Abstract
Horticultural crops are used for a variety of purposes, including nourishment and aesthetics. Human nutrition relies heavily on these plants for carbohydrates, proteins, organic acids, vitamins, and minerals. Drought, flood, nutrient inadequacy, heat, light, metal stress, and other abiotic stresses restrict crop plant development and output. A variety of tactics are used to improve abiotic stress tolerance, including the production of genetically modified cultivars by incorporating gene constructions to improve performance under stress. Nanotechnology is a multifaceted field that could be applied in every branch of research comprising medicine, industry and agriculture. Soil and water nanoremediation, plant nanoprotection and plant nanonutrition are some of the agricultural applications. To accomplish sustainable progress in horticultural plants challenged with various environmental challenges, numerous definitive directions have been developed to secure public acceptance and convenient utilization of nanoparticles. Even with the rapid increase in nanoparticle use in several applications, there is still a dearth of information on the actual outcomes of nanoparticle interaction with plants. This review assesses the role of nanomaterials in horticultural crops under abiotic stress, with a focus on recent research. In addition, this review focuses on explaining the broad roles of several nanoparticles in enhancing abiotic stress tolerance in horticulture plants.
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Introduction
Horticultural crops comprise a broad range of commodities like vegetables and fruits. They are widely grown around the world, and their production is complex (Ghosh et al. 2022a). Various factors influence production such as soil, weather, cropping systems, as well as the interplay between such factors. Environmental factors such as salinity, drought, heavy metals, extreme low or high temperatures, high ultraviolet (UV) radiation, or low light, soil alkalinity or acidity and nutrient deficiency directly or indirectly influence plant growth and development (Rao et al. 2016; Ghosh et al. 2021, 2022a, b). In accordance to the agricultural records, crop cultivation through the selection of parameters such as accelerated growth, increased seed and fruit productivity and biomass accumulation does not ameliorate stress tolerance in plants. Under stressful conditions, vegetative growth and reproductive development are restrained as the first line of defence against stress, allowing the plant to consume all metabolic precursors and energy resources to withstand the injurious impact of stress (Boscaiu et al. 2008). Based on an estimation of the Food and Agriculture Organization (FAO 2017), agricultural productivity in developing countries will be required to rise to 70% to keep up with population growth, which will increase to 9.1 billion by 2050. Indubitably, environmental factors like global warming and climate variability participate in decreasing crop productivity (Bedair et al. 2020, 2022b; Bedair 2020).
The impact of climate variation on crop productivity is inevitable and can detrimentally affect plant growth and development through higher carbon dioxide levels as well as variations in temperature and precipitation patterns. A major reduction, however, in crop productivity results from factors other than global warming and include flooding, nutrient depletion, soil erosion and salinity, and water deficiency (Bedair et al. 2020; Iqbal et al. 2020; Shaltout and Bedair 2022; Bedair et al. 2022a). Production of stress-tolerant plants can be a promising and convenient approach to overcome the issue of decreasing crop productivity. Conventional breeding approaches have not achieved sought-after success in improving crop plant tolerance to stress using inter-generic or inter-specific hybridization. This is due to the low genetic diversity of yield constituents under stressed conditions, the inadequacy of efficient and proper selection criteria, and the intricacy of stress tolerance-related traits.
Hence, it is important to explore alternative techniques for developing stress-tolerant crops. Conventional breeding technologies such as hybridization, selection, mutation and polyploidy have been employed in the genetic improvement of crop plants. Despite the prevalence of various effective crop improvement strategies, agricultural crop yields are presently immutable and there are food shortages and destitution in developing countries (Bedair et al. 2022a, b). It is important, therefore, to develop novel techniques to be utilized in tandem with available advanced and conventional breeding methods.
Novel and promising agricultural strategies, capable of reforming modern agriculture, are needed to increase food productivity and limit the use of pesticides and fertilizers to curb environmental pollution (Bedair et al. 2022a; Alduhaidhawi et al. 2022; Akinyemi et al. 2022; Raheem et al. 2021). Amongst the diverse technologies, nanotechnology is currently the most prevalent in plant biotechnology and agriculture (Diab et al. 2020a, b; Scrinis and Lyons 2007). Application of nanomaterials such as nanodevices or nanoparticles exerts positive and negative effects on all developmental stages of plant crops. Nanotechnology encompasses nanoparticles, which are administered for crop improvement as well as mitigation of stresses (Das and Das 2019; Moraru et al. 2003). Nanotechnology can be utilized to develop effective methods to manage environmental conditions, improve crop productivity and nutritional content, increase plant tolerance/resistance to adverse environmental conditions and detection of plant and animal diseases (Khan et al. 2017; Singhal et al. 2016; Tarafdar et al. 2013). The current review focuses immensely on the numerous types of nanoparticles and their implication on horticultural crop plants, particularly towards growth, performance and extenuation of abiotic stress tolerance in the plant such as salinity, high/low temperature, drought, and nutrient insufficiency to attain sustainable agriculture.
