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Review

Nitric Oxide in Plant Cold Stress: Functions, Mechanisms and Challenges

by
Jing Cui
,
Mengxiao Huang
,
Jin Qi
,
Wenjin Yu
and
Changxia Li
*
College of Agriculture, Guangxi University, Nanning 530004, China
*
Author to whom correspondence should be addressed.
Agronomy 2025, 15(5), 1072; https://doi.org/10.3390/agronomy15051072
Submission received: 15 March 2025 / Revised: 16 April 2025 / Accepted: 22 April 2025 / Published: 28 April 2025
(This article belongs to the Special Issue Physiological and Genetic Improvement of Crop Traits in Enhancing Crop Resilience)
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Abstract

:
Cold stress, as an environmental factor that seriously restricts the growth, production and survival of plants, has received extensive attention in recent years. Nitric oxide (NO), as an important bioactive molecule, has emerged as a research focus in the domain of alleviating plant cold damage. In this review, the role of NO in enhancing plant cold tolerance and its underlying mechanisms, including interactions with signaling molecules, are discussed more extensively, and novel research directions and prospects are proposed according to existing research gaps. Interestingly, exogenous NO mitigates cold stress by strengthening antioxidant defense mechanisms, raising proline levels, enhancing photosynthetic capacity, and regulating glucose metabolism. More importantly, NO also interacts with cytoplasmic calcium ions (Ca2+), reactive oxygen species (ROS), glutathione (GSH), melatonin (MT), abscisic acid (ABA), ethylene (ETH) and hydrogen sulfide (H2S). At the same time, in the process of NO alleviating cold stress, it regulates the expression of NO synthesis genes, cold response genes and antioxidant related genes, thereby improving the cold tolerance of plants, which may involve epigenetic reprogramming. This paper also points out the problems existing in the current research and the potential of NO in agricultural practice, and provides relevant theoretical references for future research in this field.

1. Introduction

As an environmental factor that has an important impact on plant growth, productivity and survival, low temperature stress can be divided into cold stress (0–15 °C) and freezing stress (<0 °C) [1]. Cold stress can inhibit plant growth and development, while long-term exposure to freezing stress can damage cell membranes and lead to cell death [2]. The sixth assessment report of the Intergovernmental Panel on Climate Change (IPCC) pointed out that since the middle of the 20th century, the global wheat and maize production has decreased by 1.9% and 1.2% each decade, respectively, and cold stress is one of the important causes [3]. Extensive research efforts are dedicated to elucidating the mechanism of cold injury and investigating effective strategies for its mitigation. Plants can exhibit unique responses to cold stress in different cell types because each cell type has different functions in the plant and different sensitivities to the environment. The cell type-specific response mechanism is critical for plant adaptation to the environment. Root cells are the main sites for plant uptake of water and nutrients. In response to cold stress, root cells undergo a series of changes to maintain their function. Root cells are the main sites for plant uptake of water and nutrients. In response to cold stress, root cells undergo a series of changes to maintain their function. Root hair cells may change the fluidity of their cell membrane to prevent membrane damage [4]. Cortical cells may accumulate osmoregulatory substances, such as proline and betaine, to maintain cell turgidity and prevent cell dehydration [5]. Endothelial cells, on the other hand, may strengthen the structure of their cell wall to prevent mechanical damage caused by low temperature. Under cold stress, leaf cells employ a variety of strategies to protect photosynthetic apparatus. Mesophyll cells may increase the activity of antioxidant enzymes to remove cold stress-induced reactive oxygen species (ROS) and reduce oxidative damage [6]. Stomatal guard cells may close stomata to reduce water loss and prevent dehydration [5]. Epidermal cells may accumulate waxy to increase leaf hydrophobicity and reduce the risk of icing. Vascular tissue cells will adjust their transport functions to ensure the normal physiological activities of the plant body. Xylem cells may change the diameter and number of their ducts to accommodate water transport requirements at low temperatures. Phloem cells may increase sucrose transport to provide energy for plants to cope with cold stress [7]. As a gas signaling molecule, nitric oxide (NO) has attracted much attention as a key signaling molecule in enhancing plant resistance to stress. Previous studies have found that the mechanism of chilling injury is mainly due to the increase of ROS and reactive nitrogen species (RNS) induced by cold stress. Excessive ROS accumulation is caused by a loss of balance between ROS formation and clearance [8]. ROS refers to oxygen-containing molecules with higher chemical reactivity than O2, mainly including superoxide anion (O2−) and hydrogen peroxide (H2O2) [9,10]. O2− has certain toxicity and can directly damage cellular components. O2− can participate in the Haber-Weiss reaction and Fenton reaction to generate more toxic hydroxyl free radicals (·OH), which aggravate oxidative damage [11]. Plants possess a series of ROS scavenging mechanisms, where a variety of antioxidant enzymes catalyze the transformation and decomposition of ROS, thereby maintaining ROS levels within a regulated range and consequently reducing or preventing oxidative damage [12,13]. Plants possess antioxidant enzyme systems such as superoxide dismutase (SOD), catalase (CAT), and peroxidase (POD), which can remove ROS and reduce oxidative damage [14]. SOD converts O2− to H2O2, and CAT and POD further decompose H2O2 into H2O and oxygen [14]. Simultaneously, the process of mitigating cold stress is being gradually unveiled. Research has shown that calcium ions (Ca2+), as a second messenger, is involved in plant vegetative growth and metabolic regulation [15]. Simultaneously, as an indicator of the flexible conformational changes in phospholipids and proteins, Ca2+ prevents subcellular structural damage, stabilizes membrane architecture, and maintains membrane integrity, enabling plants to adapt to environmental stress [15]. It can also slow down the degradation of chlorophyll, reduce the content of malondialdehyde (MDA), increase the activity of SOD and POD, and increase the content of soluble sugar and soluble protein [15]. NO can directly bind to Ca2+ to form a nitroso-mercaptan negative ion (RSNO−), which in turn affects Ca2+ signaling pathways, such as Ca2+/calmodulin-dependent protein kinase (CaMK) signaling pathway. This may lead to changes in intracellular Ca2+ concentration, which in turn affect the expression of genes and enzyme activity related to cold stress response [16]. Furthermore, some cold resistance regulatory substances, including plant hormones, can also activate the cold resistance mechanism of plants, promote the expression of some regulatory reactions, and improve the cold resistance of plants [17,18]. Treatment with 0.1 mM exogenous salicylic acid (SA) led to the accumulation or resynthesis of some apoptotic proteins in the leaf cell gap of wheat, regulating the activity of apoptotic antioxidant enzymes, the activity of ice nuclei and the type of apoptotic proteins, thereby improving the cold resistance of plants [19,20]. It has been reported that arginine enhances the NO signaling pathway mediated by nitric oxide synthase (NOS) modulates the activity of downstream antioxidant enzymes and the expression of heat shock proteins. This process reduces ROS accumulation, protects membrane proteins and nucleic acid synthesis pathways through heat shock proteins, and enhances plant cold resistance [21]. As a widely distributed gas signaling molecule in planting objects, it is very necessary to study the role of NO in cold stress [22].
NO is recognized as an important gas signaling molecule with redox activity in plants, coordinating a wide range of physiological and developmental processes in plants. In most cases, the use of NO treatment under cold stress conditions prevents cell differentiation and reduces heterogeneity, thus making plants more resistant. Numerous studies have shown that NO plays a role in seed germination [23], root formation [24], flowering [25], fruit ripening [26], and postharvest in fresh cut flowers, vegetables, and fruits [27]. Moreover, NO has emerged as a pivotal signaling molecule in plants, playing a crucial role in enhancing plant resistance to biotic stress [28,29]. Modolo et al. found that NOS inhibitor treatment inhibited the production of NO and the accumulation of plant antitoxin in soybean cotyledon [30]. Complete control of pest thrips was achieved after 3 h of NO fumigation [31]. NO can inhibit conidial development and mycelial growth of postharvest pathogens such as aspergillus niger [32], brown rot [33], and anthrax [34]. Its inhibitory mechanism involves inducing the accumulation of ROS in pathogenic fungi, and causes oxidative damage. Sodium nitroprusside (SNP, NO donor) enhanced tomato fruit resistance to Botrytis cinerea by dysregulating the expression of six ripening genes in tomato [35]. The prevention and control of disease by NO is believed to stem from the activation and enhancement of the fruit’s intrinsic defense mechanisms. This hypothesis is supported by the differential effects of NO on pathogen inhibition observed both in vivo and in vitro studies of mango [36]. NO also plays an irreplaceable role in plant resistance to abiotic stresses including salinity, drought, heavy metals, heat, cold, etc. [37,38,39]. SNP treatment significantly reduced ionic toxicity in salt-stressed Kandelia obovata, improved nutrient homeostasis, boosted antioxidant enzyme activity, thereby stimulating wheat coleoptile and radicle growth [40]. High osmotic stress induced oxidative stress response in rice and cucumber seedlings, which was significantly alleviated by exogenous SNP [41]. Li et al. showed that exogenous use of NO could reduce electrolyte leakage and lipid peroxidation in maize at high temperature, thus improving the survival rate of seedlings [42]. Under cold stress, NO can protect plants from cold damage by promoting seed germination, root growth and seedling elongation, maintaining ionic balance and activating antioxidant enzymes [43,44,45]. NO also works synergically with other plant growth regulators, such as Ca2+, ROS, and plant hormones, to improve plant cold resistance [46,47]. These studies suggest that NO may be critical for plants under cold stress.
With the deepening of scientific research, the role of NO in cold stress has been paid more and more attention. Numerous studies have shown that NO plays an important role in alleviating plant stress, and explained the functional molecular mechanism of NO as a signaling medium to induce plant adaptation to stress during specific physiological processes, including NO-induced epigenetic reprogramming. On this basis, the role of NO in improving plant cold tolerance and its regulatory mechanism were reviewed, and the roles of different genes in plant cold stress response were discussed, thus providing a new way to further explore the role of gas signaling molecules in abiotic stress.

