Chief EditorPradeep K. Sharma
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Application of Nanobiotechnology in Enabling Plants to Overcome Water-logging Stress: A Review
First Online 20-06-2023|
Oxygen deficiency in waterlogged soils is relatively fast and can occur within a few hours depending on prevailing conditions (Nishiuchi et al., 2012; Ansari et al., 2015). The diffusion rate of oxygen in water is approximately 104 times slower than in air. This reduces O2 flux by about 32×104 times when soil pores fill with water (Armstrong and Drew, 2002; Colmer and Flowers, 2008; Ansari et al., 2016). The real cause of harm to plants in waterlogged soil is the slow diffusion of gas in the water. The rapid O2 consumption by soil microorganisms, leads to insufficient oxygen uptake of subsoil tissues (Ozturk et al., 2009). In addition to O2 deficiency, CO2 and ethylene concentrations are increased in the soil. Furthermore, other toxic substances such as iron, manganese and hydrogen sulfide, are produced under waterlogged conditions; causing serious damage to plants (Pampana et al., 2016; Setter et al., 2009; Ansari et al., 2018). Thus, the growth and development of most commercial crops are impeded under waterlogged conditions (Nishiuchi et al., 2012).
Plants can build up different mechanisms to respond to negative conditions, while responses may differ even for the same species. Therefore, for sustainable agriculture and increased crop production, identification of naturally tolerant plants or increasing of stress tolerance of existing plants have important. In recent years, nanotechnology has emerged as a multi-disciplinary research area that offers significant opportunities to improve tools and technologies for research and transformation of the biological sciences (Fortina et al., 2005; Saxena et al., 2016; Manzer et al., 2015; Ansari et al., 2020) and nanobiotechnological practices for the mitigation of the adverse effects of water logging have attracted much research interest. The potential applications of nanotechnology in various agriculture sectors are given in Fig 1.
Thus, the objective of this the review is to explore the potential applications of various NPs in agriculture to achieve sustainable crop productivity, with particular emphasis on the benefits of the unique properties exhibited by a diverse range of nanoparticles and their impact on plant growth and especially on the mechanism of tolerance to water- logging stress.
Nanoparticles (NPs) are very small molecular clusters ranging between 1-100 nm (Roco, 2003) in diameter. The most important difference of nanomaterials from other materials is their increased relative surface area and quantum effects. Their exceedingly small dimensions often result in diverse and unique physicochemical properties such as diverse particle morphology, large surface area, flexible pore size and increased reactivity, when compared to their bulk material counterparts (Nel et al., 2006; Ansari et al., 2019). As NPs generally exhibit a high surface to volume ratio and high surface energy, their chemical and biochemical reactivity are also relatively higher than to their bulk counterparts (Dubchak et al., 2010).
Some important properties are summarized in (Fig 2). These include size, morphology, aspect ratio, hydrophobicity, surface area/roughness, surface contaminations /adsorption, solubility-release of toxic species, Reactive Oxygen Species (ROS) production capacity, competitive binding sites with receptor and dispersion/ aggregation, structure/composition (Somasundaran et al., 2010; Ansari et al., 2021b).
Nanoparticles can be synthesised by biological, chemical or physical means (Muruganantham et al., 2018). There is substantial previous work on the synthesis of both metal (Ag, Au, Pd) and metal oxide (Fe3O4, SiO2, TiO2, ZnO) nanomaterials. While chemical synthesis of NPs was initially popular, in the recent years, biosynthesis, also referred to as Green synthesis, of metallic NPs using plants or plants extract, has also become popular (Javad and Butt, 2018; Gude et al., 2013). This is because plants contain a wide range of phytochemicals including alcohols, amines, phenolics, terpenoids, flavonoids, latex and enzyme cofactors which can play a role as stabilizing and reducing agents during the green synthesis of metal nanoparticles from metal salt solutions. Such green synthetic methods are popular because they are cost-effective, eco-friendly and provide a controlled synthesis with well-defined shape and size (Kumar and Yadav, 2009; Siddiqui et al., 2014; Ahmed et al., 2019).
