Approaches in Enhancing Arsenic Tolerance 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.  Thirst of plants researchers are increasing for searching and establishing proper strategies to increase plant defense mechanisms upon As-induced oxidative stress. Therefore, exogenous different elicitors like plant nutrients, hormone, antioxidants, osmolytes, signaling molecules, different chelating agents, microbial inoculants, organic amendments etc. were used in different plant species upon exposure to As stress to evaluate their roles in reducing oxidative injury through upregulating antioxidants activities.

  • Plant
  • Arsenic
  • reactive oxygen species

1. Use of Plant Nutrients

Different plant nutrient receiving attention for their ability to mitigate the oxidative stress and damage upon As exposure [1][2]. Calcium (Ca)-induced lower oxidative stress was reported by Rahman et al. [1] in O. sativa upon Arsenic (As) stress, while without stress condition, Ca did not showed any changes in H2O2 and MDA levels. Calcium supplementation increased antioxidants activities including superoxide dismutase (SOD), catalase (CAT), glutathione peroxidase (GPX), glutathione S-transferase (GST) in As-stressed rice which contributed in reduction of H2O2 [1]. Calcium also causes the stimulation of AsA-GSH pool in plants upon As toxicity which has strong relationship in regulation of H2O2 detoxification and thus enhances oxidative stress tolerance with lower MDA level. For instance, higher ascorbate peroxidase (APX), monodehydroascorbate reductase (MDHAR), dehydroascorbate reductase (DHAR) activities with lower GR activity caused increment of ascorbic acid (AsA)/DHA and GSH/GSSG redox balance along with lower oxidative stress in As-treated rice with Ca [1]. Exogenous application of Ca and sulfur (S) significantly modulating ROS detoxification in As-stressed plant through strengthening the antioxidants responses [2]. Lower H2O2 accumulation by S and Ca in separate and as well as combined application resulted in reduction of MDA in As-stressed Brassica plants where Ca caused comparatively better results [2]. In addition, Ca and S-treated Brassica showed higher AsA/DHA and GSH/GSSG redox in both root and leaves tissue which were because of Ca and S-mediated elevated APX, DHAR and GR activities and thus resulted in lower ROS [2]. Arsenic-induced oxidative stress was mediated by Ca supplementation which caused higher tolerance in V. faba by suppressing both ROS generation and respective enzymatic activity resulted in lower EL and MDA level [3]. This Ca-induced higher As-tolerance was stronger in combination with melatonin where highest reduction of oxidative damage was measured along with elevated activity of antioxidant system including SOD, APX, GR, MDHAR, DHAR and GST activities.

2. Use of Phytohormones

Phytohormones are very potential to improve the plant antioxidant defense mechanism consisting of both enzymatic and non-enzymatic stuffs for suppressing metal-induced oxidative damage [4]. Methyl jasmonate (MeJA), for example, is effective to reduce oxidative stress as revealed by lowered ROS generation, elevated redox state of AsA and GSH, strengthened enzymatic antioxidants activities and better membrane stability in plants upon As toxicity [5][6]. Exogenously 1 µM MeJA caused the significant reduction of H2O2 and OH• about 20 and 17%, respectively led to decrease in lipid peroxidation (as MDA; about 27%) in 200 µM As-exposed B. napus [5]. This MeJA-induced oxidative stress tolerance in As-stressed B. napus was acquired due to increasing plant antioxidant defense mechanism through elevated AsA and GSH content along with higher activities of enzymatic components like SOD, POD, CAT, APX and GR. Likely, As-stressed rice showed lower membrane damage revealed by reduced MDA and EL with the application of MeJA led to decrease activities of SOD, POD, CAT and APX [6]. Such MeJA-induced lower membrane damage in As-stressed plants describe the lower generation of ROS which also correlated with the lesser activity of enzymatic antioxidants. Ascorbate-glutathione cycle is one of the vital mechanisms for regulating H2O2 metabolism in plant cell and thus keep its level beyond toxic, which is also strengthened by phytohormones supplementation under As stress [7][8]. The higher AsA-GSH redox status by plant hormones thus contributed in reduction of ROS and consequent oxidative damage like membrane injury, for instance, salicylic acid (SA)-mediated lower H2O2, MDA production and EL in As-stressed Z. mays [8]. Methyl jasmonate diminished oxidative stress through increasing the activity of antioxidant enzymes and decreasing As accumulation by modulating arsenic transporters of rice plants. Addition of MeJA in rice plants under As stress improved the level of AsA, AsA/DHA, GSH and GSH/GSSG, increased the activity SOD, APX and POD. The oxidative stress (H2O2 and MDA) was decreased in those MeJA treated rice plants. The augmented tolerance of those rice plants was also observed in terms of increased Chl content, Chl fluorescence and biomass production, yield components and yield [9].
Similarly, other phytohormones are also significant in reducing As-induced oxidative stress through strengthening antioxidant defense mechanism. For instance, exogenous application of jasmonic acid alleviated the As-induced oxidative stress by 36% of reducing ROS with elevated activity of SOD, CAT, APX and GR in L. valdiviana [10], while cytokinin (e.g., kinetin)-induced lower down of ROS in As-stressed P. cretica [11]. The abscisic acid (10 μM) was used in O. sativa as pretreatment for 24 h to strengthen As tolerance and this pretreatment caused the upto 50 and 38% reduction of O2•− and H2O2, respectively which resulted in 48% lower down of lipid oxidation with improvement of membrane stability [7]. This ABA-mediated relief of oxidative damage in As-stressed plant through ABA-induced elevated response of AsA-GSH pathway. Such As-mediated oxidative stress was downregulated by the exogenous SA in Z. mays [8]. Therefore, exogenous plant hormones are potential candidates for regulating As-induced oxidative stress for increasing plant tolerance through strengthening the plant antioxidant defense mechanism including both non-enzymatic and enzymatic components.