2. Synthesis of NO

NO is a free radical gas and a small molecule signaling compound that plays an essential role in the physiological and developmental processes throughout the plant life cycle. Although research on NO-mediated mechanisms is growing, the precise details of how this molecule regulates its signaling pathways remain largely elusive. So far, the main sources of NO in plants have been described as nitrate reductase (NR) pathway, NOS pathway, and non-enzymatic pathway formation (Figure 1) [48]. NR is located in cytoplasm and catalyzes nitrate or nitrite to form NO with NAD(P)H as electron donor. NR is a key and rate-limiting enzyme that controls nitrogen metabolism in higher plant cells, promoting the synthesis of NO (Figure 1) [49]. At present, many researchers have detected the activity of NR in a variety of plants. NOS catalyzed NO synthesis pathway is dependent on L-Arg (Arginine-dependent): L-Arg+NAD(P)H+H++O2→L-Citr+NAD(P)++NO, in which NADPH and oxygen molecules are required external conditions (Figure 1) [50]. However, whether a nitric oxide synthase-like (NOS) pathway exists in plants to produce NO is still controversial. NO can also be produced by non-enzymatic pathways in exosomes of plant cells. Nitration and denitrifying oxidation of Nitrous Oxide (N2O) can also produce NO (Figure 1) [50,51,52]. The aleurone layer will acidify the cell wall solution during growth, and under acidic conditions nitrite can react with protons to form nitrite (HNO2), and then interact with HNO2 to form NO and nitrogen dioxide (NO2), which can be further converted to NO. The aleux layer will acidify the cell wall solution during growth, and under acidic conditions nitrite can react with protons to form nitrite (HNO2), and then interact with HNO2 to form NO and nitrogen dioxide (NO2), which can be further converted to NO [50,51,52]. Plant hormones such as abscisic acid (ABA) and gibberellin (GA) can trigger the acidification of plant tissues. ABA treatment causes the pH of the barley aleurone cell wall solution to drop rapidly, while GA treatment causes the pH to drop to a much lower level (Figure 1) [51,53,54]. ABA accumulation can be promoted by increasing the level of histone acetylation of ABA-synthesizing genes [55]. Histone acetylation and methylation can be involved in regulating the expression of cell wall related genes (such as ZmMHA), which has an important impact on the intracellular and extracellular pH balance [56]. We infer that plant hormones such as ABA and GA may regulate exosome acidification by inducing epigenetic reprogramming.
In general, NR pathway, NOS pathway and non-enzymatic pathway are the main sources of NO in plants, which provide essential substances for plant growth and development and stress resistance.

3. NO Alleviates Cold Stress in Plants at Different Growth Stages

3.1. NO Promotes Seed Germination Under Cold Stress

Seed germination is a critical stage of plant life cycle and is susceptible to environmental factors. Over a considerable period of time, NO has been shown to play a vital role in improving the resistance of plant seeds to cold stress, including the regulation of seed dormancy release and germination initiation [57]. Irrigation of 300 μM SNP on two rapeseed (Brassica napus L.) varieties (ZY15 and HY49) at 15 °C significantly improved rapeseed resistance to cold stress, thereby increasing seed germination rate [58]. Tomato growth is inhibited at temperatures below 25 °C and almost stops at temperatures below 6 °C. In tomato seeds, SNP treatment with a concentration of 200 μM at 10 °C significantly increased amylase activity and soluble sugar content, and improved low temperature tolerance [59]. The use of exogenous NO effectively alleviates the inhibition of seed germination caused by cold stress and promotes the germination of wheat seeds [60]. When winter wheat seeds were cultured at 22 °C/18 °C (day/night), the germination rate was 97.67%, germination index (GI) was 95.07, radicle length was 9.37 cm, germ length was 8.57 cm, and the average germination time was 1.19 days. The GR of wheat seeds under cold stress (12 ± 0.5 °C) was 88.3%, accompanied by a GI of 36.8% and inhibited elongation of radicle (0.52 cm) and coleoptile (0.76 cm). However, upon application of the 100 μM SNP and subsequent exposure to a temperature range of 12 ± 0.5 °C for a duration of 7 days, significant improvements were noted in various parameters including an increased germination rate of 93.33%, enhanced germination index reaching 43.19%, substantial growth in radicle length (0.94 cm) and coleoptile length (1.12 cm), along with a reduction in average germination time from 2.67 days to 2.47 days (Table 1) [60]. Chromatin remodeling plays a crucial role in plant seed germination under cold stress [61]. It has been shown that the chromatin modifier PICKLE (PKL) is involved in the regulation of Arabidopsis seed germination under osmotic stress [61]. pkl mutant seeds were highly sensitive to ABA treatment, which was associated with abnormally high and sustained expression of ABI3 and ABI5 [62]. PKL prevents excessive germination inhibition responses by associating ABI3 and ABI5 with silenced chromatin, thereby shutting down ABI3 and ABI5 expression under mild stress [62]. Fullerenol can alleviate osmotically inhibited germination through selective penetration of pea seed coat, which is associated with chromatin remodeling and transcriptional reprogramming [61]. These results suggest that exogenous substances can regulate plant stress response by inducing chromatin remodeling. While there is no direct evidence that NO is involved in this process under cold stress, it is reasonable to speculate that NO may have an effect on chromatin remodeling.

