Abstract
Nanotechnology seems to have the potential to improve crop yields and help to meet the United Nations 2030 Goal 2: Zero Hunger. The literature is abreast with numerous reports on the application of various metallic, non-metallic, and other nanoparticles (NPs) that have been administered to various crop species over the last decade with fruitful results. The application of NPs has recently been considered as a viable option to alleviate the adverse effects of abiotic stresses on agricultural production. Typically, abiotic stress conditions include salinity, radiation, floods, heat, heavy metals, and drought. By influencing the physiological state of plants at different levels of their organization, NPs’ application has shown promising results in mitigating the negative effects of abiotic stresses. In contrast, many reports emphasize upon the toxic effects of NPs on plants, especially at higher concentrations. Therefore, adequate research is required to understand the effects of different concentrations of NPs before nanotechnology can be successfully used in commercial agricultural systems. Simultaneously, it is equally important to promulgate the statutory regulations associated with the judicial and safe use, disposal, and toxicity studies of NPs as well as approval and release of the nano-products. In the present review, we have dwelled upon the forementioned aspects related to NPs application besides summarizing an updated account of the status of NPs-mediated mitigation of major abiotic stresses in crops.
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Introduction
Since the last century, global climate change is critically viewed as one of the biggest challenges to mankind (Shahzad et al. 2021). This alarming threat has arisen because of rapid urbanization and anthropogenic activities including industrialization. As a result, significant negative externalities are being observed in both developed and developing nations of the world (Malhi et al. 2021). Over the past two decades, global climate changes have progressively disrupted the fine balance of ecological factors in nature and resulted in profound consequences in the form of floods, heatwaves, salinity, and droughts (Bandh et al. 2021; Singh et al. 2022). The crop species and the plants growing in the wild are most vulnerable to such extreme weather conditions and stresses (Malhi et al. 2021). Numerous published reports have emphasized upon the negative effect of climate change on the reduction of the world’s agricultural total productivity (Zilli et al. 2020; Ortiz-Bobea et al. 2021; Nguyen and Scrimgeour 2022). Being a multifaceted system of alterations, global climate changes directly impact both abiotic and biotic components of the plant niche(s). While, the growth, multiplication, spread, severity/infestation, and the emergence of many plant pathogens/insect pests are directly impacted by the biotic factors (Vilela et al. 2018), in the case of abiotic components, alterations both in terms of intensity and frequency, are observed for rainfall intensity, CO2 concentration, temperature fluctuations (high and low), and salinity (Singh et al. 2022).
Together, these environmental stresses act as the most common deterrents to food production and global food security. The stresses cause a cascade of morphological, physiological, anatomical, biochemical, and molecular changes in plants that eventually negatively impact their growth and productivity (Fig. 1). The stress-induced changes include ion toxicity, reactive oxygen species (ROS) production (O2−, H2O2, O, α-O, and OH−), nutritional problems, redox/osmotic imbalances, changes in leaf water content, chlorophyll content, photosynthetic capacities, and turgor pressure (Mehta et al. 2020; Zhou et al. 2021). Additionally, these stresses disrupt the ultrastructure of cellular and organellar membranes leading to the disruption of normal cellular physiological functions. Plants employ a variety of mechanisms to cope with these stresses including ion homeostasis and compartmentalization, electron transport chain, biosynthesis of osmoprotectants and phytohormones, regulation of nitric oxide production, antioxidant defenses, water balance, osmotic regulation, and changes in the expression (Gohari et al. 2020a, b; Van Zelm et al. 2020). However, the yield losses still remain substantial and farmers throughout the world are able to collect only 50% of their optimal yield potential (FAO 2014; Bayat et al. 2021). The 'yield gap' between actual and prospective production is caused by these stresses (Moshelion and Altman 2015).
Phytonanotechnology has been projected as one of the most effective and promising modern technologies with the ability to protect plants from environmental stresses, and to offer practical answers to the United Nations 'Zero Hunger 2030 Goal' (Jiang et al. 2021; Agrawal et al. 2022). Being submicroscopic particles by nature that range in size from 1 to 100 nm, nanoparticles (NPs) can be chemically, physically, or biologically generated from a variety of materials. upon application, the NPs aid plants in coping with abiotic stresses by increasing free radical scavenging (Ghareib et al. 2019), antioxidant enzymatic activities (Geremew et al. 2023), osmoprotectant concentration (Al-Khayri et al. 2023), bioavailability, and uptake of essential nutrients (Rasheed et al. 2022), all of which help to limit the cellular osmotic and oxidative damage and thus increase growth and yield potential. Because of these reasons, nanotechnology has been recognized as the ‘Key enabling technology’ by the European Union (Parisi et al. 2015). Recently, NPs have been put to commercial usage in the agriculture industry as nanofertilizers (Xu et al. 2023), nanoherbicides (Kannan et al. 2023), nanopesticides (Manzoor et al. 2023), nanofungicides (Wen et al. 2023), and nanosensors (Iavicoli et al. 2017). Indian Farmers Fertilizer Cooperative Limited (IFFCO) recently launched World’s 1st Nano Urea Liquid (Yamuna et al. 2023) for improved crop productivity. Various nano-enabled products being used in agriculture around the globe have been previously compiled by Rajput et al. (2021).