Abiotic stress and horticultural crops
Abiotic stress is a pervasive challenge, which influences the productivity and quality of horticultural crops (Helaly 2017). A variety of abiotic stresses such as soil salinity, flooding and extreme temperature (heat, frost and cold) affect the vegetative and reproductive stages of crop growth and development. Such stresses induce damage to the cellular machinery by provoking multiple molecular, physiological, and biochemical alternations in the plants (Mushtaq et al. 2020; Rai et al. 2011). Stress caused by exterior environmental stimuli can diminish yields as plants rely on their energy reserves in response to stress rather than on growth and reproduction. Boyer (1982) reported that the average yield of crops was lowered by about 70% by abiotic stresses inflicted by adverse environments (Boyer 1982; La Pena and Hughes 2007). Yields of various crops are decreased between 13% and 94% by drought stress, depending on stress duration and intensity (Farooq et al. 2009). In accordance with the future scenarios, adaptation and mitigation are of utmost importance for improved resilience capacity of agricultural systems and increased crop productivity and quality. Plant crops cannot avoid environmental stress, therefore a wide variety of multi-level strategies should be developed like agronomical technologies or breeding of highly tolerant cultivars (Mariani and Ferrante 2017).
At the 2010 annual conference of the American Society for Horticultural Sciences, Vegetable Breeding and Stress Physiology working groups highlighted the importance of “Improvement of Horticultural Crops for Abiotic Stress Tolerance” to preserve the sustainability of the horticultural industry to changing climates (Mou 2011). Recent studies on climate change effects focus on major crops, whereas only a few reports on vegetables and fruit yield, quality and the supply chain (Bisbis et al. 2018; Parajuli et al. 2019). It is essential to consider the impact of the combination of two or more unfavourable stress conditions at the same time. Most of the time, crops are exposed to a variety of stressful factors that take place simultaneously. As a result, investigating the stresses independently will not be sufficient, as plant response cannot be predicted solely from individual outcomes, but rather from a mixture of stresses (Choudhury et al. 2017; Mittler 2006; Rivero et al. 2014). Therefore, growing high-quality vegetables is an important goal to meet the needs of the population and the increasing demand for fruit and vegetables (Bulgari et al. 2019).
Horticultural crops’ tolerance to abiotic stress is important due to their relatively higher monetary value compared to field crops. Furthermore, horticultural crops are the main source of various nutrients, carbohydrates, fibres, and minerals, which are essential in a well-balanced diet (Shannon and Grieve 1998). During stressful conditions, harmful by-products are generated that negatively impact plants. Singlet oxygen (1O2), hydroxyl radicals (•OH), hydrogen peroxide (H2O2), and superoxide radicals are reactive oxygen species (ROS) derived from aerobic metabolism in plants (Thorpe et al. 2013). The ROS are produced when plants are under stress and at high concentrations negatively affect lipids, proteins, and DNA, which can ultimately lead to cellular damage and death (Nouman et al. 2014). In unstressed conditions, low concentrations of ROS are produced in organelles, but concentrations are increased when stressors affect the water potential and disrupt cellular homeostasis (Abbasi et al. 2007; Hussain et al. 2018). ROS are constantly formed in cells by leakage of electrons during respiration and photosynthesis (Kao 2017). To curb the overproduction of ROS and oxidative stress, plants develop an effective antioxidative defense system, which has non-enzymatic and enzymatic constituents to balance ROS generation and scavenging, to avoid cellular damage (Das and Roychoudhury 2014; Nadarajah 2020; Yin et al. 2015; Alkafaas et al. 2019). Plants not only are capable of producing ROS scavenging compounds but can also boost the bioaccumulation of compatible solutes or osmolytes such as proline and sugars.
Given that plants are sessile and have to overcome negative external conditions, they are required to adapt for survival. Survival strategies are advantageous when activated in a timely manner to anticipate and respond to irreversible changes brought about by external environmental conditions. There is a trade-off between growth/productivity and adaptation metabolism for plants because survival strategies consume energy and nutrients ordinarily used for growth and production (Bechtold and Field 2018).