Nanoparticles in agriculture and plant growth
NPs are used in agriculture to regulate the processes such as plant growth and development, increasing yields, and avoiding various stress factors (Saxena et al., 2016). NPs are generally classified in agriculture as carbon nanomaterials (NMs), metal NPs and metal-oxide NPs.
Various types and compositions of NPs are available, and are selected by application areas rather than through systematic studies. The most commonly used NPs in plant sciences are Ag, Au, Ti, Zn. Numerous studies have been carried out to identify the effects of different NPs on plant species, and to solve their mechanisms of action. The effects produced by these materials are believed to depend the NPs type, the species and the substrate (i.e., culture medium, hydroponics or soil) of plant. However, there are often many inconsistencies between comparable studies and therefore, many problems covering the biological effects of nanoparticles cannot be solved (Manzer et al., 2015; Ansari et al., 2021a).
Role of carbon NMs in plant growth
Carbon NMs have unique chemical, electrical, mechanical and thermal properties. The most commonly used carbon-based nanomaterials are fullerene (C70), fullerol (C60 (OH) 20) and carbon nanotubes (single walled-SWCNT and multiwalled-MWCNT) (Verma et al., 2018). It is known that Fullerene, fullerol and carbon nanotubes increase water holding capacity, biomass, fruit yield and secondary metabolite production in plants (Ahmed et al., 2019). Scientists demonstrated the impact of NMs on germination, growth and development in order to increase agricultural applications.
In a study where different concentrations of fullerol were applied to bitter melon seeds, it was found that seed productivity, biomass, fruit number, water content and secondary metabolite content increased (Husen and Siddiqi, 2016). A study carried out with tomato revealed that when seeds exposed to MWCNTs, germination rate and biomass enhanced considerably (Khodakovskaya et al., 2009).
Role of metal NPs in plant growth
A number of studies demonstrated that metal NPs raise plant growth and development. Au NPs may lead to an improvement in crop productivity, depending on the chlorophyll and sugar content, leaf area, number of leaves, plant height that (Gopinath et al., 2014). Likewise, Au NPs play a considerable role in seed germination and antioxidant defense system of Arabidopsis thaliana (Siddiqui et al., 2014).
Silver nanoparticles have been reported to possess a wide range of applications including biological tagging in medicine, coatings on domestic products, in electronics, food packaging, medical drug delivery and pesticides (Kumar and Yadav, 2009; Siddiqui et al., 2014). Silver nanoparticle treatments are also increasing in the agriculture mainly as crop improvement agents, where varied studies have shown that AgNPs have enhanced seed germination as well as growth and development in plants (Ahmed et al., 2019). The effect of silver nanoparticles (AgNPs) on seven varieties of Mill tomatoes seed germination was were investigated. This study demonstrated that seeds treated with five concentrations of AgNPs sprouted earlier than seeds germinated with deionized water (Gopinath et al., 2014). Similarly, the effects of six different silver nanoparticle concentrations (viz; 0, 25, 50, 100, 200 and 400 ppm) on the growth and antioxidative enzymes of oriental mustard seedlings were studied, exhibiting that silver nanoparticles induced an increase in chlorophyll content, root and shoot length and antioxidant defence enzymes (Husen and Siddiqi, 2016).
The role of metal oxide NPs in plant growth
Favourable effects of metal oxide nanoparticles on plant growth and development including for example, nano-sized Titanium dioxide (TiO2) , Zinc oxide (ZnO) (Saif et al., 2014), and Ca nanoparticles (Reddy et al., 2017) have been reported on plant growth and develoment.
Zheng et al., (2019), showed enhanced spinach growth when Titanium Dioxide -NPs were applied to either the seeds or leaves. This was attributed to TiO2-NPs increasing the activities of several enzymes and supporting nitrate adsorption, accelerating the formation of inorganic nitrogen to organic nitrogen (Sebastian et al., 2018).
TiO2 NP stimulated plant growth and development when applied to seeds (Setter et al., 2009). Increases in dry, fresh weight, chlorophyll content, Rubisco activity and photosynthetic rate were observed in S. oleraceae when exposed to anatase TiO2 NPs (Verma et al., 2018). Seed germination, plumule growth and radicle of canola seedlings were induced by TiO2 NPs (Husen and Siddiqi, 2016). Enhanced plant growth was caused by promoting activities of Rubisco and chlorophyll formation (Khodakovskaya et al., 2009).
