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Review

Multifarious Effects of Arsenic on Plants and Strategies for Mitigation

by
Rahul Beniwal
,
Radheshyam Yadav
and
Wusirika Ramakrishna
*
Department of Biochemistry, Central University of Punjab, Ghudda 151401, Punjab, India
*
Author to whom correspondence should be addressed.
Agriculture 2023, 13(2), 401; https://doi.org/10.3390/agriculture13020401
Submission received: 30 December 2022 / Revised: 25 January 2023 / Accepted: 4 February 2023 / Published: 8 February 2023
(This article belongs to the Section Ecosystem, Environment and Climate Change in Agriculture)
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Abstract

:
Arsenic contamination in soil and water is a major problem worldwide. Inorganic arsenic is widely present as arsenate and arsenite. Arsenic is transferred to crops through the soil and irrigation water. It is reported to reduce crop production in plants and can cause a wide array of diseases in humans, including different types of cancers, premature delivery, stillbirth, and spontaneous abortion. Arsenic methyltransferase (AS3MT) in the human body converts inorganic arsenic into monomethylarsonic acid and dimethylarsinic acid, which are later excreted from the body. Arsenic transfer from the soil to grains of rice involves different transporters such as Lsi1, Lsi2, and Lsi6. These transporters are also required for the transfer of silicate, which makes them important for the plant. Different mitigation strategies have been used to mitigate arsenic from crops, such as plant growth-promoting bacteria, fungi, and nanoparticles, as well as using different plant genotypes and plant extracts. Different factors such as nitric oxide, Fe, and jasmonate also affect the response of a plant to the oxidative stress caused by arsenic. This review highlights the various effects of arsenic on plants with respect to their biochemical, molecular, and physiological aspects and the employment of classical and innovative methods for their mitigation. The current review is expected to initiate further research to improve As remediation to mitigate the effect of heavy metal pollution on the environment.

1. Introduction

Rice is a predominant staple food in Asia [1]. One of the major issues affecting rice is the accumulation of arsenic in rice grains. Arsenic is a metalloid, showing properties of both a metal and a non-metal [2]. Arsenic is the 20th most commonly found element in the earth’s crust. As(III) (+3) and As(V) (+5) are the two dominant forms of inorganic arsenic in anaerobic and aerobic environments, respectively [3,4]. However, arsenic is also found as elemental arsenic (0) and arsine (−3). Monomethylarsonic acid (MMA) and dimethylarsinic acid (DMA) represent the dominant organic arsenic forms present in paddy fields [5]. Arsenic affects stomatal conductance, transpiration, oxidative stress, protein synthesis, and chlorophyll content [6]. The soil type, soil pH, arsenic content in irrigation water, nutrient supply, silt content, and mugineic acid excreted by some grasses affect arsenic uptake [7]. The concentration of arsenic is highest in rice roots and lowest in the grain, while at an intermediate level in the shoot [8]. Similarly, arsenic can accumulate in wheat in the following order: awns < glumes < grains < leaves < and rachises of stems < roots [9]. Polishing, washing, and rinse-free rice preparation can reduce the inorganic arsenic content in brown and white rice, but cooking does not affect the amount of inorganic As [10].
Humans are exposed to arsenic through food, air, and drinking water [2,11,12]. Vegetables, grains, meat, and fish contain arsenic naturally and can serve as a source of exposure. Arsenic contamination of the groundwater currently affects more than 70 countries, including India, China, Argentina, and Bangladesh [13,14,15,16]. In India, Assam, West Bengal, Jharkhand, Bihar, Chhattisgarh, Uttar Pradesh, and Manipur are affected by arsenic pollution [17]. Mining, the burning of fossil fuels, volcanic activities, the smelting of non-ferrous metals, the pharmaceutical industries, animal feed additives, agriculture chemicals, and glass-making are the major contributors to arsenic pollution of the water, air, and soil [13,18]. The major exit route for As from the human body is urine [19]. For the excretion of As in urine, arsenic methyltransferase (AS3MT) converts arsenic into monomethylarsonic acid and dimethylarsinic acid using S-adenosylmethionine (SAM) as a methyl group donor [20]. Single nucleotide polymorphism can affect the activity of AS3MT. In humans, a small quantity of As is also excreted as inorganic arsenic (iAs). Upon a reduction in AS3MT activity, the expression of tumor suppressor gene p16 is reduced, which leads to cancer. In one study, when mice were treated with cefoperazone, their gut microbiota was reduced about three times. When these cefoperazone-treated mice were given 25 and 100 ppm iAs in their drinking water, it resulted in up to 87 and 93% less excretion of arsenic in their stool, and a major accumulation of As occurred in the mice’s lungs [21]. The mice with cefoperazone and AS3MT knockout were more sensitive to even 25 ppm iAs, which is not the case in the wild-type or AS3MT-knockout-only mice. This study suggested that both the gut microbiota and ASS3MT are required for protection against iAs toxicity. The aim of this review is to highlight the state-of-the-art research on arsenic accumulation and toxicity in plants as well as its remediation using rhizospheric microbes, nanotechnology, and other methods.