Although the effects of NPs on crop productivity vary depending on their origin, size, form, concentration, mode of exposure, period of exposure, as well as the specialization of plant genotypes, NPs have generally been observed to exert positive effects on plant growth when applied at low or medium concentrations (Fig. 2) and help crop plants in tolerating various types of abiotic stresses by bringing about changes at genetic, biochemical, anatomical, and physiological levels (Mittal et al. 2020). However, at elevated concentrations, the NPs tend to induce metabolic alterations or even inhibit vital life processes. The mitigation of abiotic stresses by application of NPs has although been dwelled upon in some excellent reviews (Rajput et al. 2021; El-Saadony et al. 2022; Al-Khayri et al. 2023; Abdel-Aziz et al. 2023; Zia-Ur-Rehman et al. 2023), pertinent safety issues related to the commercial usage of NPs in agriculture such as (i) understanding the possible causes of toxicity of NPs at higher doses and its management and (ii) the promulgation of uniform regulatory laws related to NPs application, disposal, eco-toxicity and approval of nano-products still need to be addressed by the scientific community. Resolving these issues is important before nanobiotechnology is considered as a safe and rewarding technology to aid in global food security. The present review has attempted to raise and address these key concerns besides providing an updated account of the status of NPs mediated mitigation of major abiotic stresses in crops.
Abiotic stresses in crops and their mitigation by metal nanomaterials
Salinity and sodicity rank top among the principal abiotic stresses and represent the most potent limiting factors to agricultural production, crop yield, and usable land area (Gangwar et al. 2020; Mukhopadhyay et al. 2021). Similarly, drought is considered as the most common abiotic stress that has impacts on the crop productivity especially in the dry areas of the world (Ahmad et al. 2018; Seleiman et al. 2021; Ilyas et al. 2021). The severity of drought conditions is increasing worldwide due to changing climate and poor water resource management and every year, drought stress costs billions of dollars in crop yield losses (Alabdallah et al. 2021). The development of drought-tolerant cultivars is a time taking process and such genomic resources are not available in all crop species. This situation raises serious concerns about adequate food supply in drought-prone geographies of the world (Nuccio et al. 2018). Cumulatively, high salinity of soil, drought, and temperature stress have been observed to be the leading cause of crop loss globally (Praveen et al. 2023).
In the same vein, heavy metals (HM) contamination has become another increasingly alarming issue around the world due to disproportionate urbanization, industrialization, and mining activities (Tóth et al. 2016; Adimalla et al. 2019; Wan et al. 2021; Hananingtyas et al. 2022). Over the recent past, HMs have been reported to be present in exceedingly higher amounts than the permissible limits in agricultural soils (Wan et al. 2021; Oladoye et al. 2022) negatively affecting plant growth and eventually human health.
In this context, nanotechnology has shown promising results and metallic NPs such as ZnO, CuO, Fe2O3, TiO2, and Ag-based NPs have successfully been used to combat various abiotic stresses, including heavy metal (Hussain et al. 2018; Khan et al. 2019; Rizwan et al. 2019a, b; Jiang et al. 2020; Bashir et al. 2020), drought (Foroutan et al. 2020; Dimkpa et al. 2019; Sun et al. 2020; Adrees et al. 2021; Semida et al. 2021), cold (Song et al. 2021), salinity (Alabdallah and Alzahrani 2020; Elsheery et al. 2020a; Noohpisheh et al. 2021; Faizan et al. 2021a; Kareem et al. 2022a, b), and high-temperature (Kareem et al. 2022a, b) stresses. Specific NPs have been found to improve productivity in many crop species affected by abiotic stresses. For instance, the use of TiO2 NPs has helped crops such as wheat, Dragon’s head, rice, chickpea (Mohammadi et al. 2013, 2014; Amini et al. 2017), tomato, and maize in mitigating cold, drought, high temperature (Qi et al. 2013; Thakur et al. 2021), heavy metals, lead (Pb) and cadmium (Cd), and salt (Khan 2016; Cai et al. 2017; Dai et al. 2019; Shoarian et al. 2020; Lian et al. 2020; Mustafa et al. 2021) stresses. Silicon (Si) and Silicon dioxide (SiO2) in nanoforms have been observed to exert a positive effect on the metabolism and physiology of stressed plants. Ag NPs display peculiar physico-chemical properties that lie between copper (Cu) and gold (Au) and have been used to combat heavy metal and salinity stress in plants like tomato (Almutairi 2016), fenugreek (Hojjat and Kamyab 2017), grass pea (Hojjat 2019), Lilium (Salachna et al. 2019), pearl millet (Khan et al. 2020a, b), Yellow Lupin, wheat (Wahid et al. 2020), and Satureja hortensis (Nejatzadeh 2021; Jaskulak et al. 2019) (Tables 1, 3).
