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REVIEW
Role of Nitric Oxide in Mitigating Cadmium Stress in Plants: Mechanisms and Perspectives
1 College of Environment and Surveying and Mapping Engineering, Suzhou University, Suzhou, Anhui, China
2 Key Laboratory of Environmental Processes and Pollution Control in Tuohe River Basin, Suzhou, Anhui, China
* Corresponding Author: Haiyang Zhang. Email:
(This article belongs to the Special Issue: Regulators of Plant Growth and Environmental Stress Adaptation)
Phyton-International Journal of Experimental Botany 2026, 95(6), 1 https://doi.org/10.32604/phyton.2026.082409
Received 16 March 2026; Accepted 15 May 2026; Issue published 29 June 2026
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Cadmium (Cd) is a toxic heavy metal pollutant released from various human activities including industrial production and agricultural practices. This pollutant adversely affects plant physiology by damaging root systems, inhibiting photosynthesis, and inducing oxidative stress through the accumulation of reactive oxygen species (ROS). This review highlights the critical role of nitric oxide (NO) as a key signaling molecule that enhances plant tolerance to cadmium stress. The application of exogenous NO effectively alleviates Cd toxicity by stimulating the activity of antioxidant enzymes such as superoxide dismutase (SOD) and catalase (CAT), scavenging harmful ROS, and preventing membrane damage. Furthermore, NO improves nutrient absorption and photosynthetic efficiency under Cd stress. The review also explores the complex interactions between NO and other phytohormones, including auxin and brassinosteroids, especially in regulating root development under stressful conditions. Despite these protective effects, the review concludes that further investigations are needed to better understand the molecular mechanisms of NO signaling, its concentration-dependent responses, and its specific crosstalk with other plant signaling molecules.Keywords
Cadmium (Cd) is one of the main heavy metals that adversely affects various physiobiochemical processes of plants, including metabolism, the photosynthetic apparatus, and the antioxidant defense system, leading to a decrease in crop yield and quality [1]. Plants initiate defense strategies at the physiological, cellular, and molecular levels by controlling the cellular level of toxic ions through various pathways, including vacuolar compartmentalization, chelation with thiol-peptides, immobilization, and elimination, or by transducing stress signals to activate defense responses [2]. In recent decades, several methods have been pursued to reduce Cd toxicity, such as the use of nutrients, hormones, and biological purification, which can significantly reduce the harmful effects of Cd stress on plant physiological processes [3]. However, one of the possible strategies to increase plant adaptation to Cd-contaminated environments is the use of signaling molecules such as nitric oxide (NO) [4].
NO is a gaseous signaling molecule that is synthesized through enzymatic and non-enzymatic pathways and is widely distributed in plants, playing a role in a wide range of physiological and biochemical processes such as seed germination, regulation of normal growth and development, hormonal regulation, closure of plant stomata, maturation and senescence, and programmed cell death [3,5]. Furthermore, NO plays a crucial role in increasing plant tolerance to abiotic stresses such as drought, ultraviolet-B radiation, cold, nutrient deficiencies, salt, and heavy metal toxicity [6,7]. Evidence suggests that the exogenous application of NO alleviates oxidative stress caused by Cd stress and improves plant resistance [8,9]. Previous studies have demonstrated that the balance between NO and reactive oxygen species (ROS) is essential for plant tolerance to Cd stress, and since ROS is highly reactive, it can damage the function and structure of cells in the absence of protective mechanisms [2,8]. Moreover, ROS and NO levels in cells may cause oxidative/nitrosative stress or act as signaling molecules [10]. However, excessive intracellular ROS is scavenged through the upregulation of antioxidant enzymes and non-enzymatic antioxidants, a process that can be mediated by NO [8,11].
Literature searches were conducted using the Web of Science, Scopus, PubMed, and Google Scholar. Combinations of the following keywords were used: “nitric oxide”, “NO”, “cadmium”, “Cd stress”, “heavy metal toxicity”, and “antioxidant enzymes”. The search was limited to peer-reviewed articles published in English between 2010 and 2025. Relevant papers were selected based on their focus on the role of nitric oxide in alleviating cadmium toxicity in plants.
Despite the growing number of studies on this topic, several critical aspects remain poorly understood. The molecular mechanisms by which NO alleviates Cd toxicity, especially its concentration-dependent effects and its contrasting role under short-term versus long-term Cd exposure, are not yet clearly elucidated. Furthermore, the complex crosstalk between NO and other phytohormones under Cd stress requires deeper investigation. The present review critically examines the current literature, identifies these key knowledge gaps, and highlights important directions for future research.
2 Cadmium as a Hazardous Element
Cadmium (Cd) is one of the most toxic heavy metals and a widespread environmental pollutant. It causes detrimental effects on humans, animals, and plants [8,12,13]. Cd concentration in soil is increasing alarmingly, and research shows that approximately 5.6–38 thousand tons of Cd enter the soil globally each year, thus making it a serious environmental problem [14,15]. A rising level of Cd contamination is observed in many agricultural regions in Asia, North America, and Europe [14,16]. Cd is highly bioavailable and persistent in the environment, with a biological half-life of more than 20 years in humans. Due to its high solubility and mobility, it readily accumulates in living tissues and enters the food chain [16,17]. The World Health Organization (WHO) has listed cadmium as one of the ten chemicals of major public health concern [18]. The WHO has suggested an average monthly Cd tolerance of 25 mg/kg body weight, and Codex Alimentarius Commission (CAC) has narrowed the maximum permissible Cd level in cereal grains to 0.1 mg/g [14]. Cd is a highly carcinogenic substance that causes diseases including Itai-itai, kidney damage, cardiovascular problems, and immune disorders [9,19]. Geological processes (weathering of rocks, and volcanic activity), and human processes (application of phosphate fertilizers, cement production, fossil fuels, electroplating, metal smelting, mining, sewage sludge, municipal waste, wastewater irrigation, and leather tanning) increase Cd levels in various ecosystems [1,20,21].
In soil, Cd primarily exists as Cd2+. Elevated Cd levels disrupt the balance of macro- and micronutrients and adversely affect beneficial soil microorganisms, including nitrogen-fixing bacteri [2,22,23,24]. The low levels of Cd in the soil are also absorbed by the plant roots and then, after being loaded into the xylem, rapidly transported to the aerial organs and then to the phloem and seeds [25]. Cd enters root cells through essential nutrient transporters including ZIP, IRT, and Nramp, along with aquaporins, natural resistance-associated macrophage protein (NRAMP1), and heavy metal ATPase 3 (HMA3) [26,27,28]. Cd accumulation in plants causes disruption in the morphological, physiological, metabolic, molecular, and biochemical processes in plants [29]. Cd reduces water and nutrient absorption, cell elongation, transpiration, root growth, seed germination, respiration, and yield in plants [30,31]. In addition, Cd disrupts sugar metabolism, enzyme activity, and stomatal function [32] (Fig. 1).
Cd disrupts photosynthesis efficiency through chlorosis and necrosis of leaves, damage to the thylakoid membrane in chloroplasts, reduction of photosynthetic pigments, and changes in the configuration and structural stability of pigment-protein complexes [33,34,35]. Cd also inhibits chlorophyll biosynthesis through upregulation of chlorophyllase and replacement of Mg2+ with Cd2+ ions [36]. Furthermore, Cd can replace Ca2+ in the photosystem II (PSII) reaction center, inhibiting PSII light response activity, and decreasing photosynthetic efficiency [37]. Moreover, cadmium can reduce NADPH production in cells and disrupt the electron transport chain (ETC) from PSII to photosystem I (PSI) in chloroplasts, and from complex I to IV in mitochondria [38,39]. Cd stress in plants increases NADPH oxidase activity, which produces reactive oxygen species (ROS) such as hydrogen peroxide (H2O2), superoxide radicals (O2•−), and hydroxyl radicals (•OH) [40,41]. Oxidative stress in plants causes disruption of cellular redox homeostasis, cell membrane leakage, phospholipid degradation, enzyme inactivation, and an increase in malondialdehyde (MDA) content [4,42,43]. Plants naturally use various strategies to combat Cd toxicity, including Cd removal, limiting Cd influx, and chelation (by organic molecules such as metallothioneins, phytochelatins, and histidines) [7]. Furthermore, the root cell wall, as the main binding site for Cd in plants, plays a crucial role in Cd deposition, and reducing its toxicity in plants [44,45]. Plants can also complex Cd through various metal ligands or sequester Cd into vesicles to mitigate its harmful effects [46]. Further, plants can eliminate the toxic effects of oxidative stress by increasing the synthesis of enzymatic and non-enzymatic antioxidants [ascorbate peroxidase (APX), superoxide dismutase (SOD), catalase (CAT), glutathione reductase (GR), glutathione (GSH), and ascorbate (AsA)], nutrient homeostasis, and the production of osmolytes such as proline [4,47,48] (Fig. 1).
Figure 1: Cadmium uptake, transport, accumulation, and toxicity in plants. Cadmium is taken up by roots from the soil, where its absorption is influenced by soil factors such as pH, organic matter, root exudates, and micronutrients. Once absorbed, Cd is translocated upward through the xylem to the shoots and leaves, and further distributed to seeds via the phloem. The figure highlights the negative impacts of Cd toxicity on plant growth and development, seed germination, water relations, crop yield and quality, reactive oxygen species (ROS) production, nutrient uptake, lipids, and amino acids.