Agronomic management techniques to improve tolerance of plants to abiotic stress have developed over the years, as a consequence of climate change and variability, farmers’ experiences, as well as scientific and technological advancements. Different strategies can be applied to ameliorate abiotic stresses on plant growth such as the sowing density, perfect growth period, selection of proper cultivar, and provision of the correct amount of fertilizers and water (Mariani and Ferrante 2017). Despite the success of agronomic strategies in alleviating the adverse consequences of abiotic stresses, their application is often insufficient. Currently, scientists confer high tolerance levels to distinct abiotic stress by transferring one or multiple genes engaged in signalling and regulatory pathways, or encoding essential molecules like antioxidants and osmolytes (Wang et al. 2003). Several studies identified multiple regulatory and functional genes that conferred tolerance to abiotic stress. Results of such studies served as the basis to introduce tolerance traits in cultivated crops. Considering that various stress-tolerance-associated physiological traits are under multigenic control, the manipulation of an individual gene is not sufficient. Consequently, regulatory genes, including transcription factors, have gained interest due to their high potential to regulate a broad spectrum of downstream stress-responding genes simultaneously (Singhal et al. 2016; Zhuang et al. 2014). However, genetic improvement still encounters various challenges that make it complicated and often inefficient. These challenges include insufficient data about minor cultivars’ genomes, complex responses to abiotic factors, genetic diversity existing within vegetable species and limited available strategies. In addition to the huge germplasm diversity, there are two equally vital factors affecting plant tolerance to stress, namely stress features (frequency, time and riskiness and impacted tissue) and developmental stages of crop plants (Sade et al. 2018; Shah et al. 2018).
In vitro selection is another efficient strategy to develop plant tolerance to abiotic stress. An in vitro tissue culture-dependent approach provides an understanding of biochemical and physiological responses of plants cultured under stressful environmental conditions. The in vitro technique makes it possible to develop drought and salinity resistant lines in a variety of plant species including vegetable crops (Pérez-Clemente and Gómez-Cadenas 2012). Biostimulants such as nanoparticles can be used to induce stress tolerance when applied to vegetables grown under abiotic stress (Colla and Rouphael 2015; Van Oosten et al. 2017).
Nanotechnology a promising approach
Nanotechnology is normally recognized as the control, application, and manipulation of living and non-living matter at atomic, molecular, and supramolecular scales (Diab et al. 2020b; Kumar et al. 2020, 2021, 2022). Nanotechnology applications have spread throughout an array of sectors to such an extent that the UE Commission identified it as a “key enabling technology”, which is crucial for international competitiveness (Gallocchio et al. 2015; Parisi et al. 2015). Structures and devices smaller than 100 nm have been developed and manipulated in at least one dimension to create nanomaterials with novel properties, many of which have been developed for multi-sector applications (McNeil 2005; Pérez-Labrada et al. 2020; Qu et al. 2013; Hoet et al. 2004). Nanotechnology involves processing, synthesizing, manipulating and deploying nanomaterials (with one or various proportions in the order of 100 nm or less) (Abd Elkodous et al. 2021; Diab et al. 2020a). It has been established that nanomaterials exhibit unparalleled optical characteristics, size-dependent features, as well as large surface area, thus making a remarkable contribution to nutrition and plant protection (Liu et al. 2009; Nair et al. 2010).
Owing to their multifunctionality as well as distinctive characteristics such as large surface area, shape, solubility, chemical properties, and degree of agglomeration, nanomaterials have been used effectively in a broad range of fields including agriculture, medicine, cosmetics and engineering (Alves et al. 2018; Fakoya and Shah 2017; Hong and Dobrovolskaia 2019). In agriculture, the application of nanoparticles to crops augments their growth, development, quality and production, and also enhances tolerance to unfavourable environmental conditions. Plants have considerable potential to induce natural mineralized nano-materials production under specific conditions (Wang et al. 2001). It is envisaged that a better understanding will open up possibilities for farmers and customers to exploit nanotechnology, which will result in an economic driving force with no negative impact on the environment and human health (Saxena et al. 2016).
Examples of nanoparticles and their role in stress acclimation
Silver nanoparticles (AgNPs)
Silver nanoparticles (AgNPs) can be used in a diverse range of commercial applications and have been applied successfully in textile coatings, food packaging, pesticides and more. Their potential applications in fields such as bioengineering, drug-gene delivery, biomedical sciences and electronics are also noted (Ahamed et al. 2010; Bechert et al. 1999; Jo et al. 2009; Korkin and Rosei 2008). A thorough understanding of nanoparticles will allow their applications in agriculture, particularly in crop betterment. It has been reported that the application of AgNPs at certain concentrations can contribute considerably to seed germination, growth and development of plants (Szymanski and Dobrucka 2021; Saxena et al. 2016; Shelar and Chavan 2015). Extreme concentrations of silver are toxic to plants, but nanotechnology affects a radical change to the properties of metal nanoparticles relative to that of bulk materials.