Rui et al. (2016) evaluated the effectiveness of Fe2O3 NPs with a chelated Fe-fertilizer in peanut (Arachis hypogaea) seedlings. Foliar sprays of Fe2O3 NPs improved the activities of polyphenol oxidase (PPO), catalase (CAT), and peroxidase (POD) enzymes (Torabian et al. 2018) in sunflower (cv. Alestar). Fe2O3 NPs usage resulted in improved photosynthetic efficiency with a reduced Cd content in the wheat grains (Hussain et al. 2019a, b) thereby combating heavy metal stress (Table 3). Interestingly, Fe2O3 NPs complexed with salicylic acid have recently been utilized to reveal both positive and negative impacts on plants under salinity stress (Mozafari et al. 2018). While, positive effects included enhanced activities of antioxidant enzymes Superoxide dismutase (SOD), CAT, and POD, increase in K+ uptake and K+/Na+ ratio, and improvement in plant growth by prevention of nutrient balance by enhanced activities of H+-ATPase and H+ PPase seen in Trachyspermum ammi L. (Abdoli et al. 2020; Ghassemi-Golezani and Abdoli 2021), reduction in chlorophyll content and degradation and plasma membrane damage was reported in Pistacia vera by Karimi et al. (2020). Overall, the application of various NPs has shown great promise in mitigating abiotic stresses in crops, the details of which have been tabulated stress-wise in the following sub-sections.
Salinity stress
Around 800 million hectares of arable land are affected by soil salinity around the world (Gohari et al. 2020b). The salinity resultant ionic imbalances, nutritional and hormonal abnormalities, and osmotic stress lead to metabolic and growth alterations in plants and reduced yield and crop quality (Liu et al. 2021). To cope with sodicity, plants use several strategies such as osmotic regulation, increased chlorophyll content, electron transport chain, antioxidant responses, harmful ion uptake, and ROS production (Gohari et al. 2020b). The positive effects of ZnO NPs have been attributed to the release of zinc which plays a vital role in plant physiology primarily by stabilizing the proteins and bio-membranes under stress conditions (Kareem et al. 2022a, b). Zn NPs, at a concentration of 10 mg/L upregulated the osmolyte biosynthesis and antioxidant system in Brassica napus L. when subjected to salinity (Farouk and Al-Amri 2019) (Table 1). At a similar concentration, ZnO NPs induced an increase in the photosynthetic pigments, CAT and SOD activities, and growth parameters in Abelmoschus esculentus L. (Okra) grown under saline conditions (Nadiya et al. 2020). Being a SOD cofactor and a key component of CA (Carbonic anhydrase), zinc is also involved in ROS scavenging (in cytosol and chloroplast) and photosynthesis (Khan et al. 2021a, b; Faizan et al. 2021b). In addition, the accumulation of both total soluble sugar and proline was observed to reduce in Okra, which helped in keeping the turgor pressure and enhanced the membrane stabilization by acting as ROS scavengers. In crop plants, when applied as foliar sprays, Zn maintains water balance, regulates indole-3-acetic acid (IAA), affects the metabolism of lipids and carbohydrates, and regulates the membrane integrity and enzymatic activities (Caldelas and Weiss 2017). Moreover, ZnO NPs have also been tested in combination with zeolite, Si, and boron NPs in potatoes (Mahmoud et al. 2020), leading to increased photosynthetic efficiency, nutrient uptake, and antioxidant properties. Zinc oxide in combination with Si NPs increased the yield and quality of fruits in mango (Elsheery et al. 2020b). When applied along with biochar (Ali et al. 2019a; Bashir et al. 2020), iron oxide (Rizwan et al. 2019a, b), Fe, Cu, or Co (Linh et al. 2020), the stress mitigation effects of NPs were further improved in crop plants like wheat, rice, barley, soybean, sugarcane, and maize (Table 2).
Copper (Cu) is a metallic micronutrient that is essential for various vital processes in plants including photosynthesis (Yruela 2005, 2009). Besides, Cu also mediates several redox reactions to reduce the harmful effects of salinity by regulating photosynthesis, water relations, and nutrition. It has also been observed to upregulate antioxidant defense and levels of osmoprotectants with a higher Na+/ K+ ratio in tomatoes (Hernández-Hernández et al. 2018; Perez Lebrada et al. 2019), thereby helping the plant negotiate and ameliorate salinity stress.
