Phytoremediation ability of various aquatic and semi aquatic weeds.
Abstract
Arsenic (As) is the one the most toxic element present in earth which poses a serious threat to the environment and human health. Arsenic contamination of drinking water in South and Southeast Asia reported one of the most threatening problems that causes serious health hazard of millions of people of India and Bangladesh. Further, use of arsenic contaminated ground water for irrigation purpose causes entry of arsenic in food crops, especially in Rice and other vegetable crops. Currently various chemical technologies utilized for As removal from contaminated water like adsorption and co-precipitation using salts, activated charcoal, ion exchange, membrane filtration etc. are very costly and cannot be used for large scale for drinking and agriculture use. In contrast, phytoremediation utilizes green plats to remove pollutants from contaminated water using various mechanisms such as rhizofiltration, phytoextraction, phytostabilization, phytodegrartion and phytovolatilization. A large numbers of terrestrial and aquatic weed flora have been identified so far having hyper metal, metalloid and organic pollutant removal capacity. Among the terrestrial weed flora Arundo donax, Typha latifolia, Typha angustifolia, Vetivaria zizinoids etc. are the hyper As accumulator. Similarly Eicchornea crassipes (Water hyacinth), Pistia stratiotes (water lettuce), Lemna minor (duck weed), Hyrdilla verticillata, Ceratophyllum demersum, Spirodella polyrhiza, Azola, Wolfia spp., etc. are also capable to extract higher amount of arsenic from contaminated water. These weed flora having As tolerance mechanism in their system and thus remediate As contaminated water vis-à-vis continue their life cycle. In this chapter we will discuss about As extraction potential of various aquatic and semi aquatic weeds from contaminated water, their tolerance mechanism, future scope and their application in future world mitigating As contamination in water resources.
Keywords
- Arsenic
- Phytoremediation
- Weed
1. Introduction
Arsenic (As) is the one the most toxic element present in earth which poses a serious health hazard to animal and human health. Generally arsenic is present in the earth crust in the form minerals, especially associated with iron pyrite and zinc ores. Arsenic contamination occurs through both by natural as well as anthropogenic processes [1]. Unlike other toxic heavy metals (Cadmium, mercury and chromium) arsenic contamination in environment predominately occurs through natural biogeochemical process [2] and some manmade activities play important role (triggering the process) in that process. Anthropogenic activities such as coal mining and burning smelting of As containing metal ores and other industrial activities are also responsible for distribution of arsenic in the environment [3]. Arsenic contamination of drinking water in South and Southeast Asia reported one of the most threatening problems that causes serious health hazard of millions of people of India and Bangladesh [4]. The source of As contamination in water in those countries were due to two different natural processes; oxidation of arsenopyrite minerals lies below ground water table due to water mining process and reduction of As containing iron hydroxides [5]. Arsenic exists in the nature in −3, 0, +3 and + 5 oxidation states and environmental forms include arsenious acids, arsenic acids, arsenites, arsenates, methylarsenic acid, dimethylarsinic acid, arsine, etc. Two inorganic forms are very common in natural waters: arsenite (AsO33−) and arsenate (AsO43−), referred to as arsenic (III) and arsenic (V). Pentavalent (+5) or arsenate species are AsO43−, HAsO42−, H2AsO4− while trivalent (+3) arsenites include As(OH)3, As(OH)4−, AsO2OH2− and AsO33−. The solubility of inorganic species depends on pH and redox potential of the environment and arsenite (As3+) is the most soluble form inorganic As. Pentavalent species or arsenate (As5+) predominate in oxygen rich aerobic environments, where as trivalent arsenites (As3+) dominant in moderately reducing anaerobic environments such as groundwater [4].
Arsenic concentration in drinking water reported more than 50 μg L−1 in many areas in the world [6], whereas maximum permissible limit set by World Health Organization (WHO) is 10 μg L−1. The use of arsenic contaminated ground water for irrigation purpose causes build up of As in soil and leads to entry of As in food crops, especially in rice and vegetables [7, 8]. This causes serious health hazard, in those As containing areas. In Southeast Asian countries like Bangladesh, Eastern parts of India (West Bengal and Bihar) and Vietnam, rice is consumed as major staple food and is very efficient in As translocation in grains [9]. Thus rice crop play a major pathway for As entry in human body living in those contaminated areas apart from drinking water. Thus remediation of arsenic contaminated water is important for environmental point of view. Various technologies are for remediation of arsenic contaminated water like ion exchange, electro dialysis, membrane filtration, adsorption and coagulation-flocculation generates lot of arsenic enriched waste. That waste material generally dumped or disposed in nearby surroundings, from where arsenic can also come back to soil and water by leaching thus making system susceptible to arsenic contamination. Along with above mentioned problem, huge cost is involved in this existing arsenic remediation technology. That necessitates finding out an alternate low cost technology which can take care of arsenic contaminated water.