Chemical reduction is considered one of the most prevalent methods for the synthesis of AgNPs, which are characterized using visible ultraviolet spectrophotometry (UV-Vis). Synthesis of AgNPs is observed at maximum absorption of 425 nm. The average size range of synthesized nanoparticles, as inferred by transmission electron microscopy (TEM) was recorded between 25 and 50 nm. The specific size in a study conducted by Sharma et al. (2012) was found to be 29 nm (Sharma et al. 2012). Such a study revealed the growth-improving properties of AgNPs in Brassica juncea where the chemically synthesized particles improved the activities of antioxidant enzymes, thereby reducing the levels of hazardous reactive oxygen species (ROS). Another study demonstrated the improvement in the overall antioxidant status of pearl millet leaves based on the decline in concentrations of the stress marker proline, enhancement of the antioxidant activity and triggering ion homeostasis (Khan et al. 2020). According to this study, the growth stimulatory impact of synthesized AgNPs was dose-dependent with 20 mM AgNPs the optimum for eliciting growth and antioxidant response.
ZnO nanoparticles (ZnO NPs)
The application of micronutrient fertilizers can improve plant resistance to a diverse range of environmental stresses such as salinity and drought. Zinc is among the micronutrients that is needed for optimal plant growth and development (Baybordi 2005; Saxena et al. 2016; Akpomie et al. 2021b). The degree of impact depends on the plant type as well as the size and dose of ZnO NPs (Ma et al. 2010; Khodakovskaya et al. 2009). The ZnO NPs improve antioxidant metabolites and enzymes in plants, thereby alleviating heavy metal stress (Venkatachalam et al. 2017). In this regard, Pokhrel and Dubey (2013) reported that the use of ZnO NPs enhanced the growth of two agriculturally important crop plants, cabbage and maize (Pokhrel and Dubey 2013). Tomato seedlings treated with ZnO NPs exhibited higher seed germination, growth, and biomass production than untreated controls (Panwar 2012). Furthermore, ZnO NPs conferred tolerance in plants to a variety of abiotic stresses like salinity, drought and heavy metals by the upregulation of various antioxidant enzyme activities (Baybordi 2005; Chanu and Upadhyaya 2019; Taran et al. 2017).
Plants utilize very small Zn concentrations; therefore, nano concentrations of Zn guarantee the required amount for growth and development. Slightly elevated concentrations of ZnO were found to have minimal impact on the soil quality and were thus considered an eco-friendly and bio-friendly green reagent (Saxena et al. 2016; Pandey et al. 2010).
TiO2 nanoparticles (TiO2 NPs)
TiO2 or titanium (IV) oxide is the ninth most plentiful compound found in the earth’s crust and occurs naturally in various types of sand and rock. TiO2 nanoparticles (TiO2 NPs) significantly impact a diverse range of crops on physiological, morphological and biochemical levels (Bhatt et al. 2020; Mishra et al. 2014).
The application of nanoscale TiO2 NPs markedly increased rubisco and antioxidant enzyme activities, chlorophyll biosynthesis and photosynthetic rate, thereby enhancing overall crop productivity (Lei et al. 2008). TiO2 is considered an efficient stimulant for plants, which triggers the activation of numerous defense mechanisms in plant tolerance towards abiotic stress conditions (Lei et al. 2008). TiO2 NPs favorably influences growth, antioxidant enzyme activity, and concentrations of total amino acids, proline and soluble sugars, along with a decrease in malondialdehyde and H2O2 in broad bean plants grown under salt stress (Gohari et al. 2020).
Nano-anatase TiO2 has an underlying photocatalytic characteristic, which enhances the absorbance of light and the conversion of light energy to electrical and chemical energy, promotes carbon dioxide assimilation, and safeguards chloroplasts from aging after long periods of illumination (Hong et al. 2005; Yang et al. 2006). Nano-anatase TiO2 induced the activity of ribulose-1,5-bisphosphate carboxylase-oxygenase (RuBisCO), which led to the promotion of RuBisCO carboxylation, thus stimulating plant growth (Gao et al. 2006; Ma et al. 2008) reported that nano-anatase may act at the gene level by inducing the expression of the marker gene for RuBisCO activase (RCA) mRNA, which increases the production of proteins, leading to improved RuBisCO carboxylation and enhanced rate of photosynthetic carbon reactions (Ma et al. 2008). In addition, TiO2 NPs can be applied exogenously to enhance net photosynthetic rate, stomatal conductance and rate of transpiration in plants (Chaudhary and Singh 2020; Qi et al. 2013).