The NPs application is manifested in terms of better phenotypic and photosynthetic performance coupled with an increase in chlorophyll content and carbon assimilation rate. The other coupled changes include an increase in antioxidant enzymes and a reduction in reactive oxygen species (ROS) and malondialdehyde (MDA). The use of CeO2 NPs, including polyacrylic acid-coated nanoceria (PNC) has been shown to improve the plant’s tolerance to salinity stress in Brassica napus (Rossi et al. 2017a, b), Arabidopsis thaliana (Wu et al. 2018), rice (Zhou et al. 2020), cotton (Liu et al. 2021), and in Dracocephalum moldavica (Mohammadi et al. 2021) by improvement in agronomic traits, photosynthetic efficiency, and antioxidant enzymes. Abdel Latef et al. (2018) reported an increase in plant growth, soluble sugars, antioxidant enzymes, amino acids, and proline content, and a decrease in MDA and H2O2 contents in broad beans with the application of TiO2 NPs (0.01%) under salinity conditions. The effects of TiO2 NPs have been tested on the agronomic traits in Moldavian balm (Dracocephalum moldavica L.) plants grown under different salinity levels (Gohari et al. 2020b). The analyzed agronomic traits were observed to be negatively affected by salinity at all the tested levels. However, the application of TiO2 NPs at 100 mg/L concentration resulted in increased antioxidant enzyme activity and reduction of H2O2 levels to prevent oxidative damage, thereby, activating the enzymatic defense system of the plant to alleviate all the negative effects associated with salinity stress. Further, the NPs treated plants showed a significant increase in the oil content warranting its commercial application for growth promotion and salinity stress amelioration. The crops such as broad bean, tomato, cotton, spinach, Stevia, and Moldavian balm, have been observed to exhibit an improvement in RuBisCO levels, antioxidant enzymes levels, chlorophyll content, and photosynthetic rates in response to TiO2 NPs application (Lei et al. 2008; Khan 2016; Abdel Latef et al. 2018; Gohari et al. 2020b; Sheikhalipour et al. 2021).
In another study, Kalteh et al. (2018) reported alteration in physiological and morphological traits, increase in leaf fresh and dry weight, chlorophyll content, and growth upon the application of Si NPs in the holy Basil (Ocimum basilicum L.) grown under salinity stress. Similarly, Asgari et al. (2018) compared the effects of sodium silicate with nano-silicon at concentrations of 5 mM and 10 mM in oat plants (Avena sativa L.) grown hydroponically. They focused on xylem cell wall lignification, leaf and root cells ultrastructure, low silicon 1 (Lsi1), and phenylalanine ammonia-lyase (PAL) expression. Si NPs helped in the regulation of ion homeostasis and stomatal opening, increase in K+ uptake and K+/Na+ ratio, and water and nutrient use efficiency in cucumber (Cucumis sativus L.) under salt stress (Alsaeedi et al. 2019). Likewise, Avestan et al. (2019), observed an increase in photosynthetic pigments (chlorophyll and carotenoid), increased epicuticular wax deposition, and a decrease in proline content in salt-stressed strawberries (Fragaria x ananassa L.). SiO2 NPs (200 mg/Kg of soil) increased seed germination percentage, length, and dry mass of roots and shoots, fruits yield in common bean (Phaseolus vulgaris L.) under salinity conditions (Alsaeedi et al. 2020). When Si NPs were applied in combination with plant growth-promoting rhizobacteria (PGPR) in salt-stressed maize (Zea mays L.) a decline in oxidative stress was observed to be regulated by enzymes CAT, SOD, and POD. The resultant maintenance of K+/Na+ ionic balance resulted in a higher photosynthetic rate, growth, reduced proline content, and electrolyte leakage (Hafez et al. 2021). Although the forementioned and other reports have established the significance of Si NPs in regulating salt stress tolerance in plants, a better understanding of biochemical and molecular mechanisms and intracellular interactions of Si NPs in plant systems is highly desired.
Mn NPs can serve as micronutrients that aid plant growth by improving membrane stability index, chlorophyll content, and nitrate reductase activity in Vigna radiata (Shahi and Srivastava 2018) and protect them against various abiotic stresses (Ye et al. 2020). Similarly, Rahman et al. (2016) observed that salinity-stressed rice plants recovered from chlorosis and restricted growth, ROS detoxification, and showed an increase in the content of phenolic compounds and enzymatic activities of AsA (ascorbate), MDHAR (monodehydroascorbate reductase), DHAR (dehydroascorbate reductase), SOD and CAT in response to Mn NPs’ application. In bell peppers (Capsicum annuum L.), both scanning electron microscopy and energy-dispersive spectroscopy revealed that Mn NPs formed an NPs-Protein corona complex and resulted in improvement in the germination of seeds and growth of roots at 100 mM NaCl (Ye et al. 2020). Compared to other NPs, reports documenting the abiotic stress-mitigating potential of Mn NPs are scarce in the literature. Therefore, future research with Mn NPs will further unravel their role in mitigating other stresses as well.
Drought stress
Limited studies have been reported on the application of NPs to combat drought stress. In many cases, the ability of TiO2 in mitigating drought has been fortified by their functionalization either with sodium nitroprusside (SNP), a nitric oxide donor, or calcium phosphate (Table 2). The TiO2 NPs-based increment in vital functions hints toward its role as a stimulant to activate different enzymatic defense mechanisms as well as an inducer of secondary metabolite production against various abiotic stress factors. A significant decrease in the number of root tips has been reported upon exposure to TiO2 NPs leading to reduced root hydraulic conductivity. Further, it has been observed that a large portion of TiO2 NPs might be taken up mainly through root ruptures instead of the typical uptake route.