Phytoremediation is an alternate and low cost technology that utilizes green plant to extract arsenic from water and store it vegetative cells. Phytoremediation process includes phytoextraction, phytostabilization, phytovolatilization, phytotransformation, and rhizofiltration [10]. Researchers find out that plants uptake arsenic by roots through phosphate uptake pathway and transfer it their above ground parts (shoot and leave). But how much amount of arsenic translocated from source (water) to sink (plant parts) depends on phytoremediation efficiency of the plant concern. However, more than 90% of total arsenic accumulated into the plant is stored in roots.
The plants utilized for phytoremediation have some criteria like (1) plant have higher specific growth rate under contaminated environment, (2) higher translocation capability of the toxic element concerned [11]. Metal translocation capability depends on factors like (1) bio concentration factor (BCF) and (2) translocation factor (TF). Plants having BCF >1 are ideal for Phytoremediation. Chinese brake fern (
2. Phytoremediation pathways
The terminology “Phytoremediation” consists of two words, “Phyto” means “green plants” and “remediation” means “curative measures or restoration”. The word “phytoremediation” was first given by Chaney [18]. In phytoremediation process, generally green plants are used which uptake toxic chemical substances (such as heavy metals and metalloids, pesticide residues etc.) from contaminated sites (soil and water) by various mechanisms and remove them from environment. Various crop and weed plants are found to be suitable for phytoremediation purpose. But research results indicated that weed flora had higher phytoremediation potential than cultivated crops (Example- Brassica sp). There are various pathways of phytoremediation process such as, rhizofiltration, phytoaccumulation or phytoextraction, phytostabilization, phytodegradation or phytotransformation and phytovolatilization etc.
Rhizofiltration: Plants uptake toxics substances by their roots through adsorption or absorption process and sequester in their root system. Aquatic plants mainly exhibited this process.
Phytoaccumulation or phytoextraction: Plants uptake toxic substances by their root system and translocated to other plant parts such as stem and leave or other modified plant parts. This mechanism mainly exhibited this process are suitable for remediation of contaminated soil.
Phytostabilization: In this process, plants restrict movement of toxic substances in soil or water, thus reduced their availability to plants. In this method, plants do not uptake toxic substances from environment. Rather, plants secrets some root exudates or photochemicals which form stable chemical bond with toxic substances and increases its stability in environments.
Phytodegradation or Phytotransformation: In this process, plants uptake toxic substance from soil or water and degrade these primary toxic substances into nontoxic forms. A large number of metabolic and physiological factors are involved in this process.
Phytovolatilization: Plant uptake toxic substances by their root system and translocated to their aerial plant parts especially in leaves; and release toxic substances in the form of vapor which may not be toxic as their primary source.
Apart from this there are some other terminologies often used in phytoremediation process are bioconcentration factor (BCF) and translocation factor (TF).
BCF = toxic substance uptake by plant/toxic substance present in environment (soil or water).
TF = toxic substance present in shoot or stem/toxic substance present in roots or.
Toxic substance present in leaves/Toxic present in shoot or stem.
For, Hyper accumulator plants both BCF and TF is >1 is desired. In other words, plants suitable for phytoremediation, BCF >1 is always desirable. But for aquatic weeds, as their dominant pathways is rhizofiltration; their toxic substances BCF >1 but TF for root to shoot or shoot to leaves is <1.
