Salinity is a main stress-limiting agricultural production. Feeding over 9.3 billion populations in 2050 is a big challenge. It is estimated that in 2050, agricultural production needs to be increased over 60% at the 2005–2007 level (Fita et al., 2015). However, efficient agricultural production is always threatened by stress conditions such as salinity. In recent years, climate change, seawater backflow, groundwater infiltration, and human-being activities such as irrigation and fertilizer application increased salt concentration in soil, resulting in soil salinization (Zhang et al., 2016; Qian et al., 2021). Soil salinization inhibits plant growth, yield, and product quality (Yang and Guo, 2018a). While more than 950 million hectares of land are affected by salinity stress, the trend of soil salinization is increasing (Yang and Guo, 2018b).

The main components of salt stress in plants are osmotic stress, ionic stress, and secondary stress, i.e., ROS over-accumulation (Parihar et al., 2015; Morton et al., 2018). Firstly, upon the onset of salt stress, high salinity reduces the water potential around the plant roots, limiting root absorption of water (Negrão et al., 2016). Secondly, over-accumulation of sodium and chloride in plants causes ion toxicity. It not only disrupts ion homeostasis such as Na⁺ and K⁺ homeostasis (Zhu, 2002), but also hinders the efficient uptake of nutrient elements such as Ca²⁺, resulting in the lack of essential nutrients in plants (Zhang et al., 2017; Wu, 2018a; Li et al., 2021). Osmotic and ionic stresses lead to over-accumulation of reactive oxygen species (ROS) in plants, resulting in oxidative stress (Zhu, 2016; Wu et al., 2018b). For example, excessive superoxide anion (O₂⁻) and hydrogen peroxide (H₂O₂) are accumulated in chloroplasts and mitochondria, affecting photosynthesis and respiration of plants under salt stress (Balal et al., 2011). Moreover, the structure of macromolecules such as DNA and protein can be damaged by excessive ROS (Hu et al., 2021; Liu et al., 2021a). Nowadays, besides genetic engineering and exogenous application of antioxidants, nanomaterials showed good potential in improving plant salt tolerance although the underlying mechanisms are less addressed. Nano-enabled plant salt tolerance could be an alternative approach to help to enable efficient agricultural production.

In this review, we summarized the molecular mechanisms underlying plant salt tolerance and emphasized the importance of nanotechnology in improving plant salt tolerance. We hope this review will set up an idea to help the researchers in plant science and nanoscience to better understand possible new approaches to address issues such as salinity in agriculture.

In recent years, plant nano-biotechnology approach showed good potential to improve plant stress tolerance. Nano-enabled agriculture is a hot research topic. Nanotechnology refers to the technology of manipulating materials with a basic structure of 1–100 nm in at least one dimension (Farokhzad and Langer, 2009). The history of adoption of nanotechnology in agriculture is relatively short, but it showed great potential in agriculture, such as the development of nano-fertilizer, nano-pesticides, and smart plant construction (Giraldo et al., 2019; Kah et al., 2019). As an emerging strategy to promote agricultural production, plant nanotechnology shows good potential in agriculture, such as seed treatment and germination, plant growth and development, pathogen diagnosis, genetic engineering, plant stress tolerance, crop nutrition, and detection of toxic agrochemicals (Farooq et al., 2012; Bui, 2013; Kah et al., 2019). In recent years, use of nanomaterials (NMs) to enhance plant stress tolerance showed the potential to become an economical, effective, and sustainable strategy for efficient agricultural production. NMs enhance plant tolerance to salt by protecting plant photosynthesis, enabling ROS detoxification, and alleviating osmotic and ionic stress (Gao et al., 2007; Rico et al., 2015; Khan et al., 2016a). Nano-enabled plant salt tolerance has been reported in many species, including Arabidopsis, wheat, cotton, and so on (Mushtaq et al., 2017; Michael et al., 2018; Liu et al., 2021b). To date, the used nanomaterials which improved plant salt tolerance include silica nanoparticles, cerium oxide nanoparticles, put-carbon quantum dots (put-CQD) nanoparticles, titanium dioxide nanoparticles, carbon nanotubes, and nano-zinc (Figure 1). For example, multi-walled carbon nanotubes (MWCNTs), cerium oxide nanoparticles, and zinc oxide nanoparticles (SeNPs and ZnONPs) can significantly alleviate the inhibition of salt stress on the growth of rapeseed seedlings. Seed priming using cerium oxide nanoparticles, SeNPs and ZnONPs, also significantly improves the germination rate of rapeseed seeds under salt stress (Rossi et al., 2017; Zhao et al., 2019; El-Badri et al., 2021; Khan et al., 2021; Li et al., 2022). For more details, please refer to Table 1.