NO is a small gaseous molecule with a short half-life that plays a crucial role in plant signaling [2,49]. NO, which is part of the nitrogen cycle in plants, plays a widespread function in increasing growth and in the activity of defense mechanisms under abiotic stress conditions (heavy metals, ozone, salinity, and ultraviolet radiation) [32,50,51]. NO, which is soluble in water and fat, can diffuse intracellularly and modulate its capacity directly through post-translational modifications (PTMs) of proteins or interaction with other signaling molecules [5,52,53]. NO is produced as an intracellular and intercellular signaling molecule through various pathways, including non-enzymatic, reductive, and oxidative reactions [54,55]. Nitrate reductase (NR) is one of the key enzymes for NO synthesis/accumulation in various organelles such as the cytoplasm, cytosol, peroxisomes, chloroplasts, and mitochondria [56,57,58]. NR uses NADH/NADPH as an electron donor to catalyze nitrate and nitrite reduction into NO, and is considered the main source of NO [56]. Additionally, in higher plants, NR activity is dependent on PTMs of proteins, such as redox and phosphorylation, which affect NO production [44,59]. Other enzymes are also involved in NO production, including copper amine oxidase (CuAO), polyamine oxidase (PAO), pyrroline-5-carboxylate reductase (POR), cytochrome P450 (CYP), xanthine dehydrogenase (XDH), and xanthine oxidoreductase (XOR) [5]. Furthermore, under low oxygen conditions, several molybdoenzymes can oxidize nitrite to NO, including sulfite oxidase (SO), aldehyde oxidases (AOs), and xanthine oxidase (XO) [60] (Fig. 2).
Figure 2: A diagram shows the major routes for the synthesis of nitric oxide (NO). Nomenclature is as proposed by Lau, et al. [61]. In the oxidative pathway (left), NO is synthesized from L-arginine by a NOS-like enzyme in the presence of Ca2+, calmodulin, NADPH, FMN, and FAD. Additional contributions come from polyamine and hydroxylamine oxidation. In the reductive pathway (right), NO is produced from nitrate (NO3−) and nitrite (NO2−) through the activity of nitrate reductase (NR) and several nitrite: NO reductases, including cytosolic NR, PM-NiNOR, Mt-NiNOR, and xanthine oxidoreductase (XOR), particularly under acidic and hypoxic conditions. This diagram highlights the dual enzymatic routes that maintain NO levels in plant cells.
NO, along with S-nitrosoglutathione (GSNO), dinitrogen trioxide (N2O3), and peroxynitrite (NO3−), are known as reactive nitrogen species (RNS) in plants, and are produced in large quantities when plants are exposed to adverse stresses [62,63]. It has been shown that different types of RNS affect each other, for example, NO3− synthesis causes a decrease in cellular NO levels [64]. Evidence suggests that low levels of RNS are not toxic to plant cells, however excessive nitrosylation caused by RNS can damage carbohydrates, proteins, membrane lipids, and DNA, affecting cellular function [65,66]. The researchers stated that NO readily interacts with a wide range of biological molecules such as lipids, proteins, and nucleic acids in plant cells and modulates their activity [2,67]. In addition, NO can limit ROS toxicity and levels by regulating plant antioxidant defenses [68]. Studies have also shown that there is a signalling topology between H2O2 and NO [69]. NO mitigates oxidative stress by modulating the activity of antioxidant enzymes such as catalase (CAT), ascorbate peroxidase (APX), and superoxide dismutase (SOD), thereby regulating H2O2 levels. Additionally, NO can directly react with superoxide radicals (O2•−) to form peroxynitrite (ONOO−), which influences cellular redox signaling [70,71]. Furthermore, NO has direct chemical interactions with O2•− in one of the fastest reactions in biological systems, ultimately forming NO3− [2,72]. NO prevents ROS carbonylation of thiol proteins, as well as improving membrane peroxidation and reducing ion leakage [73,74]. NO has a significant effect on many metabolic and physio-biochemical processes in plants, including photosynthesis, seed germination, flowering, growth of pollen tubes, stomatal closure, regulation of auxin transport, root formation, and regulating element absorption (iron and sulfur) [4,32,48,75,76]. NO also plays a role in fruit development and fruit quality characteristics including texture, color, flavor, and nutritional content [50,77].
The results of findings indicate that Cd increases endogenous NO levels [78,79]. In a study conducted on peas and mustard treated with 100 M Cd for one day, endogenous NO production in the roots increased significantly [80]. Although the role of NO in the response and protection of plants against Cd stress has been elucidated, nevertheless, the metabolic and molecular mechanisms of NO-induced Cd stress reduction and the precise mechanisms of NO signaling remain to be clarified [2,81,82]. However, changes in endogenous NO levels in plants under Cd stress are influenced by various factors such as plant genotype and species, plant size, Cd concentration, and treatment time [5]. On the other hand, some studies also indicate that Cd stress inhibits endogenous NO production in plants [78]. As an example, a study on alfalfa showed that treating seedlings with 50 M Cd for two days significantly reduced NO levels in roots, as well as in peas treated with Cd for 14 days, NO levels in roots and leaves were decreased [83]. Several authors have reported that although short-term stress may increase NO production levels, long-term stress decreases NO levels [84]. Some studies have suggested that the reduction of NO in plants may be due to calcium (Ca) deficiency caused by Cd stress in the leaves, which leads to a reduction in enzyme activity, such as nitric oxide synthase (NOS) [85]. During recent decades, numerous studies have reported the role of exogenous NO application as an efficient method of increasing plant resistance to Cd stress [9,86]. One of the most widely used methods to improve plant resistance in Cd-contaminated environments is the foliar application of sodium nitroprusside (SNP), which is a NO donor [87,88]. The effect of SNP application on increasing various plants’ resistance to Cd stress has been reported, such as perennial ryegrass, peanuts, wheat, Medicago truncatula, and rice [32].
4.1 NO’s Role in Cd Toxicity, Absorption, and Transport in Plants
Various studies have shown that exogenous NO affects Cd uptake by plants but also its stabilization within cell walls, thereby improving plants’ resistance to Cd stress [5,22,89]. When applied exogenously, NO acts as a cell membrane regulator and protector of plant cells under Cd stress [22]. Furthermore, NO, due to its significant role in the lignification of plant cell walls, regulates Cd uptake by plants and increases their resistance to stress [90,91]. Additionally, exogenous NO, by affecting the composition of root cell wall components, in addition to inducing Cd fixation and removal in the roots, regulates Cd distribution in plants and prevents its transfer to aerial organs [12,45]. Pectin, cellulose, and hemicellulose are the main components of the cell wall, and research has also shown that adding NO increases the content of these cell wall components, leading to increased Cd deposition in root cell walls [92,93]. In a study conducted on Panax notoginseng under Cd stress, it was shown that the use of Sodium Nitroprusside (SNP) as a NO donor caused a significant increase (about 2.9-fold) in Cd accumulation in root cell walls by increasing the synthesis of pectin and hemicellulose 1, and pectin methylesterase activity [45]. NO, as a gaseous signaling molecule, can regulate the expression of Cd-related genes, by enhancing the signaling cascade, thereby increasing plant resistance to Cd stress [94]. It is well documented that NO can increase cytoplasmic Ca2+ concentration by regulating transporter proteins, Ca2+ channels, and some protein kinases, as well as activate some other secondary signaling factors such as cyclic adenosine diphosphate ribose (cADPR) and cyclic guanosine monophosphate (cGMP), thereby enhancing the signaling cascade [95]. Research has also shown that exogenous NO elevates metallothioneins (MTs), which are cysteine-rich metal-binding proteins [96]. MTs bind to Cd through sulfhydryl groups and prevent Cd toxicity to plant cells by forming less toxic or non-toxic complexes [5,97] (Table 1).
On the other hand, studies have shown that endogenous NO accumulation caused by Cd stress can increase Cd toxicity to plants through the following factors [5]. Excessive production of endogenous NO stimulates genes related to iron absorption (FRO2, IRT1, and FIT) and leads to enhanced uptake and accumulation of Cd by plants [7,98]. In addition, Cd-induced endogenous NO through s-nitrosylation can bind to phytochelatins (PCs) (which chelate and sequester Cd within vesicles), thereby reducing their detoxifying effect on Cd [87,99,100]. Excess endogenous NO also binds to metal ions, tyrosine residues, and proteins containing cysteine residues (sulfhydryl groups) via S-nitrosylation, weakening their detoxifying effect on cadmium [5,101]. Furthermore, NO contributes to Cd toxicity to plants by increasing the activities of apoptosis-related enzymes such as caspase-3 [102,103]. In a study on Arabidopsis, it was shown that the application of gibberellin (GA) also reduces Cd toxicity and absorption through the expression of the IRT1 gene and mediating NO accumulation [104] (Table 1).