It was noticed that the germination rate increased when sage seeds were exposed to TiO2 nanoparticles (Sebastian et al., 2018). Feizi et al., (2010) detected an increase in Salvia’s germination rate when they exposed 21-day-old seeds to 60 mg.L-1 batch of nano-sized Titanium Dioxide. This application did not have any important effect on biomass or root-shoot elongation. The lowest average germination time was observed when 60 mg L-1 concentration was applied; and the average germination time did not improve at higher concentrations.
TiO2 NPs are photocatalytic in nature and can perform an oxidation-reduction reaction to form hydroxide and superoxide anion radical when exposed to light (Villagarcia et al., 2012).
Fe oxide NPs improved root length in pumpkin (Saif et al., 2014), and the pod and leaf dry weight in soybean (Saxena et al., 2014). According to Singh and Nara (2013), RuO2 nanoparticles increased the germination rate and seedling growth of the oriental mustard.
Many studies have been undertaken in controlled aquatic environments so that a complete ecosystem and food chain could be represented and variations induced by high sensitivity to environmental factors could be eliminated. For example, Juhel et al., (2015), examined the alumina effects NPs on the photosynthesis, growth and morphology of Lemna minor. Since Lemnaceae family is ideal in stress adaptation and / or toxicity studies; these plants are preferred for regulatory toxicity tests and ecotoxicological tests of chemicals. The hypothesis was that aluminium oxide NPs (alumina and Al2O3-NP) could enhance L. minor growth, of based on published results demonstrating that Al NPs could improve the electron transfer efficiency of isolated photosynthetic reaction centres (Roco, 2018). They used engineered Al NPs to study basic mechanisms of the alumina NP-mediated growth stimulation and to investigate the effects on photosynthesis, growth and morphology.
Zinc (Zn), is an essential micronutrient for optimum plant growth and development, facilitating critical metabolic reactions in plants. Zn is required at low concentrations, so the presence of Zn at nano levels provides an appropriate amount of Zn distribution to the plant to be used by plants for growth and development. Therefore, ZnO may be conceived as bio-friendly as well as eco-friendly material that can be used as a green reagent for plants (Rehman et al., 2016). Low concentrations of ZnO NPs are known to increase seed germination in wheat (Phukan et al., 2016). Few studies have shown that suitable concentrations (1.5 mg/mL) of ZnO nanoparticles yielded increases in biomass production in Cicer arietinum as compared to ZnSO4 treatment (Siddiqui et al., 2014). Cyamopsis tetragonoloba subjected to ZnO NPs, showed increased chlorophyll content, root-shoot length, protein synthesis and biomass (Rey et al., 2019).
Silicon (Si), being abundant in soil, is one of the most important nanoparticles and its role in plant plant growth, development and defence is acknowledged and well documented (Pampana et al., 2016). Si NPs also demonstrated growth-promoting effect during the development stages in corn, particularly on seed germination, RWC, photosynthetic pigment, root and shoot elongation. Considerable increase in these features were observed when exposed to various concentrations of SiO2 compared to the control group (Fortina et al., 2015). Many other studies have investigated the effect of Silicon oxide nanoparticles on the germination and growth of plants. Some of them have shown that nano-SiO2 particles were absorbed faster and better than micro- SiO2, H4SiO4, Na2SiO3. When applied on seeds and root of corn, were they could be instantly utilized by plants for their growth and development (Reddy et al., 2017). No toxic consequences were found on plants when pear seedlings were irrigated with nano-SiO2 high concentrations (Fortina et al., 2015).
Thus, NPs have numerous positive impacts on plant growth and the effectiveness of NPs differs from plant to plant, depending on the concentrations used (Table 1). The role of nanoparticles is dependent on their size, surface area, reactivity, chemical composition and concentration level to which they respond positively (Thombre et al., 2014). More work is required to understand the relationship between the identified growth response and the environment. This chapter discusses the role of NPs in promoting seed germination, photosynthesis and plant growth.