2. Effect of Arsenic on Plants

Arsenic, when present in the soil or irrigation water, is toxic to plants [22]. Although the degree of toxicity varies with the plant species, the effects are almost the same. Arsenic exhibits both physiological and morphological effects on plants. Increased lipid peroxidation, superoxide dismutase (SOD), ascorbate peroxidase (APX), and glutathione reductase (GR) activity are common symptoms shown by plants such as soybean, rice, black gram, spinach, and barley under arsenic stress (Table 1). Exposure to arsenic further activates phosphate transporters, which are responsible for As and phosphate uptake [23].
Exposure to As can bring about epigenetic changes in plants. For example, in Pteris cretica (L.) var. Albo-lineata, exposure to 100 mg As kg−1 reduced the methylation at cytosine (5 mC) [32]. Arsenic affects oxidative phosphorylation and adenosine triphosphate synthesis because of its similar structure to adenosine triphosphate [33]. Ethylene production, membrane damage, hindered root hair growth, reduced chlorophyll content, transpiration efficiency, abscission in plant leaves, and increased oxidative stress weaken the protein synthesis system in the presence of arsenic, which in turn hinders plant growth [14,24,34,35]. Plant exposure to As can also lead to chlorosis and necrosis [36]. Arsenic accumulation in the root and shoot is dose-dependent [37]. The exposure of rice to arsenate leads to reduced glutathione content, a reduced glutathione/glutathione disulfide ratio, and increased phytochelatins (PCs) [34]. Ceratophyllum demersum pigments showed the first sign of arsenic toxicity, while the change in the arsenic form and its distribution was a lethal sign of toxicity. Arsenic is accumulated in young mature leaves when they are exposed to 1µM of arsenic, where it may replace phosphate or interfere with nucleic acid synthesis. The effect of As on chlorophyll is attributed to hampered synthesis rather than degradation [38]. Electron transfer inhibition during photosynthesis is responsible for oxidative stress in plants under As stress [39].