4.2 Involvement of NO in Cd-Stressed Plant Growth
Recent findings indicate that NO improves the carotenoids and chlorophyll content in plants under Cd stress [22]. Furthermore, NO spraying under Cd stress conditions, besides preserving the chloroplast structure, maintains the function and integrity of stomatal components and enhances gas exchange [4,105]. NO can also accept electrons from the electron transport chain in addition to reducing Cd toxicity by improving the function of PSII [106,107]. Therefore, NO improves plant growth by increasing photosynthesis indices in plants under Cd toxicity [22,108]. Moreover, numerous studies have shown that exogenous NO application can improve plant growth and biomass by increasing physiological functions, antioxidant enzyme activity, nutrient absorption, and cell expansion, as well as reducing Cd accumulation in various plant organs and membrane ion leakage [3,109,110] (Table 1).
Cd stress, in addition to reducing NO levels in lateral roots (LRs) and adventitious roots (ARs), suppresses auxin transport and biosynthesis, reduces primary roots (PRs) length, and inhibits the quiescent center’s (QC) function, ultimately leading to abnormal cell proliferation and root morphological abnormalities [2,78,111]. Additionally, Evidence suggests that NO modulates auxin (IAA, and IBA) levels under normal and Cd stress conditions by increasing the expression of the AUXIN-RESISTANT 1 (AUX1) gene, as well as affecting signaling, distribution, conjugation, degradation, and biosynthesis [97,112]. Thus, exogenous NO application reduces Cd effects on the root system and promotes AR, LR, and PR growth and development [78,113]. On the other hand, some studies show that NO accumulation caused by Cd stress in roots suppresses auxin levels and transport, inhibiting root growth [114,115]. The results of the research showed that high levels of NO have an adverse effect on auxin accumulation and root length, while low levels of NO lead to increased root length under Cd stress conditions [113]. It has been shown that brassinosteroids (BRs) play a positive role in exopetal auxin transport, interaction with auxin signaling, and control of QC cell identity [116,117]. Research has also shown that exogenous BR application induces endogenous NO production whilst enhancing AR formation [118]. Furthermore, BRs do not cause any changes in NO signaling in the presence of Cd exposure, suggesting that synergy between exogenous BR and NO does not occur in the presence of Cd [78]. However, using lower levels of BRs neutralized the negative effects of cadmium on the apical structure and greatly increased the formation of AR and LR, confirming the significant protective role of BRs in the root system [78] (Table 1).
4.3 NO Improves Antioxidant Activity in Plants under Cd Stress
Plant cells produce ROS during their normal growth to participate in various physiological and metabolic activities such as respiration and photosynthesis [119]. However, environmental stresses such as Cd stress cause excess ROS production in plant cells, leading to oxidative stresses such as protein denaturation, DNA damage, hydrogen peroxide (H2O2) accumulation, and membrane lipid peroxidation [86,120]. NO enhances plant tolerance to Cd stress by alleviating oxidative damage through several mechanisms: (1) increasing antioxidant defense capacity, (2) regulation of peroxisomal proteins, (3) preservation of ultrastructural configuration and chloroplast membranes, (4) direct reaction with superoxide anion (O2−•) to form peroxynitrite, and (5) formation of peroxynitrite, which is less toxic than ROS [4,121,122] (Table 1; Fig. 3).
Table 1: Effect of exogenous nitric oxide on alleviation of cadmium toxicity in different plant species.
| Plant Type | NO Dose | Cd Dose | Experiment Results and Observations | References | |
|---|---|---|---|---|---|
| 1 | Arundinaria pygmaea | 200 μM | 200 μM | Increased antioxidant activity | [22] |
| Increased protein content | |||||
| Increased photosynthetic properties | |||||
| Increased plant growth and plant biomass | |||||
| Limiting Cd movement from roots to shoots | |||||
| 2 | Oryza sativa L. | 50 and 100 μM | 100 μM | Reducing root system changes caused by Cd | [2] |
| Reduced Cd absorption | |||||
| Reducing ROS levels | |||||
| 3 | Festuca arundinacea Schreb | 100 and 200 μM | 50 mg/L | Increased antioxidant capacity | [81] |
| Accumulation of secondary metabolites related to Cd chelation and sequestration | |||||
| Activity of ABC transporters | |||||
| Increased nitrogen metabolism | |||||
| Expression of genes encoding CAT, GLT1, GSTs and ADH1 | |||||
| Reduced isotrifolin and acastin content | |||||
| 4 | Arachis hypogaea L. | 250 μM | 5 and 200 μM | Improve plant growth | [32] |
| Improve chlorophyll content | |||||
| Regulation of the antioxidant system | |||||
| Reducing the rate of superoxide radical production | |||||
| Reducing malondialdehyde content | |||||
| 5 | rice | 50 μM | 50 μM | Suppression of Cd absorption | [8] |
| Increases antioxidant levels | |||||
| Reduce oxidative stress | |||||
| Improving growth | |||||
| 6 | Satureja Hortensis L. | 0, 75, 100 and 150 μM | 0, 50, 100 and 200 μM | Improve plant growth | [3] |
| Increased proline | |||||
| Increased chlorophyll (a, b and carotenoids) | |||||
| Increased carbohydrates | |||||
| Increased peroxidase activity | |||||
| Reducing Cd accumulation in shoots and roots | |||||
| 7 | Aromatic Rice | 50 or 100 μM | 0 and 50 mg·kg−1 of soil | Reduce oxidative stress | [4] |
| Improving the photosynthetic apparatus | |||||
| Reducing Cd concentration in leaves and seeds | |||||
| Increase grain yield | |||||
| Improving 2-Acetyl-1-pyrroline (2AP) content |
Existing studies have shown that Cd stress causes a decrease in endogenous NO content in plants, which can be enhanced through the exogenous application of NO compounds such as SNP [123]. Several Current literature shows that SNP application increases the antioxidant capacity (GST, APX, GR, POD, CAT, and SOD) in yellow lupine, clover, lobelia, and sunflower under Cd stress and leads to the removal of ROS compounds in various plant organs [5,85,89,124,125]. On the other hand, exogenous NO increases the activity of the AsA-GSH cycle and consequently reduces the levels of EL, MDA, and H2O2 in plants under Cd stress [4,126,127]. Since GSH is a precursor of phytochelatins (PCs), and NO can enhance the expression of glycosyl hydrolases (GHs) and gamma-glutamylcysteine synthetase (γ-ECS) genes, it can be assumed that NO may increase PC synthesis [5]. NO can also react with GSH to produce GSNO, which serves as the main internal stored form of NO and mediates protein nitrosylation modification [128]. Furthermore, NO can scavenge Cd-induced ROS directly without crossing through the antioxidant system and reduce oxidative damage [5]. SNP also increases nitrate reductase activity and proline content (by regulating P5CS1, which encodes 1-pyrroline 5-carboxylate synthetase) in plants under Cd stress [129,130]. In general, it is well documented that exogenous NO application significantly reduces Cd-induced MDA and H2O2 accumulation and limits lipid peroxidation, possibly due to improved antioxidant activities, reduced ROS production, and increased membrane stability [3,4,131] (Table 1; Fig. 3).
Figure 3: In plants, nitric oxide (NO)-regulates the response to cadmium stress. Nomenclature is as proposed by Zhu, Ai, Hu, Du, Sun, Chen and Chen [81]. Under Cd stress, NO regulates the expression of various genes and accumulation of metabolites involved in different defense pathways. These include genes and metabolites associated with flavonoid and flavonol biosynthesis (CYP75A, isorifolin, acacetin), ABC transporters (ABCB1, ABCC10), nitrogen metabolism (nR, GLT, nirA, NRT, L-asparagine), antioxidant defense (CAT, GLT1, GSTs, ADH1), and phenylpropanoid biosynthesis (POD, CCR, CYP73A, CYP84A, trans-cinnamic acid). This diagram summarizes the key molecular mechanisms by which NO alleviates Cd toxicity in plants.
4.4 Molecular Mechanisms of NO-Mediated Cd Tolerance
Nitric oxide mediates cadmium tolerance primarily through S-nitrosylation, a reversible post-translational modification that directly alters the function of target proteins [132]. This modification regulates key antioxidant enzymes such as SOD, CAT, and APX, enhancing their activity and improving ROS scavenging capacity [133]. Additionally, S-nitrosylation modulates metal transporters including IRT1 and HMA3, thereby reducing cadmium uptake and root-to-shoot translocation [133]. NO also upregulates the expression of genes involved in glutathione and phytochelatin biosynthesis (GSH1, GSH2, and PCS1), which increases the plant’s capacity for Cd chelation and vacuolar sequestration [134,135]. Furthermore, NO interacts with calcium signaling pathways by activating Ca2+-dependent protein kinases (CDPKs) and cyclic GMP (cGMP), forming a complex signaling cascade that coordinates stress responses [136]. These molecular events collectively enable NO to maintain cellular redox homeostasis, protect photosynthetic apparatus, and promote root system remodeling under Cd stress [137]. Despite these advances, the specific S-nitrosylated target proteins and the complete downstream signaling networks vary among plant species and remain to be fully characterized through proteomic and transcriptomic studies [138].
This review indicates that nitric oxide (NO) plays a vital role as a signalling molecule in mitigating Cd-induced toxicity in plants. Exogenous NO application can effectively reduce Cd uptake and translocation, enhance antioxidant defense systems, improve photosynthetic efficiency, and promote plant growth under Cd stress. Most studies report NO’s beneficial effects without sufficiently addressing its concentration-dependent responses or the differences between short-term and long-term Cd stress. While low NO concentrations enhance plant tolerance, high concentrations may disrupt auxin signaling or exacerbate stress. Additionally, endogenous NO levels tend to increase during acute exposure but decline under prolonged Cd stress, suggesting a complex temporal regulation that remains poorly understood.