Silicon nanoparticles (SiNPs)
Silicon is the second most plentiful element in the earth’s crust, after oxygen and also one of the major mineral constituents of several plants (Epstein 1999). More than 25% of the earth’s crust is silicon (Currie and Perry 2007). Silicon occurs within plants when it is absorbed from the soil as monosilicic acid [Si(OH)4]. Silicon influences plant growth, development, and stress responses. During the past years, silicon has been considered a feasible option in the adaptation of plants to abiotic stresses such as salinity, heavy metal toxicity and drought (Tripathi et al. 2016; Liang et al. 2007) reported principal mechanisms of Si application in the mitigation of abiotic stress (Liang et al. 2007). Firstly, inducement of stress response systems through an improved synthesis of antioxidants. Secondly, co-precipitation or complexation of noxious metal ions with Si. Thirdly, immobilization of toxic ions in growth media. Fourthly, compartmentalization of metal ions within plants. Fifthly, modification of uptake rates of toxic or rare elements (Liang et al. 2007; Hegazy et al. 2015). SiO2 nanoparticle application was reported to promote seed germination and antioxidant enzyme activity in tomato and squash plants under salinity stress (Haghighi et al. 2014; Siddiqui et al. 2014).
Generally, nanomaterials comprise a number of molecules smaller than 100 nm. The SiNPs assume novel biological, chemical, and physical characteristics (Ruffini Castiglione and Cremonini 2009). Derosa et al. (2010) reported that SiNPs application increased plant growth and productivity under harsh stresses (DeRosa et al. 2010). This function is attributed to SiNPs absorption by roots where they form films at the cell walls, thus enabling the plant to combat stress toxicity and induce productivity. Seemingly, the addition of high levels of SiNPs during irrigation of pear seedlings did not produce any acute toxicity on plant biology. Furthermore, Alsaeedi et al. (2017) reported the growth-promoting impact of SiNPs on the development stages of Phaseolus vulgaris (Alsaeedi et al. 2017). They demonstrated that Phaseolus vulgaris treated with 300 mg/L SiNPs improved seed germination, shoot and root elongation rate, as well as seedling dry and wet contents compared to non-treated controls.
Iron nanoparticles (FeNPs)
Micronutrients, namely copper, iron, and zinc actively contribute to optimal growth and development in plants. They are considered to be the essential elements and serve as cofactors and components for the regulation of several biochemical pathways within plant cells. Iron nanoparticles (FeNPs) are part of iron-sulfur-binding and haem proteins that are involved in sulfur and nitrogen assimilation as well as photosynthetic processes in plants (Bhatt et al. 2020; Van Hoewyk et al. 2007; Akpomie et al. 2021a). Iron has the potential to augment crop production and yield as well as regulate environmental contamination. This is ascribed to the ability of iron to improve efficiency by slowing down nutrient release, reducing nutrient loss by limiting transformation from uptake to discarded forms, lowering the required expenses and mitigating salinity stress toxicity by decreasing soluble salt accumulation in roots (Huang et al. 2015; Davar Zareii et al. 2014; Atar et al. 2015) indicated the stimulatory effect of iron oxide nanoparticles on enzymes such as peroxidase, catalase, and cytochrome oxidase (Atar et al. 2015). Iron oxide nanoparticles exhibit a key role in expurgating the environment from heavy metals/metalloids like cadmium, arsenic, lead, and mercury owing to their intrinsic properties of ligand sorption by forming inner-sphere complexes (Li et al. 2014; Yoon et al. 2014). Their significant role in the removal of organic contaminants including atrazine and chlorinated organic solvents from water, is also recognized and well documented (Li et al. 2015; Zhao et al. 2015; Zia-ur-Rehman et al. 2018).
Intrinsic reactivity between antioxidant enzymes and nanoparticles
Nanoparticles improve water stress in plants by increasing water uptake and root hydraulic conductance and amending the quantity of proteins involved in oxidation-reduction reactions, ROS detoxification, stress signalling, and hormone pathways (Das and Das 2019). Metal nanoparticles limit the generation of ROS by acting as antioxidants and enhancing the antioxidant activity of plant cells (Ye et al. 2019). Catalytic reactivity, small size, and huge surface area of nanoparticles facilitate chemical and mechanical interaction with biological systems (Das and Das 2019).