3. Arsenite and Arsenate Transporters Mediated Transport from Soil and Root to Various Plant Tissues

In the reduced environment of the rice fields, As(V) is converted into As(III) [34]. Although As can be transported into caryopsis at any growth stage, this occurs mainly during the grain-filling stage. Arsenic accumulation in the roots occurs from the seedling to the heading stage, while transport to the shoot occurs from the heading to the milk stage in rice [40]. The generally accepted model of the apoplastic and symplastic movements of nutrients is not followed by rice plants, because they have two Casparian strips at the exodermis and endodermis [41]. As a result, influx and efflux transporters are required in both the exodermis and the endodermis, a structure that is referred to as the coupled transcellular pathway. Arsenic is stored mainly intracellularly in the epidermis of the leaf tissue rather than the mesophyll. The arsenic distribution in the leaf tissue of Ceratophyllum demersum is dose-dependent. It is stored in the nucleus at low concentration and in the vacuole at high concentration. This may be due to the lack of a driving force inside the nucleus after reaching a certain concentration, leading to other compartments serving as storage targets [38]. As(III) is taken up via low silicon rice (Lsi) transporters: Lsi1, Lsi2, and Lsi6. Lsi1 is a member of the Nodulin 26-like intrinsic protein (NIPs) group of aquaporins and transfers As(III) passively from the soil to the root, while Lsi2 actively translocates As(III) to the shoot (Figure 1) [39,40,42,43]. Lsi1 is an influx transporter, while Lsi2 is an efflux transporter, and the two are localized in the exodermal and endodermal cells, respectively, with different plasma membrane polarities [44]. OsLsi1 and OsLsi2 are located on the distal and proximal sides of the Casparian strip, respectively (Table 2) [40]. OsLsi is also responsible for the efflux of As(III), which is the main form transported from root to shoot [45,46,47]. High sulfur content can reduce the root-to-shoot distribution by as much as 10% and bring the translocation factor down to 0.1. High sulfur treatment can decrease arsenic transporters OsLsi1, OsLsi2, and OsNIP1;1, which indicates that high sulfur can decrease the arsenic accumulation in the shoot as compared to low sulfur [37]. Rice low arsenic line 3 (las3), which has a single base substitution in the alcohol dehydrogenase (ADH2) gene, accumulated almost 30% less arsenic in the grain and more than 60% less arsenic in the straw as compared to the wild type [48]. Mutated OsADH2 was unable to accumulate arsenic in the roots. Due to the mutated OsADH2, the rice did not accumulate As and Si after the heading stage, but the non-mutated plants continued to accumulate arsenic and silicate. The expression of OsLsi1 and OsLsi2 was found to be downregulated [48]. OsNRAMP1 (Natural Resistance-Associated Macrophage Protein transporter 1) is upregulated in both arsenic-tolerant and sensitive rice cultivars under arsenite stress. OsNRAMP1 expression in Arabidopsis increased the plant’s tolerance to arsenite and cadmium, which was accompanied by an increased accumulation of both heavy metals in the root and shoot tissues. AtABCC1 and AtABCC2 expression increased in the transgenic Arabidopsis that had OsNRAMP1, which may be the reason for the higher accumulation of arsenite [49]. OsNRAMP1 may contribute to xylem loading, as its expression was enhanced in the plasma membrane of the endodermis and pericycle cells based on the OsNRAMP1:green fluorescent protein (GFP) fusion protein in Arabidopsis.
AtPht1;1 and AtPht1;4, located on the plasma membrane, and belonging to the Phosphate transporter 1 (Pht1) superfamily, are responsible for As(V) uptake in Arabidopsis [51]. AtPHT1;8 and AtPHT1;9 contribute to arsenate uptake under P-deficient conditions. AtPHT1;5 are responsible for translocating arsenate and Pi from source to sink [52]. OsMATE2, belonging to the multidrug and toxic compound extrusion (MATE) family, is upregulated six-fold in seeds under arsenate exposure [53]. The heterologous overexpression of OsMATE2 in tobacco resulted in a change in the As transfer coefficient from root to shoot, increased cell injury, and increased ROS. The downregulation of OsMATE2 in rice grains resulted in decreased arsenic levels in the rice grains. Once inside the cell, As(V) is reduced to As(III) by arsenate reductases OsHACs inside the cell. In rice, the As(V) uptake is mediated through the P transporters OsPht1;4 and OsPht1;8 (Figure 1) [44,47,54]. The overexpression of a vacuolar phosphate transporter 1 (VPT1) gene makes Arabidopsis more sensitive to arsenate, and a mutation in this gene leads to an increased tolerance. The root hair length is improved in the VPT1 mutant of Arabidopsis as compared to the wild-type Arabidopsis under arsenic stress. VPT1 overexpression also leads to higher arsenic accumulation, and VPT1 mutation leads to lower arsenic accumulation. Under Pi-sufficient conditions, a mutation in VPT1 leads to a higher Pi content in the cytosol, which downregulates the expression of phosphate transporters [55]. Both phosphate deficiency and arsenic exposure can induce PvPht1;4 [41]. The overexpression of OsNIP1;1 and OsNIP1;3 reduced As(III) xylem loading and, hence, translocation to the rice shoot [23]. OsNIP1;1 and OsNIP3;3 overexpression resulted in a decrease in As(III) transport to the shoots, which led to the bidirectional nature of both transporters. On the other hand, the knockout of both did not affect the As(III) transport to shoot and root, which indicates that OsLsi1 and OsLsi2 are the principal As(III) transporters [23]. The role of OsLsi1 further extends to the uptake of monomethylarsonic acid (MMA) and dimethylarsinic acid (DMA) (Figure 1). As(V) has a high affinity with minerals and is relatively immobile [56,57]. The silicate efflux transporter Lsi2 is responsible for the transfer of As(III) to the xylem, thereby providing access to the rice shoot. Phytochelatins are metal-binding peptides derived from glutathione. Phytochelatins perform the first step in arsenic detoxification by chelating arsenic with their thiol group, after which this metalloid-PCs complex is taken up by the vacuole. The ABCC-type transporters AtABCC1 and AtABCC2 are responsible for transferring this As-PCs complex in the vacuole of Arabidopsis thaliana [58]. The storage form of arsenic in the aerial parts of the Pteris gametophyte is As(III) [59]. Although a mutant for Lsi2 reduced the As content by 51-63% compared to the wild type, it also reduced the rice grain yield by 60%, as it reduced silicon uptake [60,61]. The OsABCC1 expression is tissue-specific when compared to its ubiquitous expression in transgenic rice [62]. From the seedling to the heading stage, the OsABCC1 expression is increased, and it reaches a maximum at the jointing stage [40]. The C-type ATP-binding cassette (ABC) transporter OsABCC7, with efflux transport activity for both As-PCs/GS3, is localized in the xylem parenchyma cells in the stele of rice roots and is involved in the root to the shoot transport of As(III), with a moderate contribution to As accumulation in the shoot (Table 2) [47].
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Figure 1. Different transporters for arsenic uptake, their roles, and factors affecting arsenic uptake. Low silicon rice gene 1 (OsLsi1) product transfers AsIII, monomethylarsonic acid (MMA), and dimethylarsinic acid (DMA) from soil to root, Low silicon rice gene 2 (OsLsi2) product transfers AsIII from root to shoot, phosphate transporters (OsPht1:4 and OsPht1:4) transfer arsenate from soil to root, and C-type ATP-binding cassette (ABC) transporter (OsABCC7) transfers arsenite-phytochelatins complex (AsIII-PCs) from root to shoot. Soil pH, soil type, irrigation water nutrient supply, slit content, and muginic acid affect arsenic uptake by roots. Adapted from Khan et al. [63].
Figure 1. Different transporters for arsenic uptake, their roles, and factors affecting arsenic uptake. Low silicon rice gene 1 (OsLsi1) product transfers AsIII, monomethylarsonic acid (MMA), and dimethylarsinic acid (DMA) from soil to root, Low silicon rice gene 2 (OsLsi2) product transfers AsIII from root to shoot, phosphate transporters (OsPht1:4 and OsPht1:4) transfer arsenate from soil to root, and C-type ATP-binding cassette (ABC) transporter (OsABCC7) transfers arsenite-phytochelatins complex (AsIII-PCs) from root to shoot. Soil pH, soil type, irrigation water nutrient supply, slit content, and muginic acid affect arsenic uptake by roots. Adapted from Khan et al. [63].
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The arsenite efflux protein ACR3 is present in bacteria, fungi, moss, ferns, and gymnosperms, but is absent in angiosperms [58]. ACR3 acts as an As(III) antiporter and increases the translocation of free As(III) [50]. ACR3 localized in the vacuolar membrane of Pteris vittata gametophyte and sporophyte roots is upregulated in the presence of arsenic. Among the four ACR3, PvACR3;2, located on the plasma membrane, increased the translocation factor four to seven times in tobacco plants. The effect of PvACR3;3 is quite opposite to that of PvACR3;2, as it decreases translocation to the shoots, which indicates that it may be involved in the vacuolar transport of As in the root. Further, PvACR3;1 increased the As(III) accumulation into the root vacuole and decreased the As(III) translocation to the shoots under both As(III) and As(V) exposure [44]. PvACR3;1 also decreases the As levels in the grain.