Future research should prioritize systematic dose-response experiments across a wide range of NO concentrations and conduct time-course studies comparing short-term versus chronic cadmium exposure. A deeper understanding of the molecular mechanisms underlying NO signaling and its crosstalk with other phytohormones under varying stress durations is also essential.
Acknowledgement:
Funding Statement: This work was supported by Tuohe River Basin Environmental Processes and Pollution Control Key Laboratory of Suzhou City (2024KYPT03); Cross-Fusion and Demand Orientation: Construction and Practice of a Geoscience-Environment-Surveying Discipline Cluster under the Guidance of the Master’s Program in Resources and Environment (szxy2026jyjf67).
Author Contributions: Mohammad Reza Boorboori wrote, and Haiyang Zhang edited the manuscript. All authors reviewed and approved the final version of the manuscript.
Availability of Data and Materials: Not applicable.
Ethics Approval: Not applicable.
Conflicts of Interest: The authors declare no conflict of interest.
References
1. El Rasafi T , Oukarroum A , Haddioui A , Song H , Kwon EE , Bolan N , et al. Cadmium stress in plants: A critical review of the effects, mechanisms, and tolerance strategies. Crit Rev Environ Sci Technol. 2022; 52( 5): 675– 726. doi:10.1080/10643389.2020.1835435. [Google Scholar] [CrossRef]
2. Piacentini D , Ronzan M , Fattorini L , Della Rovere F , Massimi L , Altamura M , et al. Nitric oxide alleviates cadmium-but not arsenic-induced damages in rice roots. Plant Physiol Biochem. 2020; 151: 729– 42. doi:10.1016/j.plaphy.2020.04.004. [Google Scholar] [CrossRef]
3. Azizi I , Esmaielpour B , Fatemi H . Exogenous nitric oxide on morphological, biochemical and antioxidant enzyme activity on savory (Satureja hortensis L.) plants under cadmium stress. J Saudi Soc Agric Sci. 2021; 20( 6): 417– 23. doi:10.1016/j.jssas.2021.05.003. [Google Scholar] [CrossRef]
4. Imran M , Hussain S , Rana MS , Iqbal A , Rehman NU , Chen X , et al. Exogenously applied sodium nitroprusside alleviated cadmium toxicity in different aromatic rice cultivars by improving nitric oxide accumulation and modulating oxidative metabolism. Agronomy. 2024; 14( 8): 1857. doi:10.3390/agronomy14081857. [Google Scholar] [CrossRef]
5. Meng Y , Jing H , Huang J , Shen R , Zhu X . The role of nitric oxide signaling in plant responses to cadmium stress. Int J Mol Sci. 2022; 23( 13): 6901. doi:10.3390/ijms23136901. [Google Scholar] [CrossRef]
6. Nahar K , Hasanuzzaman M , Alam MM , Rahman A , Suzuki T , Fujita M . Polyamine and nitric oxide crosstalk: Antagonistic effects on cadmium toxicity in mung bean plants through upregulating the metal detoxification, antioxidant defense and methylglyoxal detoxification systems. Ecotoxicol Environ Saf. 2016; 126: 245– 55. doi:10.1016/j.ecoenv.2015.12.026. [Google Scholar] [CrossRef]
7. Wu Q , Zhu X , Zhao X , Shen R . Potassium affects cadmium resistance in Arabidopsis through facilitating root cell wall Cd retention in a nitric oxide dependent manner. Environ Exp Bot. 2020; 178: 104175. doi:10.1016/j.envexpbot.2020.104175. [Google Scholar] [CrossRef]
8. Singh P , Singh I , Shah K . Alterations in antioxidative machinery and growth parameters upon application of nitric oxide donor that reduces detrimental effects of cadmium in rice seedlings with increasing days of growth. S Afr J Bot. 2020; 131: 283– 94. doi:10.1016/j.sajb.2020.02.022. [Google Scholar] [CrossRef]
9. Wang T , Song J , Liu Z , Liu Z , Cui J . Melatonin alleviates cadmium toxicity by reducing nitric oxide accumulation and IRT1 expression in Chinese cabbage seedlings. Environ Sci Pollut Res. 2021; 28: 15394– 405. doi:10.1007/s11356-020-11689-w. [Google Scholar] [CrossRef]
10. Farnese FS , Menezes-Silva PE , Gusman GS , Oliveira JA . When bad guys become good ones: The key role of reactive oxygen species and nitric oxide in the plant responses to abiotic stress. Front Plant Sci. 2016; 7: 471. doi:10.3389/fpls.2016.00471. [Google Scholar] [CrossRef]
11. Chen J , Liu X , Wang C , Yin SS , Li XL , Hu WJ , et al. Nitric oxide ameliorates zinc oxide nanoparticles-induced phytotoxicity in rice seedlings. J Hazard Mater. 2015; 297: 173– 82. doi:10.1016/j.jhazmat.2015.04.077. [Google Scholar] [CrossRef]
12. Nabaei M , Amooaghaie R . Melatonin and nitric oxide enhance cadmium tolerance and phytoremediation efficiency in Catharanthus roseus (L.) G. Don. Environ Sci Pollut Res. 2020; 27( 7): 6981– 94. doi:10.1007/s11356-019-07283-4. [Google Scholar] [CrossRef]
13. Mishra S , Bharagava RN , More N , Yadav A , Zainith S , Mani S , et al. Heavy metal contamination: An alarming threat to environment and human health. In: Environmental biotechnology: For sustainable future. Singapore: Springer; 2018. p. 103– 25. doi:10.1007/978-981-10-7284-0_5. [Google Scholar] [CrossRef]
14. Qiu CW , Zhang C , Wang NH , Mao W , Wu F . Strigolactone GR24 improves cadmium tolerance by regulating cadmium uptake, nitric oxide signaling and antioxidant metabolism in barley (Hordeum vulgare L.). Environ Pollut. 2021; 273: 116486. doi:10.1016/j.envpol.2021.116486. [Google Scholar] [CrossRef]
15. Han Y , Yin Y , Yi H . Decreased endogenous nitric oxide contributes to sulfur dioxide derivative-alleviated cadmium toxicity in foxtail millet roots. Environ Exp Bot. 2020; 177: 104144. doi:10.1016/j.envexpbot.2020.104144. [Google Scholar] [CrossRef]
16. Hasan S , Sehar Z , Khan NA . Gibberellic acid and sulfur-mediated reversal of cadmium-inhibited photosynthetic performance in mungbean (Vigna radiata L.) involves nitric oxide. J Plant Growth Regul. 2020; 39: 1605– 15. doi:10.1007/s00344-020-10175-4. [Google Scholar] [CrossRef]
17. Rao ZX , Huang DY , Wu JS , Zhu QH , Zhu HH , Xu C , et al. Distribution and availability of cadmium in profile and aggregates of a paddy soil with 30-year fertilization and its impact on Cd accumulation in rice plant. Environ Pollut. 2018; 239: 198– 204. doi:10.1016/j.envpol.2018.04.024. [Google Scholar] [CrossRef]
18. Shiyu Q , Hongen L , Zhaojun N , Rengel Z , Wei G , Chang L , et al. Toxicity of cadmium and its competition with mineral nutrients for uptake by plants: A review. Pedosphere. 2020; 30( 2): 168– 80. doi:10.1016/S1002-0160(20)60002-9. [Google Scholar] [CrossRef]
19. Chaney RL . How does contamination of rice soils with Cd and Zn cause high incidence of human Cd disease in subsistence rice farmers. Curr Pollut Rep. 2015; 1: 13– 22. doi:10.1007/s40726-015-0002-4. [Google Scholar] [CrossRef]
20. Chen Q , Wu F-B . Breeding for low cadmium accumulation cereals. J Zhejiang Univ Sci B. 2020; 21( 6): 442– 59. doi:10.1631/jzus.B1900576. [Google Scholar] [CrossRef]
21. Chellaiah ER . Cadmium (heavy metals) bioremediation by Pseudomonas aeruginosa: A minireview. Appl Water Sci. 2018; 8( 6): 154. doi:10.1007/s13201-018-0796-5. [Google Scholar] [CrossRef]
22. Emamverdian A , Ding Y , Barker J , Mokhberdoran F , Ramakrishnan M , Liu G , et al. Nitric oxide ameliorates plant metal toxicity by increasing antioxidant capacity and reducing Pb and Cd translocation. Antioxidants. 2021; 10( 12): 1981. doi:10.3390/antiox10121981. [Google Scholar] [CrossRef]
23. Ahad RIA , Syiem MB . Influence of calcium on cadmium uptake and toxicity to the cyanobacterium Nostoc muscorum Meg 1. Biotechnol Res Innov. 2019; 3( 2): 231– 41. doi:10.1016/j.biori.2019.06.002. [Google Scholar] [CrossRef]