SiO2 NPs have been found to be useful in alleviating drought stress in Hawthorn (Crataegus sp.) (Ashkavand et al. 2015) wherein their application resulted in improvement in growth parameters. Zahedi et al. (2020) reported an increase in the photosynthetic parameters in strawberries grown under drought conditions in the presence of SiO2 and Se NPs (Table 2). Further, Cu NPs alone (Van Nguyen et al. 2021) or in combination with Zn (Taran et al. 2017) and Ag NPs (Ahmed et al. 2021) have been shown to successfully counter drought stress in maize and wheat, respectively. Similarly, Iron oxide (IO NPs) and Hydrogel NPs (HG NPs) (Ahmed et al. 2021) have been used in strawberries and rice, respectively to successfully negotiate drought stress and improve vital metabolic parameters. Just like Mn NPs, the use of Cu NPs in combating various abiotic stresses is still in the infancy stage and more research is desired to establish the mode of action of Cu NPs to exploit their full potential for agricultural productivity.
Metal stress
ZnO NPs alone or in combination with other NPs (Tables 1 and 3) have been observed to result in increased chlorophyll content, number of leaves, gaseous exchange, germination, plant height, fresh roots, shoot length, and root and shoot biomass. While improvement was observed in antioxidant enzymes, a reduction in electrolyte leakage, hydrogen peroxide, MDA content, and heavy metal accumulation has also been observed. More recently, Shah and colleagues affirmed that a combination of K silicate and ZnO NPs modulated the antioxidant system, membranous H+-ATPase, and nitric oxide content in faba bean (Vicia faba) seedlings when exposed to As toxicity (Shah et al. 2022).
Cerium oxide (CeO2), is a pale yellow-white powder that is also known as ceric oxide, ceria, or cerium dioxide. While, Rossi et al. (2017a, b) and Wang et al. (2018) showed no effect of CeO2 NPs on heavy metal stress amelioration in soybean (at 500 mg CeO2 NPs/Kg of dry soil) and rice (at 100 mg/L), respectively. On the other hand, Wang et al. (2019) reported a positive impact of the same on mitigation of heavy metal stress in rice at 100 mg /L of CeO2 NPs. While tolerance against drought was observed in wheat and Dragon’s head, tolerance against heavy metal stress was observed in rice, maize, and wheat. In a study by the group led by Lui, the foliar application (at 250 mg/L) mitigated heavy metal stress, while the root application had negative repercussions (Lian et al. 2020). The basic reason behind this observation rested upon the stronger effect of foliar spray on changing the water and metabolite profiling which could have occurred due to better uptake and translocation of NPs via leaves. In contrast, NPs are poorly accumulated by plants through roots under soil conditions due to mucilage and root exudates that are reported to trap NPs or modify their surface (Shang et al. 2019). Several such studies have been listed in Table 3.
Low-temperature stress
Plants need an optimum temperature for their growth and reproduction. Due to climate change-inflicted fluctuations and extremities of average global temperature in terms of chilling and freezing or heat stress, the crops in field conditions have been negatively affected (Adhikari et al. 2022; Al-Khayri et al. 2023; Shakeh et al. 2023) with a significant reduction in agricultural productivity.
Low temperature or chilling and freezing stress leads to many physiological disorders in plant cells resulting in slow growth and altered metabolism (El-Mahdy et al. 2018; Sharma et al. 2020; Hassan et al. 2021; Aslam et al. 2022). Cold stress adversely affects cellular membrane structure and photosynthetic rates (Barajas-Lopez et al. 2021; Burnett and Kromdijk 2022). Different NPs have been used to cope with cold stress in various crops (Kim et al. 2017). For instance, Si NPs and cold plasma have been successfully used in Astragalus fridges to alleviate cold stress (Moghanloo et al. 2019). Chitosan and TiO2 NPs have been used in many studies in chickpea to impart cold stress tolerance (Mohammadi et al. 2013, 2014; Hasanpour et al. 2015; Amini et al. 2017). Under cold stress conditions, the application of TiO2 NPs elevated glycyrrhizin content in licorice (Ghabel and Karamian 2020), Chitosan NPs reduced ROS and enhanced osmoprotectants in banana (Wang et al. 2021), ZnO NPs in a foliar application stimulated the antioxidative system and transcriptional machinery in rice and increase in SOD, MDA and electrolyte leakage in summer and winter cultivars of wheat (Song et al. 2021; Shakeh et al. 2023) and Si NPs increased the photosynthetic ability in sugarcane (Elsheery et al. 2020b) to combat chilling stress. The cold stress ameliorating properties of many other NPs in wheat, rice, Eruca sativa, Astragalus, plum, and strawberry crops along with the combined use of many NPs such as SiO2, ZnO, and Se have been detailed in Table 4.