4. Phytoremediation and Rhizoremediation to Mitigate the Toxic Effects of Arsenic

Plants produce osmolytes, proline and glycine betaine (GB), and enzymatic and nonenzymatic antioxidants to cope with the increased amount of ROS [6]. Phytoremediation is a method that uses the plant to absorb contaminants from the water and soil [36,64]. Pteris vittata (Chinese brake fern) is the first known hyperaccumulator of arsenic with a highly efficient root-to-frond translocation of As with a translocation factor of more than 20 [50,54]. Long-term arsenic presence in soil may put selective pressure on the rhizosphere bacteria [35,65]. Rhizospheric microorganisms affect the speciation and bioavailability of arsenic, resulting in a changed phytotoxicity (Figure 2). The bioaccumulation factor is used to measure the capacity of a plant to accumulate As. The bioaccumulation in Brassica juncea plants occurs in the vegetative phase. Brassica juncea produces brassinosteroids such as castasterone, typhasterol, teasterone, and 24-Epibrassinolide under As stress, which contribute to the stress protection response [24]. E. crassipes roots have a higher bioaccumulation factor than its leaves, and more arsenic is accumulated in the roots [36]. Rhizosphere bacteria with plant-growth-promoting ability and As tolerance can be utilized for bioremediation and rhizoremediation [66,67,68].
Brevundimonas diminuta has been reported to localize As in the roots, reduce As uptake by the shoot, and have a plant-growth-promoting activity [35]. The ability of bacteria to reduce arsenic uptake and increase plant growth was observed in both C3 (barley) and C4 (maize) plants. An actinomycete, Nocardiopsis lucentensis S5, isolated from As-contaminated soil, reduced the arsenic uptake in both maize and barley by increasing the As retention in the rhizosphere [69]. It increased the citric acid production by the roots. Citric acid has a chelating activity and affects pH, which in turn affects the arsenic’s bioavailability (Figure 2). Nocardiopsis lucentensis S5 improved the biomass compared to plants with As alone, which is attributed to improved detoxification mechanisms [69].
The fungus Piriformospora indica colonized the roots of rice plants and reduced the translocation of As to the shoot (Figure 2) [14]. The presence of As can increase fungal colonization up to four times, which may indicate that plant–fungus interaction is plant need dependent or controlled by the plant. P. indica treatment of arsenic-treated plant improves the growth, biomass, primary root growth, secondary root number, and proline content and decreases the translocation factor in hydroponic rice plants. P. indica adsorbs 4 mg of arsenic per gram of cell wall and stores it in the vacuoles and the cell wall. P. indica immobilizes arsenic in the root and improves the oxidative damage status of the plant [14]. An increase in the pigment content, carotenoid content, non-photochemical quenching, transpiration rate, net photosynthesis, Fe accumulation, glyoxalase system I and II activity and ascorbic acid/oxidized ascorbic acid, and a reduced glutathione (GSH) to oxidized glutathione (GSSG) ratio, reduced MDA and methylglyoxal content, and As translocation to the shoot by downregulating Lsi2 expression were observed under As stress [42]. P. indica further increased the expression of phytochelatins by upregulating the OsPCS1 and OsPCS2 genes, which increased the sequestration of As sequestration in the vacuole (Figure 2).
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Figure 2. Remediation methods and their effects on the plant under arsenic (As) stress. Rhizospheric microbes regulate arsenic speciation, decrease translocation from root to shoot, and enhance citric acid production by roots, which in turn influences soil pH and bioavailability of arsenic in the soil. P. indica downregulates low silicon rice (Lsi2) and upregulates phytochelatins encoding genes (OsPCS1 and OsPCS2) which decrease As translocation to shoot. Continuous flooding increases arsenic uptake and translocation and regulates arsenic speciation in soil. Methyl jasmonate and magnesium oxide nanoparticles (MgO-NPs) reduce arsenic translocation from root to shoot. (Adapted from [42,63,70].
Figure 2. Remediation methods and their effects on the plant under arsenic (As) stress. Rhizospheric microbes regulate arsenic speciation, decrease translocation from root to shoot, and enhance citric acid production by roots, which in turn influences soil pH and bioavailability of arsenic in the soil. P. indica downregulates low silicon rice (Lsi2) and upregulates phytochelatins encoding genes (OsPCS1 and OsPCS2) which decrease As translocation to shoot. Continuous flooding increases arsenic uptake and translocation and regulates arsenic speciation in soil. Methyl jasmonate and magnesium oxide nanoparticles (MgO-NPs) reduce arsenic translocation from root to shoot. (Adapted from [42,63,70].
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5. Arsenic Accumulation Depends on Plant Genotype