3. Potential of various aquatic plants for phytoremediation
3.1 Phytoremediation by free floating aquatic weeds
The capability of removing arsenic from contaminated water was earlier observed by Misbahuddin and Fariduddin [20] and they observed that water hyacinth can removes arsenic from water within 3–6 hr. exposure time. Amount of arsenic removed depends on number of the plant used, exposure time, presence of air and sunlight. They concluded that whole plants were more effective than fibruous roots alone. It was observed that dried roots of water hyacinth can rapidly reduces As content in contaminated water within below WHO recommended critical level (<10 μg Lg−1) [21]. A fine powder was prepared from dried roots of water hyacinth plants (obtained from Dhaka, Bangladesh) removed more than 93% arsenite and 95% of arsenate from a solution containing As @ 200 μg L−1 within 1 hr. exposure time [21]. Higher biomass production ability of water hyacinth allow it to remove As at higher rate (600 mg As ha−1 day−1) and greater efficiency (17%) compared to lower biomass producing aquatic macrophytes such as lesser duck weed (
However nutrients like phosphate addition may suppressed As uptake by duckweeds as both phosphorus and arsenic belongs same group-V(b) element family in periodic table [33]. In most of the phytoremediation study carried out in laboratory condition, As is provided either in the form of arsenite (As3+) or arsenate (As5+). But some studies included dimethyl arsenic acid (DMAA), an organic form of arsenic for evaluation of As phytoremediation potential of duckweed species. In a lab study,
3.2 Phytoremediation of arsenic by semi aquatic weeds
Some semi aquatic weed such as
3.3 Phytoremediation by submerged aquatic weeds
Among the submerged aquatic weeds
In natural conditions, submerged weeds grow in water bodies in association with floating macrophytes. Use of Combinations of submerged and floating weeds found more effective for phytoremediation purpose than submerged and floating weeds alone. Research work carried out using Hydrilla, Certophyllum, lemna and Wolfia at various combinations showed that Ceratophyllum + lemna combination (3326 μg) combination removed maximum total As followed by
Name of the plants | Key findings | Reference |
---|---|---|
Removed 600 mg As ha−1 day−1 within 21 days with 18% removal efficiency when As was applied @ 0.15 mg L−1 | [13] | |
Removal rate 140 mg As ha−1 day−1 within 21 days with 5% removal efficiency when As was applied @ 0.15 mg L−1 | [13] | |
Removed relatively higher As3+ (17408 μg g−1) and lower As5+ (8674 μg g−1As) from As containing solutions (64 μM As each) | [35] | |
Accumulates 1120 μg g−1 As in | [31] | |
Accumulates 50 μg g−1 As in roots | [41] | |
Removed sum total 8546 μg (348 μg g−1) of As from contaminated water (As concentration 1500 μg L−1) | [49] | |
Accumulates 525 μg g−1 (dry weight baisis) from 250 μM As5+ solution for 7 days | [22] | |
Accumulates 1000 mg kg−1 (dry weight basis) from As contaminated environment | [52] | |
Accumulates 1000 mg kg−1 (dry weight basis) from As contaminated environment | [52] | |
Vallisnaria natans | Accumulates 1000 mg kg−1 (dry weight basis) from As contaminated environment | [52] |
Extract 12.94 mg kg−1 total As (dry weight basis) from pulp paper industry effluents | [61] | |
Accumulates As at the rate 9 mg kg−1 with TF = 4.93 and BF = 15.00 for the arsenic containing solution 600 μg L−1. | [16] | |
Phragnites austratlis | Accumulates 32.5 mg kg−1 As in root | [62] |
4. Mechanisms of arsenic uptake and detoxification in aquatic weeds
4.1 Mechanisms of arsenic uptake in aquatic macrophytes
Three pathways for arsenic uptake in marine macrophytes have been described – (i) active uptake through phosphate uptake transporters, (ii) passive uptake through aquaglyceroporins, and (iii) physicochemical adsorption on root surfaces. Plants mainly uptake As(V) through phosphate uptake transporters [63, 64]. As(III), DMAA and MMAA gets into the plants by passive mechanism through the aquaglyceroporin channels [64].
