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Francisco Javier Romera
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Alfred Zheng
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Romera, F.J.; García, M.J.; Lucena, C.; Angulo, M.; Pérez-Vicente, R. Nitric Oxide and S-nitrosoglutathione in Plants. Encyclopedia. Available online: https://encyclopedia.pub/entry/48164 (accessed on 27 July 2024).
Romera FJ, García MJ, Lucena C, Angulo M, Pérez-Vicente R. Nitric Oxide and S-nitrosoglutathione in Plants. Encyclopedia. Available at: https://encyclopedia.pub/entry/48164. Accessed July 27, 2024.
Romera, Francisco Javier, María José García, Carlos Lucena, Macarena Angulo, Rafael Pérez-Vicente. "Nitric Oxide and S-nitrosoglutathione in Plants" Encyclopedia, https://encyclopedia.pub/entry/48164 (accessed July 27, 2024).
Romera, F.J., García, M.J., Lucena, C., Angulo, M., & Pérez-Vicente, R. (2023, August 17). Nitric Oxide and S-nitrosoglutathione in Plants. In Encyclopedia. https://encyclopedia.pub/entry/48164
Romera, Francisco Javier, et al. "Nitric Oxide and S-nitrosoglutathione in Plants." Encyclopedia. Web. 17 August, 2023.
Nitric Oxide and S-nitrosoglutathione in Plants
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This entry is adapted from the peer-reviewed paper 10.3390/ijms241612617

Iron (Fe) is abundant in soils but with a poor availability for plants, especially in calcareous soils. To favor its acquisition, plants develop morphological and physiological responses, mainly in their roots, known as Fe deficiency responses. Most of these substances, including auxin, ethylene, glutathione (GSH) and nitric oxide (NO), increase their production in Fe-deficient roots while S-nitrosoglutathione (GSNO), derived from GSH and NO, decreases its content. This paradoxical result could be explained with the increased expression and activity in Fe-deficient roots of the GSNO reductase (GSNOR) enzyme, which decomposes GSNO to oxidized glutathione (GSSG) and NH3. The fact that NO content increases while GSNO decreases in Fe-deficient roots suggests that NO and GSNO do not play the same role in the regulation of Fe deficiency responses. 

GSNO NO

1. Introduction

Iron (Fe) is very abundant in most soils, mainly as Fe3+, although its availability to plants is low, especially in calcareous soils [1][2]. This low availability is mainly related to the low solubility of Fe oxides and hydroxides at a high pH [2]. Dicot (Strategy I) plants, such as Arabidopsis and the tomato, need to reduce Fe3+, abundant in most soils, to Fe2+, by means of a ferric reductase (encoded by FRO2 in Arabidopsis) at the root surface, prior to its subsequent uptake through an Fe2+ transporter (encoded by IRT1 in Arabidopsis; Refs. [3][4]). When grown under an Fe deficiency, dicot plants develop several physiological and morphological responses, mainly in roots, known as Fe deficiency responses and aimed at facilitating Fe mobilization and uptake (Refs. [3][5]). Once Fe has been acquired in enough quantity, Fe deficiency responses need to be switched off, to save energy and to avoid toxicity. It should be noted that the responses spend a lot of energy and resources for being activated and that Fe in excess can be very toxic. Among other effects, Fe can cause the formation of extremely reactive hydroxyl radicals through the Fenton reaction [4][6]. To solve both problems, a low availability of Fe in soils and toxicity when Fe is acquired in excess, plants have evolved sophisticated mechanisms to tightly control Fe acquisition and homeostasis [4]. In dicot plants, several hormones and signaling molecules, including ethylene, auxin, nitric oxide (NO) and glutathione (GSH), have been implicated in the activation of most physiological and morphological responses to Fe deficiency [3][5][7][8][9][10][11][12][13]. All the above cited substances enhance their production in Fe-deficient roots and are closely inter-related in a complex manner since some of them can affect the production and/or distribution of the other ones (Refs. [8][9][14]). Paradoxically, S-nitrosoglutathione (GSNO), which is formed from GSH and NO, decreases its production in Fe-deficient roots, where it has also been involved in the regulation of Fe deficiency responses [11][15][16]. These results suggest that GSNO, which is considered a relatively stable store for NO and a vehicle for its long-distance transport [17], does not play exactly the same roles that NO does in the regulation of Fe-deficient responses.