Different genotypes respond differently to As toxicity in terms of their biomass and length. For instance, black gram with a longer root length and more shoot weight are less affected by arsenic toxicity [17]. A negative correlation of silica with arsenic was observed in temperate japonica and tropical japonica, but no correlation was found in indica, aus, and aromatic rice varieties [43]. Applying silica to reduce the arsenic in the grain does not solve the problem, as silica only reduces 20% of grain As [60]. The arsenic concentration in the shoots is significantly affected by genotype. Indica genotypes accumulate less arsenite in the shoot as compared to the hybrid genotypes Xiangfengyou9 (‘XFY-9’) and Shenyou9586 (‘SY-9586’) [71]. Arsenic accumulates differently in diverse wheat varieties [9]. Similarly, an As-sensitive barley variety, ZDB475, accumulated about nine times the arsenic compared to the As-resistant variety ZDB160 [25]. The genotype also affects the shoot silicon in rice varieties, but the correlation between shoot As and shoot silicon is subpopulation specific. Temperate japonica shows a strong correlation between shoot silicon and grain As, while the correlation is weaker in tropical japonica, and no correlation was observed in aus and indica [43].
Bacteria can tolerate arsenic by either detoxifying it or utilizing it as an energy source [72]. Bacteria use the arsenic resistance (ars) system and arsenic methylation and related pathways for detoxifying organoarsenicals and inorganic arsenic, while the arsenite oxidation system and arsenate reduction system are used for energy generation [4]. When arsenic is accumulated or adsorbed by bacteria, its appearance can become wrinkly [35]. Bacteria can affect the As toxicity to plants by either reducing the bioavailability, and, hence, the uptake or increasing the bioavailability and, hence, the phytoremediation [33]. Halomonas sp. Exo1 isolated from the rhizosphere of the Avicennia marina can bioadsorb arsenic up to 43 mg kg−1 (dry weight) of dead cell biomass [73]. The secretion of exopolysaccharides may also increase the tolerance towards heavy metals, as reported for Halomonas sp. Exo1 against [As(III)], Cr, Cd, and Mn. Halomonas sp. Exo1 was reported to bioremediate As by bio adsorption on exopolysaccharide and by converting arsenite into arsenate. Halophilic bacteria AB402 and AB403 have a reported resistance against both As and Cu, but their tolerance is reduced in the presence of arsenic alone [33]. The tolerance in these cells was due to the adsorption of As on extracellular substances and intracellular storage.