4.1.1 Active uptake through phosphate uptake transporters
As(V) and phosphate are chemical analogs, and compete for uptake carriers in the plasmalemma [65]. As a result, as the phosphate content rises, more As (V) is required to be desorbed in the solution. Mkandawire and Dudel. [32] and Rahman et al. [33] showed that As (V) is taken up by aquatic plants through the phosphate uptake pathway, it competes with phosphate for uptake in tissues of
4.1.2 Passive uptake through aquaporins/aquaglyceroporins
Physiological studies indicate that these arsenic species are transported in rice through aquaporins /aquaglyceroporins via passive uptake mechanisms [66, 67]. Molecular studies revealed that Nodulin26-like intrinsic membrane proteins (NIPs), one of the major subfamilies of aquaporins transporters that promote the transport of neutral molecules like water, glycerol, and urea, are responsible for transporting As(III) into rice roots [68]. Aquaporins and aquaglyceroporins are two of three subfamilies of water channel proteins (WCPs), the transmembrane proteins that have a specific three-dimensional structure with a pore that permeates water molecules [69], which are permeable to water, glycerol, and/or other small, neutral molecules. Glycerol and As(III) compete for uptake in rice (
4.1.3 Physicochemical adsorption on root surfaces
Arsenic is adsorbing and accumulating on the surfaces of aquatic plants due to suspended iron oxides (Fe-plaque). Robinson et al. [70] discovered a strong association between arsenic and iron concentrations in aquatic plants, which is believed to be due to arsenic adsorption on plant surfaces’ iron oxides. Rahman et al. [14] investigated arsenic species adsorption on precipitated iron oxides on
4.2 Arsenic metabolism and detoxification in aquatic macrophytes
Arsenic occurs primarily as As (V) in an oxic environment and as As (III) in a reduced environment [64]. In plants, As (V) and phosphate share the same transporter, while As(III) enters plant cells through NIPs’aquaporins [57, 64]. Because of their distinct molecular properties, these two types of arsenic elicit different biochemical responses in aquatic plants [71]. As (V) has no affinity for thiol ligands, while As(III) has a strong affinity for peptides with sulfhydryl (-SH) groups, such as glutathione (GSH) and phytochelatins (PCs) [64, 72]. Even though plants had been exposed to As, arsenic speciation in plant tissues indicates that arsenic is primarily present in the As(III) oxidation state (V).This suggests that As(V) is effectively reduced to As(III) in plant cells after uptake, and that most plants have high As(V) reduction competence [64]. The reduction of As(V) to As(III) is mediated by GSH [73] and by enzyme [74], which is thought to be a detoxification mechanism of the plants. As(V) and As(III) have been shown to generate reactive oxygen species (ROS) within cells when they are taken up [75], and plants counteract the generation of ROS by various enzymes and cellular compounds [76]. The GSH can act as an antioxidant and is required for the synthesis of Phytochelatins which are required for metalloid chelation [71].
The mechanism of arsenic accumulation and detoxification was studied by many others in aquatic plant
5. Biotechnological interventions for phytoremediation
Plants have been utilized for phytoremediation of toxic metals and metalloids, however due to heavy metal phytotoxicity to plants; this process has been slow and largely rendered ineffective [77]. Natural heavy metal hyperaccumulators are also available, however, they are limited to specific geo-climatic conditions and also lack the crucial biomass required for efficient phytoremediation. Phytoremediation has a lot of potential using genetic engineering technologies to improve plant tolerance and heavy metal accumulation. Furthermore, various new studies using omics technologies such as genomics, transcriptomics, proteomics, and metabolomics to elucidate the genetic determinants and pathways involved in heavy metal and metalloid tolerance in plants have been identified. Presently there are three main biotechnological approaches for the phytoremediation of heavy metals and metalloids are currently being used to engineer plants for phytoremediation of heavy metals and metalloids: (1) manipulating metal/metalloid transporter genes and uptake systems; (2) enhancing metal and metalloid ligand production; (3) conversion of metals and metalloids to less toxic and volatile forms [78] (Figure 3).
