Arsenic Toxicity in Plants: History
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Contributor:
Mirza Hasanuzzaman
,
Kamrun Nahar
,
Mohammad Saidur Rhaman
,
Khursheda Parvin
,
Kirti Bardhan
,
Deyvid Novaes Marques
,
Pedro García Caparrós

 The non-essential metalloid arsenic (As) is widely distributed in soil and underground water of many countries. Arsenic contamination is a concern because it creates threat to food security in terms of crop productivity and food safety. Plants exposed to As show morpho-physiological, growth and developmental disorder which altogether result in loss of productivity. At physiological level, As-induced altered biochemistry in chloroplast, mitochondria, peroxisome, endoplasmic reticulum, cell wall, plasma membrane causes reactive oxygen species (ROS) overgeneration which damage cell through disintegrating the structure of lipids, proteins, and DNA. Therefore, plants tolerance to ROS-induced oxidative stress is a vital strategy for enhancing As tolerance in plants. Plants having enhanced antioxidant defense system show greater tolerance to As toxicity. Depending upon plant diversity (As hyperaccumulator/non-hyperaccumulator or As tolerant/susceptible) the mechanisms of As accumulation, absorption or toxicity response may differ. There can be various crop management practices such as exogenous application of nutrients, hormones, antioxidants, osmolytes, signaling molecules, different chelating agents, microbial inoculants, organic amendments etc. can be effective against As toxicity in plants. 

  • Arsenic
  • Toxicity
  • plants

1. Introduction

Arsenic (As) is an environmental non-essential metalloid that poses a severe risk to all forms of plant and animal life [1][2]. It is a naturally occurring 20th most plentiful and widely distributed element on the planet. At present, more than 2.5 billion people on the earth depend on groundwater, and contamination of groundwater by As-tainted toxicity has become a serious concern [3]. Contamination of As in groundwater is increasing daily and it is estimated that 500 million people round the globe will be affected by As contamination. This metalloid enters into the ecosystem via natural activities such as weathering and mineralization of earth crust and also by anthropogenic activities that include application of As-based pesticides, insecticides, fertilization with municipal solid wastes, and irrigation with As-tainted groundwater [4]. Thus, animals and humans are irradiated to As directly through the consumption of As-tainted water or indirectly by ingestion of foods from the ecosystem. It is well-known that food chain is affected by As when agricultural products become contaminated [5].
Plants exhibit morphological and physio-biochemical disorders due to As toxicity. It has been reported that root proliferation and extension are inhibited by As because root is the foremost organ to be subjected to As [6]. Arsenic contamination reduces nodule formation in roots and shows wilting, curling, and necrosis of leaf blades. Arsenic toxicity hampers plant growth by decreasing cell proliferation and biomass buildup. Arsenic binds to enzymes and proteins, impairing cell biochemistry and disrupting physiological processes like photosynthesis, respiration, transpiration in plants [4]. It can deplete plants reproductive capacity, obstructing photosynthetic processes and resulting in decreased plant growth and yield [7][8].