3.2. NO Alleviates Cold Injury in Seedling Stage

Exogenous application of NO can also greatly improve the survival rate of plant seedlings. Zhao et al. showed that the survival rate of Arabidopsis leaves treated with NO donor SNP under −7 °C for 4 h could reach 91% [64]. Application of NO scavengers 5-tetramethylimidazolin-1-oxygen-3-oxide (cPTIO) and NO inhibitors okada acid (OA) and Nω-nitroL-arginine (L-NNA) at −7 °C resulted in total leaf death of Arabidopsis thaliana [64]. These results suggest that NO greatly improved cold tolerance in Arabidopsis (Table 1) [64]. Prior research has demonstrated that the positive effects of NO are also evident in enhancing seedling growth under cold stress conditions. Elymus nutans seedlings exhibited significant increases in root surface area, root volume, root diameter, and number of root tips following treatment with 100 μM SNP for 12 h and subsequent exposure to 5 °C cold stress for 5 days. However, these effects were attenuated in seedlings treated with 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide potassium salt (PTIO, an NO scavenger) or L-NNA (Table 1) [73]. The surface of maize seedlings was sprayed with SNP for 12 days and then placed at cold stress (10/7 °C day/night temperature and 50% relative humidity with a 16 h photoperiod) for additional 21 days (Table 1) [76]. The chilling index (CI) of the leaves treated by SNP was about 65%, while the control reached 100%, indicating that exogenous NO could enhance the cold resistance of maize [76]. In addition, root system is the main organ of plant to absorb water and nutrients, and its function is directly related to whether the plant can obtain enough growth resources. Cold stress can inhibit the absorption of water and nutrients by plant roots and affect the normal growth of seedlings [78]. In Arabidopsis, cold stress (0.5 °C) inhibited primary root growth and caused an increase in the diameter anisotropy of epidermal cells. Application of SNP at a concentration of 100 µM could directly regulate the organization of actin fibers in Arabidopsis primary root cells under low temperature, and promotes root growth [79]. The low temperature-triggered signal might be transmitted to actin filaments by NO, whether directly (posttranslational modifications), causing changes in their orientation/organization [79]. Although low concentration of NO can alleviate the damage to plants caused by cold stress, high concentration of NO can cause nitrosation stress and damage to plant cells [80].
In summary, the role of NO in plant seedling stage is mainly to greatly improve the survival rate and promote the growth of seedlings under cold stress, which plays an important role in alleviating the harm brought by cold stress to seedlings. Previous studies have shown that plant epigenetic reprogramming may be more sensitive at the seedling stage. Cold stress-induced epigenetic changes affect seedling growth and development, including adjustment of metabolic pathways, synthesis of antifreeze proteins, and optimization of energy allocation [81]. Meanwhile, epigenetic reprogramming helps plant seedlings better adapt to cold stress by dynamically regulating gene expression patterns. This regulation not only affects the current generation of plants, but may also enhance the tolerance of future generations to cold stress through genetic mechanisms [81]. Certain histone modifications (such as H3K27me3 and H3K4me3) may change under cold stress to regulate gene expression related to cold response [81]. Although there is a lack of evidence on the effect of NO on epigenetic reprogramming under cold stress, it can be discussed as a research direction.

3.3. NO Enhances Cold Resistance of Fruit

Plants exposed to cold stress will inevitably show symptoms such as internal browning and fruit hardening. In recent years, studies on the reduction of cold damage by exogenous NO treatment have gradually increased. The application of NO can enhance the cold resistance of the plant, thereby reducing these symptoms. For instance, in the study by Xu et al., loquat fruits pretreated by N-Nitro-L-Arginine Methyl Ester (L-NAME, NO inhibitors) and cPTIO suffered from 1 °C cold stress for 4 days, the symptoms of cold injury were significantly exacerbated compared to control, exhibiting higher firmness and internal browning index [13]. The above results indicate that endogenous NO can resist cold stress and reduce the effects of cold injury, and it is speculated that the application of exogenous NO may have a similar effect. Such effect of NO was also confirmed experimentally by Esim and Atici [76]. Banana fruit treated with SNP was exposed to 7 °C for 7 days. It was found that the CI was 45.6% lower than that of control. At the same time, the accumulation of polyamines (PAs), γ-aminobutyric acid (GABA) and proline was enhanced. This suggests that NO can relieve freezing of bananas at cold stress [75]. The findings of a peach study indicated that exposure to SNP (25 and 50 μM) at 4 °C protects peach fruits from chilling injury through suppressing ethylene (ETH) production, maintaining firmness, antioxidant capacity and vitamin C and enhancing anti-oxidative enzyme activity (Table 1) [68]. Exogenous NO treatment can increase antioxidant enzyme activity by inhibiting the respiration rate of mango fruits [82]. Dong et al. found that when cucumbers were soaked in 0.5 g·L−1 yeast polysaccharide solution for 10 min and stored at 4 °C for 15 days, the endogenous NO content of cucumbers soaked in yeast sugar increased, and the degree of cold damage was correspondingly reduced [83]. However, in cucumbers treated with NO scavenger cPTIO and NO synthesis inhibitor, the synthesis of NO was reduced and the chilling injury of cucumber was aggravated (Table 1) [83]. The alleviating effect of NO on cold stress was also confirmed in bamboo shoots [84], zucchini [85] and other fruits.

4. Physiological Effects of NO in Alleviating Cold Stress in Plants

4.1. Increase Antioxidant Capacity

Cold stress induces in vivo S-nitrosylation of more than 240 proteins [86], whereas inappropriate histone modifications may lead to loosened or overcompressed chromatin structures, affecting DNA accessibility and gene transcription [87,88]. NO can regulate protein function through S-nitrosylation, in which NO groups covalently bind to the thiol side chain of cysteine residues in proteins [89]. NO is thought to have an antioxidant effect, which can scavenge ROS and reduce lipid peroxidation, thereby mitigating oxidative damage [90]. Under cold stress, the antioxidant system in plant cells may not be able to effectively remove all the ROS produced, resulting in a significant increase in CAT activity, but there is still a large amount of ROS that fails to be removed, thus causing harm to the pitaya seedlings [91]. When ROS accumulate in plants, they can cause damage to cellular structures, such as lipid peroxidation, protein denaturation and DNA damage [92]. NO, as a signaling molecule, can remove ROS in plants through a direct reaction, thereby reducing oxidative stress damage to plants [93]. NO can directly react with O2− to generate peroxynitrite (ONOO−), a more stable compound that reduces the direct cell damage caused by ROS [94]. NO can also react directly with H2O2 to form hydroxyl radicals (·OH), which is a more powerful oxidant, but it has a very short half-life and is usually rapidly scavenged near the site of production [95]. More importantly, endogenous and exogenous NO can indirectly scavenge ROS by regulating the activity of antioxidant enzymes [13]. However, excessive accumulation of NO can interact with ROS to form RNS, which can reduce the survival ability of poplar trees under long-term cold stress. Under cold stress conditions, NO could activate the activities of antioxidant enzymes and S-nitrosoglutathione reductase (GSNOR), thereby reducing the toxicity of ROS and RNS, and enhancing the tolerance of poplar to cold stress (Figure 2) [70,96]. Treatment of maize seeds with SNP could enhance the activities of SOD and POD in maize leaves, reduce the excessive accumulation of ROS and MDA, and improve the cold tolerance of maize (Figure 2; Table 1) [76]. Treatment of bermudagrass plants with the SNP (100 μM) at 4 °C resulted in a reduction of tissue electrolyte release due to cold stress and prevented an increase in MDAcontent, a product of lipid peroxidation within cells. SOD, POD, and CAT activities were higher in plants treated with the SNP at 4 °C (Table 1) [69]. The exposure to 15 μM SNP effectively mitigated the chilling stress in peach fruits by activating the alternate oxidase pathway, thereby enhancing the antioxidant resistance [71]. Beyond that, the application of 500 μM SNP protects the orange fruits at 3 °C by inducing antioxidant levels, reducing H2O2 content and lipid peroxidation, thereby enhancing resistance to chilling injury (Table 1) [67]. Research has demonstrated that 5-aminolevulinic acid (5-ALA) serves as a crucial plant growth regulator (PGR) that is involved in regulating growth, development, and diverse physiological responses [97]. NO and 5-ALA significantly improve the activities of SOD, CAT, ascorbate peroxidase (APX), and GR, thereby improving the cold tolerance of Elymus nutans (Table 1) [73].