5.1 Manipulating metal/metalloid transporter genes and uptake system
Enhanced heavy metal tolerance and bioaccumulation has been attained in different plant species by genetic manipulation of metal transporter genes. For example, the overexpression of full length
Recent research findings have revealed arsenite is transported in plants by proteins belonging to the aquaporins [83, 84]. It is observed that in efficient arsenic hyperaccumulators such as
Genome-wide gene expression analysis in
5.2 Enhancing metals and metalloids ligand production
Complexation of Arsenic with phytochelatins (PCs), or metallothionein (MTs) or glutathione (GSH) is an proficient way to detoxify As(III), since these complexes are sequestered in the vacuoles, this process is catalyzed by the homologs of multidrug resistance proteins (MRPs) [92, 93]. Enhancing the accumulation or synthesis of PCs and/or GSH and/or MTs may be one way to increase phytoremediation of arsenic. The overexpression of
Arsenic (As) tolerance in plants can also be increased by modifying GSH and PCs. Dhankher et al. [96] transferred and co-expressed two bacterial genes,
The
5.3 Conversion of metals and metalloids to less toxic and volatile forms
There are several reports for developing phytoremediation strategies for heavy metals with the help of biotechnological interventions by conversion of these metals to less toxic and volatile forms. It is observed that many organisms, including bacteria, fungi, and animals, methylate arsenic. Methylated arsenic have been discovered in several plant species, including rice grain [100, 101], and suggest that this is the process is a result of endogenous methylation by the plants themselves. The final product of this pathway is the gas trimethylarsine (TMAs(III)), that can be volatilized from the plant. Qin et al. [102] have cloned a gene encoding an As(III)-S-adenosylmethionine methyltransferase (arsM) from the soil bacterium
6. Conclusions
Contamination of soils and water by arsenic is one the serious threat for food security and human health in throughout the world. Some severe skin and other diseases occur due to continuous consumption of As contaminated foods and water. This necessitates a suitable technology to handle arsenic contaminated water carefully, so that above mentions points can be satisfied. Phytoremediation of arsenic contaminated water by aquatic and semi aquatic weeds offers low cost, economically feasible and eco-friendly technology to remove arsenic from contaminated water for long term. Some weeds have tremendous potential to accumulate higher amount of arsenic in their plant parts such as Eichhornia crassipes, Hydrilla verticillata, Spirodella polyrhiza, Arundo donax and Vetivaria spp. More specifically semi aquatic weeds like Arundo donax and Vetivaria sp. (perennial) can be used with in combination with Eicchornia, Spirodella and Hydrilla to remove arsenic more efficiently from treatment tanks or constructed wetland system. Although management of plant biomass will be another concern for disposal, but these plant materials can be used for making fiber (water hyacinth), handcraft items (Arundo and Typha stems) and biofuel purpose. Moreover, with advancement of molecular genetics in future As tolerance genes can be transferred to food crops (specially rice) which can store huge amount of As in their roots or very low transfer co-efficient from root to grain so that transgenic rice crops will able to grow using As contaminated water and contribute in food security in upcoming days.
References
- 1.
Shukla A, Srivastava S. A review of phytoremediation prospects for arsenic contaminated water and soil. Phytomanagement of polluted sites. 2019 Jan 1:243-54 - 2.
Bhattacharyya R, Chatterjee D, Nath B, Jana J, Jacks G, Vahter M. High arsenic groundwater: mobilization, metabolism and mitigation–an overview in the Bengal Delta Plain. Molecular and cellular biochemistry. 2003 Nov; 253(1):347-55 - 3.
Shaji E, Santosh M, Sarath KV, Prakash P, Deepchand V, Divya BV. Arsenic contamination of groundwater: A global synopsis with focus on the Indian Peninsula. Geoscience Frontiers. 2020 Oct 1 - 4.
Srivastava S, Suprasanna P, D’souza SF. Mechanisms of arsenic tolerance and detoxification in plants and their application in transgenic technology: a critical appraisal. International journal of phytoremediation. 2012 May 1;14(5):506-17 - 5.
Saha D, Sahu S. A decade of investigations on groundwater arsenic contamination in Middle Ganga Plain, India. Environmental geochemistry and health. 2016 Apr 1;38(2):315-37 - 6.
Mukherjee AB, Bhattacharya P, Jacks G, Banerjee DM, Ramanathan AL, Chandan M, Chandrashekharam D, Debashis C, Naidu R. Groundwater arsenic contamination in India: extent and severity. CSIRO Publishing; 2006 - 7.
Tuli R, Chakrabarty D, Trivedi PK, Tripathi RD. Recent advances in arsenic accumulation and metabolism in rice. Molecular Breeding. 2010 Aug; 26(2):307-23 - 8.
Spognardi S, Bravo I, Beni C, Menegoni P, Pietrelli L, Papetti P. Arsenic accumulation in edible vegetables and health risk reduction by groundwater treatment using an adsorption process. Environmental Science and Pollution Research. 2019 Nov; 26(31):32505-16 - 9.
