Nitric Oxide in Plants. Группа авторов

propagation of cluster roots, whereas NO scavengers (e.g. cPTIO [2-4-carboxyphenyl-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide]) eradicate this progression (Palavan-Unsal and Arisan 2009).

2.5.2 Salinity

      In addition to drought and low mineral content, salinity is one of the most prolonged and unfavorable conditions that has a negative effect on plant health. Significantly, not all plants react in a similar manner to those compounds (lethal osmotic constituents) due to the existence of an array of resistance mechanisms that assist the plant to overcome the stress. These adaptive mechanisms might consist of accumulation of organic components, and the regulation of antioxidant machinery (van Zelm et al. 2020). It has been detected that rice plants exposed to SNP (NO donor) had improved overall growth. This shielding influence exerted by exogenous application of NO was related to the preservation of high relative moisture content and chlorophyll, whereas ionic discharge was sustained at a low level. Likewise, a clear effect on the accumulation of Na⁺ and K⁺ was also witnessed. These results proposed that NO has a protective effect on plants including managing water levels, sustaining ionic balance, and minimizing the damage imposed during early stages of the salinity response (Suzuki et al. 2014; Bashir et al. 2019; Hernández 2019).

      2.5.3 Ultraviolet Radiation

Sunlight is the principal source of energy for plants, and a portion of this energy exists in the form of ultraviolet (UV) radiation. It is typically partitioned into three categories: (i) UV-A (315–400 nm), (ii) UV-B (280–315 nm), and (iii) UV-C (200–280 nm). It is well known that the atmospheric gases completely absorb UV-C radiation, while UV-B rays are moderately absorbed by tropospheric ozone, and only a trivial fraction is transferred to the surface, and UV-A is scarcely absorbed by the ozone. Since the destruction of the ozone layer, the levels of UV-B radiation rise on the Earth’s surface. UV-B has high energy and induces production of ROS that employ harmful morphological and molecular changes in plants (Simontacchi et al. 2015). Chloroplasts are highly affected by UV-B radiation and the light-induced impairment is directed primarily to photosystem II (PSII), with the inhibition of the respiratory chain and oxidative damage to the D1 protein. UV-B treatment increased leakage of ions, hydrogen peroxide levels, and oxidation of thylakoid membrane protein in bean (Phaseolus vulgaris) leaves. It was also observed that the proficiency of PSII photochemistry (F _v/F _m) and the considerable production of PSII was decreased under UV radiation. But after exposure to NO, carbonyl groups of thylakoid membrane and levels of H₂O₂ were decreased. Thus, NO could exert a protective role against protein oxidation under stress conditions as was previously reported regarding lipid oxidation (Vanhaelewyn et al. 2016; Mannucci et al. 2020).

      UV-B adversely affects the chloroplast and mesophyll cells of a plant. It has been reported that UV-B increases the level of plant hormone ABA, activates the NADPH oxidase, and generates H₂O₂. Pretreatment with apocynin (an inhibitor of NADPH oxidase), minimizes the UV-B-induced oxidative damage by reducing the breakdown of chlorophyll (Tewari et al. 2013; Bajguz 2014).

      Ozone is formed by a photochemical reaction in NOx and volatile organic compounds (VOCs) and enters the plants through stomata where it accumulates in parenchyma tissues. As a pollutant, it affects the plant by generating oxidative stress via releasing ROS, e.g. superoxide O²⁻, singlet oxygen, hydroxyl radicals, and hydrogen peroxide in the plant cells. This oxidative stress can further damage the DNA, carbohydrate, lipids, and proteins (Vaultier and Jolivet 2015; Li et al. 2018). The contribution of NO in response to UV-B rays acts through ABA-mediated pathways (Xu et al. 2012). It has been proposed that in plant cells, UV-B radiation stress leads to an increase in ABA levels, which stimulates an increase in cytosolic Ca²⁺ concentration that ultimately starts NO production via NOS and/or NOS-like activities. This increase in NO production increase a plant’s tolerance for higher doses of UV-B indirectly by protecting cell redox homeostasis from uncontrolled generation of ROS and associated deleterious effects provoked by UV-B radiation.