2. Arsenic Uptake and Accumulation in Plants

In soil, organic As compounds remain in addition to inorganic As. The inorganic and organic both forms of As in soil can be uptaken by plants while the higher rate and part is the inorganic As. Arsenate [As(V)]/AsO43− and arsenite [As(III)]/AsO33− are the inorganic entities. Generally inorganic forms, As(III) and As(V) are more toxic than the organic form. Aerobic soil predominates the generation of As(V) and anaerobic/inundated soil is predominated by the occurrence of As(III) [9]. Methylated As [monomethylarsinic acid (CH3AsO(OH)2; MMA) along with dimethylarsinic acid ((CH3)2AsOOH); DMA)] are commonly demonstrated organic As compound. Microorganisms are involved in conversion of As(V)/As(III) to MMA and DMA by distinct pathway. It is very usual that root is the first organ through which As enters the plants but As can enter through all the submerged parts of plants [10]. After crossing the root epidermis and passing through the apoplastic and symplastic pathways, As enters the xylem or phloem through which bulk flow of As occurs and can be distributed to different plant organs including stem, leaf, reproductive parts and even seeds. However, cell wall, especially the membrane plays pivotal responsibility for controlling the rate and amount of As transport though it is variable among As accumulators and non-accumulators. Plant’s root/membrane selective transporters and pathways are concerned for the entrance, uptake and translocation of inorganic and organic As [11].
Arsenite [As(III)/AsO33−] mainly enters through the root nodulin 26-like intrinsic proteins (NIPs) and these are as a group recognized as aquaporin channels (AQPs) in together. Expression of OsNIP2;1 (Lsi1), in rice (Oryza sativa) root were reported in distant part of the plasma membrane in the zone of Casparian strips. OsNIP2;1 (Lsi1) regulates the influx of silicic acid (Si(OH)4) and As(III) [12]. Another aquaporin channel OsNIP2;2 (Lsi2) is also found in plasma membrane of cells in both exodermis and endodermis of O. sativa root. These are Si(OH)4 efflux transporters. Here, Lsi2 is restricted to the proximal side cell [13]. Influx of Si(OH)4) as well as As(III) occur through Lsi1 whereas efflux of Si(OH)4 occur through Lsi2; this process hinders As(III) entrance [12]. As(III) entrance in a number of plant species is bi-directional and is regulated by concentration difference. Similar mechanism was noticed in different plants like Pteris vittata, Lotus japonicas and Arabidopsis thaliana [14][15][16].
Plasma membrane intrinsic proteins (PIPs), such as OsPIP2;4, OsPIP2;6 and OsPIP2;7 can also control As(III) entrance but the mechanism is still ambiguous [17]. When As is present attaching the root zone, it can enter the root or efflux from the root or because of its affinity it can be bound to GSH as well as its derivatives phytochelatins (PCs) [18]. Once forming the As(III)-PCs it is sequestrated in vacuole mediated by C-type ATP-binding cassette transporter (OsABCC1) [19].
Arsenate [As(V)]/AsO43− is the most common form of As under aerobic and dry condition and structurally it is resembled to PO43−; this is the cause for using the same transporter/pathway by both species [11]. PO43− transporter genes (OsPHTs) were recognized and phosphate transporter, OsPHT1;8 (OsPT8) and OsPHT1;1 showed high affinity for PO43− and As(V) in O. sativa L. [20]. However, after uptaking As(V), it is quickly converted into As(III) where As(V) reductase (AR) activity is involved. There are two As (V) reductases, OsHAC1;1 and OsHAC1;2 in the root of O. sativa [21]. This converted As (III) can be released outside of the root through efflux or it can be converted into As(III)-PC complexes.
Aquaporin Lsi1 has been proposed to be involved in entrance of MMA(V) as well as DMA(V) in O. sativa [22]. So, Lsi1 is involved in both the inorganic As (III) in addition to organic As transportation. Occurrence of MMA(V)-thiol complexes were also documented [23] whereas little is known about DMA(V) and it needs further study.
Arsenic transfer from root to other vegetative parts and to reproductive parts has been studied, moreover described in few reports which are mostly on O. sativa L. As(III) is more quickly taken up by root than the other organic species of As. OsNIP2;1 (Lsi1) is accountable for As(III) entrance, and Lsi2 is for As(III) efflux from root to xylem as reported in O. sativa L. [24]. Lsi1 and Lsi2 work sequentially or together for controlling the root entrance of Si along with As(III). Besides, Lsi1, Lsi2 and Lsi6 transpiration pool is also vital to manage As uptake [25]. In O. sativa, various Pi transporter genes (OsPT) have been reported which transport P and As(V) towards the root; some of which are OsPT1, OsPT2, OsPT4, OsPT6 [26]. AsV in converted to As(III) within root, after that it can enter the xylem via Lsi 2 [27]. The organic DMA as well as MMA cross aquaporin channels [28]. The DMA is tremendously mobile all through the vascular tissues; it can be transported very quickly from root to shoot and from leaves to seed in O. sativa. In O. sativa L. grain, As(III) is mainly translocated via phloem whereas DMA is translocated via both kinds of vascular tissues. A putative peptide transporter, OsPTR7 functions for in the long-distance transportation and accumulation of DMA [29]. Also, inositol transporters, AtINT2 and AtINT4 may function for the entrance of As(III) to phloem and its translocation into grain.