High-temperature stress
High temperature known as heat stress prevalent for a persistent period, potentially jeopardizes the plant’s normal cellular functions and prolonged exposure to abnormally high temperatures causes a significant yield loss (Hu et al. 2020; Zhao et al. 2020; Bharti et al. 2021). Heat stress also causes both osmotic and oxidative stresses at the secondary level. In order to tackle high-temperature stress, plants employ various cellular, physiological, and molecular modifications to sustain cellular homeostasis (Bharti et al. 2021). The application of various NPs such as Se NPs in Sorghum ameliorated membrane damage, reduced pollen germination and yield inflicted due to increased temperature (Djanaguiraman et al. 2018). Likewise, Ag NPs (Iqbal et al. 2019) and Zn NPs (Hassain et al. 2018) resulted in increased growth and antioxidant enzymes and a reduction in lipid peroxidation to combat heat stress in wheat plants. The foliar application of Si NPs in tomato helped the plants cope with the heat stress (Kim et al. 2017). Table 5 highlights NPs mediated heat stress amelioration reports in various crop species.
Combined use of NPs to combat abiotic stresses
Global climatic changes have resulted in the exacerbation of various stresses and co-occurrence of multiple stresses in the farmers’ fields complicating the situation further. Considering this, scientists around the globe have started working on elucidating the interactive effects of multiple NPs used simultaneously in plants to cope with the stressful environment (Ramegowda and Senthil-Kumar 2015; Pandey et al. 2015). For instance, to combat salinity stress, Se, Si, and Cu NPs were used together in bell peppers, and an increase in chlorophyll, B carotene, and lycopene, glutathione peroxidase was observed in the leaves, while fruits showed enhanced enzyme activity and reduction in glutathione and flavonoids level (González-García et al. 2023). In another study by Mozafari et al. (2018), iron (Fe) and K silicate NPs were used together in grapes (Koshnaw cv.) and an increase in total protein content and reduction in proline and H2O2 and an increase in membrane stability were observed. The combined application of ZnO and Si NPs in mango improved plant growth, nutrient uptake, carbon assimilation, increased annual crop load, and fruit quality under salinity stress (Elsheery et al. 2020b). Likewise, the combined use of Zn, B, Si, and zeolite NPs in potatoes (Solanum tuberosum L.) under salinity stress, improved plant height, branching, shoot dry weight, chlorophyll content, net photosynthetic rate, stomatal conductance, tuber yield, and nutrient concentration along with protein and carbohydrates content (Mahmoud et al. 2020). In another report, TiO2 and chitosan-functionalized Selenium (Cs-Se) NPs used together helped in combating salinity stress in Stevia rebaudiana and resulted in an increase in plant growth, photosynthetic performance, antioxidant potential, and stevioside and rebaudioside contents (Sheikhalipour et al. 2021). Although the above-mentioned reports show that NPs had a positive impact on salinity stress amelioration, the combined use of CeO2 and TiO2 NPs in barley (Hordeum vulgare L.) showed a negative impact and resulted in growth inhibition and generation of oxidative stress in terms of generation of ROS (Mattiello 2015). Similarly, the combined application of CeO2 NPs and ZnO NPs on Pisum sativum L. at two different concentrations revealed that the CeO2 NPs stimulated the photosynthesis rate, while ZnO NPs prompted stomatal and biochemical limitations. However, in the mixed ZnO and CeO2 treatments, the latter effects were decreased (Skiba et al. 2021).
All the above reports convincingly indicate that NPs have an important role to play in combating various stresses and assisting food production amidst the changing climatic scenario. Therefore, extensive research especially in understanding the intracellular interactions of different NPs applied singly or in combination, nano-bio interface, and impact analysis is the need of the hour.
Environmental concerns of NPs usage in coping abiotic stress
As discussed in the above sections, nanotechnology offers immense applications in the agriculture sector with the potential to increase overall agricultural productivity and yield, protect against environmental stresses, and reduce chemical pollutants in the environment (Tables 1, 2, 3, 4, and 5). The bibliographic survey reveals that the positive effects of NPs directly depend upon specific genotype/cultivar, shape, size, dose, composition, surface area, surface coatings, redox state, application procedures, and growth matrices (Sarraf et al. 2022). However, various NPs like CeO2, Se, TiO2, and ZnO have been shown to produce toxic effects in many plant species including soybean, Sorghum, broad bean, sweet basil, tomato, wheat, onion, and barley (Lopez-Moreno et al. 2010; Djanaguiraman et al. 2018; Rastogi et al. 2019; Filho 2019; Kushwah and Patel 2020; Gohari et al. 2020a, b; Thwala et al. 2021; Feizi et al. 2022) (Table 6).
The NPs’ phytotoxicity results from the interaction with the cellular biomolecules and damage to DNA and/or membranes. For example, by using an FT-interacting protein 7 (Osftip7) mutant, a group of scientists from China demonstrated that the (OsFTIP7) facilitates the toxic effects of CuO NPs and ZnO NPs in rice (Jiang et al. 2021). A loss of function of OsFTIP7 reduced the toxicity of Zn and Cu NPs by improving auxin biosynthesis, biomass, and chlorophyll content. It is noteworthy that OsFTIP7 is a transmembrane protein with several metal binding domains, therefore, a direct interaction of this protein with metallic NPs is possible.