As mentioned in Table 1, many nanomaterials are used to improve plant salt tolerance. Among them, cerium oxide nanoparticles (nanoceria) are one of the widely used nanomaterials. Thus, here, we used nanoceria as example to discuss how nanomaterials can help to improve plant salt tolerance. Nanoceria are known as nanozyme and potent catalytic ROS (reactive oxygen species) scavenger, having a large number of surface oxygen vacancies which can convert ROS, i.e., H₂O₂, O₂⁻, and ^•OH to its non-radical counterparts. To date, the mechanisms behind nanoceria improved plant salt tolerance (Figure 2) are: (1) maintaining ROS homeostasis via direct scavenging of ROS or modulating antioxidant system (Rossi et al., 2017; Wu et al., 2018c), (2) improving mesophyll cells’ ability to retain K⁺ (Wu et al., 2018d), (3) improving shoot Na⁺ exclusion ability to avoid over-accumulation of Na⁺ in leaf (Liu et al., 2021a), (4) improving the production of gas signaling molecules, i.e., NO (nitric oxide; Zhou et al., 2021), (5) increasing α-amylase activities to improving seed germination (Khan et al., 2021), (6) decreasing lipoxygenase activities to reduce membrane oxidative damage (Li et al., 2022 ES Nano), and (7) allowing Na⁺ being transported to shoot via shortening root apoplastic barriers (Rossi et al., 2017). Some of these mechanisms might be shared between different nanomaterials in terms of improving plant salt tolerance. For example, Mn₃O₄ nanoparticles scavenged over-accumulated ROS to improve salt tolerance in cucumber (Lu et al., 2020). Zinc oxide nanoparticles modulated the activities of antioxidant enzymes to help to maintain ROS homeostasis in tomato plants (Faizan et al., 2021). These results suggested that in different nanomaterials can execute similar role to improve salt tolerance in varied plant species. Further, MWCNTs increased rapeseed plants’ ability to tolerate salinity by maintaining Na⁺/K⁺ ratio (Zhao et al., 2019). This is similar to the findings that nanoceria can help to maintain Na⁺/K⁺ ratio to improve cotton salt tolerance (Liu et al., 2021a), further confirming that some common mechanisms might be employed in nano-enabled plant salt tolerance. More efforts are needed to investigate what are the commonly employed mechanisms in nano-enabled plant salt tolerance and what are the mechanisms specially associated with one or few types of nanomaterials.