4.2. Enhanced Photosynthesis

NO helps to maintain or increase chlorophyll content, ensuring adequate light capture capacity. After low temperature treatment, application of a NO donor prevents chlorophyll degradation and maintains a high maximum photochemical efficiency (Fv/Fm) of PSII [98]. NO also can reduce the damage caused by cold stress in poplar seedlings which are cultured hydroponically with cPTIO and then subjected to cold stress for 3 days. The leaf photosynthesis of control is significantly inhibited and sensitivity to cold stress is increased, as evidenced by reduced Fv/Fm fluorescence and increased ion leakage [70]. At 4 °C, 100 mM SNP alleviated chlorophyll and fluorescence reduction, decreased ion leakage and lipid peroxidation, and enhanced photosynthetic efficiency in cold-stressed walnut seedlings, thereby protecting them from oxidative damage and improving cold resistance (Figure 2; Table 1) [69]. Cold stress often leads to stomatal closure, reducing water loss but also limiting the uptake of carbon dioxide (CO2) by plants [99]. The reduction of CO2 supply directly inhibits the progress of photosynthesis and reduces the photosynthetic rate [100]. Exogenous NO can also alleviate the negative effects of low temperature stress on plant stomatal conductance through various mechanisms. In cucumber seedlings, exogenous NO significantly increased endogenous NO content and increased the initial and total activity of ribulose-1, 5-bisphosphate carboxylase/oxygenase (RuBisCO), RuBisCO carboxylation rate (Vc, max), RuBP regeneration rate (Jmax), and the total activity of ribulose-1, 5-bisphosphate carboxylase/oxygenase (Rubisco). All these indicate that NO contributes to maintaining or enhancing photosynthetic efficiency [21].

4.3. Protect Cell Membrane Structures

NO can stabilize the cell membrane structure by regulating intracellular signaling pathways. Treatment with 100 μM exogenous NO effectively reduced the increase of cell membrane permeability, significantly improved seedling growth and dry matter accumulation, and maintained the integrity of cell membrane structure in cold-wounded pumpkin seedlings [101]. NO can reduce membrane lipid peroxidation and maintain membrane integrity by scavenging free radicals or inhibiting the activity of lipid peroxidase [77]. The 15-month-old Taiwan golden Phalanthi orchid was sprayed with 200 μM SNP and treated at 12 °C/7 °C for 5 and 10 days, respectively. Studies have found that SNP can inhibit the electrolyte leakage caused by cold stress, maintain the ion balance between inside and outside cells, prevent cell dehydration and death, and protect the cell membrane system [77].

4.4. Promoting Osmoregulation

Under cold stress, NO accumulates rapidly in plants and promotes the accumulation of proline while inhibiting its degradation, thereby improving the cold tolerance of Arabidopsis (Figure 2) [64,70]. Applying SNP to cold-stressed walnut seedlings increased soluble sugar content, lowered the freezing point of the cytoplasm, prevented ice crystal formation, protected leaf cells, and enhanced cold resistance (Figure 2) [70]. It is well known that proline accumulation is necessary to improve plant cold tolerance, and the mechanism of NO in improving cold tolerance in Arabidopsis is also related to proline accumulation. In plants responding to osmotic stress, changes in histone modifications can regulate the expression of genes related to stress response. Histone acetylation is often associated with gene activation, whereas histone methylation may lead to gene silencing [102,103]. Previous studies have shown that osmotic stress-induced DNA methylation changes in rice are non-random. Genetic upregulation of P5CS and δ-Ornithine aminotransferase (δ-OAT) resulted in increased proline accumulation in rice plants even under non-stress conditions. Osmotic stress rapidly produced a heritable phenotype of high constitutive expression of related genes and proline accumulation within 1–2 generations. DNA demethylation regulates the expression of P5CS and δ-OAT, leading to their upregulation [104]. The application of SNP in walnut seedlings under cold stress could significantly increase the content of soluble sugar in seedlings, reduce the freezing point of cytoplasmic solution in leaves, prevent the condensation of cell liquid and the formation of small ice crystals to cause damage to leaves, ensure the smooth progress of metabolism in leaf cells, and improve the cold resistance of walnut seedlings (Figure 2) [70]. Moreover, the role of NO in enhancing plant response to cold stress-induced oxidative stress can be achieved by increasing the accumulation of reduced glutathione (GSH) and the ratio of reduced GSH to oxidized GSH (Table 1) [79]. A study on rice showed that arbuscular mycorrhizal fungi (AMF) can promote proline metabolism in rice at low temperature with the participation of NO. The main performance is that the secretion of AMF can enhance the glutamate pathway to stimulate the root system of host plants to release NO, and NO can further induce the host plants to release other signaling substances, such as flavonoids and cell wall polysaccharides, which can promote the growth and settlement of AMF, thus inducing the resistance of rice to cold stress [105].

5. Molecular Mechanisms of NO Alleviates Plants Cold Stress

5.1. NO Regulates Gene Expression

The exposure to cold stress induces an upregulation of NO synthesis in plants, in most instances, this effect is believed to serve as one of the crucial signals required for triggering an adaptive response [106]. Consequently, the expression of specific cold-sensitive genes such as CBF1, CBF2, CBF3, LTI30, LTI78, and COR15A has been demonstrated to be independent of the plant’s physiological state, while NO may affect the expression of these genes through post-translational modifications such as S-nitrosylation and tyrosine nitration (Table 2) [107]. In Arabidopsis, NO up-regulated the gene expression of Δ(1)-pyrroline-5-carboxylatesynthase (P5CS) and down-regulated the gene expression of proline dehydrogenase (ProDH), thereby reducing the degradation of proline and increasing its accumulation and improving the cold tolerance of Arabidopsis (Table 2) [98,108]. NO was involved in the up-regulation of LeCBF1 gene expression to protect tomato from cold injury [88]. Exogenous NO increased the expression of the PAs biosynthesis enzymes LeODC, LeADC and LeADC1 in tomato leaves under cold stress, and increased the endogenous Put (putrescine) and Spd (spermidine) levels, thereby improving the cold resistance of tomato (Table 2) [47]. CBF gene family is an important transcription factor controlling plant response and adaptation to cold stress [109]. NO can improve the cold tolerance of wild type Arabidopsis by up-regulating the expression of CBF-related cold response genes, including CBF1, CBF3, COR15A, LTI30 and LTI78 (Table 2) [108]. NO positively regulates the transcriptional activity of CmCBF1 and CmCBF3 genes, which are involved in cold-responsive pathways and contribute to cantaloupe’s tolerance against chilling injury, thereby facilitating mitigation and delayed onset of chilling injury in cantaloupe fruit [110]. Zhang et al. investigated the role of NO signaling in the cold domestication process of two alfalfa species, namely Medicago falcata (resistant alfalfa) and Medicago truncatula (low resistant alfalfa) [72]. The application of tungstate (NR inhibitor) and PTIO hindered the cold acclimation effect [111]. Treatment with NO donors and cold acclimation both contributed to enhanced cold resistance in both species. Specifically, under cold stress combined with NO donor treatment, key antioxidant enzyme genes such as Cu/Zn-SOD2, Cu/Zn-SOD3, CAT and chloroplast ascorbate peroxidase (APX1) were induced (Table 2) [112]. Previous studies have shown that phosphatidylinositol 3 kinase (PI3K)/Akt pathway and nuclear faction-B (NF-κB) are involved in the regulation of Cu/Zn-SOD expression. These two pathways are involved in the process of NO alleviating cold stress in alfalfa [113]. COR.