24. Zhang XL , Jia XF , Yu B , Gao Y , Bai JG . Exogenous hydrogen peroxide influences antioxidant enzyme activity and lipid peroxidation in cucumber leaves at low light. Sci Hortic. 2011; 129( 4): 656– 62. doi:10.1016/j.scienta.2011.05.009. [Google Scholar] [CrossRef]
25. Uraguchi S , Fujiwara T . Cadmium transport and tolerance in rice: Perspectives for reducing grain cadmium accumulation. Rice. 2012; 5: 1– 8. doi:10.1186/1939-8433-5-5. [Google Scholar] [CrossRef]
26. Clemens S , Ma JF . Toxic heavy metal and metalloid accumulation in crop plants and foods. Annu Rev Plant Biol. 2016; 67( 1): 489– 512. doi:10.1146/annurev-arplant-043015-112301. [Google Scholar] [CrossRef]
27. Przedpelska-Wasowicz EM , Wierzbicka M . Gating of aquaporins by heavy metals in Allium cepa L. epidermal cells. Protoplasma. 2011; 248: 663– 71. doi:10.1007/s00709-010-0222-9. [Google Scholar] [CrossRef]
28. Khan MA , Castro-Guerrero N , Mendoza-Cozatl DG . Moving toward a precise nutrition: Preferential loading of seeds with essential nutrients over non-essential toxic elements. Front Plant Sci. 2014; 5: 51. doi:10.3389/fpls.2014.00051. [Google Scholar] [CrossRef]
29. Boorboori MR , Zhang H . The effect of cadmium on soil and plants, and the influence of Serendipita indica (Piriformospora indica) in mitigating cadmium stress. Environ Geochem Health. 2024; 46( 11): 426. doi:10.1007/s10653-024-02231-9. [Google Scholar] [CrossRef]
30. Rizwan M , Ali S , Abbas T , Zia-ur-Rehman M , Hannan F , Keller C , et al. Cadmium minimization in wheat: A critical review. Ecotoxicol Environ Saf. 2016; 130: 43– 53. doi:10.1016/j.ecoenv.2016.04.001. [Google Scholar] [CrossRef]
31. Boorboori M , Qiu HS , Liu JY , Zhang HY . Application of silicon and selenium in rice for reducing cadmium stress. Phyton. 2023; 92( 6): 1873. doi:10.32604/phyton.2023.027924. [Google Scholar] [CrossRef]
32. Dong Y , Chen W , Liu F , Wan Y . Physiological responses of peanut seedlings to exposure to low or high cadmium concentration and the alleviating effect of exogenous nitric oxide to high cadmium concentration stress. Plant Biosyst-Int J Deal All Asp Plant Biol. 2020; 154( 3): 405– 12. doi:10.1080/11263504.2019.1651771. [Google Scholar] [CrossRef]
33. Yang Y , Zhang L , Huang X , Zhou Y , Quan Q , Li Y , et al. Response of photosynthesis to different concentrations of heavy metals in Davidia involucrata. PLoS One. 2020; 15( 3): e0228563. doi:10.1371/journal.pone.0228563. [Google Scholar] [CrossRef]
34. Haider FU , Liqun C , Coulter JA , Cheema SA , Wu J , Zhang R , et al. Cadmium toxicity in plants: Impacts and remediation strategies. Ecotoxicol Environ Saf. 2021; 211: 111887. doi:10.1016/j.ecoenv.2020.111887. [Google Scholar] [CrossRef]
35. Boorboori MR . Investigating the role of silicon in reducing the risk of arsenic, cadmium, drought and salinity stresses in wheat (Triticum aestivum L.). J Crop Sci Biotechnol. 2023; 26( 4): 387– 404. doi:10.1007/s12892-022-00191-z. [Google Scholar] [CrossRef]
36. Li S , Yang W , Yang T , Chen Y , Ni W . Effects of cadmium stress on leaf chlorophyll fluorescence and photosynthesis of Elsholtzia argyi—A cadmium accumulating plant. Int J Phytoremediat. 2015; 17( 1): 85– 92. doi:10.1080/15226514.2013.828020. [Google Scholar] [CrossRef]
37. Faller P , Kienzler K , Krieger-Liszkay A . Mechanism of Cd2+ toxicity: Cd2+ inhibits photoactivation of Photosystem II by competitive binding to the essential Ca2+ site. Biochim Et Biophys Acta Bioenerg. 2005; 1706( 1–2): 158– 64. doi:10.1016/j.bbabio.2004.10.005. [Google Scholar] [CrossRef]
38. Mir IR , Rather BA , Sehar Z , Masood A , Khan NA . Nitric oxide in co-ordination with nitrogen reverses cadmium-inhibited photosynthetic activity by interacting with ethylene synthesis, strengthening the antioxidant system, and nitrogen and sulfur assimilation in mustard (Brassica juncea L.). Sci Hortic. 2023; 314: 111958. doi:10.1016/j.scienta.2023.111958. [Google Scholar] [CrossRef]
39. Shivaraj SM , Vats S , Bhat JA , Dhakte P , Goyal V , Khatri P , et al. Nitric oxide and hydrogen sulfide crosstalk during heavy metal stress in plants. Physiol Plant. 2020; 168( 2): 437– 55. doi:10.1111/ppl.13028. [Google Scholar] [CrossRef]
40. Qiao W , Li C , Fan LM . Cross-talk between nitric oxide and hydrogen peroxide in plant responses to abiotic stresses. Environ Exp Bot. 2014; 100: 84– 93. doi:10.1016/j.envexpbot.2013.12.014. [Google Scholar] [CrossRef]
41. Rather BA , Mir IR , Sehar Z , Anjum NA , Masood A , Khan NA . The outcomes of the functional interplay of nitric oxide and hydrogen sulfide in metal stress tolerance in plants. Plant Physiol Biochem. 2020; 155: 523– 34. doi:10.1016/j.plaphy.2020.08.005. [Google Scholar] [CrossRef]
42. Demidchik V . ROS-activated ion channels in plants: Biophysical characteristics, physiological functions and molecular nature. Int J Mol Sci. 2018; 19( 4): 1263. doi:10.3390/ijms19041263. [Google Scholar] [CrossRef]
43. Boorboori MR , Lin W , Fang C . Comparison of Japonica and Indica rice (Wild type and Lsi1 transgenic) in the use of silicon in reducing arsenic toxicity. Silicon. 2023; 15( 14): 6199– 214. doi:10.1007/s12633-023-02485-5. [Google Scholar] [CrossRef]
44. Li D , Xiao S , Ma WN , Peng Z , Khan D , Yang Q , et al. Magnesium reduces cadmium accumulation by decreasing the nitrate reductase-mediated nitric oxide production in Panax notoginseng roots. J Plant Physiol. 2020; 248: 153131. doi:10.1016/j.jplph.2020.153131. [Google Scholar] [CrossRef]
45. Kan Q , Wu W , Yu W , Zhang J , Xu J , Rengel Z , et al. Nitrate reductase-mediated NO production enhances Cd accumulation in Panax notoginseng roots by affecting root cell wall properties. J Plant Physiol. 2016; 193: 64– 70. doi:10.1016/j.jplph.2016.01.017. [Google Scholar] [CrossRef]
46. Emamverdian A , Ding Y , Mokhberdoran F , Xie Y . Heavy metal stress and some mechanisms of plant defense response. Sci World J. 2015; 2015( 1): 756120. doi:10.1155/2015/756120. [Google Scholar] [CrossRef]
47. Li K , Yu H , Li T , Chen G , Huang F . Cadmium accumulation characteristics of low-cadmium rice (Oryza sativa L.) line and F1 hybrids grown in cadmium-contaminated soils. Environ Sci Pollut Res. 2017; 24: 17566– 76. doi:10.1007/s11356-017-9350-5. [Google Scholar] [CrossRef]
48. Mir IR , Rather BA , Masood A , Khan NA . Nitric oxide-and sulfur-mediated reversal of cadmium-inhibited photosynthetic performance involves hydrogen sulfide and regulation of nitrogen, sulfur, and antioxidant metabolism in mustard. Stresses. 2022; 2( 4): 550– 77. doi:10.3390/stresses2040037. [Google Scholar] [CrossRef]
49. Domingos P , Prado AM , Wong A , Gehring C , Feijo JA . Nitric oxide: A multitasked signaling gas in plants. Mol Plant. 2015; 8( 4): 506– 20. doi:10.1016/j.molp.2014.12.010. [Google Scholar] [CrossRef]
50. Rather BA , Mir IR , Masood A , Anjum NA , Khan NA . Nitric oxide pre-treatment advances seed germination and alleviates copper-induced photosynthetic inhibition in Indian mustard. Plants. 2020; 9( 6): 776. doi:10.3390/plants9060776. [Google Scholar] [CrossRef]
51. Singh AP , Dixit G , Kumar A , Mishra S , Kumar N , Dixit S , et al. A protective role for nitric oxide and salicylic acid for arsenite phytotoxicity in rice (Oryza sativa L.). Plant Physiol Biochem. 2017; 115: 163– 73. doi:10.1016/j.plaphy.2017.02.019. [Google Scholar] [CrossRef]
52. He J , Ren Y , Chen X , Chen H . Protective roles of nitric oxide on seed germination and seedling growth of rice (Oryza sativa L.) under cadmium stress. Ecotoxicol Environ Saf. 2014; 108: 114– 9. doi:10.1016/j.ecoenv.2014.05.021. [Google Scholar] [CrossRef]