Alabdallah and Alzahrani (2020) reported that okra treated with ZnO NPs or foliar applied bulk ZNO increased chlorophyll a and b, total chlorophyll, and carotenoid under salt stress compared to control plants (Alabdallah and Alzahrani 2020). Additionally, the bulk ZnO and ZnO NPs controlled proline and total soluble sugar accumulation in the stressed okra. Application of ZnO NPs resulted in a higher Zn concentration that improved protochlorophyllide formation, favorably influenced chloroplast development, and aided in photosystem II repair (Hänsch and Mendel 2009; Salama et al. 2019).The addition of ZnO NPs increased superoxide dismutase and catalase activity in saline stressed plants, with the superoxide dismutase expression in leaves making them more effective at reducing oxidative stress (Pavithra et al. 2017; Alabdallah and Alzahrani 2020) found that okra treated with ZnO NPs resulted in high levels of both these antioxidant enzymes (Alabdallah and Alzahrani 2020). The increase in catalase activity in plants treated with ZnO NPs indicates effective enzyme alteration.
Sharma et al. (2012) showed that AgNPs reduced the concentration of ROS in plants and increased the activity of antioxidant enzymes (ascorbate peroxidase, guaiacol peroxidase, and catalase) (Sharma et al. 2012). In stressed Brassica juncea, gold nanoparticles (GNPs) enhanced the antioxidant enzyme activity of ascorbate peroxidase, guaiacol peroxidase, catalase and glutathione reductase, along with the higher accumulation of H2O2 and proline (Gunjan and Zaidi 2014). Application of GNPs substantially increased H2O2 and proline content. Furthermore, Gunjan et al. (2014) observed an increase in the activity of glutathione reductase, ascorbate peroxidase and guaiacol peroxidase when 400 ppm GNPs was applied; maximum activity of glutathione reductase was observed at 200 ppm GNPs. Also, cerium oxide (CeO2) nanoparticles enhanced responses of antioxidant enzymes (ascorbate peroxidase, catalase and guaiacol peroxidase) activity in leaves, roots and stems of stressed kidney beans (Majumdar et al. 2014). Furthermore, CeO2 nanoparticle exposure increased the activity of guaiacol peroxidase in leaves, which helped to maintain cellular homeostasis (Yang et al. 2017).
Effect of nanoparticles on antioxidant enzymes at the molecular level
A proteomic study revealed that the application of different concentrations of AgNPs on plant roots resulted in the dissipation of a proton motive force. Accumulated protein precursors, which involved an oxidative stress pathway, Ca2+ regulation, signaling, transcription, protein degradation, cell wall synthesis and DNA/RNA/protein direct damage, cell division, and apoptosis (Mirzajani et al. 2014; Landa et al. 2012) showed the effect of ZnO NPs and TiO2 NPs on gene expression in roots of Arabidopsis thaliana (Landa et al. 2012). It was observed that gene expression differed more than 2-fold before and after application of nanoparticles where there was down regulation of 826, 189, 74 genes and up-regulation of 232, 660 and 80 genes (Das and Das 2019). The genes triggered by ZnO NPs and TiO2 NPs were mostly stress-related ontology groups, which encompassed both abiotic (oxidative, salt, and water deprivation) and biotic (wounding and pathogen defense) stimuli (Das and Das 2019).
Effect of nanoparticles on plant hormones
Plant hormones are active organic molecules produced by the plant’s metabolism that can regulate physiological and stress responses during growth and act as a toxicity index (Santner et al. 2009). Plant hormone synthesis was significantly influenced by nanoparticles. Phytohormone concentrations decreased after rice seedlings were exposed to carbon nanotubes (Hao et al. 2016). CeO2 NPs application showed no significant effect on indole-3-acetic acid, abscisic acid and gibberellic acid, and decreased the content of transzeatin-riboside by 25% in plant leaves (Nhan et al. 2015; Bleecker and Kende 2000) observed that the interaction between indole-3-acetic acid and ethylene significantly decreased because Ag ions prevented the synthesis of ethylene (Bleecker and Kende 2000). In a study conducted on Arabidopsis thaliana, the biosynthesis of cytokinins and auxins in shoot apices was gradually reduced when the concentration of ZnO NPs was increased. In contrast, cis-zeatin levels in roots were extremely high. In addition, greater doses of ZnO NPs increased abscisic acid levels, particularly in the apices and leaves (Van Oosten et al. 2017). Furthermore, in Brassica napus, treatment with nano selenium and nano zinc oxide reduced the expression of abscisic acid-related genes while considerably increasing the expression of gibberellic acid-related genes (El-Badri et al. 2021).