3. Arsenic Toxicity in Plants

Many studies reported that As availability in the soil can hamper the morphological and physio-biochemical functioning of plants consequently reducing crop yield; [2][30][31][32]. For instance, plants exposed to As showed discoloration, lignification, and plasmolysis of root cells which resulted in stunted plant growth [33]. In addition, As contamination severely reduced germination percentage, shoot and root elongation, root and leaf biomass, and seed vigor index of different plants [34][35][36]. Likewise, As exposure has been shown to reduce the leaf numbers, area of leaf, height of plant, and fresh and dry biomass of plants [37][38]. Reduced biomass in the presence of As was possibly an outcome of enhanced permeability of the cell membranes, consequently increased leakage of cellular constituents/basic nutrients essentially required for energy generation, and optimum growth and development of plants [39].
Arsenic stress regulates water relation in plants [1][40]. For example, As stress reduced relative water content in wheat and pea plants [41][42]. Likewise, As stress in lettuce reduced water use efficiency (WUE), stomatal conductance, and increased plant transpiration rate [43]. In Hydrilla verticillata, As exposure reduced WUE and increased transpiration rate [44]. The As stress may disrupt the cell wall structure in leaves, resulting in decreased leaf water content.
Many studies described that As stress inhibited the activities of photosynthetic machineries in plants [40][45]. Arsenic toxicity causes decrease in the synthesis of photosynthetic pigments, distortion of chloroplast, and reduction of photosystem I (PSI) and photosystem II (PSII) activities [46]. Several plants such as Zea mays, Trifolium pratense, and Lactuca sativa decreased biosynthesis of chlorophyll (Chl) due to As stress [47][48][49]. In chickpea (Cicer arietinum) plants, As toxicity reduced Chl contents and consequently resulted in chloroplast distortion [50]. In soybean, As stress reduced the efficacy of PSII, stomatal conductance, and rate of photosynthesis [51]. Arsenic stress reduced Chl fluorescence and photosynthetic rate in P. cretica and Spinacia oleracea [32]. Arsenic-induced reduction in Chl content may be due to the reduction in ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO) activity and degrading biosynthetic enzymes, δ-aminolevulinic acid dehydratase and protochlorophyllide reductase [52]. It has been reported that As toxicity initiates disruption of microtubules that hampers the formation of stomata which results in abnormal stomata [53]. Arsenic stress triggers phosphatidic acid (PA) signaling and that PA involved in stomatal closure of soybean [54]. Arsenic-induced injurious effects on roots may affect the uptake of water and ions, which consequently, reduces the photosynthetic and transpiration rate and inhibits stomatal regulation [55][56].
Arsenic toxicity damages cell membranes and it is well-known that chloroplast membranes are quite sensitive to As-induced damages [2]. Arsenic-stressed P. vittata and Leucaena leucocephala leaves showed abnormal internal membranes of chloroplasts [57][58]. Literature shows that As stress led to perturbations in the chloroplast membranes organizations such as thylakoid membrane rupture and swelling [5]. In addition, Upadhyaya et al. [59] reported that As toxicity distorted chloroplast membrane and reduced carotenoids. Arsenic toxicity-induced dilapidation of chloroplasts and modification in its interior membranes, which adversely affect the photosynthetic pigments and the rate of carbon assimilation. Arsenic negatively affects the Chl a content and Chl b content, maximal photochemical efficiency of PSII (Fv/Fm), the actual PSII photochemical efficiency (ΦPSII), the quantum yield of CO2 assimilation (ΦCO2), and the non-photochemical quenching (NPQ), net photosynthesis rate (A), stomatal conductance to water vapor (gs) and internal CO2 concentration (Ci) in Pistia stratiotes L. plants. The final result of As toxicity was lowered starch concentration, sucrose concentration, and glucose concentration in P. stratiotes [60].
Overall, As toxicity hampers crop growth by altering root plasmolysis, reducing photosynthetic attributes such as degradation of pigments, reduction of the rate of CO2 fixation, reduction of stomatal conductance, and distortion of cell membranes integrity.