Awasthi S, Chauhan R, Srivastava S, Tripathi RD. The journey of arsenic from soil to grain in rice. Frontiers in Plant Science. 2017 Jun 20; 8:1007 - 10.
Rahman MA, Hasegawa H. Aquatic arsenic: phytoremediation using floating macrophytes. Chemosphere. 2011 Apr 1;83(5):633-46 - 11.
Nazir A, Malik RN, Ajaib M, Khan N, Siddiqui MF. Hyperaccumulators of heavy metals of industrial areas of Islamabad and Rawalpindi. Pak J Bot. 2011 Aug 1;43(4):1925-33 - 12.
Ma LQ, Komar KM, Tu C, Zhang W, Cai Y, Kennelley ED. A fern that hyperaccumulates arsenic. Nature. 2001 Feb;409(6820):579-.579 - 13.
Alvarado S, Guédez M, Lué-Merú MP, Nelson G, Alvaro A, Jesús AC, Gyula Z. Arsenic removal from waters by bioremediation with the aquatic plants Water Hyacinth ( Eichhornia crassipes ) and Lesser Duckweed (Lemna minor ). Bioresource technology. 2008 Nov 1;99(17):8436-40 - 14.
Rahman MA, Hasegawa H, Ueda K, Maki T, Rahman MM. Arsenic uptake by aquatic macrophyte Spirodela polyrhiza L.: Interactions with phosphate and iron. Journal of hazardous materials. 2008 Dec 30; 160(2-3):356-61 - 15.
Roy C, Jahan M, Rahman S. Characterization and treatment of textile wastewater by aquatic plants (macrophytes) and algae. European Journal of Sustainable Development Research. 2018; 2(3):29 - 16.
Mirza N, Mahmood Q, Pervez A, Ahmad R, Farooq R, Shah MM, Azim MR. Phytoremediation potential of Arundo donax in arsenic-contaminated synthetic wastewater. Bioresource technology. 2010 Aug 1;101(15):5815-9 - 17.
Mirza N, Mubarak H, Chai LY, Yong W, Khan MJ, Khan QU, Hashmi MZ, Farooq U, Sarwar R, Yang ZH. The potential use of Vetiveria zizanioides for the phytoremediation of antimony, arsenic and their co-contamination. Bulletin of environmental contamination and toxicology. 2017 Oct;99(4):511-7 - 18.
Chaney, R.L., 1983. Plant uptake of inorganic waste constituents. In: Parr, J.F.E.A. (Ed.), Land Treatment of Hazardous Wastes. Noyes Data Corp, Park Ridge, NJ, pp. 50-76 - 19.
Ebel M, Evangelou MW, Schaeffer A. Cyanide phytoremediation by water hyacinths ( Eichhornia crassipes ). Chemosphere. 2007 Jan 1;66(5):816-23 - 20.
Misbahuddin, M.I.R. and Fariduddin, A.T.M., 2002. Water hyacinth removes arsenic from arsenic-contaminated drinking water. Archives of Environmental Health: An International Journal, 57(6), pp.516-518 - 21.
Al Rmalli SW, Harrington CF, Ayub M, Haris PI. A biomaterial based approach for arsenic removal from water. Journal of environmental monitoring. 2005;7(4):279-82 - 22.
Mishra, V.K., Upadhyay, A.R., Pathak, V. and Tripathi, B.D., 2008. Phytoremediation of mercury and arsenic from tropical opencast coalmine effluent through naturally occurring aquatic macrophytes. Water, air, and soil pollution, 192(1), pp.303-314 - 23.
Taleei MM, Ghomi NK, Jozi SA. Arsenic removal of contaminated soils by phytoremediation of vetiver grass, chara algae and water hyacinth. Bulletin of environmental contamination and toxicology. 2019 Jan 15;102(1):134-9 - 24.
Islam A, Saha PK, Iqbal M, Islam MN, Nayeem M. Removal of arsenic by water hyacinth from arsenic contaminated water. Water Int. 2016;1(2):36-41 - 25.
Rodrigues AC, do Amaral Sobrinho NM, dos Santos FS, dos Santos AM, Pereira AC, Lima ES. Biosorption of toxic metals by water lettuce ( Pistia stratiotes ) biomass. Water, Air, & Soil Pollution. 2017 Apr 1;228(4):156 - 26.