Mechanism behind nanoparticle, plant system interaction
Many factors affect nanoparticle uptake, translocation, and accumulation including plant species as well as type, size, chemical composition, functionalization and stability of the nanoparticle (Das and Das 2019; Dietz and Herth 2011) clarified that lateral root connections allow nanoparticles to enter the plant root system, and the cortex and pericycle allow access to the xylem (Dietz and Herth 2011). When nanoparticles enter the plant and interact with the intrinsic systems, chemical processes occur, which create ROS, ion cell membrane transport activity, oxidative damage and lipid peroxidation. Kurepa et al. (2010) and Watanabe et al. (2008) demonstrated that when nanoparticles enter plant cells, they react with sulfhydryl and carboxyl groups, altering protein function (Kurepa et al. 2010; Watanabe et al. 2008). The nanoparticles may bind to membrane transporters or root exudates and then be transferred into the plants. Nanoparticles, when used as a spray on the leaves, move from the leaves to the roots, stems, and developing grain, as well as from one root to the next. The xylem is one of the key pathways for uptake and transfer to the plant’s shoots and leaves (Miralles et al. 2012). Nanoparticles can penetrate the leaf cuticle, enter the cytoplasm and bind to various organelles, interfering with metabolic processes at that location (Zhang and Monteiro-Riviere 2009). According to Unrine et al. (2012), AgNPs, 20 nm in size, may be transported inside the cells through the plasmodesmata (Unrine et al. 2012).
Abiotic stress in horticulture crops and the impact of nanoparticles
Literature on the impact of nanoparticles on abiotic stress in horticultural crops is summarised in Table 1.
Effect of nanoparticles on salt stress
Dwindling high-quality water resources and a growing population force farmers to irrigate crops with highly saline water (Rossi et al. 2016). It is well recognized that salinity negatively affects negatively on plant physiology and biochemistry, leading to a serious threat to crop production and food security (Rossi et al. 2016). Meanwhile, engineered nanoparticles are increasingly detected in irrigation water and agricultural soils due to the rapid advancement of nanotechnology (Rossi et al. 2016).
The application of K2SO4 nanoparticles enhanced plants’ physiological response to salt stress by reducing electrolyte leakage, increasing catalase and proline content, and increasing antioxidant enzyme activity (El-Sharkawy et al. 2017). SiO2 nanoparticles increased the activity of antioxidant enzymes of potato (Gowayed et al. 2017). The AgNPs improved seed germination and seedling growth in tomato (Almutairi 2016). In addition, ZnO NPs improved salinity resistance in banana (Deepika et al. 2018) and tomato (Alharby et al. 2017). Fe2O3 nanoparticles induced plant adaptation to salinity stress in ajowan (Abdoli et al. 2020).
Heat stress and nanomaterials
The greenly synthesized AgNPs using Moringa oleifera leaf extract was proved to protect wheat plants against heat stress by improving morphological growth (Iqbal et al. 2019). Se nanoparticles were found to improve chlorophyll content, hydration and growth of tomato plants (Djanaguiraman et al. 2018). Furthermore, the application of TiO2 on tomato enhanced photosynthesis and induced stomatal opening, leading to cooling of leaves (Qi et al. 2013). Heat stress in cucumber plants has been reported to be alleviated by foliar application of Se NPs, which increased relative water content, proline, CAT, and POD activities (Shalaby et al. 2021).
Computational modeling of abiotic stresses
Computational techniques for the modeling of abiotic stress have been conducted in previous studies. Different computational approaches have been applied to study processes leading to or arising from abiotic stresses. Most studies have been performed using density functional theory (DFT), molecular dynamics (MD) simulations, and quantum mechanics/molecular mechanics (QM/MM) simulations. In addition, there are also a few studies based on machine learning and finite element methods that have been reported related to the modeling of abiotic stress. Generally, the computational approaches that have been applied to the modeling of abiotic stress involve solving differential equations (Lai et al. 2020).
Several processes are occurring around stress in plants making exceptionally challenging computational modeling. Therefore, computational modeling is being performed to understand specific mechanisms around abiotic stress. Iron dioxygenases that take part in several processes important for plants (and living organisms in general) also operate as stress responses (Li et al. 2017; Liu et al. 2013). Flavanone-3β-hydroxylase, a nonheme dioxygenase, transforms naringenin into dihydroflavonol on an iron (II) center. This transformation has been studied by Zeb et al. (2019) using density functional theory(Zianna et al. 2019). Solvent effects have been taken into account using the continuum polarized conductor model (CPCM) with the dielectric constant of chlorobenzene. They have identified the active sites of Flavanone-3β-hydroxylase and calculated the reaction rates constants by identifying all the stable and transition state structures along the formation paths (Zeb et al. 2019).
It should be noted that DFT has been used in the identification of active sites of different molecules involved in abiotic stress (Tong et al. 2020; Mateyise et al. 2021). Molecular modeling of iron deficiency specific clone 3 (IDS3) has been performed by Mathpal et al. (2018) on hexaploid wheat (Mathpal et al. 2018). They have performed molecular dynamics simulations in order to test the fluctuations and the stability in the protein model of IDS3. Leaf transpiration is a crucial parameter to understand plant stress. Defraeye et al. (2014) have performed three-dimensional cross-scale modeling approach to understand the convective mass transport in leaves. They have used computational fluid dynamics to explicitly model the stomata which materialize the leaf transpiration (Defraeye et al. 2014).