4. Arsenic Toxicity and ROS Generation in Plants

ROS generation is a common response in abiotic and biotic stresses [61]. ROS overproduction impaired plant health under stress by adversely affecting range of physiological process including lipid metabolism, DNA, photosynthesis, respiration, enzyme deactivation and growth retardation [62]. Several studies demonstrated As(III) and As(V) induce generation of ROS viz. superoxide (O2•−), the hydroxyl radical (OH•), and H2O2 [63][64]. As(III) is more detrimental to plant growth and generate more O2•− than As(V), which generate more H2O2 [65]. Although root cells sense first As, though generation of ROS started in leaves well before the As accumulation in the leaves tissues, suggested that root cells communicate As toxicity to leaves, probably by H2O2 [66]. Under aerobic condition, As(V) is the main form which enter plant roots by phosphate transporter and within the cell it transform into As(III), which is the main source of ROS generation; [67]. The conversion of As(V) into As(III) is both, enzymatic and nonenzymatic [4]. Enzymatic reaction mediated by arsenate reductase (glutaredoxin) where GSH acts as electron donor [68]. This reduction is followed by methylation process and produces MMA, DMA, tetramethyalarsonium ion (TETRA) and trimethylarsonium oxide (TMAO), arsenocholine, arsenobetaine and arseno-sugars [69]. These methylated products react directly with molecular oxygen and produce ROS. Non enzymatic reduction of As(V) into As(III) occurs through GSH [70]. This conversion, further causes severe oxidative stress as As(III) bind and consume GSH, and impairs antioxidant system. In chloroplast, As(V) is reduced into As(III) by cytochrome/cytochrome oxidase, disturbed electron transport chain and generated ROS [30][60]. In root meristematic cells, mitochondrial arsenate reductase is also found and transforms As(V) into As(III) [71].
Lipid peroxidation, a common toxic effect of As induced ROS, also observed in hyperaccumulating P. vittata [72], hampered cellular and membrane functions [73]. Lipid peroxidation due to ROS is mostly monitored as malondialdehyde (MDA) content, a main product of lipid peroxidation, along with membrane leakage [74][75]. Overproduction of ROS increases polyunsaturated fatty acid (PUFA) and reduces saturated fatty acid of membrane lipids and membrane fluidity, thereby increases membrane leakage [63][76]. ROS also affects enzyme and protein structure and activity by oxidation of side chains, cross-linking and inducing fragmentation of backbone [5][77]. ROS generation under As-stress also modifies nitrogenase base, nucleotide deletion, disrupts protein-DNA binding and may lead DNA cracks [78][79]. In Pisum sativum, chromosome or microtubule damage has been reported under As stress which restricted root meristem activity [80]. Restricted root growth under As-stress may attribute to ROS-induced arrest of mitotic division due to down regulation of cell cycle genes and slow progression of G1 to G2 and from S to M stage, and decreases mitotic index (number of cells progressing into mitosis to the total number of cells) [81][82]. Root growth is also restricted due to root tip death. ROS induces programmed cell death by affecting vacuolar processing enzymes, signaling and triggers programmed cell death [83]. As toxicity caused asymmetric distribution of peroxisomes in A. thaliana root cells and a greater number of peroxisomes occurs in root meristematic zone as compared to root differentiation zone, and the higher peroxisomal ROS generation at root tip induces programmed cell death [84]. The differences in peroxisomal number may be due to As-induced pexophagy, a selective autophagy of peroxisomes [85]. Though it seems roots may have strong antioxidant defense against As toxicity than leaves [36], growing evidence suggested that root gravitropism, cell death, stomatal regulation and other growth and developmental response, under varied abiotic stresses are results of interplay between ROS and phytohormones [86][87]. The ROS and hormonal interplay control gene expression and induce stress responses. As stress upregulated abscisic acid, ethylene and jasmonic acid signaling [88]. ROS generated in chloroplast and mitochondria disrupt ETC by damaging internal and outer membranes of chloroplast and mitochondria [60]. The disruption of chloroplast membrane reduced photosynthetic pigment and carbon fixation [58][89]. Even, chloroplast membrane of old leaves of As hyperaccumulator, P. vittata was also disrupted with high accumulation of As [57].

This entry is adapted from the peer-reviewed paper 10.3390/stresses2020013

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