53. Terrón-Camero LC , Rodríguez-Serrano M , Sandalio LM , Romero-Puertas MC . Nitric oxide is essential for cadmium-induced peroxule formation and peroxisome proliferation. Plant Cell Environ. 2020; 43( 10): 2492– 507. doi:10.1111/pce.13855. [Google Scholar] [CrossRef]
54. León J , Costa Á , Castillo MC . Nitric oxide triggers a transient metabolic reprogramming in Arabidopsis. Sci Rep. 2016; 6( 1): 37945. doi:10.1038/srep37945. [Google Scholar] [CrossRef]
55. Delledonne M . NO news is good news for plants. Curr Opin Plant Biol. 2005; 8( 4): 390– 6. doi:10.1016/j.pbi.2005.05.002. [Google Scholar] [CrossRef]
56. Rockel P , Strube F , Rockel A , Wildt J , Kaiser WM . Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. J Exp Bot. 2002; 53( 366): 103– 10. doi:10.1093/jxb/53.366.103. [Google Scholar] [CrossRef]
57. Planchet E , Kaiser WM . Nitric oxide production in plants: Facts and fictions. Plant Signal Behav. 2006; 1( 2): 46– 51. doi:10.4161/psb.1.2.2435. [Google Scholar] [CrossRef]
58. Fu YF , Zhang ZW , Yuan S . Putative connections between nitrate reductase S-nitrosylation and NO synthesis under pathogen attacks and abiotic stresses. Front Plant Sci. 2018; 9: 474. doi:10.3389/fpls.2018.00474. [Google Scholar] [CrossRef]
59. Bellin D , Asai S , Delledonne M , Yoshioka H . Nitric oxide as a mediator for defense responses. Mol Plant-Microbe Interact. 2013; 26( 3): 271– 7. doi:10.1094/MPMI-09-12-0214-CR. [Google Scholar] [CrossRef]
60. Maia LB , Moura JJ . Nitrite reduction by molybdoenzymes: A new class of nitric oxide-forming nitrite reductases. JBIC J Biol Inorg Chem. 2015; 20: 403– 33. doi:10.1007/s00775-014-1234-2. [Google Scholar] [CrossRef]
61. Lau SE , Hamdan MF , Pua TL , Saidi NB , Tan BC . Plant nitric oxide signaling under drought stress. Plants. 2021; 10( 2): 360. doi:10.3390/plants10020360. [Google Scholar] [CrossRef]
62. Ahmad P , Tripathi DK , Deshmukh R , Pratap Singh V , Corpas FJ . Revisiting the role of ROS and RNS in plants under changing environment. Environ Exp Bot. 2019; 161: 1– 3. doi:10.1016/j.envexpbot.2019.02.017. [Google Scholar] [CrossRef]
63. Kolbert Z , Barroso JB , Brouquisse R , Corpas FJ , Gupta KJ , Lindermayr C , et al. A forty year journey: The generation and roles of NO in plants. Nitric Oxide. 2019; 93: 53– 70. doi:10.1016/j.niox.2019.09.006. [Google Scholar] [CrossRef]
64. Wulff A , Oliveira HC , Saviani EE , Salgado I . Nitrite reduction and superoxide-dependent nitric oxide degradation by Arabidopsis mitochondria: Influence of external NAD(P)H dehydrogenases and alternative oxidase in the control of nitric oxide levels. Nitric Oxide. 2009; 21( 2): 132– 9. doi:10.1016/j.niox.2009.06.003. [Google Scholar] [CrossRef]
65. Corpas FJ , Barroso JB . Peroxynitrite (ONOO−) is endogenously produced in Arabidopsis peroxisomes and is overproduced under cadmium stress. Ann Bot. 2014; 113( 1): 87– 96. doi:10.1093/aob/mct260. [Google Scholar] [CrossRef]
66. Corpas FJ , Barroso JB , Carreras A , Valderrama R , Palma JM , del Río LA . Nitrosative stress in plants: A new approach to understand the role of NO in abiotic stress. In: Nitric Oxide in Plant Growth, Development and Stress Physiology. Berlin/Heidelberg, Germany: Springer; 2007. p. 187– 205. doi:10.1007/7089_2006_091. [Google Scholar] [CrossRef]
67. Corpas FJ , González-Gordo S , Cañas A , Palma JM . Nitric oxide and hydrogen sulfide in plants: Which comes first? J Exp Bot. 2019; 70( 17): 4391– 404. doi:10.1093/jxb/erz031. [Google Scholar] [CrossRef]
68. da-Silva CJ , Canatto RA , Cardoso AA , Ribeiro C , de Oliveira JA . Oxidative stress triggered by arsenic in a tropical macrophyte is alleviated by endogenous and exogenous nitric oxide. Braz J Bot. 2018; 41: 21– 8. doi:10.1007/s40415-017-0431-y. [Google Scholar] [CrossRef]
69. Groß F , Durner J , Gaupels F . Nitric oxide, antioxidants and prooxidants in plant defence responses. Front Plant Sci. 2013; 4: 419. doi:10.3389/fpls.2013.00419. [Google Scholar] [CrossRef]
70. Zheng C , Jiang D , Liu F , Dai T , Liu W , Jing Q , et al. Exogenous nitric oxide improves seed germination in wheat against mitochondrial oxidative damage induced by high salinity. Environ Exp Bot. 2009; 67( 1): 222– 7. doi:10.1016/j.envexpbot.2009.05.002. [Google Scholar] [CrossRef]
71. Saxena I , Srikanth S , Chen Z . Cross talk between H2O2 and interacting signal molecules under plant stress response. Front Plant Sci. 2016; 7: 570. doi:10.3389/fpls.2016.00570. [Google Scholar] [CrossRef]
72. Beckman JS , Beckman TW , Chen J , Marshall PA , Freeman BA . Apparent hydroxyl radical production by peroxynitrite: Implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci U S A. 1990; 87( 4): 1620– 4. doi:10.1073/pnas.87.4.1620. [Google Scholar] [CrossRef]
73. Baena G , Feria AB , Echevarría C , Monreal JA , García-Mauriño S . Salinity promotes opposite patterns of carbonylation and nitrosylation of C4 phosphoenolpyruvate carboxylase in sorghum leaves. Planta. 2017; 246: 1203– 14. doi:10.1007/s00425-017-2764-y. [Google Scholar] [CrossRef]
74. Fan H , Guo S , Jiao Y , Zhang R , Li J . Effects of exogenous nitric oxide on growth, active oxygen species metabolism, and photosynthetic characteristics in cucumber seedlings under NaCl stress. Front Agric China. 2007; 1: 308– 14. doi:10.1007/s11703-007-0052-5. [Google Scholar] [CrossRef]
75. Agurla S , Gayatri G , Raghavendra AS . Nitric oxide as a secondary messenger during stomatal closure as a part of plant immunity response against pathogens. Nitric Oxide. 2014; 43: 89– 96. doi:10.1016/j.niox.2014.07.004. [Google Scholar] [CrossRef]
76. Sun H , Feng F , Liu J , Zhao Q . Nitric oxide affects rice root growth by regulating auxin transport under nitrate supply. Front Plant Sci. 2018; 9: 659. doi:10.3389/fpls.2018.00659. [Google Scholar] [CrossRef]
77. Mukherjee S . Recent advancements in the mechanism of nitric oxide signaling associated with hydrogen sulfide and melatonin crosstalk during ethylene-induced fruit ripening in plants. Nitric Oxide. 2019; 82: 25– 34. doi:10.1016/j.niox.2018.11.003. [Google Scholar] [CrossRef]
78. Della Rovere F , Piacentini D , Fattorini L , Girardi N , Bellanima D , Falasca G , et al. Brassinosteroids mitigate cadmium effects in Arabidopsis root system without any cooperation with nitric oxide. Int J Mol Sci. 2022; 23( 2): 825. doi:10.3390/ijms23020825. [Google Scholar] [CrossRef]
79. Asgher M , Per TS , Masood A , Fatma M , Freschi L , Corpas FJ , et al. Nitric oxide signaling and its crosstalk with other plant growth regulators in plant responses to abiotic stress. Environ Sci Pollut Res. 2017; 24: 2273– 85. doi:10.1007/s11356-016-7947-8. [Google Scholar] [CrossRef]
80. Wang X , Du H , Ma M , Rennenberg H . The dual role of nitric oxide (NO) in plant responses to cadmium exposure. Sci Total Environ. 2023; 892: 164597. doi:10.1016/j.scitotenv.2023.164597. [Google Scholar] [CrossRef]
81. Zhu H , Ai H , Hu Z , Du D , Sun J , Chen K , et al. Comparative transcriptome combined with metabolome analyses revealed key factors involved in nitric oxide (NO)-regulated cadmium stress adaptation in tall fescue. BMC Genom. 2020; 21: 1– 13. doi:10.1186/s12864-020-07017-8. [Google Scholar] [CrossRef]
82. Romero-Puertas MC , Terron-Camero LC , Pelaez-Vico MA , Olmedilla A , Sandalio LM . Reactive oxygen and nitrogen species as key indicators of plant responses to Cd stress. Environ Exp Bot. 2019; 161: 107– 19. doi:10.1016/j.envexpbot.2018.10.012. [Google Scholar] [CrossRef]