      2.5.4 Heavy Metals

      Present industrial development has been achieved at the cost of the contamination of natural resources. The increasing concentration of heavy metals (HMs) in the environment has led to stress and toxicity for the biotic component of the ecosystem (plant, animals, and microorganisms) (Delledonne 2005). In the rhizosphere, heavy metal concentration changes the plant physiology, morphology, and cellular and biochemical functions, thus creating negative impacts on plant growth, cell division, differentiation, reproduction, photosynthesis, and antioxidant activities (Sharma and Dietz 2009).

The mechanisms of toxicity are composed of functional groups that block essential molecules, e.g. enzymes, nutrient/ion transport, polynucleotides, displacement/replacement of ions from cells, disruption of cell and organelle membrane integrity, denaturation, and inactivation of enzymes (Hall 2002). How the heavy metals affect plants and how plants tolerate these stresses are still under research (Brouquisse 2019; Syed Nabi et al. 2019). However, many research studies have validated the role of NO in relieving heavy metal stress (Solórzano et al. 2020) either produced endogenously or applied exogenously. NO can ameliorate the toxicity of heavy metal in two possible ways: (i) scavenging the ROS overproduction directly in the cell by increasing enzymatic and nonenzymatic antioxidants; or (ii) acting as a signaling molecule to modify the antioxidative expression of the gene (Verma et al. 2013; Zhao et al. 2016). Furthermore, it might change root cell wall components, which leads to increased heavy metal accumulation in plant roots, with heavy metal levels consequently decreased in aerial parts.

      ROS consist of superoxide anions, H₂O₂, hydroxyl free radicals, and oxygen-free species (Singh et al. 2016), which are formed in various organelles (mitochondria and chloroplasts) of cells (Singh et al. 2016). Hydrogen peroxide can produce hydroxyl free radicals and oxygen-free species by Harber Weiss and Fenton reactions under heavy metals like Cu⁺ and Fe²⁺ (redox-active metals) thus causing oxidative strain in the plant.

      This oxidative stress can be ameliorated by enzymatic antioxidants, i.e. catalase (CAT), superoxide dismutase (SOD), glutathione peroxidase (GPX), and ascorbate peroxidase (APX), and nonenzymatic antioxidants like ascorbic acid (AsA), glutathione (GSH), phenolic compounds, tocopherols, and other nonprotein amino acids that are capable of scavenging ROS (Zhao et al. 2016). Studies have revealed that endogenous and exogenous sources of NO can activate the production of antioxidant species both by enzymatic and nonenzymatic pathways. Different types of strategies are related to the presence of NO in the plants, e.g. protection of phospholipid bilayers, cell wall relaxation, and whole growth of plants. The main role in the maintenance of osmotic pressure, the viscosity of cytoplasm, and the protection of chloroplast membranes as well as chlorophyll pigment under heavy metal stress is played by NO (Ahmad et al. 2018; Syed Nabi et al. 2019). Induction of metallochaperones (genes in the heavy metal-associated domain) by NO has been shown to result in the site-specific and safe transport of metallic ions within the cell. Fourteen new heavy metal-associated domains have been discovered. Genes in these domains have shown distinct expression of NO donor S-nitroso-l-cysteine (CySNO) in RNA sequence-based transcriptomic studies (Imran et al. 2016; Syed Nabi et al. 2019).

      Endogenous concentration of NO in a plant varies under stress depending upon factors like type of metal, plant species, specific type of tissue/organ exposed to heavy metals, exposure duration, and method of quantification of NO (Syed Nabi et al. 2019). In Arabidopsis, lead (Pb) stress leads to the overproduction of endogenous NO, which starts a chain of different catalytic reactions in peroxisomes that cause lateral root enlargement (Chen et al. 2016). Heavy metals can increase or decrease endogenous NO, e.g.in Arabidopsis exogenous melatonin reduced the Al-induced NO production, hence hindering root elongation and arresting the cell cycle (Zhang et al. 2019). However, in the case of soya bean exposure to Cd for 72 h, increased production of endogenous NO has been detected (Kopyra et al. 2006).

Both endogenous and exogenous NO application have lessened heavy metal stress in different plants including rice, wheat, pea, and many others (Bartha-Dima et al. 2005; Singh et al. 2008; Xiong et al. 2009; Zhao et al. 2016). Exogenous NO increases