Role of nanoparticles on mitigating adverse environmental conditions
In addition to their role in growth and development, nanoparticles also play an important role in increasing various stress tolerances and reducing deleterious effects of heavy metals in the environment.
It was demonstrated that TiO2 nanoparticles increased various stress tolerances (Drought, Salinity and water) by affecting different processes such as malondialdehyde (MDA) and superoxide radicals accumulation, and by simultaneously inducing activities of antioxidant defence enzymes such as ascorbate peroxidise, catalase, guaiacol peroxidase and superoxide dismutase of Spinach (Rehman et al., 2016).
González-Melendi et al., (2011) have shown, that carbon-coated iron NPs have potential use in plants as nano-device delivery systems. Their hypothesis was that NPs binding to agricultural chemicals (or other substances including pollutants) could reduce the contaminant amounts released to the environment, reducing the damage to plant tissues (Sebastian et al., 2018). Their studies attempted to validate the hypothesis by providing a set of tools for the determination and analysis of carbon-coated Fe magnetic core shell nanoparticles applied to plants. The concentration of magnetic NPs in selected plant tissues was determined by the magnetic field gradients. This study revealed that NPs can be loaded with diverse substances before they are taken up by plants and can be concentrated into localized areas using magnets, providing evidence for the wide potential applications of magnetic NPs in agriculture (Thombre et al., 2014).
Water logging stress
Among the abiotic stresses, alkalinity, drought, salinity, water-logging are the main factors that conduce to reduce crop growth and productivity (Pucciariello et al., 2014). Heavy rains can result in fields flooding if appropriate drainage is not provided. Other effective causes are flooding of water in rivers and increased groundwater table. Besides, extreme irrigation also results upshots in temporary water-logging in plants. All of these conditions cause either hypoxia (partial anaerobiosis) or anoxia (full anaerobiosis) in the soil and air is expelled from the soil pores (Gopinath et al., 2014).
Water logging not only causes an oxygen deficiency, which is dissipated 104 times less in water than in air (Gopinath et al., 2014), it also produces toxic compounds that inhibit growth and eventually cause the death of plants. Anoxia and hypoxia cause suppression of breathing, a state of energy deficiency, and an increase in genes associated with abscisic acid and ethylene synthesis. These are important strategies in adaptation to waterlogging (Phukan et al., 2016). Two of the other adaptable strategies are the nodal root formation in the air-water interphase and the aeranchymatous cell developments in the root cortex to ease diffusion of oxygen (Nishiuchi et al., 2012).
Thus, in the efforts to minimize these adverse effects using nanoparticles, it is important to know if the observed effect in plants is increasing water-logging tolerance or decreasing the harmful effects of water-logging (Ahmad et al., 2019). The study with saffron, an aromatic and medicinal plant species (Phukan et al., 2016), demonstrated a decrease in the root length, number of roots, root biomass caused and leaf biomass raise by water- logging stress. When Ag NPs at concentrations of 40-80 ppm was applied to saffron corms, the adverse effects of water retention stress were alleviated.
Nanotechnological applications have a potential to reduce the waterlogging stress in plants. Recently, a number of studies have evaluated nanoparticle-mediated effects on plants under different stresses, as shown in Table 2 (Fortina et al., 2005).
Plants strategies to cope with water logging
Under water-logging conditions plant roots are damaged due to lack of O2. Consequently, water-logging decreases gas exchange between the plant and the atmosphere. In fact, when plants do not receive enough oxygen for respiration, they form aerenchyma in their roots which acts as an oxygen reservoir (Ahmad et al., 2019). Longitudinal diffusion of oxygen to the root apex could be increased by induction of a barrier to radial O2 loss (ROL) that reduces oxygen loss to the environment (Fig 3, 4). Moreover, this barrier can block the movement of toxins such as reduced metal ions, and gases such as methane and carbon dioxide, from the soil to the roots (Thombre et al., 2014). The most important adaptation to flooded conditions is the formation of aerenchyma. It can occur in roots and shoots of plant species such as corn and rice.