3. Use of Signaling Molecules

Supplementation of signaling molecules like nitric oxide (NO), hydrogen sulfide (H2S) and H2O2 causes the stimulation in the antioxidants system, leads to reduction of oxidative stress in plants.
Exposure of As-induced higher ROS and structural injury of cellular integrity including lipid peroxidation and membrane injury were significantly improved in all NO, H2S and H2O2-treated plants [2][12][13]. The accumulation of ROS was reduced in signaling molecules treated As-stressed plant, for instance, both NO and H2S reduced O2•− and H2O2, OH• accumulation while exogenous application of lower concentration of H2O2 has the capability to suppress O2•− and H2O2 later resulted in better cellular function as well as lowered the oxidative damage as caused lower lipid and protein oxidation. Consequently, regulation of As-induced ROS metabolism requires the intensive involvement of antioxidants activities. Other studies reported about the participation of NO, H2S and H2O2 as external approaches to empower both enzymatic and non-enzymatic antioxidants directly or indirectly to mitigate As-induced oxidative stress [12][14][15].
Exogenous sodium nitroprusside (SNP; as NO donor) in presence of As caused the reduction of enzymatic antioxidants activity like SOD, CAT and POD which in accordance with NO-induced lowered level of O2•−, H2O2, EL by 1.4-, 1.5- and 1.5-fold with lower MDA in Spirodela intermedia [16]. Transcriptional expression of the PCS, GSH1, MT2, and ABC1 were improved by NO supplementation in As stressed tomato plants which increased sequestration of As in root and decreased further translocation of As to the shoot. Exogenous NO also modulated proline metabolism and caused higher accumulation of GSH. The resulted oxidative stress relaxation was evident from H2O2 reduction and protection of photosynthetic apparatus [17]. In another study, the function of nitrate reductase (NR)-synthesized nitric oxide (NO) in the MeJA-induced tolerance of arsenic (As) stress was studied in rice. The positive effects were clear from the increased expression of GSH1, PCS, and ABCC1 genes, higher GSH and PCs contents in the roots and leaves, and increased activity of SOD, CAT, APX and GR. The ultimate oxidative stress reduction is apparent from decreased H2O2, MDA and EL [18]. As an emerging signaling molecule, H2S regulates the key antioxidants activities for keeping lower-level ROS and subsequent better integrity of cellular components. In P. sativum, non-enzymatic antioxidants AsA and GSH contents were elevated with the supplementation of H2S in exposure to As through the higher activity of responsible enzymes like APX, MDHAR, DHAR and GR [12]. Therefore, both of AsA and GSH were actively worked on scavenging As-induced higher H2O2 level through the regulation of the redox status of AsA and GSH. Not only that, exogenous H2S also raised the activity of SOD, and CAT which are also acted on O2•− converting into H2O2 for further action by AsA-GSH cycle. Higher GST activity and GSH also described the roles of GSH in detoxification of lipid and protein peroxidation products used as substrate and thus recovered plant from oxidative status. Although H2O2 is harmful at extreme level but under threshold level it also acts as signaling molecules to regulate plant stress tolerance. Regarding this, it was reported that exogenous H2O2 (1 µM) regulated the ROS metabolism to keep them under beneficial level through the activation of APX, MDHAR, DHAR, and GR in stressed plants due to its signaling roles [2]. However, the actual mechanism of signaling molecules-mediated plants recovery upon As stress is still lacking which demand further extensive studies.