Reactive oxygen species (ROS) mainly include superoxide anion (O₂⁻), hydrogen peroxide (H₂O₂), hydroxyl radical (•OH), and singlet oxygen (¹O₂). Under normal conditions, there is a dynamic balance between the production and scavenging of ROS in plant cells. When plants are subjected to salt stress, apoplast and organelles such as chloroplasts and mitochondria accumulate excessive ROS, which in turn results in lipid peroxidation and damage of the structure of DNA and protein, causing oxidative stress (Mignolet-Spruyt et al., 2016; Wang et al., 2017; Jia et al., 2020). ROS scavenging in plants mainly involves the antioxidant enzyme system and the non-enzymatic system. The former one mainly includes superoxide dismutase (SOD), peroxidase (POD), catalase (CAT), ascorbate peroxidase (APX), and glutathione peroxidase (GPX), and the latter one mainly includes ascorbic acid, glutathione, vitamin E, carotenoid, and mannitol (Deinlein et al., 2014; Liang et al., 2017; Irshad et al., 2021; Li et al., 2021). SOD mainly catalyzes O₂⁻ to produce H₂O₂ and O₂. This process was often regarded as the first defense for plants to scavenge excessive ROS (Zhu, 2002, 2016). POD, CAT, and APX mainly scavenge H₂O₂ accumulated in plants (Petridis et al., 2012; Hou et al., 2016; Liu et al., 2020). After being subjected to salt stress, the activity of antioxidant enzymes in salt tolerant plants is generally higher than the sensitive ones (Zhu, 2002, 2016; Wu et al., 2020). Overexpression of GhSOD1 and GhCAT significantly improves salt tolerance of cotton (Luo et al., 2000). Similarly, applying nanozymes with ROS scavenging ability in plants helped to improve plant salt tolerance via maintaining ROS homeostasis (Wu, 2018a; Wu et al., 2018c; Zhao et al., 2020). For example, nanozyme poly(acrylic) acid-coated cerium oxide nanoparticles (PNC) can improve salinity stress tolerance of cotton mainly by alleviating ROS accumulation in seedling roots (An et al., 2020). Similar results were also found in wheat (Mushtaq et al., 2017), tomato (Faizan et al., 2021), soybean (Farhangi-Abriz and Torabian, 2018), and rapeseed (Khan et al., 2021). Carbon quantum dots can significantly improve the activity of antioxidant enzyme system to reduce the content of ROS and to alleviate oxidative damage on cell membrane, thus enhancing grape salt tolerance (Gohari et al., 2021). Cucumber plants with foliar-delivered Mn₃O₄ nanoparticles showed less ROS accumulation and better salt tolerance than the control without nanoparticles (Lu et al., 2020). Spraying zinc oxide NMs on leaves can also significantly improve the protein content and antioxidant enzyme activity of POX, SOD, and CAT in tomato plants under salt stress (Faizan et al., 2021). It was found that compared with salt control, zinc oxide NMs upregulated the expression levels of SOD and GPX genes in tomato under salt stress (Alharby et al., 2016). Thus, improving the ability to maintain ROS homeostasis could be one of the important mechanisms under nano-enabled plant salt tolerance.

Nanomaterials might also improve plant salt tolerance via modulating the production of antioxidants. Glutathione, proline, and ascorbic acid are important soluble antioxidants in plant cells, playing an important role in maintaining ROS homeostasis in cells (Zhu, 2002). (1) Reduced glutathione (GSH) is a widely distributed antioxidant in cells. The dynamic balance between GSH and oxidized glutathione is also an important indicator of the antioxidant capacity of plant cells (Hameed et al., 2014). Indeed, exogenously applied GSH can improve salt tolerance in many plant species such as onion (Hamed and Al-Mutawa, 2009), tomato (Zhou et al., 2017), and mung bean (Nahar et al., 2015). To our surprise, to date, the role of GSH and how it works in nano-enabled plant salt tolerance is rarely investigated. CuNPs improved tomato salt tolerance via increasing the content of glutathione (Pérez-Labrada et al., 2019). Future studies are encouraged to investigate the role of GSH and its biosynthesis in nano-enabled plant salt tolerance. (2) Proline is known as one of the most important and effective organic osmotic regulatory substances, which plays an vital role in maintaining osmotic balance and cell membrane integrity (Siddiqui et al., 2015; Hu et al., 2021). Besides being effective osmotic regulatory substance, proline is also known as antioxidants to scavenge ROS (Siddiqui et al., 2015; Brahimova et al., 2021; Hu et al., 2021). Proline is often used as an important physiological indexes in plant salt tolerance (Siddiqui et al., 2015; Hu et al., 2021). There are some reports about the role of proline in nano-enabled salt tolerance. For example, nano-SiO₂ can improve plant salt tolerance mainly by increasing proline content, photosynthetic rate, and water use efficiency of plant leaves (Siddiqui et al., 2015). Titanium dioxide NMs-treated plants not only induced the increase of antioxidant enzyme activity but also increased the content of proline and soluble sugar to improve osmotic balance in cells (Abdel-Latef et al., 2017). (3) Ascorbic acid plays an important role in plant growth and development (Zhu, 2002). After plants are subjected to abiotic stress, ascorbic acid can alleviate oxidative damage by maintaining ROS homeostasis and participating into the ASA-GSH cycle (Zhang et al., 2012). For example, exogenous nano-silicon can alleviate the damage of salt stress to soybean seedlings by increasing ascorbic acid content and enhancing antioxidant enzyme activity (Farhangi-Abriz and Torabian, 2018). Other studies showed that Cu NPs (Pérez-Labrada et al., 2019) and SiO₂ nanoparticles (Pinedo-Guerrero et al., 2020) improved tomato salt tolerance via increasing ascorbic acid contents. Furthermore, it is well known that phenols and anthocyanins are also key members of non-enzymatic antioxidant system (Pinedo-Guerrero et al., 2020). ZnO NPs can increase the content of total phenols and anthocyanins in potatoes (Raigond et al., 2017). Adding copper nanoparticles (CuNPs) to chitosan–polyvinyl alcohol hydrogel (Cs-PVA) can also significantly increase the content of phenols, β-carotene, ascorbic acid, and lycopene in tomato, finally improving tomato salt tolerance (Hernández-Hernández et al., 2018a,b).