Zhou YQ, Li SY, Shi YD, Lv W, Shen TB, Huang QL, Li YK, Wu ZL. Phytoremediation of Chromium and Lead Using Water Lettuce Pistia stratiotes L. InApplied Mechanics and Materials 2013 (Vol. 401, pp. 2071-2075). Trans Tech Publications Ltd - 27.
Odjegba VJ, Fasidi IO. Accumulation of trace elements by Pistia stratiotes : implications for phytoremediation. Ecotoxicology. 2004 Oct;13(7):637-46 - 28.
Lee CK, Low KS, Hew NS. Accumulation of arsenic by aquatic plants. Science of the total environment. 1991 Apr 15;103(2-3):215-27 - 29.
Basu A, Kumar S, Mukherjee S. Arsenic reduction from aqueous environment by water lettuce ( Pistia stratiotes L.). Indian Journal of Environmental Health. 2003 Apr 1;45(2):143-50 - 30.
Farnese FD, Oliveira JA, Lima FS, Leão GA, Gusman GS, Silva LC. Evaluation of the potential of Pistia stratiotes L.(water lettuce) for bioindication and phytoremediation of aquatic environments contaminated with arsenic. Brazilian Journal of Biology. 2014 Aug;74(3):S108-12 - 31.
De Campos FV, de Oliveira JA, da Silva AA, Ribeiro C, dos Santos Farnese F. Phytoremediation of arsenite-contaminated environments: is Pistia stratiotes L. a useful tool?. Ecological Indicators. 2019 Sep 1;104:794-801 - 32.
Mkandawire M, Dudel EG. Accumulation of arsenic in Lemna gibba L. (duckweed) in tailing waters of two abandoned uranium mining sites in Saxony, Germany. Science of the Total Environment. 2005 Jan 5;336(1-3):81-9 - 33.
Rahman MA, Hasegawa H, Ueda K, Maki T, Okumura C, Rahman MM. Arsenic accumulation in duckweed ( Spirodela polyrhiza L.): a good option for phytoremediation. Chemosphere. 2007 Sep 1;69(3):493-9 - 34.
Duman F, Ozturk F, Aydin Z. Biological responses of duckweed (Lemna minor L.) exposed to the inorganic arsenic species As (III) and As (V): effects of concentration and duration of exposure. Ecotoxicology. 2010 Jun;19(5):983-93 - 35.
Zhang X, Hu Y, Liu Y, Chen B. Arsenic uptake, accumulation and phytofiltration by duckweed ( Spirodela polyrhiza L.). Journal of environmental sciences. 2011 Apr 1;23(4):601-6 - 36.
Favas PJ, Pratas J, Prasad MN. Accumulation of arsenic by aquatic plants in large-scale field conditions: opportunities for phytoremediation and bioindication. Science of the total Environment. 2012 Sep 1;433:390-7 - 37.
Zhang X, Zhao FJ, Huang Q, Williams PN, Sun GX, Zhu YG. Arsenic uptake and speciation in the rootless duckweed Wolffia globosa . New Phytologist. 2009 Apr;182(2):421-8 - 38.
Zhang X, Uroic MK, Xie WY, Zhu YG, Chen BD, McGrath SP, Feldmann J, Zhao FJ. Phytochelatins play a key role in arsenic accumulation and tolerance in the aquatic macrophyte Wolffia globosa . Environmental Pollution. 2012 Jun 1;165:18-24 - 39.
Da Silva AA, Oliveira JA, Campos FV, Ribeiro C, Farnese FD. Role of glutathione in tolerance to arsenite in Salvinia molesta , an aquatic fern. Acta Botanica Brasilica. 2017 Dec;31(4):657-64 - 40.
Hoffmann T, Kutter C, Santamaria J. Capacity of Salvinia minima Baker to tolerate and accumulate As and Pb. Engineering in Life Sciences. 2004 Feb 5;4(1):61-5 - 41.
Rahman MA, Hasegawa H, Ueda K, Maki T, Rahman MM. Influence of phosphate and iron ions in selective uptake of arsenic species by water fern ( Salvinia natans L.). Chemical Engineering Journal. 2008 Dec 15;145(2):179-84 - 42.
Sood A, Uniyal PL, Prasanna R, Ahluwalia AS. Phytoremediation potential of aquatic macrophyte, Azolla. Ambio. 2012 Mar;41(2):122-37 - 43.