5.2. NO Interacts with Signaling Molecules to Alleviate Cold Stress

The unique combination of water solubility and hydrophobicity allows NO to readily diffuse through the hydrophobic bilayer of biofilms without the need for specific membrane transporters, thereby endowing NO with a distinctive role as a signaling molecule. NO can regulate plant stress resistance by interacting with various secondary messengers such as cytoplasmic Ca2+, ROS, GSH, melatonin (MT), hydrogen sulfide (H2S), and plant hormones [113,114,115,116].

5.2.1. NO Interacts with Ca2+

In the signal transduction network induced by various external environmental stimuli, Ca2+ is the second messenger of signal transduction, which can transmit extracellular signals to the cell through spatial and temporal concentration changes in the cytoplasm and be interpreted by various Ca2+ “sensitive elements” to regulate physiological reactions such as plant growth, development and stress resistance. Studies have shown that Ca2+ dependent protein kinase CPK is indirectly involved in Ca2+ mediated signal transduction by linking Ca2+ transients and downstream phosphorylation events triggered by cold stress [117]. The accumulation of ROS and NO was attenuated in OsCPK27-silenced mutant plants at cold stress [118]. Activation of MAPK cascades, such as MPK1/2, was suppressed in OsCPK27-silenced mutant plants. OsCPK17 participates in cold stress and induces NO accumulation through its potential substrate nitrate reductase 1 (OsNR1), which is involved in NO metabolism [119]. In a study on tea plant, cold-induced NO was found to be involved in the process of inhibiting pollen tube growth, resulting in abnormal distribution of organelle ultrastructure and cell wall components at the tip of pollen tube, disruption of cytoplasmic Ca2+ gradient, increase of ROS content, and acidification of cytoplasmic pH, which caused secondary and tertiary changes in organelle ultrastructure and cell wall structure (Figure 3) [75]. This eventually leads to a block in pollen tube extension [75]. But cPTIO could alleviate this destruction [75]. This suggests that Ca2+ is closely related to NO in plant response to cold stress.

5.2.2. NO Interacts with ROS

NO signal can directly interact with ROS to regulate abiotic stress damage in plants [120]. NO anabolism also affects ROS levels, indicating that NO and ROS interact as signaling molecules (Figure 3) [121]. Elevated levels of NO/ROS are linked to impaired plant antioxidant systems, and maintaining a balanced NO/ROS homeostasis is crucial for optimal nitrogen nutrition and plant immunity [122]. These processes are mainly regulated by NR, and NR activity plays an important role in mediating NO signaling after stress induction. As a type of ROS, H2O2 has been shown to play a dual role in plant responses to cold stress, as both a signaling molecule and a toxic compound [123]. Previous studies have shown that NO can enhance the activities of dehydroascorbic acid reductase (DHAR) and glutathione S-transferase (GST) through S-nitrosylation under cold stress conditions and promote the detoxification of H2O2 [124]. NO can enhance the activity of antioxidant enzymes, such as CAT, which can detoxify H2O2 in cucumber [31]. Similarly, NO could also inhibit the accumulation of H2O2 and thus alleviate chilling injury. For instance, in Elymus nutans, the synergistic application of NO and 5-ALA can significantly decrease electrolyte leakage, MDA accumulation, and H2O2 content, thereby alleviating cold stress-induced damage to plants [73]. Similar results have been reported for cantaloupe, zucchini, and fresh vegetable grapes [85,86,110]. In conclusion, the crosstalk between NO and H2O2 signaling pathways is critical for plant response to postharvest cold stress.

5.2.3. NO Interacts with GSH

GSH is a group of important reducing substances in plants, which can remove ROS in plants. Under cold stress, NO directly reacts with glutathione to form GSNO (S-nitroso glutathione), which can stably provide NO to plants (Figure 3) [69]. This conclusion was tested in a study on alfalfa. Zhang et al. showed that exogenous addition of 100 μM diethylamine NONOate diethylamine salt (DEA, NO donor) could increase the total glutathione level in mesophyll cells of both cold tolerant and intolerant alfalfa plants under 5 °C [111]. Both NR inhibitors or NO scavengers reduced cold-induced total GSH levels [111]. Recalcitrant Baccaurea ramiflora seeds showed sensitivity to low temperature stress (−8 °C), while exogenous 2,2′-(hydroxynitrosohydrazino)-bis-ethanamine (NOC-18; NO donor) treatment significantly increased the activity of GSH accumulation GSNOR, enhanced the activities of antioxidant enzymes involved in the glutathione ascorbic acid (AsA) cycle, reduced the contents of H2O2 and RNS, and improved the tolerance of seeds to low temperature stress (Table 1) [63]. Conversely, inhibiting NO production, removing GSH, or blocking GSNOR activity resulted in increased ROS and RNS and impaired seed germination under low temperature stress [63].

5.2.4. NO Interacts with MT

MT, as a novel amine-derived hormone, plays a significant role in various aspects of plant physiology including growth, development, senescence, and responses to abiotic stress. Specifically, under cold stress conditions, MT is actively involved in regulating membrane integrity, stomatal conductance, photosynthetic efficiency, antioxidant defense mechanisms, redox homeostasis, accumulation of osmoregulatory substances, hormonal levels, secondary metabolites, and the expression of stress-responsive genes (Figure 3) [125,126]. Studies on cucumber showed that about 100 μM MT significantly increased NR activity, NR-related messenger RNA (mRNA) expression and endogenous NO accumulation in cucumber seedlings under cold stress (5 °C) [74]. The SNP (75 μM) did not significantly affect the expression of genes critical for MT synthesis and endogenous MT levels [74]. MT and SNP reduced the electrolyte leakage (EL), MDA, and ROS accumulation in cucumber seedlings by activating the antioxidant system (Table 1) [74]. MT and SNP also enhanced photosynthetic carbon assimilation. In addition, exogenous MT and SNP significantly upregulated the expression of CBF expression inducer (ICE1), C Repeat Binding Factor (CBF1), and Cold Response gene (COR47) [74]. It is worth noting that cPTIO inhibited MT-induced cold tolerance, whereas p-chlorophenylalanine (p-CPA), an mt synthesis inhibitor, did not affect NO-induced cold tolerance, suggesting that NO acts as a downstream signal in MT-induced plant tolerance to cold stress [74]. A study on litchi demonstrated that the application of exogenous MT to litchi fruit significantly enhanced cold tolerance, thereby reducing the incidence of CI. This effect may be attributed to the activation of the antioxidant system and the improvement in the repair capacity of oxidatively damaged proteins [127]. The combined treatment of melatonin and a NO scavenger (cPTIO) significantly impaired the regulation of melatonin in physiological and biochemical processes related to cold tolerance in litchi fruits [127]. Melatonin treatment enhanced endogenous NO production in litchi fruits by activating NR and NOS-dependent pathways, which may contribute to the increased S-nitrosylation level of proteins [127]. These results suggest that endogenous NO may be involved to some extent in melatonin-induced cold tolerance of litchi fruit and may be involved in the regulation of redox status [127].