The toxicity of NPs toward plants is not the only concern of the present times, but a growing body of evidence also indicates the possibility of detrimental effects of NPs on the tertiary consumers, humans (Dudefoi et al. 2017; Rajput et al. 2020; Bischoff et al. 2022). For instance, E171 (a TiO2 NPs-based food additive), which is added in foods such as ice creams, candies, gums, and puddings, was recently shown to facilitate colorectal tumor formation and progression by affecting the processes like inflammation, immune responses, cancer signaling, and cell cycle in mouse system (Bischoff et al. 2022).
The negative impacts of NPs on plants are reflected in terms of reduction in seed germination and root elongation, reduction in photosynthetic efficiency, biomass, growth inhibition, hampered mineral uptake; oxidative stress (ROS), induction of e− hole pairs, damage to the cell wall and cell membrane, and aggregation of NPs leading to increased ROS species and tissue toxicity (Fig. 3). At the cytological levels changes in mitotic index, chiasma frequency, and the number of univalents have been shown in onion and faba bean (Patlolla et al. 2012; Rajeshwari et al. 2016; Kushwah and Patel 2020).
The NPs toxicity, however, has been observed to depend on various factors like specific plant species and genotype, concentration, and size of the NPs, and the duration of the exposure and indicates the involvement of certain factors that are governed by these conditions. Interestingly, one such actor known as NPs protein corona (PC) is formed upon the entry of NPs into the cell by the adsorption of proteins from their surroundings (Muller et al. 2018). Protein corona has been extensively studied by medical and environmental scientists but it has remained poorly deciphered in plants until recently (Prakash and Deswal 2019; Li et al. 2019; Kurepa et al. 2020; Ye et al. 2020; Khanna et al. 2021). Our group recently reviewed the current status of NPs associated protein corona in plants (Prakash et al. 2022a) and showed that protein corona determines NPs uptake, translocation, its effects, and fate as well. Recent efforts to understand corona formed in plants showed the ability of PC to influence major cellular pathways or plant responses like energy synthesis, pathogenesis, salt tolerance, and leaf senescence. More research studies are required to corroborate these findings in various groups of plants. Therefore, future research should be aimed to elucidate molecular mechanisms of NPs action under tightly controlled reaction conditions such as the NPs concentration, size, and duration of exposure in desirable plant species before they can be exploited in a commercial agricultural system.
It is imperative to first understand the effect of various physiochemical characteristics, means of introduction, uptake, translocation, aggregation, and parameters like size, number, concentration, surface activity, modification, and most importantly intracellular interaction of NPs with cellular organelles and its effects on cellular metabolism, before nanobiotechnology becomes fruitful to be utilized commercially (Sarraf et al. 2022). Therefore, keeping in mind these limitations, the future course of research must be focused on finding possible solutions to the safe and efficient use of NPs in agriculture. Additionally, more efforts need to be directed toward studies about the nano-bio interface and impact analysis to avoid ecotoxicological risks for both plants and humans (Prakash et al. 2022a; Singh et al. 2022). Yet another important aspect that needs the attention of the scientific community is the safe disposal of NPs. The given guidelines for the NPs’ disposal state that NPs should be discarded in sealed boxes in an area dedicated to hazardous materials or they must be incinerated. However, unfortunately, NPs are being used in several laboratories/institutions around the world that lack such facilities. It is absolutely essential to have proper safety protocols and regulations in place for the use and disposal of NPs (Paramo et al. 2020). The present review recommends the use of NPs with caution in the current scenario.
Regulatory laws on the application of NPs and NPs-based commercial products
As described earlier, the application of NPs on plant species largely has a positive effect on plant growth and metabolic processes under abiotic stress conditions. With the advent of nanotechnology, many nano-based chemicals have been commercialized throughout the world (Mittal et al. 2020). However, the major pool of patented chemicals relates to controlling biotic stresses only (Vijayakumar et al. 2022). The commercial products that directly relate to abiotic stress mitigation are scarce and only a few have been used as nanofertilizers like Nano urea, Nubiotek, Fértil Calmag, Nano Bor, and Nano Zinc.
As a whole, several ordinances, regulatory laws, governance structures, and policies have been formed over the past fifty years related to the judicial use of nanotechnology in the laboratory and in field conditions. The list includes the European Food Safety Authority National Nanotechnology Initiative (by National Science and Tech. Council for Enhancement of Nanotechnology), BMBF (Federal German Ministry for Education and Research), NANOKOMMISION, Regulation (EC) No. 1107/2009, Regulation (EC) No. 396/2005, and REACH Regulation (EC) No. 1907/2006 (discussed in Vijayakumar et al. 2022).
In case of developing countries like India, regulatory frameworks and policies have been recently drafted by the Department of Biotechnology (DBT), Ministry of Science and Technology, Government of India, on August 1, 2019. The policy aims to ensure the safe usage of nano-Agri input products (NAIP) and nano-agriproducts (NAP) to prevent environmental and human health hazards. Similarly, as part of the Nano Mission, a Nano Science and Technology Initiative (NSTI), launched by the Department of Science and Technology (DST), India has issued “Guidelines and Best Practices for Safe Handling of Nanomaterials in Research Laboratories and Industries”.