2. NO and GSNO in Plants

NO is a simple gaseous molecule (NO) which, due to its free radical nature, can react with cellular targets to form reactive nitrogen species, such as S-nitrosothiols, including S-nitrosoglutathione (GSNO; see below; Ref. [18]). NO can also bind to transition metal ions, such as Fe or Cu, to form metal–nitrosyl complexes, and to fatty acids to form nitro-fatty acids, which play an important role in the adaptation of plants to abiotic stresses [19][20]. NO is lipophilic and can easily diffuse across membranes [21]. In the 1980s, NO was recognized as a signaling molecule in mammals and later on, around the 1990s, also in plants [19][21]. NO has been involved in a myriad of developmental and physiological processes of plants, including seed germination, stomatal closure, flower development, root branching and senescence [20][22][23][24][25]. In addition, NO has been implicated in the responses of plants to both biotic and abiotic stresses, including pathogen infection, salinity, drought stress, nutrient deficiencies, an excess of heavy metals and others (Refs. [20][22][23][26][27][28][29][30][31][32]).
NO synthesis has been reported in different plant organs, including roots, stems, leaves and flowers, and, at the subcellular level, both in the apoplast and in the symplast, and in different organelles, such as mitochondria, chloroplasts and peroxisomes [20][33]. NO can be synthesized by both enzymatic and non-enzymatic pathways [19][20][22][24][33]. In mammals, NO synthases (NOS) catalyze the conversion of L-arginine to NO and citrulline. However, although there is some evidence of NOS-like activity in plants, until now, no functional NOS protein has been isolated and characterized in higher plants [20][22]. It seems that, in plants, nitrate reductase (NR) plays the main role in the enzymatic NO production [19][20]. There are mutants impaired in NO production, including the Arabidopsis nia1nia2 mutants, altered in the NIA1 and NIA2 genes, encoding NRs [19][34], and mutants that overproduce NO, such as the Arabidopsis cue/nox1 mutants [19][35][36]. NO is usually detected and determined by using the permeable NO-sensitive fluorophore 4-amino-5-methylamino-2′,7′-difluoro-fluorescein diacetate (DAF-FM DA) [13][34].
NO is considered a phytohormone for some authors [37] while other ones do not consider it as such since no specific receptors for NO have been identified [21]. The action of NO is mainly mediated with its roles through post-translational modifications, including tyrosine nitration, metal nitrosylation and S-nitrosylation [19][25]. Tyrosine nitration is mediated with the peroxynitrite anion (OONO−), formed from NO and a superoxide radical, while metal nitrosylation is due to the interaction of NO with metalloproteins [19][25]. S-nitrosylation is a redox-based covalent addition of NO to the sulfhydryl group of a cysteine on a target protein and is the most prominent of the post-translational modifications caused with NO [19][25]. It can affect protein activity (activation or inhibition), translocation and protein function [38]. S-nitrosylation is a reversible process, involving nitrosylation, denitrosylation and transnitrosylation. The nitrosylation is considered a non-enzymatic process mediated directly with NO, or indirectly with S-nitrosothiols (e.g., GSNO) or other NO-derived compounds [19][25]. The specificity of the protein S-nitrosylation is mainly determined with the structure of the target protein and the local NO concentration in its vicinity [19]. Denitrosylation is mediated by the thioredoxin system and the transnitrosylation, the transfer of a NO group from one protein to another, is mediated by transnitrosylases, not yet found in plants [19][25].
As previously stated, S-nitrosothiols are NO-derived compounds. Among them, GSNO is the most abundant low-molecular one and is formed non-enzymatically from glutathione (GSH) and NO under aerobic conditions (Refs. [17][18][32][39]. GSH and NO are inter-related since NO can influence GSH synthesis in roots [40]. Since the NO lifetime is relatively short (less than 10 s), GSNO is considered a relatively stable store for NO, being its main reservoir and a vehicle for its long-distance transport [17][18][39][41]. The levels of GSNO can be determined with several methods, including LC-ES/MS, chemiluminescence-based methods and a diamino-rhodamine fluorimetric-based method [15][42]. GSNO is tightly controlled with the GSNO reductase (GSNOR) enzyme, which decomposes it to oxidized glutathione (GSSG) and NH3 (Refs. [41][43][44]). GSNOR is a class III Alcohol Dehydrogenase, which was originally identified as a GSH-dependent Formaldehyde Dehydrogenase [18][43][45][46][47][48]. GSNOR is expressed in both roots and shoots [49]. In Arabidopsis, GSNOR1 is the only gene encoding this enzyme [50]. There are Arabidopsis mutants that present a loss of AtGSNOR1 function, such as the gsnor1-3 mutant, which has higher GSNO contents, and Arabidopsis mutants that overexpress AtGSNOR1, such as the gsnor1-1 mutant, which has lower GSNO contents [19][36][50]. Besides mutants, there are also transgenic lines that overexpress GSNOR, and transgenic lines where GSNOR is blocked by RNAi [51][52][53]. In addition to its decomposition with GSNOR, GSNO can be non-enzymatically decomposed to generate NO and GSSG in the presence of reductants (including GSH and ascorbate) and Cu (Refs. [17][18][32]).
Similarly to NO, GSNO and, consequently, GSNOR have also been involved in the responses of plants to different biotic and abiotic stresses [27][39][43][44][45][48][50][52]. GSNOR activity generally increases under stress conditions [45][48]. Recently, Rudolf et al. [23] proposed that GSNO promotes the methylation of the repressive chromatin mark H3K9, which would impair the expression of stress-responsive genes. According to this proposal, GSNOR, by degrading GSNO, would positively affect the expression of stress-responsive genes [23].

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Subjects: Plant Sciences
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
Francisco Javier Romera
,
María José García
,
Carlos Lucena
,
Macarena Angulo
,
Rafael Pérez-Vicente
View Times: 263
Revisions: 3 times (View History)
Update Date: 21 Aug 2023
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