6. Application of Nanotechnology to Counter Negative Effects of Arsenic on Plants

Supplementation with zinc oxide nanoparticles (ZnO–NPs) enhanced the shoot length, transpiration rate, shoot dry weight, ascorbate–glutathione cycle enzymes, net photosynthesis rate, total chlorophyll, stomatal conductance, carotenoid content, photochemical quenching, leaf relative water content, and root length under As stress compared to the control and reduced the MDA content, Methyl Glyoxal (MG) content, and electrolyte leakage in soybean plants (Figure 3) [6]. ZnO helped in reducing the MG content by enhancing the activities of Gly I and Gly II. ZnO supplies Zn to plants, which, under stress conditions, binds to sulfhydryl groups and phospholipids, maintaining their stability. Additional Zn also helps in the uptake of K, Mg, Ca, Fe, and P, hence maintaining organelle functionality [6]. Wu et al. [74] reported similar findings that ZnO–NPs increased the biomass, nutrients of Zn, and germination, and decreased the As uptake in rice. Iron (III) oxide nanoparticles (Fe2O3-NPs) have been reported to reduce the negative effects caused by As in Vigna radiata. Ferric chelate reductase (FCR) embedded in the plasma membrane converts Fe3+ to Fe2+, which is then transported to the plant via the Fe(II) transporter protein. Fe2O3-NPs increase the root length, dry biomass, and Fe level while decreasing the root FCR activity, H2O2, and proline content in the seedlings, as well as the MDA content. Fe2O3-NPs adhere to the seedling/plant surface and adsorb As and reduce its uptake by the plant [26]. Furthermore, composite NZVI@SiO2@ celluloses (FSC) showed a high adsorbent capacity, and they can be utilized for the removal of arsenic from water [75]. However, their utilization for different crops needs to be tested. Magnesium oxide nanoparticles (MgO-NPs) improve the plant growth, biomass, and chlorophyll content, reduce the amount of ROS, and increase antioxidant enzyme activity [76]. MgO-NPs reduce arsenic accumulation and translocation factors in a dose-dependent manner, which makes them more effective in making rice safer for consumption. B. subtilis S4 application with iron oxide nanoparticles (IONPs) on Cucurbita moschata enhances the plant growth under normal and arsenic stress [77]. Although B. subtilis S4 alone can enhance the chlorophyll, indole acetic acid, putrescine, spermidine content, net photosynthetic rate, CAT, SOD, and APX, it showed a synergistic effect in combination with IONPs. A similar synergistic effect can be seen in the reduction of the H2O2 and arsenic uptake under As stress, both of which are reported to alleviate stress.

Plant Extracts Mitigate Arsenic Effects

The As uptake by rice was reduced by 70% by the addition of Neem (Azadirachta indica) or tulsi (Ocimum sanctum) extract [77]. Both extracts also restored plant biomass and length, and decreased H2O2 and OH-, thereby protecting the seedlings by lowering lipid peroxidation. Most importantly, both extracts seem to protect protein thiols and protein carbonylation under arsenic toxicity. β-pinene at a concentration of 10µM reduces the effect of As on the root and shoot length, along with reducing the As accumulation and H2O2 content, but has no significant effect on lipoxygenase (LOX) and MDA [39]. β-pinene can protect plants by providing stability to the membrane and inducing a systemic acquired resistance. It can quench singlet oxygen species due to the presence of a double bond and provide membrane stability under Cr and As stress [39,78]. Volatile oil and aqueous extracts of Rosmarinus officinalis can reduce the chromosome aberrations caused by arsenic exposure in Allium cepa and promote DNA repair [79].