4. Use of Chelating Agents

Chelating agents mediated higher upregulation of plant antioxidant defense system for getting relief from As-induced oxidative stress is still not explored widely. Therefore, this approach for getting As-tolerance behavior in cultivated crop species could be vital as these also have metal elimination properties. Citric acid (CA) is known as harmless compound which is able to increase the plant antioxidants capability and thus reduced As-induced oxidative damage through declining the ROS accumulation and lipid peroxidation [19]. Citric acid mediated mitigation of oxidative stress and the plant tolerance in As exposure was due to the upregulation of antioxidant enzymes like SOD, CAT, and [20]. However, the role of chelating compound is very species-dependent along with their dose level. Effect of ethylenediaminetetraacetic acid (EDTA) was studied in regulation of As-induced oxidative stress by declining ROS and lipid peroxidation [21][22]. Application of EDTA enhanced As-induced H2O2 production, but reduced lipid peroxidation [22].

5. Use of Soil Amendments

Soil amendments are an eco-friendly and cost-effective approach for betterment of soil health to achieve food safety in this era of climate change. Therefore, researchers have been tried biochar to amend As toxicity and thus improve plant tolerance. Toxic level of As treated higher oxidative stress markers like membrane damage, H2O2 and MDA in G. max were declined when biochar (made from waste wood chips) was applied [23]. Due to the addition of biochar antioxidants defense mechanisms were upregulated in As-treated plants, for instance, SOD, CAT, APX, GPX, GR and GST oxidative injury was prohibited significantly resulted in protection of G. max for oxidative stress [23].
Peanut and canola straw biochar was used to evaluate its potentiality as an organic amendment to improve plant tolerance and growth upon As toxicity [24]. This greenhouse-based study showed the protective effects of biochar on suppressing As-induced oxidative stress (indicated by lowering MDA, H2O2 and O2•− about 82, 49, and 45%, respectively) in soybean which gave the indication of biochar mediated stronger antioxidants defense mechanism in stressed plant and forecast its future useability. Kamran et al. [24] also disclosed about the comparative better performance of peanut straw biochar than canola based.

6. Use of Beneficial Microbes

Microbial inoculants effectively regulate the plant antioxidants defense capacity upon As-induced oxidative stress and thus enhance plant tolerance [25]. In addition, this protective effects of microbes in stimulating plant antioxidants mechanism depends on microbes’ species, stains which can be said as strain-specific or specifically antioxidants-specific, As toxicity levels and plants species [26]. Bacterial influence for plant has been documented as beneficial in some extent. Previously, some researchers reported about plant growth-promoting rhizobacteria (PGPR) significantly regulated plant antioxidants enzymes activity. About 100 mg kg−1 of both As(III) and As(V) treatments-induced higher enzymatic antioxidants responses were reduced significantly in V. radiata [27]. Incubation of As-stressed V. radiata with Exiguobacterium showed lower activity of SOD, CAT, APX and GPX near to control treatment thus resulted bacteria-mediated suppression of oxidative stress (as lessening ROS generation. Likely, several PGPR documented for increasing antioxidants activity like SOD by Bacillus cereus [28], SOD and CAT by Populus deltoides [29], APX and CAT by B. licheniformis [30], SOD and CAT (about 27 and 62%, respectively) by B. aryabhattai [31] in As-stressed plant. Consequently, in study of Xiao et al. [25] was about modulation of antioxidants defense system in As-stressed rice by different PGPR for attuning lower ROS production. Pseudomonas mosselii, B. thuringiensis, and Bacillus sp. JBS-28 inoculation showed the reduction of As-mediated oxidative damage through promoting the antioxidants capacity like SOD and POX activity which directly scavenge the ROS. Thereafter, in case of wheat, Brevundimonas intermedia and P. gessardii modulated higher SOD and APX activities were revealed by the higher expression of their respective gene at As exposure [32]. Ghosh et al. [33] reported about Pantoea dispersa–modulated higher SOD and CAT activities with less MDA and thus As-tolerant bacterial strains were recommended for using in improving membrane stability of O. sativa upon As toxicity. However, the innate mechanisms in antioxidant defense modulation in As-stressed plants by PGPR are still unknown and which demand further extensive studies. Piriformospora indica improved the root sequestration of As, decreased As translocation and improved the AsA-GSH homeostasis which altogether contributed better photosynthetic performance and reduced the oxidative stress. P. indica sequestrated As in the roots through upregulating the expression of PCS1 and PCS2 genes. It also reduced As accumulation in shoot by downregulating the expression of Lsi2, Lsi6, Nramp1 and Nramp5. Modulating AsA-GSH homeostasis P. indica decreased the MDA level of rice plant [34].

