced Cd-dependent O2- accumulation and restored NO accumulation to the level observed in control plants (Rodríguez-Serrano et al. 2009).

Fig. 9.2 Cadmium induces differential response in plants depending on the period of treatment. A short period of treatment produces oxidative and NO burst, which induces gene expression to prevent oxidative damages caused by the metal. Long-term treatment produces overaccumula-tion of ROS and a reduction of NO giving rise to severe damages. Gene regulation in long-term treatment is focused on repairing oxidative damages and cell death. PCs phytochelatins, HSPs heat shock proteins

Fig. 9.2 Cadmium induces differential response in plants depending on the period of treatment. A short period of treatment produces oxidative and NO burst, which induces gene expression to prevent oxidative damages caused by the metal. Long-term treatment produces overaccumula-tion of ROS and a reduction of NO giving rise to severe damages. Gene regulation in long-term treatment is focused on repairing oxidative damages and cell death. PCs phytochelatins, HSPs heat shock proteins

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