7. Interrelationship among Flooding, Nitric Oxide Production, Methyl Jasmonate, Iron, and Arsenic in Plants

Continuous flooding increased the concentration of As by 50%, from which the contribution of DMA increased from 15.5% to 29.2% in brown rice [8]. Continuous flooding increased the grain DMA 1.5-fold compared to intermittent flooding. It also increased the expression of OsLsi1 and OsLsi2 at an early filling stage in the rice while reducing the OsPCS1 and OsABCC1 expression, leading to more translocation of arsenic to the shoot. This increase in the arsenic concentration in brown rice under continuous flooding was due to the following four factors: (1) the enhanced bioavailability of arsenic to roots in the soil, (2) the upregulation of OsLsi1 and OsLsi2, (3) the decrease in PCs synthesis, and (4) the decreased vacuolar sequestration in the rice roots. However, in continuous flooding, the order of arsenic concentration inside the plant remains the same, i.e., root > shoot > grain (Figure 4) [8]. Arsenic is sequestered to Fe(hydr)oxides under non-flooded conditions, but, upon flooding, it is released into the water due to the dissolution of the Fe(hydr)oxides where As(V) is converted into As(III), which is a more mobile inorganic form [71]. Aeration reduces the arsenite concentration in the roots but increases arsenate concentration.
Nitric oxide (NO) is produced endogenously in rice roots and leaves under As stress [83]. NO is a gaseous free radical and has been reported as a stress response regulator, and it plays a role in signaling cascades [15,84]. Nitric oxide reduces the membrane damage caused by As. It can reduce the membrane damage through O2. elimination and the elimination of H2O2 by activating antioxidant signal transduction. NO also keeps the arsenic absorption system of the plant active [36]. It can reduce the H2O2 accumulation by 35% in the shoot and by 16% the H2O2 in the roots of the rice with an 25µM treatment. The 50µM treatment was more effective, as it reduced the As in the shoot by 39% and that in the root by 27%. NO also reduces MDA in As-treated plants [34]. It copes with ROS using two different strategies: firstly, it can act as a signaling molecule and trigger the plant’s antioxidative system, and, secondly, it can act as a free radical and reacting with generated ROS to neutralize them [15]. NO can increase the cell viability, the amino acids, and the nitrogen content and decrease the superoxide content and the occurrence of cell death [15,84]. It modulates the expression of aquaporins under As(III) stress to reduce its uptake. L-allo-threonine aldolase, serine acetyltransferase, and nitrate reductase involved in glycine biosynthesis, cysteine biosynthesis, and nitrogen metabolism, respectively, are upregulated by NO treatment [84]. Two glutaredoxins (GRXs), OsGRX9 and GRX4, involved in GSH maintenance and the modulation of aquaporin expression, were upregulated by NO treatment. The endogenous levels of methyl jasmonate (MJ) have been reported to increase under heavy metal stress, ozone stress, wounding, and pathogen infection. Rice plants supplemented with methyl jasmonate exhibited improved physiological and biochemical traits and reduced MDA and H2O2 contents and arsenic accumulation. MJ application under As stress also downregulated the expression of Lsi1, Lsi2, and Lsi6 [85]. When rice is treated with MJ+sodium nitroprusside (SNP) under arsenic stress, photosynthetic pigments increase significantly along with GSH1, ABCC1, and PCS gene upregulation. Nitrate reductase (NR) is one of the key enzymes responsible for the production of endogenous NO. Sodium tungstate (inhibitor of NR activity) prevents the positive effect of MJ under As stress. However, the exogenous application of NO restores the MJ-mediated impact [83]. The application of MJ under As(III) stress reduces the membrane damage caused by As(III) (Figure 4) [86].
Rice roots cause the oxidation of Fe2+ into Fe3+ by releasing O2, which leads to iron plaque formation on the root surface [87]. Iron plaque causes the adsorption of As, which increases the latter’s concentration in the rhizosphere. An Fe plaque around rice roots may act as a barrier to arsenic [56,57]. The root length increases when Fe is supplied under arsenate stress in rice as compared to arsenate alone. Fe supplementation also reduces As uptake by the root and shoot while reducing oxidative stress biomarkers such as lipid oxidation, H2O2, CAT activity, GSH, and shoot ascorbate produced under arsenic stress. Metallothionines (MTs) help in maintaining the homeostasis of essential metals while detoxifying heavy metals [88]. Overall, the arsenic levels are regulated by multiple mechanisms in plants, influenced by internal and external factors.
The efficient employment of existing technologies and the development of innovative and environment-friendly technologies is the way forward for the remediation of arsenic. The employment of phytoremediation, rhizospheric microbes, nanotechnology, and genetic engineering to improve phyto/rhizoremediation, along with other emerging technologies, can lead to arsenic mitigation. Gene editing with CRISPR/Cas9 technology can be exploited to develop non-transgenic plants [89] with the desired attributes for arsenic remediation. Another promising non-transgenic approach is to use low-cost and long shelf-life bionanofertilizers with bacteria capable of promoting plant growth and accumulating arsenic. A major challenge lies in the translation of biology-based technologies for the benefit of farmers and agriculture. It requires collaboration among all the stakeholders: academic/research institutions, industry, government regulating agencies, and farmers.

Author Contributions

R.B. prepared the initial draft of the manuscript. R.Y. wrote part of the manuscript and revised the manuscript and helped in making some figures. W.R. prepared the final manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

There are no data and materials associated with this manuscript.