5.2.5. NO Interacts with ABA

Sometimes, the interaction of NO with some plant hormones can also enhance the tolerance of plants to cold stress. In some cases (stomatal regulation, seed dormancy and germination, expression and transcription of antioxidant oxidase genes), NO is thought to play a crucial role in ABA-mediated signaling pathways [118,128,129]. Other studies have shown that ABA can enhance cold resistance in plants by regulating the biosynthesis of NO [130]. Exogenous ABA (100 μM) solution could increase NO content of peach fruit during storage at 0 °C through the NR pathway but not the NOS-like pathway. Exogenous NO does not regulate ABA biosynthesis, but it can increase endogenous NO content through the NR pathway. It was also found that NO scavenger 2-(4-carboxyphenyl)-4,4,5, 5-tetramethylimidazoline 1-oxo-3-oxide (cPTIO) and NR inhibitor tungstate partially blocked the protective effect of ABA on peach fruits stored at low temperature. This seems to indicate that ABA acts upstream of NO production in peach fruits [131,132]. ABA stimulates the production of H2O2 in protective cells, which then triggers endogenous NO synthesis, thus promoting stomatal closure in protective cells (Figure 3) [47]. Closing stomata reduces excessive water loss and thus maintains intracellular water balance, which is essential to prevent cell freezing damage. Stomatal closure can regulate a series of physiological responses in plants, such as increasing Ca2+ influx in the cytoplasm and triggering the expression of cold-responsive genes, which contribute to the enhancement of plant tolerance to low temperature [133].

5.2.6. NO Interacts with ETH

Accumulating evidence also suggests a close interaction between NO and ETH, two gas transmitters, in fruit cold hardens. Different doses of NO fumigation treatments (nitrogen, 10–40 µL L−1) significantly reduced ETH production during fruit ripening after 2 and 4 weeks of refrigeration, reduced chilling damage, delayed fruit color development, and significantly reduced softening and ripening of refrigerated mango fruits [65]. Similar changes were observed in pear (Pyrus bretschneideri). After 60 days of NO (20 µL L−1) fumigation at 0 °C, the ETH yield and soluble sugar content decreased, while fruit softening and ripening were concurrently delayed [66]. Some studies also found that after 4 weeks of NO fumigation, the ETH and antioxidant enzymes (SOD; CAT; POD) activity was decreased, while sucrose phosphate synthase activity was increased, resulting in higher sucrose content in peach fruits [134]. A substantial body of research has demonstrated that the postharvest application of NO inhibits senescence in Japanese plums [135], peach [136], and mango [65,137]. In addition, 1-methylcyclopropene (1-MCP) and ETH can inhibit endogenous NO production by reducing NOS activity in peaches [138]. Thus, antagonism between NO and ETH plays a crucial role in fruit refrigeration, delaying many aspects of fruit aging and affecting fruit quality.

5.2.7. NO Interacts with H2S

H2S and NO are two signaling molecules that play an important role in a variety of physiological processes, and their direct interaction can effectively relieve cold stress. The application of H2S promoted the production of endogenous NO and increased the activities of NOS-like and NR, while changing the activity of GSNOR, which induced the cold hardinness of peach fruit [139]. Exogenous NO reduced endogenous H2S content by decreasing the activities of L-/D-cysteine desulfurase (L-/D-CD), O-acetylserine (thiol) lyase (OAS-TL), and sulfite reductase (SiR). The NO scavenger c-PTIO and the inhibitor of NO synthesis reversed the effect of NO on H2S metabolism in refrigerated peach [140]. In the study by Wu et al., pretreatment with NaHS and SNP reduced MDA content, H2O2 accumulation and O2− generation rate induced by cold stress at 5 °C [141]. The activities and mRNA abundance of SOD, POD, APX and glutathione reductase (GR) were higher than those of the water treatment. NaHS and SNP enhanced the accumulation of AsA and GSH, and mitigated the decline in the AsA/DHA and GSH/GSSG ratios in stressed seedlings, thereby alleviating oxidative damage [141]. The ASA-GSH cycle, also known as the ascorbic acid-glutathione cycle, is a key antioxidant pathway in plant cells that plays a central role in scavenging ROS and maintaining cellular redox homeostasis [142]. This cycle mainly occurs in multiple cellular compartments of plant cells, including chloroplasts, cytoplasm and peroxisomes [143]. Conversely, pretreatment with the H2S scavenger hypotaurine (HT) and the NO scavenger hemoglobin (Hb) prior to hypothermic stress exacerbated these injury symptoms [141]. These results suggest that H2S can alleviate cold stress by enhancing the antioxidant system of cucumber seedlings, which is related to the interaction of NO signaling [141]. However, the interaction of other signaling molecules with NO under cold stress is unclear and needs further study.

6. Challenges of NO in Agricultural Production Practices

As a gas signaling molecule, NO has been widely reported, and the mechanism by which it alleviates cold stress has been extensively studied. Although we mentioned in the introduction that NO plays an important role in plant growth and lower stress, there are some limitations and challenges in using NO to improve plant cold tolerance in agricultural production. Regarding application techniques, NO can be administered through various methods such as spray, irrigation, or soil application. Each method differs in terms of uptake efficiency and its impact on plant physiology, making it challenging to select the most suitable approach. Commonly used NO donors (such as SNP) are susceptible to light, heat, and microbial degradation when sprayed, resulting in rapid failure of the active ingredient. Strong light, high humidity or frost accompanied by low temperatures may change the adhesion and penetration efficiency of foliar spray. Frost covering leaves may hinder spray absorption. Traditional spraying equipment can lead to uneven distribution of agents, and variable spraying technology can improve efficiency, but the current penetration rate is low and the equipment cost is high. The concentration of NO must be meticulously controlled. An excessively high concentration may exert toxic effects on plants, whereas an insufficiently low concentration will fail to achieve the desired outcomes. Excess NO can be oxidized to nitrite in plants (NO2−). When the concentration of nitrite exceeds the metabolic capacity of the plant, it can accumulate and cause toxic reactions, such as destroying chloroplast structure, inhibiting photosynthesis, and even leading to apoptosis. Excessive NO may also inhibit rhizosphere beneficial flora activity, destroy nitrogen cycle balance, and long-term use may lead to soil degradation. The optimal application frequency of NO may vary among different crops, different growth stages, and different environmental conditions. Therefore, further studies are needed to determine the optimal frequency of NO application to ensure its effectiveness and efficiency in agricultural production. The stability of NO in the environment is poor, and it is easy to react with other molecules to form other compounds, which affects its effect in practical use. The environmental impact of NO also faces challenges. NO is a kind of atmospheric pollutant. In the process of denitrification, NO is the intermediate product of N2O. High concentration of NO in soil may inhibit the activity of N2O reductase, resulting in an increase in N2O emissions. NO metabolites (such as nitrates) may accumulate in agricultural products, and residues need to be strictly monitored to meet food safety standards. NO is expensive to produce and store, which makes its application in agricultural production more difficult. Although NO can improve crop cold tolerance, its economic benefits need to be further verified in large-scale applications. Against the backdrop of escalating global climate change, the compounded stresses from multiple factors, such as the concurrent effects of cold and drought, are exerting increasingly detrimental impacts on crop growth, development, and yield formation. Besides the use of exogenous NO, there are many other measures that can be used to alleviate cold stress in agricultural production, such as adjusting planting time, selecting cold resistant varieties, and improving soil conditions. However, the synergy between these measures and exogenous NO is unknown. How to effectively deal with multiple combined stresses and improve crop tolerance through NO or other means is a big challenge.