The evaluation of nano-products used in agriculture and food is challenging with the existing assessment procedures. The major limitation associated with nano-products assessment and evaluation is the lack of unanimously acceptable international guidelines and definitions for nanomaterials and nano-agriproducts. The US FDA and environmental protection agency (EPA) are yet to consider ‘nanomaterials’ as the new chemicals. Further, adding to the woes, existing methods for environmental risk assessment have been questioned by various groups of scientists around the world (Kookana et al. 2014; Mwaanga 2018). Though the industrial stakeholders rigorously promote the risk-free usage of NPs, delays in approvals of nano-products which are being assessed on a case-to-case basis become a deterrent in the commercialization of NP-based products in agriculture. Therefore, uniform and transparent guidelines need to be formulated for regulatory frameworks, approvals, safe disposal, environmental risk, and toxicity assessments for all nations across the world (Prakash et al. 2022b). Considering that nanobiotechnology is a relatively new domain, all the above important concerns need to be urgently addressed by world leaders and policymakers for effective and fruitful commercial utilization of nanotechnology for the enhancement of agricultural output.
Concluding remarks and future perspectives
Under the shade of globalization and industrialization, the agriculture sector faces several challenges, especially in the form of biotic and abiotic stresses. Over the past few decades, NPs have gained immense popularity in the agricultural sector due to their tunable physio-chemical properties and ability to penetrate plants. In this review, we have highlighted the most recent reports on the beneficial effects of NPs in several plant species exposed to the most common detrimental abiotic stresses, such as drought, salinity, heavy metals contamination as well as both high- and low-temperature-based conditions. Generally, NPs exert positive effects at the molecular, metabolic, and physiological levels in plants. The NPs-induced positive responses are manifested through the expression of various genes, improvement in antioxidant defense, osmotic potential, chlorophyll content, photosystem performance, root exudation, influenced uptake of nutrients, and through discouraging secondary stresses when observed under controlled greenhouse and field conditions.
The positive impact of all types of NPs has been observed to be dependent on several factors that include the type of NPs used, application method, dose, simultaneous or individual use of NPs, and extent of stress exposure. Besides the forementioned advantages, there are a few reports documenting the toxic effects of NPs generally at high concentrations in a few plant species. Nevertheless, overall NPs display an immense potential for improving plant performance under abiotic stresses but most of the studies have been carried out in laboratory conditions. It is of utmost importance to replicate the performance of NPs in stress amelioration in field conditions for nanotechnology to be used as a sustainable strategy and to offer practical solutions for enhancing the abiotic stress tolerance capability.
In the future, it is foremost essential to understand the exact mechanism of synthesis of NPs from a variety of biological entities. Detailed investigations also need to be carried out to better understand the mode and mechanisms of action of NPs in plants. Further, it is important to investigate the synergistic effect of the different NPs with growth-promoting microbes against abiotic stresses to find out the best possible combinations and doses. More focused research studies need to be planned on the combined application of NPs against simultaneously occurring stresses in a practical scenario in field conditions. Knowledge of how different NPs influence the signaling mechanisms and plant antioxidant machinery using multi-omics technologies will be quite helpful in understanding the mode of action of various NPs for their better utilization. Future research should also focus on fabricating novel metallic/non-metallic NPs using untapped elements from the periodic table. Finally, the standard guidelines and protocols for evaluation of optimum dosages, disposal protocols, and risk analysis of the possible accumulation of NPs in edible plant parts, their safe and acceptable limits for human consumption, and the effect of different nano-formulations on different organisms (biotic components) and environments (abiotic components of the ecosystem) must be performed before we develop biodegradable/self-degradable, non-toxic, cheap, and environmentally safe NPs that can be commercially utilized in crop systems for sustainable agriculture production to fruitfully utilize nanotechnology for human welfare.
Data availability
Enquiries about data availability should be directed to the authors.
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Acknowledgements
All authors would like to acknowledge the anonymous peer reviewers for their constructive remarks that helped to improve the manuscript.
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The work is partially supported by the Institute of Eminence (IoE) Grant (No.: IoE/FRP/LS/2020/27 & No.: IoE/2021/12/FRP) received by RD and fellowship received by SP from Govt. of India, Council of Scientific and Industrial Research (CSIR), (Grant No. F 3-5/2018(DRS II). VDR and TM acknowledge the support by the Russian Science Foundation, project no. 21-77-20089.
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VRR wrote and VRR and SP edited the manuscript. SM provided the illustrations. VRR, TM, VDR and RD structured the hypothesis and edited manuscript.
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Rajpal, V.R., Prakash, S., Mehta, S. et al. A comprehensive review on mitigating abiotic stresses in plants by metallic nanomaterials: prospects and concerns. Clean Techn Environ Policy (2023). https://doi.org/10.1007/s10098-023-02561-9
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DOI: https://doi.org/10.1007/s10098-023-02561-9