Acknowledgments

RB acknowledges the Council of Scientific and Industrial Research (CSIR), New Delhi, India, for their financial assistance in the form of the Junior Research Fellow (JRF) and Senior Research Fellow (SRF). RB acknowledges that Figure 1, Figure 3, Figure 4 and the graphical abstract were adapted from “Rice Grain Callout”, by BioRender.com, retrieved from https://app.biorender.com/illustrations/6260d621c8550fd239870934.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 3. B. subtilis S4 application with iron oxide nanoparticles (IONPs), magnesium oxide nanoparticles (MgO-NPs), iron (III) oxide nanoparticles (Fe2O3-NPs), and zinc oxide nanoparticles (ZnO–NPs) reduce arsenic uptake in plant under arsenic stress. B. subtilis S4 with iron oxide nanoparticles (IONPs) further exerts its effect through the increased activity of catalase (CAT), glutathione reductase (GR), and ascorbate peroxidase (APX). ZnO–NPs help plants in overcoming the negative effects of arsenic stress by increasing phospholipid stability and decreasing Methyl Glyoxal (MG) content and electrolyte leakage. (Adapted from [6,27,76]).
Figure 3. B. subtilis S4 application with iron oxide nanoparticles (IONPs), magnesium oxide nanoparticles (MgO-NPs), iron (III) oxide nanoparticles (Fe2O3-NPs), and zinc oxide nanoparticles (ZnO–NPs) reduce arsenic uptake in plant under arsenic stress. B. subtilis S4 with iron oxide nanoparticles (IONPs) further exerts its effect through the increased activity of catalase (CAT), glutathione reductase (GR), and ascorbate peroxidase (APX). ZnO–NPs help plants in overcoming the negative effects of arsenic stress by increasing phospholipid stability and decreasing Methyl Glyoxal (MG) content and electrolyte leakage. (Adapted from [6,27,76]).
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Figure 4. Continuous flooding increases arsenic (As) uptake by rice through the downregulation of phytochelatin encoding gene OsPCS1 and ABCC-type transporter gene OsABCC1 and upregulating low silicon rice genes Lsi1 and Lsi2. Methyl jasmonate (MJ) decreases translocation by downregulating Lsi1, Lsi2, and Lsi6 and upregulating ABCC1 and phytochelatin encoding genes (PCs). (Adapted from [80,81,82]).
Figure 4. Continuous flooding increases arsenic (As) uptake by rice through the downregulation of phytochelatin encoding gene OsPCS1 and ABCC-type transporter gene OsABCC1 and upregulating low silicon rice genes Lsi1 and Lsi2. Methyl jasmonate (MJ) decreases translocation by downregulating Lsi1, Lsi2, and Lsi6 and upregulating ABCC1 and phytochelatin encoding genes (PCs). (Adapted from [80,81,82]).
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Table
Table 1. Effect of arsenic on morphological and physiological parameters of different plants.
Table 1. Effect of arsenic on morphological and physiological parameters of different plants.
PlantChange in Morphological and Physiological Parameters Reference
Black Gram Vigna mungoIncreased activity of APX, SOD, and peroxidase (POD), decreased activity of Catalase (CAT), reduced photosynthetic pigment, and increased lipid peroxidation[3]
Wheat
Triticum
aestivum 		Decreased biomass of roots, stems and spikes, decreased number of spikes per plant, stunted root and stems, necrosis, and wilting of leaf margins[9]
Soybean
Glycine max		Decreased number of lateral roots, thickening and darkening of roots, necrotic and slimy root tips, darker and thicker stems, inhibited leaf development, affected biomass and root cell death, thin-walled parenchyma cells, reduced root cortex area, increased total peroxidase and superoxide dismutase (SOD) activity in As(III) treatment compared to As(V), and decreased chlorophyll a[13]
Blackgram Vigna mungoRoot and shoot growth decreased, fresh root weight, fresh shoot weight, and fresh total biomass reduced, and shoot weight more affected than root weight[17]
B. junceaDecreased shoot length and number of leaves, increased activity of enzymes SOD, CAT, POD, APX, GR, and MDA content in a 30-day old plant, while only SOD and GR increased in 60 days old, protein content enhanced in 30-day old plant[24]
Barley Hordeum vulgareDecreased root and shoot dry weight, SOD and CAT activity increase[25]
V. radiata
Length, root oxidizing capacity of seedling, and dry biomass decreased, ferric chelate reductase (FCR) activity increased, increased proline, H2O2, malondialdehyde (MDA), SOD, and CAT[26]
C. moschataReduced phenolic compound and flavonoids, root length, reduced shoot length, root and shoot fresh weight, root and shoot dry weight. Reduced Chl a and Chl b, increased H2O2 and MDA content while increasing the activity of SOD, CAT, and APX[27]
RiceDecreased number of tillers, above-ground biomass, and grain yield[28]
Rice cultivar Lalat Oryza sativa ssp. indicaDecreased germination with weight more affected than length, roots turned black, more accumulation in shoots when As(V) used, otherwise more in roots, increased lipid peroxidation, SOD, APX, and glutathione reductase (GR) activity[29]
SpinachDecreased plant biomass and chlorophyll-a and b content, increased oxidative stress through high H2O2, upregulated CAT, guaiacol peroxidase (GPX), APX, and SOD[30]
Maize
Zea mays		Decreased dry weight of roots and shoot, As(V) decreased chlorophyll content [31]
Table
Table 2. Transporter proteins, their location and their function in plants.
Table 2. Transporter proteins, their location and their function in plants.
Transporter As(III) or As(V)LocationActive or PassivePlant Reference
Lsi1As(III)Distal side of plasma membranePassiveRice[23]
Lsi2As(III) Proximal side of plasma membraneActiveRice[23]
OsNIP1;1As(III)Plasma membranePassiveRice[23]
OsNIP3;3As(III)Plasma membranePassiveRice[23]
OsABCC1As(III)Tonoplast of roots, stems, leaves, and husks of rice Rice[40]
PvPht1;4As(V)Plasma membrane
(roots and fronds)		 P. vittata[41]
PvACR3;1As(III)Vacuolar membrane P. vittata[44]
OsABCC7As(III)Xylem parenchymaActiveRice[47]
PvACR3;2As(III)Plasma membrane P. vittata[50]
PvACR3;3As(III)Vacuolar membrane P. vittata[50]
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Beniwal, R.; Yadav, R.; Ramakrishna, W. Multifarious Effects of Arsenic on Plants and Strategies for Mitigation. Agriculture 2023, 13, 401. https://doi.org/10.3390/agriculture13020401

AMA Style

Beniwal R, Yadav R, Ramakrishna W. Multifarious Effects of Arsenic on Plants and Strategies for Mitigation. Agriculture. 2023; 13(2):401. https://doi.org/10.3390/agriculture13020401

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Beniwal, Rahul, Radheshyam Yadav, and Wusirika Ramakrishna. 2023. "Multifarious Effects of Arsenic on Plants and Strategies for Mitigation" Agriculture 13, no. 2: 401. https://doi.org/10.3390/agriculture13020401

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