83. Xu J , Wang W , Yin H , Liu X , Sun H , Mi Q . Exogenous nitric oxide improves antioxidative capacity and reduces auxin degradation in roots of Medicago truncatula seedlings under cadmium stress. Plant Soil. 2010; 326: 321– 30. doi:10.1007/s11104-009-0011-4. [Google Scholar] [CrossRef]
84. Terrón-Camero LC , Peláez-Vico MÁ , Del-Val C , Sandalio LM , Romero-Puertas MC . Role of nitric oxide in plant responses to heavy metal stress: Exogenous application versus endogenous production. J Exp Bot. 2019; 70( 17): 4477– 88. doi:10.1093/jxb/erz184. [Google Scholar] [CrossRef]
85. Kopyra M , Gwóźdź EA . Nitric oxide stimulates seed germination and counteracts the inhibitory effect of heavy metals and salinity on root growth of Lupinus luteus. Plant Physiol Biochem. 2003; 41( 11–12): 1011– 7. doi:10.1016/j.plaphy.2003.09.003. [Google Scholar] [CrossRef]
86. Ahmad P , Ahanger MA , Alyemeni MN , Wijaya L , Alam P . Exogenous application of nitric oxide modulates osmolyte metabolism, antioxidants, enzymes of ascorbate-glutathione cycle and promotes growth under cadmium stress in tomato. Protoplasma. 2018; 255: 79– 93. doi:10.1007/s00709-017-1132-x. [Google Scholar] [CrossRef]
87. Arasimowicz-Jelonek M , Floryszak-Wieczorek J , Gwóźdź EA . The message of nitric oxide in cadmium challenged plants. Plant Sci. 2011; 181( 5): 612– 20. doi:10.1016/j.plantsci.2011.03.019. [Google Scholar] [CrossRef]
88. Cao S , Pan J , Rehman M , Luo D , Wang Q , Jin G , et al. Exogenous nitric oxide alleviates cadmium toxicity in kenaf (Hibiscus cannabinus L.) through modulating cd deposition and regulating key genes and involved pathways. Ind Crops Prod. 2024; 221: 119359. doi:10.1016/j.indcrop.2024.119359. [Google Scholar] [CrossRef]
89. Xu J , Wang W , Sun J , Zhang Y , Ge Q , Du L , et al. Involvement of auxin and nitric oxide in plant Cd-stress responses. Plant Soil. 2011; 346: 107– 19. doi:10.1007/s11104-011-0800-4. [Google Scholar] [CrossRef]
90. Lux A , Martinka M , Vaculík M , White PJ . Root responses to cadmium in the rhizosphere: A review. J Exp Bot. 2011; 62( 1): 21– 37. doi:10.1093/jxb/erq281. [Google Scholar] [CrossRef]
91. Kováčik J , Grúz J , Klejdus B , Štork F , Marchiosi R , Ferrarese-Filho O . Lignification and related parameters in copper-exposed Matricaria chamomilla roots: Role of H2O2 and NO in this process. Plant Sci. 2010; 179( 4): 383– 9. doi:10.1016/j.plantsci.2010.06.014. [Google Scholar] [CrossRef]
92. Loix C , Huybrechts M , Vangronsveld J , Gielen M , Keunen E , Cuypers A . Reciprocal interactions between cadmium-induced cell wall responses and oxidative stress in plants. Front Plant Sci. 2017; 8: 1867. doi:10.3389/fpls.2017.01867. [Google Scholar] [CrossRef]
93. Xiong J , An L , Lu H , Zhu C . Exogenous nitric oxide enhances cadmium tolerance of rice by increasing pectin and hemicellulose contents in root cell wall. Planta. 2009; 230: 755– 65. doi:10.1007/s00425-009-0984-5. [Google Scholar] [CrossRef]
94. Qiao W , Fan LM . Nitric oxide signaling in plant responses to abiotic stresses. J Integr Plant Biol. 2008; 50( 10): 1238– 46. doi:10.1111/j.1744-7909.2008.00759.x. [Google Scholar] [CrossRef]
95. Sandalio LM , Rodríguez-Serrano M , del Río LA , Romero-Puertas MC . Reactive oxygen species and signaling in cadmium toxicity. In: Reactive oxygen species in plant signaling. Berlin/Heidelberg, Germany: Springer; 2009. p. 175– 89. doi:10.1007/978-3-642-00390-5_11. [Google Scholar] [CrossRef]
96. Wang L , Yang L , Yang F , Li X , Song Y , Wang X , et al. Involvements of H2O2 and metallothionein in NO-mediated tomato tolerance to copper toxicity. J Plant Physiol. 2010; 167( 15): 1298– 306. doi:10.1016/j.jplph.2010.04.007. [Google Scholar] [CrossRef]
97. Qu W , Liu J , Fuquay R , Shimoda R , Sakurai T , Saavedra JE , et al. The nitric oxide prodrug, V-PYRRO/NO, protects against cadmium toxicity and apoptosis at the cellular level. Nitric Oxide. 2005; 12( 2): 114– 20. doi:10.1016/j.niox.2005.01.005. [Google Scholar] [CrossRef]
98. Besson-Bard A , Gravot A , Richaud P , Auroy P , Duc C , Gaymard F , et al. Nitric oxide contributes to cadmium toxicity in Arabidopsis by promoting cadmium accumulation in roots and by up-regulating genes related to iron uptake. Plant Physiol. 2009; 149( 3): 1302– 15. doi:10.1104/pp.108.133348. [Google Scholar] [CrossRef]
99. Elviri L , Speroni F , Careri M , Mangia A , di Toppi LS , Zottini M . Identification of in vivo nitrosylated phytochelatins in Arabidopsis thaliana cells by liquid chromatography-direct electrospray-linear ion trap-mass spectrometry. J Chromatogr A. 2010; 1217( 25): 4120– 6. doi:10.1016/j.chroma.2010.02.013. [Google Scholar] [CrossRef]
100. Zhang H , Xu W , Guo J , He Z , Ma M . Coordinated responses of phytochelatins and metallothioneins to heavy metals in garlic seedlings. Plant Sci. 2005; 169( 6): 1059– 65. doi:10.1016/j.plantsci.2005.07.010. [Google Scholar] [CrossRef]
101. De Michele R , Vurro E , Rigo C , Costa A , Elviri L , Di Valentin M , et al. Nitric oxide is involved in cadmium-induced programmed cell death in Arabidopsis suspension cultures. Plant Physiol. 2009; 150( 1): 217– 28. doi:10.1104/pp.108.133397. [Google Scholar] [CrossRef]
102. Grün S , Lindermayr C , Sell S , Durner J . Nitric oxide and gene regulation in plants. J Exp Bot. 2006; 57( 3): 507– 16. doi:10.1093/jxb/erj053. [Google Scholar] [CrossRef]
103. Arasimowicz M , Floryszak-Wieczorek J . Nitric oxide as a bioactive signalling molecule in plant stress responses. Plant Sci. 2007; 172( 5): 876– 87. doi:10.1016/j.plantsci.2007.02.005. [Google Scholar] [CrossRef]
104. Zhu XF , Jiang T , Wang ZW , Lei GJ , Shi YZ , Li GX , et al. Gibberellic acid alleviates cadmium toxicity by reducing nitric oxide accumulation and expression of IRT1 in Arabidopsis thaliana. J Hazard Mater. 2012; 239: 302– 7. doi:10.1016/j.jhazmat.2012.08.077. [Google Scholar] [CrossRef]
105. Fatma M , Khan NA . Nitric oxide protects photosynthetic capacity inhibition by salinity in Indian mustard. J Funct Environ Bot. 2014; 4( 2): 106– 16. doi:10.5958/2231-1750.2014.00009.2. [Google Scholar] [CrossRef]
106. Kolbert Z , Feigl G , Bordé Á , Molnár Á , Erdei L . Protein tyrosine nitration in plants: Present knowledge, computational prediction and future perspectives. Plant Physiol Biochem. 2017; 113: 56– 63. doi:10.1016/j.plaphy.2017.01.028. [Google Scholar] [CrossRef]
107. Zhuo Y , Qiu S , Amombo E , Zhu Q , Tang D , Huang M , et al. Nitric oxide alleviates cadmium toxicity in tall fescue photosystem II on the electron donor side. Environ Exp Bot. 2017; 137: 110– 8. doi:10.1016/j.envexpbot.2017.02.008. [Google Scholar] [CrossRef]
108. Khan MN , Siddiqui MH , AlSolami MA , Alamri S , Hu Y , Ali HM , et al. Crosstalk of hydrogen sulfide and nitric oxide requires calcium to mitigate impaired photosynthesis under cadmium stress by activating defense mechanisms in Vigna radiata. Plant Physiol Biochem. 2020; 156: 278– 90. doi:10.1016/j.plaphy.2020.09.017. [Google Scholar] [CrossRef]
109. Sehar Z , Masood A , Khan NA . Nitric oxide reverses glucose-mediated photosynthetic repression in wheat (Triticum aestivum L.) under salt stress. Environ Exp Bot. 2019; 161: 277– 89. doi:10.1016/j.envexpbot.2019.01.010. [Google Scholar] [CrossRef]
110. Zhao H , Jin Q , Wang Y , Chu L , Li X , Xu Y . Effects of nitric oxide on alleviating cadmium stress in Typha angustifolia. Plant Growth Regul. 2016; 78: 243– 51. doi:10.1007/s10725-015-0089-z. [Google Scholar] [CrossRef]