Besides modulating antioxidant enzymes and no enzymatic pathways, nanomaterials can also be used as delivery tool to deliver antioxidants to regulate plant salt tolerance. Chloroplast guiding peptide modified β-cyclodextrin conjugated quantum dots are able to do targeted delivery of methyl viologen and ascorbic acid to chloroplasts to regulate its redox status (Santana et al., 2020). Calcium-induced cross-linked pea protein nanoparticles can stably deliver the antioxidant resveratrol (Yf et al., 2020). The combination of resveratrol and α-tocopherol significantly improved the salt adaptability of citrus seedlings (Kostopoulou et al., 2014). Overall, use of nanomaterials to maintain ROS homeostasis through either direct ROS scavenging, or modulating antioxidant system, or delivery of antioxidants, could be an alternative way to improve plant salt tolerance.

Maintaining Na⁺/K⁺ homeostasis is a hallmark for plant salt tolerance (Alsaeedi et al., 2018; Zhang et al., 2020; Liu et al., 2021a). Under salinity stress, plants evolved fine mechanisms to avoid over-accumulation of Na⁺ and massive loss of K⁺ to maintain Na⁺/K⁺ homeostasis. Shoot Na⁺ exclusion, root Na⁺ extrusion, and vacuolar Na⁺ sequestration are the main strategies for plants to avoid over-accumulation of Na⁺ in cytosol and thus the resulted Na⁺ toxicity (Yue et al., 2012; Flowers and Colmer, 2015; Wu, 2018a; Wu et al., 2018b, 2019, 2021; Zelm et al., 2020; Shah et al., 2021). For example, Wu et al. reported that vacuolar Na⁺ sequestration in the mature root zone might be responsible for the stronger salt tolerance of bread wheat than durum wheat (Wu et al., 2018b). Interestingly, previous studies showed that in root, the vacuolar Na⁺ sequestration was more important than Na⁺ exclusion for salinity tolerance in barley (Flowers and Colmer, 2015). These results suggest that the employed mechanisms for salt tolerance might be differed at tissue level in plant or between different plant species. No doubt, avoiding Na⁺ over-accumulation is also an important mechanism for nano-enabled plant salt tolerance. It has been reported that nanomaterials such as PNC (poly acrylic acid-coated cerium oxide nanoparticles) can enhance shoot Na⁺ exclusion to improve salt tolerance of cotton (Liu et al., 2021b). Also, cerium oxide nanoparticles shorten the apoplast barrier of Brassica roots to transport more Na⁺ to shoot, thus reducing the accumulation of Na⁺ in plant roots to improve its salt tolerance (Rossi et al., 2017). Other studies showed that silica nanoparticles can improve germination and growth of cucumber by decreasing Na⁺ content and maintaining K⁺/Na⁺ ratio under salinity stress (Alsaeedi et al., 2018).