7. Conclusions and Perspectives

NO functioning as a key gas transmitter, plays a crucial role in regulating the adaptive response of plants to cold stress, which involves a complex whole-cell signaling process. In this process, the production of NO can promote the synthesis of SOD, POD, CAT and APX and GR, thereby reducing the levels of H2O2 and O2− and alleviating plant chilling injury. The increase of proline content, the enhancement of photosynthetic capacity and the regulation of glucose metabolism were also significantly affected by NO and played an important role in this process. NO also regulates plant cold tolerance through interactions with cytoplasmic Ca2+, ROS, GSH, MT, ABA, ETH and H2S. The expression of genes related to NO synthesis, cold response and antioxidant was up-regulated or down-regulated by NO, leading to the improvement of plant cold resistance. These complex links undoubtedly demonstrate the importance of NO to plants under cold stress, so it is very important to study its role and mechanism.
There exist diverse approaches to generate NO, particularly in the enclosed greenhouse. NO gas exerts a considerable influence on vegetables and crops. The utilization of chemical pesticides and fertilizers in the greenhouse, the employment of traditional heating equipment, and the activity of soil microorganisms are the principal causes for the higher NO content in the greenhouse compared to the outdoor environment. However, limited research has been conducted on the impact of NO gas on vegetables within controlled gaseous environments in facilities. At present, the regulation of NO synthesis by plant rhizomes and its effects on host cold resistance have not been clarified. In the future, it is possible to study how the microbiome remodels plant immune and cold resistance gene expression through NO signaling. Meanwhile, the effect of NO on DNA methylation and histone modification, as well as the role of non-coding RNAs (such as miRNAs and lncRNAs) in NO signaling have not been clarified. The current NO donor (such as SNP) has problems such as uncontrolled release, toxicity and side effects. In the future, precise delivery systems of NO based on synthetic biology can be designed, using a photosensitive promoter (such as phyB) or a low-temperature responsive promoter (such as CBF) to regulate the spatiotemporal expression of NO synthase genes. Biodegradable nanoparticles loaded with NO precursors can also be developed to achieve low temperature triggered release. Plants may translate short-term NO signals into long-term cold-resistance adaptation through epigenetic modification, but the exact mechanism is unknown. Whether NO, by regulating SiRNA-mediated epigenetic inheritance across generations (such as the RdDM pathway), enables offspring to retain cold resistance even when they do not experience low temperature stress. Based on the exploration of molecular mechanisms, it is feasible to develop NO-containing fertilizers in agricultural production to improve the cold resistance of plants. NO can be combined with osmoregulatory substances, hormones or microbial bacteria to form a multi-effect cold resistant formula, while NO composite fertilizers containing growth promoting bacteria can be developed. Different crops may have different response mechanisms to NO, and specific studies should be carried out for major cash crops. The duration of low temperature and light intensity may affect the NO release efficiency, so it is necessary to design an environmentally responsive fertilizer. Future research needs to break through the traditional signaling pathway framework and focus on the intersection of NO with novel molecules, microbiome, synthetic biology tools, and cross-generation inheritance.

Author Contributions

C.L. contributed to the study conception and design. The writing of the first draft of the manuscript and the drawing of the pictures were performed by J.C. References collection was performed by M.H. Table were made by J.Q. The manuscript was revised by W.Y. and C.L. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the National Nature Science Foundation of China (31660568), Guangxi science and technology major project (GuikeAA22068088) and start-up funding for introduced talents in Guangxi University (to C.L.). Inclusive support policy for young talents, scientific research start-up funds (to C.L.). The Guangxi Colleges and Universities Young and Middle-aged Teachers’ Basic Scientific Research Ability Improvement Project (2024KY0010), Guangxi Graduate Education Innovation Program (YCSW2024093), the Guangxi University Student Innovation and Entrepre-neurship Training Program Funding Project (202310593704; 202310593714; 202410953044S).

Data Availability Statement

There are no new data associated with this article.

Conflicts of Interest

The authors declare no conflicts of interest.