111. Yuan HM , Huang X . Inhibition of root meristem growth by cadmium involves nitric oxide-mediated repression of auxin accumulation and signalling in Arabidopsis. Plant Cell Environ. 2016; 39( 1): 120– 35. doi:10.1111/pce.12597. [Google Scholar] [CrossRef]
112. Liu M , Zhang H , Fang X , Zhang Y , Jin C . Auxin acts downstream of ethylene and nitric oxide to regulate magnesium deficiency-induced root hair development in Arabidopsis thaliana. Plant Cell Physiol. 2018; 59( 7): 1452– 65. doi:10.1093/pcp/pcy078. [Google Scholar] [CrossRef]
113. Piacentini D , Della Rovere F , Sofo A , Fattorini L , Falasca G , Altamura MM . Nitric oxide cooperates with auxin to mitigate the alterations in the root system caused by cadmium and arsenic. Front Plant Sci. 2020; 11: 1182. doi:10.3389/fpls.2020.01182. [Google Scholar] [CrossRef]
114. Motte H , Vanneste S , Beeckman T . Molecular and environmental regulation of root development. Annu Rev Plant Biol. 2019; 70( 1): 465– 88. doi:10.1146/annurev-arplant-050718-100423. [Google Scholar] [CrossRef]
115. Bücker-Neto L , Paiva ALS , Machado RD , Arenhart RA , Margis-Pinheiro M . Interactions between plant hormones and heavy metals responses. Genet Mol Biol. 2017; 40( 1 suppl 1): 373– 86. doi:10.1590/1678-4685-gmb-2016-0087. [Google Scholar] [CrossRef]
116. Wei Z , Li J . Brassinosteroids regulate root growth, development, and symbiosis. Mol Plant. 2016; 9( 1): 86– 100. doi:10.1016/j.molp.2015.12.003. [Google Scholar] [CrossRef]
117. Xuan W , Beeckman T . Plant signaling: Interplay of brassinosteroids and auxin in root meristems. Curr Biol. 2021; 31( 20): R1392– 5. doi:10.1016/j.cub.2021.09.007. [Google Scholar] [CrossRef]
118. Li Y , Wu Y , Liao W , Hu L , Dawuda MM , Jin X , et al. Nitric oxide is involved in the brassinolide-induced adventitious root development in cucumber. BMC Plant Biol. 2020; 20: 1– 12. doi:10.1186/s12870-020-2320-y. [Google Scholar] [CrossRef]
119. Mittler R , Vanderauwera S , Gollery M , Van Breusegem F . Reactive oxygen gene network of plants. Trends Plant Sci. 2004; 9( 10): 490– 8. doi:10.1016/j.tplants.2004.08.009. [Google Scholar] [CrossRef]
120. Ben Ammar W , Nouairi I , Zarrouk M , Jemal F . Cadmium stress induces changes in the lipid composition and biosynthesis in tomato (Lycopersicon esculentum Mill.) leaves. Plant Growth Regul. 2007; 53: 75– 85. doi:10.1007/s10725-007-9203-1. [Google Scholar] [CrossRef]
121. Qiu ZB , Guo JL , Zhang MM , Lei MY , Li ZL . Nitric oxide acts as a signal molecule in microwave pretreatment induced cadmium tolerance in wheat seedlings. Acta Physiol Plant. 2013; 35: 65– 73. doi:10.1007/s11738-012-1048-1. [Google Scholar] [CrossRef]
122. Sandalio LM , Gotor C , Romero LC , Romero-Puertas MC . Multilevel regulation of peroxisomal proteome by post-translational modifications. Int J Mol Sci. 2019; 20( 19): 4881. doi:10.3390/ijms20194881. [Google Scholar] [CrossRef]
123. Xuan Y , Zhou S , Wang L , Cheng Y , Zhao L . Nitric oxide functions as a signal and acts upstream of AtCaM3 in thermotolerance in Arabidopsis seedlings. Plant Physiol. 2010; 153( 4): 1895– 906. doi:10.1104/pp.110.160424. [Google Scholar] [CrossRef]
124. Hill BG , Dranka BP , Bailey SM , Lancaster JR , Darley-Usmar VM . What part of NO don’t you understand? Some answers to the cardinal questions in nitric oxide biology. J Biol Chem. 2010; 285( 26): 19699– 704. doi:10.1074/jbc.R110.101618. [Google Scholar] [CrossRef]
125. Liu S , Yang R , Pan Y , Ma M , Pan J , Zhao Y , et al. Nitric oxide contributes to minerals absorption, proton pumps and hormone equilibrium under cadmium excess in Trifolium repens L. plants. Ecotoxicol Environ Saf. 2015; 119: 35– 46. doi:10.1016/j.ecoenv.2015.04.053. [Google Scholar] [CrossRef]
126. Sun C , Liu L , Yu Y , Liu W , Lu L , Jin C , et al. Nitric oxide alleviates aluminum-induced oxidative damage through regulating the ascorbate-glutathione cycle in roots of wheat. J Integr Plant Biol. 2015; 57( 6): 550– 61. doi:10.1111/jipb.12298. [Google Scholar] [CrossRef]
127. Mir IR , Rather BA , Masood A , Anjum NA , Khan NA . Nitrogen sources mitigate cadmium phytotoxicity differentially by modulating cellular buffers, N-assimilation, non-protein thiols, and phytochelatins in mustard (Brassica juncea L.). J Soil Sci Plant Nutr. 2022; 22( 3): 3847– 67. doi:10.1007/s42729-022-00935-4. [Google Scholar] [CrossRef]
128. Feng J , Chen L , Zuo J . Protein S-nitrosylation in plants: Current progresses and challenges. J Integr Plant Biol. 2019; 61( 12): 1206– 23. doi:10.1111/jipb.12780. [Google Scholar] [CrossRef]
129. Rejeb KB , Abdelly C , Savouré A . How reactive oxygen species and proline face stress together. Plant Physiol Biochem. 2014; 80: 278– 84. doi:10.1016/j.plaphy.2014.04.007. [Google Scholar] [CrossRef]
130. Jahanbakhshi A , Rasooli Sharabiani V , Heidarbeigi K , Kaveh M , Taghinezhad E . Evaluation of engineering properties for waste control of tomato during harvesting and postharvesting. Food Sci Nutr. 2019; 7( 4): 1473– 81. doi:10.1002/fsn3.986. [Google Scholar] [CrossRef]
131. Singh HP , Batish DR , Kaur G , Arora K , Kohli RK . Nitric oxide (as sodium nitroprusside) supplementation ameliorates Cd toxicity in hydroponically grown wheat roots. Environ Exp Bot. 2008; 63( 1–3): 158– 67. doi:10.1016/j.envexpbot.2007.12.005. [Google Scholar] [CrossRef]
132. Mata-Pérez C , Sánchez-Vicente I , Arteaga N , Gómez-Jiménez S , Fuentes-Terrón A , Oulebsir CS , et al. Functions of nitric oxide-mediated post-translational modifications under abiotic stress. Front Plant Sci. 2023; 14: 1158184. doi:10.3389/fpls.2023.1158184. [Google Scholar] [CrossRef]
133. Zhang S , Liu L , Wu Z , Wang L , Ban Z . S-nitrosylation of superoxide dismutase and catalase involved in promotion of fruit resistance to chilling stress: A case study on Ziziphus jujube Mill. Postharvest Biol Technol. 2023; 197: 112210. doi:10.1016/j.postharvbio.2022.112210. [Google Scholar] [CrossRef]
134. Song J , Feng SJ , Chen J , Zhao WT , Yang ZM . A cadmium stress-responsive gene AtFC1 confers plant tolerance to cadmium toxicity. BMC Plant Biol. 2017; 17( 1): 187. doi:10.1186/s12870-017-1141-0. [Google Scholar] [CrossRef]
135. Hasan MK , Liu C , Wang F , Ahammed GJ , Zhou J , Xu MX , et al. Glutathione-mediated regulation of nitric oxide, S-nitrosothiol and redox homeostasis confers cadmium tolerance by inducing transcription factors and stress response genes in tomato. Chemosphere. 2016; 161: 536– 45. doi:10.1016/j.chemosphere.2016.07.053. [Google Scholar] [CrossRef]
136. Atif RM , Shahid L , Waqas M , Ali B , Rashid MAR , Azeem F , et al. Insights on calcium-dependent protein kinases (CPKs) signaling for abiotic stress tolerance in plants. Int J Mol Sci. 2019; 20( 21): 5298. doi:10.3390/ijms20215298. [Google Scholar] [CrossRef]
137. Wani KI , Naeem M , Castroverde CDM , Kalaji HM , Albaqami M , Aftab T . Molecular mechanisms of nitric oxide (NO) signaling and reactive oxygen species (ROS) homeostasis during abiotic stresses in plants. Int J Mol Sci. 2021; 22( 17): 9656. doi:10.3390/ijms22179656. [Google Scholar] [CrossRef]
138. Lin W , Shang JX , Li XY , Zhou XF , Zhao LQ . Nitric oxide regulates multiple signal pathways in plants via protein S-nitrosylation. Curr Issues Mol Biol. 2025; 47( 6): 407. doi:10.3390/cimb47060407. [Google Scholar] [CrossRef]
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