Nitric Oxide in Plants. Группа авторов

the stomatal closure (Li et al. 2020; Wang et al. 2020; Falak et al. 2021).

Salicylic acid (SA) is another organic plant compound that contributes to the modulation of seed germination, vegetative defense, and response to changing environment. The association between NO and the non-expressors of pathogenesis-related proteins, i.e. NPR1, NPR3, and NPR4 (SA receptor genes), is well recognized for plant defense (Prakash et al. 2021). These NPR proteins regulate various transcription factors (TFs) and endure posttranslational changes (modulated by SA). S-nitrosylation of NPR proteins modifies NO signaling through oligomerization of NPR (Falak et al. 2021; Prakash et al. 2021). NO also controls the expression of NPR1 during plant defense. In Arabidopsis, the SA-dependent defense response has been shown to be triggered by NO. For instance, the application of the NO donor “GSNO” (S-nitrosoglutathione) enhanced the expression of NPR1 and its analogous protein, which subsequently improved the SA content and induced PR genes, conferring resistance against Pseudomonas. Moreover, a rapid change in the levels of glutathione, which is important for the activation of NPR1 and accumulation of SA, has been induced by NO (Fatima et al. 2021; Hediji et al. 2021; Kaur et al. 2021).

      2.4 Role of NO in Metabolic and Developmental Pathways

NO has been shown to play an important role in the modulation of various physiological processes of plants mentioned in Table 2.1. Some of those processes include germination of seed and pollen, plant growth and development, closing and opening of stomata, senescence, flower development, and fruit ripening (Kopyra 2004; Delledonne 2005; Wilson et al. 2008). NO was documented to induce germination in light-dependent Arabidopsis and lettuce seeds, which indicates that NO takes part in root development (Li et al. 2016). Various NO donors stimulated root tip enlargement of Zea mays, in a dosage-related mode, and its length was prohibited by a NO scavenger (methylene blue) (Kopyra 2004). It has been proposed that NO and indole-3-acetic acid share some common steps in cell signaling, as they both stimulate the same plant response. Various studies have been suggested that stress regulates the endogenous levels of indole-3-acetic acid. As well as root growth and development, NO was found to be involved in the development and realignment of pollen tubes, best studied in A. thaliana (Pagnussat et al. 2003, 2004). It has been reported that NO has also been involved in the synthesis of several biological constituents including saponin and phytoalexin (Pagnussat et al. 2003, 2004).

Table 2.1 Role of nitric oxide (NO) during abiotic stress.

Abiotic stress	NO-mediated effect	Plant species	Reference
Drought	Abscisic acid signaling and closure of stomata	Pisum sativum	Syed Nabi et al. 2019
Salt	Increased tolerance of root growth	Oryza sativaNicotiana tabacum	van Zelm et al. 2020
Heavy metals	Heightened response in terms of root growth and oxidative stress	LupinusChlorella vulgaris	Solórzano et al. 2020
Temperature	Release of NO and increased tolerance of seedlings	Oryza sativaNicotiana tabacum	Syed Nabi et al. 2019
Ultraviolet radiation	Nitric oxide synthase activity	Arabidopsis thaliana	Tossi et al. 2009

Plants have established multifaceted innate/induced and hypersensitive mechanisms (HR) to protect themselves from pathogenic microorganisms, which subsequently terminate in systemic acquired resistance (SAR). An initial significant event is the elevation of Ca²⁺by using the plasma membrane cyclic nucleotide-gated ion channels (CNGCs). This is consistent with a role for cyclic guanosine monophosphate (cGMP) in plants, and various putative guanylate cyclase activity proteins including phytosulfokine receptor (PSKR). In PSKR, the cytosolic guanylate cyclase domain is activated by its biologically active ligand, a sulfonated phytosulfokine. An increase in Ca²⁺triggers the creation of SA, NO, and reactive oxygen species (ROS), which stimulates apoptosis in the proximity of the infection, thereby restraining pathogen progression (Heath 2000; Mur et al. 2019; Noman et al. 2020).

      2.5 Role of NO in Overcoming Abiotic Stress

Plants are static creatures confined to the particular place where the seed sprouts. During its life cycle, a plant experiences a diverse and changing environment. With time, plants have established various mechanisms to handle the different kinds of stress environments. Although stresses are numerous, plant’s reactions commonly comprise similar components and signaling pathways. NO is an important constituent in numerous plant acclimation responses to biotic and abiotic strains (Figure 2.2) (Verma et al. 2016; Nowicka et al. 2018; Gong et al. 2020). The response mechanisms for NO signaling are generally similar for all types of stresses. Figure 2.3 contains details of the NO signaling pathway to scavenge ROS during different abiotic stresses.

      Figure 2.2 General role of nitric oxide molecule in plant growth.

      Figure 2.3 Activation of nitric oxide signaling and osmolyte pathways in plant cell under abiotic stress.

      2.5.1 Drought and Low Mineral Nutrient Supply

      During water deficit, plant functioning (plant growth and photosynthesis) is affected adversely. However, through stomatal closure, plants can overcome a temporary drought. But in long-term drought situations, suppressed leaf expansion, leaf excision, and changes in root morphology have been observed. The vulnerability of different plants to water deficiency is largely dependent upon their structural and physiological modifications to water stress (Santisree et al. 2015).

      It has been speculated that slight water deficiencies lead to an increased level of NO production in the roots of cucumber plant. Pretreatment with extrinsic NO, e.g. 100 μM sodium nitroprusside (SNP) and GSNO was capable of neutralizing drought-induced membrane impairment and peroxidation of lipid in water-deficient plants. SNP (200 μM), an NO donor, has also been recognized to employ a shielding effect (improved growth, rise in water content, and less oxidative destruction) in wheat plantlets under polyethylene glycol-induced water stress (Zeppel et al. 2015). The capability of NO to manage drought stress might be linked to its direct effect as an antioxidant, the effects on root physiology, and a role in closure of stomata. In guard cells, NO is involved in the stimulation of intracellular Ca²⁺release, and regulates Ca²⁺-sensitive K⁺ and Cl⁻ channels in the plasma membrane (Simontacchi et al. 2015).

      In agriculture, one limitation is the low accessibility of some essential nutrients, which delivers varied surroundings to the plant. Plants have numerous mechanisms to extract minerals from the soil including major changes in the root growth pattern, the improved ability to obtain nutrients from depleted environments, and also the release of different substances that facilitate nutrient availability in the close proximity of roots, thus favoring their accumulation by roots. Recent study indicates that NO is involved in the modulation of these aforementioned mechanisms (Lambers et al. 2011). For example, in white lupin (Lupinus albus) at low phosphorus levels, the contribution of NO in plant responses has been observed and confirmed. Along with this plant, in other dicots and monocots, phosphorus deficiency mediates root branching followed by the release of exudates, comprising organic acids (Wang et al. 2014), which facilitate plants to increase P acquisition. From this perspective, it has been indicated that white lupin roots exposed to P deficiency exhibited heightened accumulation of NO, which was directly linked to the clustering of roots and increased exudation of citrate compounds. Sequentially, the addition of NO donors (e.g. SNP and GSNO)