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Agronomy 15 01072 g001
Figure 1. The endogenous NO synthesis pathway in plant. NO, nitric oxide; NO2−, nitrite ion; NO3−, nitrate ion; N2, nitrogen; NH4+, ammonium ion; N2O, nitrous oxide; NO2, nitrogen dioxide; NR, nitrate reductase; NOS, nitric oxide synthase. Symbol explanations: “→” indicates facilitation, dotted arrows indicate that this process is yet to be verified. Symbols are used for all figures, and following is the same.
Figure 1. The endogenous NO synthesis pathway in plant. NO, nitric oxide; NO2−, nitrite ion; NO3−, nitrate ion; N2, nitrogen; NH4+, ammonium ion; N2O, nitrous oxide; NO2, nitrogen dioxide; NR, nitrate reductase; NOS, nitric oxide synthase. Symbol explanations: “→” indicates facilitation, dotted arrows indicate that this process is yet to be verified. Symbols are used for all figures, and following is the same.
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Agronomy 15 01072 g002
Figure 2. NO can regulate the antioxidant system of plants by increasing the activity of antioxidation-related enzymes, reducing ROS accumulation and lipid peroxidation, thus alleviating cold stress. ROS, reactive oxygen species; H2O2, hydrogen peroxide; O2−, superoxide anion; MDA, malonaldehyde; RNS, reactive nitrogen species; SOD, superoxide dismutase; CAT, catalase; APX, ascorbate peroxidase; GPX, glutathion peroxidase; AsA, ascorbic acid; GSH, glutathione. Meanwhile, cold stress caused the decrease of chlorophyll content, and NO inhibited the decrease of chlorophyll. RCC, red chlorophyll catabolite; pFCC, primer fluorescent chlcatabolite. Cold stress decreased proline content, and NO promoted proline accumulation by regulating genes related to proline synthesis and degradation. Glu, glutamic acid; P5CS, Δ1-pyrroline-5-carboxylate synthetase; P5CDH, Δ1-pyrroline-5-carboxylate dehydrogenase; Orn, ornithine; OAT, ornithine aminotransferase; Glutamyl semi-aldehyde; P5CR, Δ1-pyrroline-5-carboxylate reductase; proline dehydrogenase; P5C, Δ1-pyrroline-5-carboxylic acid. Symbol explanations: “→” indicates facilitation, blocking line “┫” indicated inhibition.
Figure 2. NO can regulate the antioxidant system of plants by increasing the activity of antioxidation-related enzymes, reducing ROS accumulation and lipid peroxidation, thus alleviating cold stress. ROS, reactive oxygen species; H2O2, hydrogen peroxide; O2−, superoxide anion; MDA, malonaldehyde; RNS, reactive nitrogen species; SOD, superoxide dismutase; CAT, catalase; APX, ascorbate peroxidase; GPX, glutathion peroxidase; AsA, ascorbic acid; GSH, glutathione. Meanwhile, cold stress caused the decrease of chlorophyll content, and NO inhibited the decrease of chlorophyll. RCC, red chlorophyll catabolite; pFCC, primer fluorescent chlcatabolite. Cold stress decreased proline content, and NO promoted proline accumulation by regulating genes related to proline synthesis and degradation. Glu, glutamic acid; P5CS, Δ1-pyrroline-5-carboxylate synthetase; P5CDH, Δ1-pyrroline-5-carboxylate dehydrogenase; Orn, ornithine; OAT, ornithine aminotransferase; Glutamyl semi-aldehyde; P5CR, Δ1-pyrroline-5-carboxylate reductase; proline dehydrogenase; P5C, Δ1-pyrroline-5-carboxylic acid. Symbol explanations: “→” indicates facilitation, blocking line “┫” indicated inhibition.
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Figure 3. NO interacts with Ca2+, GSH, ROS, MT, H2S and ABA to improve cold resistance of plants. Ca2+, calcium ions; Cyt, cytoplasm, GSH, glutathione; GSNO, S-nitrosoglutathione; NR, nitrate reductase; NOS, nitric oxide synthase; ROS, reactive oxygen species; RNS, reactive nitrogen species; H2O2, hydrogen peroxide; H2S, hydrogen sulfide; ABA, abscisic acid; MT, melatonin; NCED, 9-cis-epoxycarotenoid dioxygenase; HT, hypotaurine; Hb, hemoglobin; H2S, hydrogen sulfide. Symbol explanations: “→” indicates facilitation, blocking line “┫” indicated inhibition, dotted arrows indicate that this process is yet to be verified.
Figure 3. NO interacts with Ca2+, GSH, ROS, MT, H2S and ABA to improve cold resistance of plants. Ca2+, calcium ions; Cyt, cytoplasm, GSH, glutathione; GSNO, S-nitrosoglutathione; NR, nitrate reductase; NOS, nitric oxide synthase; ROS, reactive oxygen species; RNS, reactive nitrogen species; H2O2, hydrogen peroxide; H2S, hydrogen sulfide; ABA, abscisic acid; MT, melatonin; NCED, 9-cis-epoxycarotenoid dioxygenase; HT, hypotaurine; Hb, hemoglobin; H2S, hydrogen sulfide. Symbol explanations: “→” indicates facilitation, blocking line “┫” indicated inhibition, dotted arrows indicate that this process is yet to be verified.
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Table 1. Recent works associated with exogenous NO during cold stress in plants.
Table 1. Recent works associated with exogenous NO during cold stress in plants.
TemperatureTreatmentPlants UsedImpactReference
−8 °CNOC-18 (30 Μm)Baccaurea ramifloraIt increased the GSH and GSNOR accumulation activities in Bacillus goatensis embryos, enhanced the activities of antioxidant enzymes involved in glutathione ascorbic acid cycle, reduced the contents of H2O2 and RNS, and improved the tolerance of seeds to low temperature stress[63]
−7 °CSNP (200 μM)ArabidopsisSNP effectively increased the survival rate of Arabidopsis seedlings.[64]
0 °CNitric oxide (10/20/40 µL L−1)MangoReduced ETH production during fruit ripening after cold storage, reduced cold storage damage, delayed fruit color development, and significantly reduced softening and ripening of refrigerated mango fruits.[65]
0 °CNitric oxide (20 µL L−1)MangoAfter 60 days of NO fumigation, ETH production and soluble sugar content decreased, and fruit softening and ripening were simultaneously delayed.[66]
3 °CSNP (500 μM)Citrus sinensis L.Induced antioxidant levels, decreased H2O2 content and lipid peroxidation levels. [67]
4 °CSNP (25/50 μM)Prunus persica L.Suppressing ETH production, maintaining firmness, antioxidant capacity and vitamin C and enhancing anti-oxidative enzyme activity[68]
4 °CSNP (100 μM)BermudagrassThe activities of SOD, POD and CAT were increased.[69]
4 °CSNP (100 mM)WalnutAlleviated the decrease of and chlorophyll fluorescence parameters, reduced ion leakage and lipid peroxidation, improved photosynthetic efficiency, increased GSH and GSH/GSSG ratio, promoted proline accumulation and inhibited proline degradation.[70]
4 °CSNP (15 μM)Prunus persica L.The alternate oxidase pathway is activated, thereby increasing antioxidant levels.[71]
5 °CSNP (100 μM)AlfalfaExogenous addition of 100 μM diethylamine NONOate diethylamine salt (DEA, NO donor) increased total glutathione levels in mesophyll cells of both cold tolerant and cold intolerant alfalfa.[72]
5 °CSNP (100 μM)Elymus nutansElymus nutans seedlings showed significant increases in root surface area, root volume, root diameter, and root tip number and the activities of SOD, CAT, APX and GR were increased.[73]
5 °CSNP (75 μM)CucumberMT and SNP interacted to reduce electrolyte leakage (EL), MDA and ROS accumulation in cucumber seedlings by activating antioxidant system.[74]
7 °CSNP (50 μM)BananaThe chilling index was decreased, and the accumulation of PAs, GABA and proline was enhanced.[75]
10/7 °CSNP (0.1 μM)MaizeThe CI of leaves was decreased in the SNP treatment and the activities of SOD and POD were increased, and the accumulation of ROS and MDA was reduced.[76]
10 °CSNP (200 μM)TomatoSNP treatment significantly increased the amylase activity and soluble sugar content of tomato seeds, and improved the low temperature tolerance of tomato seeds.[59]
12 °C/7 °CSNP (200 μM)Phalanthi orchidSNP can inhibit electrolyte leakage caused by cold stress, maintain intracellular and extracellular ion balance, prevent cell dehydration and death, and protect the cell membrane system.[77]
12 ± 0.5 °CSNP (100 μM)Winter wheatSNP effectively alleviated the inhibition of cold stress on seed germination and increased germination rate, germination index, radicle and coleoptile length of seeds under cold stress.[60]
15 °CSNP (300 μM)Brassica napus L.The cold resistance of rapeseed was significantly improved, thus the seed germination rate was increased[58]
Notes: NOC-18, 2,2′-(hydroxynitrosohydrazino)-bis-ethanamine, NO donor; SNP, sodium nitroprusside; GSH, glutathione; H2O2: hydrogen peroxide; RNS, reactive nitrogen species; ETH, ethylene; SOD, superoxide dismutase; CAT, catalase, POD, peroxidase; APX, ascorbate peroxidase; GR, glutathione reductase; EL, electrolyte leakage, MDA, malondialdehyde; ROS, reactive oxygen species; MT, melatonin; PAs, polyamines; GABA, γ-aminobutyric acid; CI, chilling index.
Table 2. Overview of NO regulated genes under cold stresses in plants.
Table 2. Overview of NO regulated genes under cold stresses in plants.
Gas MoleculeSpeciesGeneExpressionFunctionReference
NOArabidopsisP5CS↑Positive[108]
ArabidopsisProDH↓Positive[98]
TomatoCBF1↑Positive[107]
ArabidopsisCBF1, CBF3,↑Positive[108]
COR15A, LTI30, LTI78
TomatoODC, ADC, ADC1↑Positive[47]
CantaloupeCmCBF1, CmCBF3↑Positive[110]
Medicago falcataCu/Zn-SOD2, Cu/Zn-SOD3, CAT APX1↑Positive[112]
Notes: NO, nitric oxide. “↑”, up-regulate; “↓”, down-regulate.
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Cui, J.; Huang, M.; Qi, J.; Yu, W.; Li, C. Nitric Oxide in Plant Cold Stress: Functions, Mechanisms and Challenges. Agronomy 2025, 15, 1072. https://doi.org/10.3390/agronomy15051072

AMA Style

Cui J, Huang M, Qi J, Yu W, Li C. Nitric Oxide in Plant Cold Stress: Functions, Mechanisms and Challenges. Agronomy. 2025; 15(5):1072. https://doi.org/10.3390/agronomy15051072

Chicago/Turabian Style

Cui, Jing, Mengxiao Huang, Jin Qi, Wenjin Yu, and Changxia Li. 2025. "Nitric Oxide in Plant Cold Stress: Functions, Mechanisms and Challenges" Agronomy 15, no. 5: 1072. https://doi.org/10.3390/agronomy15051072

APA Style

Cui, J., Huang, M., Qi, J., Yu, W., & Li, C. (2025). Nitric Oxide in Plant Cold Stress: Functions, Mechanisms and Challenges. Agronomy, 15(5), 1072. https://doi.org/10.3390/agronomy15051072

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