An aerenchyma formation in plants
The aerenchyma formation is significant for the functioning and survival of plants faced with waterlogging. It provides the transfer of oxygen and aeration of gases (i.e. CO2, CH4) from roots to shoots (Prathna et al., 2011). Aerenchyma forms as a result of exposure to various stress factors such as waterlogging, nutrient deficiencies and mechanical impedance in corn roots. Under waterlogged conditions, ethylene can accumulate in submerged tissue, inducing genes involved in the aerenchyma formation (Sebastian et al., 2018). The aerenchyma could be providing a photosynthetic advantage by collecting carbon dioxide from root respiration and transferring it to the leaf intercellular spaces in various species (Saif et al., 2014).
Aerenchyma can be generated by one of two mechanisms: (i) schizogeny, (ii) lysigeny (i) Schizogenous aerenchyma, that improves by extremely regulated cell separation and differential cell enlargement, which forms spaces between cells without causing death of cells (e.g. Rumex palustris) and (ii) while lysogenous aerenchyma, which is formed by programmed cell death (PCD), creating gas spaces in the plants root cortical region (Saif et al., 2014); for example, it was observed in maize (Reddy et al., 2017), rice (Gopinath et al., 2014), and wheat (Verma et al., 2018).
Aerenchyma can be created by both mechanisms in many species like duck potatoes (Husen and Siddiqi, 2016). While lysogenous aerenchyma occurs in the cortex of the roots, it can occur in the cortex and pith cavity of the stems (Khodakovskaya et al., 2009). Under normal growth conditions, lysigenous aerenchyma in most wetland plants might be developed mainly in their roots, e.g., in for example, common rush and rice. Its formation is enhanced when the soil is full with water. Lysigenous aerenchyma is stimulated during waterlogging in the dryland plants, such as corn (Gopinath et al., 2014) and its formation could be further increased during waterlogging (Fig 3) (Srinivasan and Saraswathi, 2010).
During the formation of aerenchyma in the root of rice, cells in the mid-cortex die first and then cell death radially spreads to other cortical cells (Lin and Xing, 2007). The epidermis, endodermis, exodermis and stele could be unaffected, demonstrating that lysigenous aerenchyma formation took place via closely controlled mechanisms (Saif et al., 2014). However, root lysogenic aerenchyma of non-wetland species (barley, corn, wheat, etc.) may not occur in well-drained soils, indicating that insufficient aeration may have a stimulating effect (Khodakovskaya et al., 2009).
Signalling mechanism of lysigenous aerenchyma formation
In maize and rice, ethylene, a hydrocarbon that could be diffuse inside and outside of plant tissues from both exogenous and endogenous reservoirs and which is also a gaseous plant hormone, plays a key role in hypoxic stress (Husen and Siddiqi, 2016). Ethylene promotes lysogenic aerenchyme formation (Khodakovskaya et al., 2009). Ethylene is simply produced from methionine and is first converted to S-adenosylmethionine (AdoMet) through Sadenosylmethionine synthase. AdoMet is then converted to 1-aminocyclopropane-1-carboxylate (ACC) by ACC synthase (ACS). ACC oxidase (ACO) generates ethylene via oxidizing ACC in a reaction which is also produces carbon dioxide (CO2) and hydrogen cyanide (HCN), respectively. Ethylene as a plant hormone is concerned with regulating processes of cell death (Husen and Siddiqi, 2016). Several of the adaptive growth responses take place in response to ethylene that is accumulated in under submerge water tissues (Reddy et al., 2017). This accumulation yields a reduction in diffusion from the plant to the wrap around water and simultaneous stimulation of the biosynthesis of this hormone during stress conditions (Khodakovskaya et al., 2009). The roots of rice form lysigenous aerenchyma even under well-ventilated conditions (Srinivasan and Saraswathi, 2010). Corn roots promote the expression of the biosynthetic mechanism that results in increased ethylene production under hypoxic conditions (Ahmad et al., 2019). The process of programmed cell death (PCD), that appears in the corn roots during the lysigenous aerenchyma formation, seems be regulated through ethylene (Husen and Siddiqi, 2016). Surprisingly, the hypoxic treatment sharply enhanced production of ethylene in maize roots within few hours, for example; in 3 h as compared to under aerobic conditions. Exposure of corn roots to ethylene action inhibitors, such as silver ions, or biosynthesis inhibitors such as aminooxyacetic acid, aminoethoxyvinylglycine, and cobalt chlorethylene prevents the formation of aerenchyma in the hypoxic stuation (Ahmad et al., 2019). The 1-methylcyclopropene use, an ethylene inhibitor, in corn roots completely stops the formation of aeranchyma under hypoxic states (Husen and Siddiqi, 2016).