Choudhury et al. (2021) have examined the metalloid stress in rice arising from six metal ions, namely As3+, As5+, Cd2+, Cu2+, Pb2+ and Zn2+ (Choudhury et al. 2021). They have calculated the related binding geometry, the relative affinity, and the electrostatic surfaces of the interaction of these ions with dehydroascorbate reductase (DHAR). Using molecular docking simulations, it has been reported that the binding free energies of the ions vary from − 16.21 to -16.23 kcal/mol, while those of the metabolites range from − 50.64 to -81.56 kcal/mol. They have concluded that the metabolites could enhance the metal/metalloid-induced stress responses in high quantities (Choudhury et al. 2021). Recently, Filiz and Kurt (2019) and Filiz and Aydın Akbudak (2020) have investigated the genes responsible for iron homeostasis and transport in different plants (Filiz and Kurt 2019; Filiz and Aydın Akbudak 2020). The permease in the chloroplast 1 (PIC1) gene has been investigated in four plants: sorghum, tomato, maize, and arabidopsis. The investigation has been performed using different online computational tools for genes analysis. It has been found that up to 21 GO terms related to PIC1 are responsible for iron transport and homeostasis (Filiz and Aydın Akbudak 2020). In addition, the authors have also examined the FIT (Fer-like iron deficiency-induced transcription factor) genes in ten plants in order to investigate iron uptake in these plants (Filiz and Kurt 2019). Several online computational tools have been used for the analysis of the genes. It has been found that FIT is a vital target to regulate stress responses (Filiz and Kurt 2019).
In addition to the aforementioned methodological approaches, some studies have used machine learning to examine stresses in plants. Ma et al. (2014) have examined abiotic stress expression in Arabidopsis thaliana using machine learning. The machine learning used is implemented in R as machine learning-based differential networks analysis (mlDNA). The authors have trained a machine to learn 32 expressions of known stress-related genes. The trained machine has been used to predict candidate stress-related genes (Ma et al. 2014; Ni et al. 2016) have also used machine learning to predict gene regulatory networks in arabidopsis. The authors have developed a machine learning model based on a support vector machine (SVM) model (Ni et al. 2016).
Data availability
Not applicable.
Abbreviations
- AgNPs:
-
Silver nanoparticles
- CeO2 NPs:
-
Cerium oxide nanoparticles
- DFT:
-
Density functional theory
- FeNPs:
-
Iron nanoparticles
- FAO:
-
Food and Agriculture Organization
- Fe2O3 :
-
Ferric oxide
- FIT:
-
Fer-like iron deficiency-induced transcription factor
- GNPs:
-
Gold nanoparticles
- H2O2 :
-
Hydrogen peroxide
- K2SO4 :
-
Potassium sulphate
- MDS:
-
Molecular dynamics simulations
- mlDNA:
-
Machine learning-based differential networks analysis
- 1O2 :
-
Singlet oxygen
- •OH:
-
Hydroxyl
- PIC1:
-
Permease in the chloroplast 1
- QM/MM:
-
Quantum mechanics/molecular mechanics
- RuBisCO:
-
Ribulose-1,5-bisphosphate carboxylase-oxygenase
- RCA:
-
RuBisCO activase
- ROS:
-
Reactive oxygen species
- SiNPs:
-
Silicon nanoparticles
- SVM:
-
Support vector machine
- TEM:
-
Transmission electron microscopy
- TiO2 NPs:
-
Titanium dioxide nanoparticles
- UV:
-
Ultraviolet
- UV-Vis:
-
Ultraviolet spectrophotometry
- ZnO NPs:
-
Zinc oxide nanoparticles
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The authors gratefully acknowledge the support from Tanta University, Tanta, Menofia University, Menofia, Egypt and University of Maroua, Maroua, Cameroon. The authors also thankful to University of the Free State, Bloemfontein, South Africa for their constant support for the accomplishment of this study. We are also thankful to Dr. Swagata Ghosh, Assistant Professor of English, Symbiosis Institute of Technology, Symbiosis International University, Pune, India for editing this manuscript.
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Abdelsalam, I.M., Ghosh, S., AlKafaas, S.S. et al. Nanotechnology as a tool for abiotic stress mitigation in horticultural crops. Biologia 78, 163–178 (2023). https://doi.org/10.1007/s11756-022-01251-z
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DOI: https://doi.org/10.1007/s11756-022-01251-z