Nitric Oxide Level Is Self-Regulating and Also Regulates Its ROS Partners.

Abstract

Nitric oxide (NO) is a free radical recognized as an omnipresent inter- and intra-cellular signaling molecule involved in the regulation of an extraordinary range of diverse cellular functions in plants (Besson-Bard et al., 2008). All NO derivatives are called reactive nitrogen species (RNS) which include more favorable structures such as nitrosonium cation (NO+) and nitroxyl radical (NO−) as a result of NO gaining or losing electrons, and the products of the reaction between NO and its close partners, reactive oxygen species (ROS), such as peroxynitrite (ONOO−), and the NOx compounds (NO2, N2O3, and N2O4; Bellin et al., 2013). Although it is known that NO may regulate gene transcription and activate secondary messengers, the ways in which NO functions are still mostly unidentified (Besson-Bard et al., 2008; Palmieri et al., 2008; Gaupels et al., 2011). In the last decade, however, it has been shown that NO is also able to control different biological processes in plants by directly modifying proteins through covalent post-translational modifications (PTMs) giving rise to nitration, nitrosylation or S-nitrosylation (Romero-Puertas et al., 2013). S-nitrosylation is the covalent binding of a NO group to a cysteine residue and probably the better known NO-dependent PTM as more than 1000 proteins have been shown as targets of S-nitrosylation (Kovacs and Lindermayr, 2013), although the functional effect of this modification has only been analyzed in around 2% of these proteins (Astier et al., 2012; Kovacs and Lindermayr, 2013; Romero-Puertas et al., 2013). Nitration, in which 3-nitrotyrosine is produced after a nitrite group is added to the ortho-position of Tyr residues, is another NO-dependent PTM, although so far analyzed to a lesser degree than S-nitrosylation (N-Tyr; Vandelle and Delledonne, 2011). These PTMs are able to modify the activity, location, aggregation, or even stability of proteins (de Pinto et al., 2013; Gibbs et al., 2014; Albertos et al., 2015). We should bear in mind that NO function depends on the rate and location of its production and that NO level will determine a cytotoxic or stimulating effect (Beligni and Lamattina, 2001; Serrano et al., 2012). Thus, a precise control of NO level by switching the NO signaling off or not seems to be a crucial event for plant survival, and it appears that plants have developed many strategies to achieve it. Reactive oxygen species (ROS) comprises oxygen derivatives species produced by the reduction of oxygen, such as superoxide radicals (O2.-), hydroxyl radicals (·OH), peroxyl radicals (ROO·), and alkoxyl radicals (RO·) and also some non-radical compounds such as hydrogen peroxide (H2O2), the singlet oxygen (1O2), ozone (O3), and hypochlorous acid (HOCl−) (Halliwell and Gutteridge, 2007). Although research on ROS, which have strong oxidizing potential, initially focused on cytotoxicity, in recent years, it has become clear that they can also function as signaling molecules in most cellular processes (Baxter et al., 2014). Thus, plants have developed a means of utilizing lower concentrations of ROS as signaling molecules under certain physiological and stress conditions (Petrov and Van Breusegem, 2012). Genetic and pharmacological techniques have demonstrated that different ROS species can affect nuclear gene expression by responding to a variety of environmental stimuli (Sandalio and Romero-Puertas, 2015). However, a finely tuned balance between ROS scavenging and ROS production is necessary to determine their level and impact as damaging and signaling molecules (de Pinto et al., 2012; Baxter et al., 2014).