Potassium plays important role in plant cell activities, i.e., adjusting of cell osmotic potential and charge balance, acting as a cofactor of many enzymes such as malate dehydrogenase and pyruvate kinase, promoting sugar transport and water retention of cells, and controlling of stomatal movement (Osakabe et al., 2013). Plants’ ability to maintain root and mesophyll K⁺ is known as important mechanisms for plant salt tolerance (Chen et al., 2005; Wu et al., 2013, 2014, 2015, 2018d). Not surprisingly, improving the ability to maintain K⁺ in plants is also a mechanism involved in nano-enabled plant salt tolerance. For example, through scavenging of ROS, cerium oxide nanoparticles modulate ROS-activated NSCC channels (non-selective cation channels) to reduce K⁺ loss to improve salt tolerance in Arabidopsis (Wu et al., 2018c). Similar results were also found in cotton (Liu et al., 2021b) and rapeseed (Khan et al., 2021). The foliar-applied poly(acrylic) acid-coated cerium oxide nanoparticles can promote shoot K⁺ retention and Na⁺ exclusion but not vacuolar Na⁺ sequestration to maintain Na⁺/K⁺ ratio to improve cotton salt tolerance (Liu et al., 2021b). It showed that nanoceria modulated the relative expression level of HKT1 (upregulation) and KOR (downregulation) genes and showed no effects on the relative expression level of NHX1 gene. This is in accordance with the findings of subcellular distribution of Na⁺ and K⁺ dye signals between control plants and nanoceria-treated cotton plants under salinity (Liu et al., 2021b). Nanosilica (SiNPs) treatment can increase K⁺ content of cucumber seedlings under high salt stress, thus improving cucumber salt tolerance mainly by maintaining K⁺/Na⁺ ratio (Alsaeedi et al., 2019). In addition, MWCNTs were also found to increase the transcriptional abundance of Na⁺ and K⁺ transporters through NO (nitric oxide) participation to maintain K⁺/Na⁺ ratio to increase rapeseed salt tolerance (Zhao et al., 2019). Taken together, maintaining Na⁺/K⁺ homeostasis might be a commonly employed mechanism for nano-enabled plant salt tolerance.

Plant hormones and plant growth regulators are essential for plant growth and development, especially in regulating plant response to stress (Hou et al., 2016; Zhu, 2016; Yu et al., 2020; Zhao et al., 2020). Abscisic acid (ABA), gibberellin (GA), brassinosteroids (BR), jasmonic acid (JA), and salicylic acid (SA) are common hormones that play a vital role in crop salt stress response (Zhu, 2002; Yu et al., 2020). However, its role in nano-enabled plant salt tolerance are not well explored. How phytohormones was involved in nano-enable plant salt tolerance and the possible effect of nanomaterials on plant growth-related processes under salinity stress are still largely unknown. Regarding the role of these hormones in plant resistance to abiotic stress such as salinity stress and plant growth-related processes, some good review papers are available (Huang et al., 2017; Wang et al., 2020; Yu et al., 2020).

Abscisic acid (ABA) signal transduction pathway, protein kinase pathway, and salt overly sensitive (SOS) signal transduction pathway are the common and well-studied signal pathways of plants in response to salt stress (Zhu, 2002; Shaki et al., 2018). Here, the discussion will be focused more on these pathways.

Nowadays, nanomaterials showed potential in improving plant salt tolerance. However, the relevant mechanisms need to be further explored. Also, to date, nano-enabled plant salt tolerance is still largely demonstrated at the laboratory research stage. To facilitate the adoption of nano-enabled plant salt tolerance in agricultural production, discussions and setup of widely accepted policies and regulations are urgently called on task. Also, more studies should be conducted to explore the possible effect of nanomaterials on plants under salt stress from the viewpoint of source-sink regulation. For example, if nanomaterials are foliar-sprayed to plants, its effects on sink capacity should be studied. Studies have shown that Zn chitosan nanomaterials significantly increased the accumulation of starch biosynthetic enzymes in wheat grains and thus the yield (by 21%) compared with the control group treated with ZnSO₄, which further verified that the wheat treated with nanomaterials on the leaf had better sink strength (Kumar et al., 2021). Overall, we believe that nanotechnology can play an important role in sustainable development of agriculture.

HW and ZZ conceived this review paper. ZL and LZ summarized and analyzed literatures regarding mechanisms underlying plant salinity stress tolerance and nano-enabled plant salt tolerance. FZ and JL contributed to make the tables and figures. XZ and XK contributed to the discussion of manuscript. HW, ZZ, ZL, and LZ wrote the manuscript. All authors contributed to the article and approved the submitted version.

This work was supported by National Natural Science Foundation of China (32071971, 31901464), joint project SZYJY2021008 from Huazhong Agricultural University and Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, and project 2662020ZKPY001 supported by the Fundamental Research Funds for the Central Universities to HW and the Key Science and Technology Special Project of Xinxiang City of China (ZD2020004), Leading Talent Project in Science and Technology Innovation of Central Plain of China (214200510021), and the Program for Innovative Research Team (in Science and Technology) in the University of Henan Province (21IRTSTHN023) to ZZ.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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