7. Other Chemical Elicitors

Plant researchers are also interested to explore the new, most adaptive and efficient technology for increasing plant tolerance against As stress. Therefore, antioxidants, osmolytes, polyamine and other chemical elicitors likely have been used in small scale previously and still now need more exploration to understand and develop these exogenous protectant-mediated mechanisms involved in plant oxidative stress tolerance. Notable, melatonin has gained the attention of plant researchers’ community due to its antioxidant’s potentiality specially its mitigating nature against the oxidative stress-mediated cellular damage [35]. Exogenous melatonin caused the stimulation in defense system of rosemary seedlings upon As stress as it improved cell membrane integrity with reduction of oxidative damage through increment of enzymatic antioxidants capacity [36]. Samanta et al. [37] reported that melatonin treatment improved As-induced oxidative stress tolerance by triggering the antioxidative machinery where increased the total antioxidants activity with elevated non-enzymatic antioxidants content like AsA, phenolic compound resulted in the reduction of oxidative damage. Similarly, melatonin-mediated reduction of ROS with upregulation of antioxidants activity like APX, SOD, CAT, POD was reported in As-stressed Camellia sinensis [38].
As stress management approach, use of non-enzymatic antioxidants is also efficient for suppressing oxidative stress by improving plant antioxidant capacity of plant upon As-toxicity. Exogenous AsA (250 and 500 mg kg−1) showed the amelioration of 15 µM As-induced oxidative stress through enhancing the capacity of AsA-GSH cycle in rice maintaining the sufficient level of both AsA and GSH [39]. Ascorbate-treated plant showed the reduction of ROS and MDA contents as indication of lowered oxidative damage with higher AsA/DHA and GSH/GSSG ratios. Jung et al. [40] studied the role of exogenous GSH (50 and 100 mg kg−1) on biochemical responses of ROS and antioxidant levels in 14 d-old O. sativa seedlings at As (15 µM) exposure. This GSH treatment reversed the As-induced oxidative damage with the improvement of antioxidants activity. Hydroponically grown rice seedling with the foliar application of GSH declined As-induced oxidative stress indicated by lower ROS (O2•− and H2O2) and lipid peroxidation (MDA content), whereas increased the redox balance of AsA/DHA and GSH/GSSG with higher activity of MDHAR, DHAR and GR. Therefore, it can be suggested from both of above-mentioned studies that exogenous AsA and GSH causes the higher induction of AsA–GSH cycle, which re-established the cellular redox status.
The osmolyte Pro also regulates antioxidants capacity in stressed plant besides of its role on maintaining osmotic status. As a vital amino acid, Pro helps in scavenging stress-mediated higher ROS and protects plants from oxidative damage and thus stabilizes cellular structure including membrane [13]. In the experiment [13], Pro (25 μM) was applied in As-treated (25 μM) Solanum melongena and Pro fed plants showed the decline of O2•−, H2O2 and MDA level which were elevated in stress treatment alone which were because of the stimulation in activities of SOD, CAT and POD.
Phenolic compounds like chlorogenic acid and hesperidin are also well recognized as non-enzymatic antioxidants those are strongly able to neutralize the harmful free radicals besides of their metal chelating actions. Both chlorogenic (100 μM) and hesperidin (50 μM) were selected for using them singly or combined on maize plants upon As-stress (100 μM) [41]. This treatment altered the stress-induced reduction of antioxidants mechanism in maize by elevated the actions of SOD, CAT, POD, GST, GPX, MDHAR and GR which resulted in suppressing of ROS and TBARS content with maintaining higher redox status of AsA/DHA and GSH/GSSG. Thus, phenolic compounds are able to contributing in maintaining the cellular redox balance through the regulating the AsA-GSH cycle along with other potential antioxidants enzymes activities [41].
In recent years, nanoparticles (NPs), which are ultrafine particles presenting at least one dimension in <100 nm range, have gained much attention in topics related to modern agricultural research [42]. This novel and emerging nanotechnology approach has been reported to improve the production of some plant species by enhancing tolerance to environmental stresses [42][43] and promote beneficial changes regarding antioxidants. This includes increased enzyme activities and non-enzymatic contents in As-exposed plants of several species such as rice [44][45][46], soybean [47], maize [48], tomato [49] and mung bean [50]. Thus, besides covering the field of environmental protection and As toxicity alleviation in plants [51][52], the potential application of NPs highlights the role of antioxidant enzymes and non-enzymatic antioxidant molecules as important molecules for the modulation of tolerance to As-induced oxidative stress. Zinc nanoparticles (ZNO NPs) positively affect As-induced oxidative stress in rice by stimulating enzymatic antioxidants activity including SOD and CAT which lead to about 13–30% reduction of MDA content [53]. Similarly, ZNO NPs mediated further higher SOD activity was also measured in As-stressed (2 mg L−1) rice where 10 and 100 mg L−1 concentration of ZnO NP showed better results [45].

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