Lysigenous aerenchyma formation in the rice root could be enhanced more via ethylene treatment under aerated conditions, however, a reduction through application with an ethylene perception inhibitor, for example; Ag ions below stagnant (0.1% agar) deoxygenated a condition that mimics anoxic conditions (Husen and Siddiqi, 2016). In these days ethylene has been found to increase aerenchyme formation of root in a rice variety which is known as Calrose (Villagarcia et al., 2012).
Cell wall degradation during lysigenous aerenchyma formation
Although there are many physiological studies on lysigenous aerenchyma formation, there is very little literature on the genes that make for this formation. of late a study done by Rajhi et al., (2014) in maize roots exposed a gene related to the lysigenous aerenchyma formation by using a microarray investigation together with a laser microdissection technique. It was reported that under waterlogged conditions, calcium depending signalling genes encoding those are potentially known as calcineurin and calmodulin-like proteins was more modulated and simultaneously the expression levels of these two proteins were more prominent in the cortical cells, as compared to the stelar cells of roots of maize (Husen and Siddiqi, 2016). Interestingly, waterlogging also stimulates the expression of genes associated with the cell wall. Stimulation of the expressions of Ca2+signalling and cell wall alteration associated genes is supposed to be inhibited via the treatment with 1-methylcyclopropene. These findings confirm the mechanisms of ethylene-arbitrated lysigenous aerenchyma formation (Fig 3) (Prathna et al., 2011).
Radial oxygen loss (rol) barrier formation
During waterlogging conditions, internal aeration is supposed to be very essential for the root growth and development of plants. Moreover, in some wetland species a structural barrier that hinders O2 outflow from the roots, basal part is known as a radial oxygen loss barrier (Prathna et al., 2011). This radial oxygen loss barrier sharply reduces the oxygen-transported loss through the aerenchyma to the root tips and modifies root growth into anoxic soil. Interestingly, a few plant roots successfully develop the radial oxygen loss barrier during waterlogging conditions (Ahmad et al., 2017). Moreover, the roots of some wetland plants may comprise well-developed aerenchyma that generally maintains a low resistance pathway for oxygen diffusion from the shoots to the roots (Nishiuchi et al., 2012). Interestingly, a few wetland species also can form a barrier to radial oxygen loss (Phukan et al., 2016). This radial oxygen loss barrier forms from the root basal parts and ultimately suppresses the oxygen transported loss through aerenchyma to the root apex.
CONCLUSIONS AND PROSPECTS
Waterlogging, defined as the soil condition where excess water limits the gas diffusion, is one such environmental stress causing substantial yield losses. Waterlogging conditions hinder the internal aeration necessary for the growth and development of roots in plants. Although different mechanisms including aerenchyma formation and a barrier to radial oxygen loss have been discussed, more work also has to be done on the chemical and anatomical nature of the barrier to ROL barrier versus nutrient and water uptake, respectively.
In recent years, nanobiotechnology has been gaining momentum as a possible means for enhancing crop yields and mitigating the adverse effects of various environmental stresses. However, it is imperative to elucidate the exact mechanisms of the interactions of NPs with plants at both the molecular, genetic and cellular levels, so that these aforementioned favourable effects of nanoparticles can be fully exploited. Rigorous studies are required to understand the molecular, biochemical, and physiological mechanisms of plants in response to NP treatment as well as their influence on the gene expression regulation in plants regarding stress management, including the stress of waterlogging.
STATEMENTS OF DECLARATIONS
The authors have no relevant financial or non-financial interests to disclose.
Conflict of interest
The authors declare no potential conflict of interest ralated to this study.
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