Pandey VC. Phytoremediation of heavy metals from fly ash pond by Azolla caroliniana . Ecotoxicology and Environmental Safety. 2012 Aug 1;82:8-12 - 44.
Rai PK. Phytoremediation of Hg and Cd from industrial effluents using an aquatic free floating macrophyte Azolla pinnata . International journal of phytoremediation. 2008 Jul 23;10(5):430-9 - 45.
Mahmud R, Inoue N, Kasajima SY, Shaheen R. Assessment of potential indigenous plant species for the phytoremediation of arsenic-contaminated areas of Bangladesh. International Journal of Phytoremediation. 2008 Apr 3;10(2):119-32 - 46.
Rofkar JR, Dwyer DF, Bobak DM. Uptake and toxicity of arsenic, copper, and silicon in Azolla caroliniana andLemna minor . International journal of phytoremediation. 2014 Feb 1;16(2):155-66 - 47.
Zhang X, Lin AJ, Zhao FJ, Xu GZ, Duan GL, Zhu YG. Arsenic accumulation by the aquatic fern Azolla: comparison of arsenate uptake, speciation and efflux by A. caroliniana andA. filiculoides . Environmental Pollution. 2008 Dec 1;156(3):1149-55 - 48.
Srivastava S, Sounderajan S, Udas A, Suprasanna P. Effect of combinations of aquatic plants ( Hydrilla ,Ceratophyllum ,Eichhornia ,Lemna andWolffia ) on arsenic removal in field conditions. Ecological engineering. 2014 Dec 1;73:297-301 - 49.
Srivastava S, Mishra S, Dwivedi S, Tripathi RD. Role of thiol metabolism in arsenic detoxification in Hydrilla verticillata (Lf) Royle. Water, Air, & Soil Pollution. 2010 Oct;212(1):155-65 - 50.
Khang HV, Hatayama M, Inoue C. Arsenic accumulation by aquatic macrophyte coontail ( Ceratophyllum demersum L.) exposed to arsenite, and the effect of iron on the uptake of arsenite and arsenate. Environmental and experimental botany. 2012 Nov 1;83:47-52 - 51.
Chen G, Liu X, Brookes PC, Xu J. Opportunities for phytoremediation and bioindication of arsenic contaminated water using a submerged aquatic plant: Vallisneria natans (Lour.) Hara. International journal of phytoremediation. 2015 Mar 4;17(3):249-55 - 52.
Norouznia H, Hamidian AH. Phytoremediation efficiency of pondweed ( Potamogeton crispus ) in removing heavy metals (Cu, Cr, Pb, As and Cd) from water of Anzali wetland. International Journal of Aquatic Biology. 2014 Sep 10;2(4):206-14 - 53.
Krayem M, Baydoun M, Deluchat V, Lenain JF, Kazpard V, Labrousse P. Absorption and translocation of copper and arsenic in an aquatic macrophyte Myriophyllum alterniflorum DC. in oligotrophic and eutrophic conditions. Environmental Science and Pollution Research. 2016 Jun;23(11):11129-36 - 54.
Li B, Gu B, Yang Z, Zhang T. The role of submerged macrophytes in phytoremediation of arsenic from contaminated water: A case study on Vallisneria natans (Lour.) Hara. Ecotoxicology and environmental safety. 2018 Dec 15;165:224-31 - 55.
Datta R, Quispe MA, Sarkar D. Greenhouse study on the phytoremediation potential of vetiver grass, Chrysopogon zizanioides L., in arsenic-contaminated soils. Bulletin of environmental contamination and toxicology. 2011 Jan 1;86(1):124-8 - 56.
Jomjun N, Siripen T, Maliwan S, Jintapat N, Prasak T, Somporn C, Petch P. Phytoremediation of arsenic in submerged soil by wetland plants. International journal of phytoremediation. 2010 Nov 18;13(1):35-46 - 57.
Raj A, Jamil S, Srivastava PK, Tripathi RD, Sharma YK, Singh N. Feasibility Study of Phragmites karka andChristella dentata Grown in West Bengal as Arsenic Accumulator. International journal of phytoremediation. 2015 Sep 2;17(9):869-78 - 58.
Guarino F, Miranda A, Castiglione S, Cicatelli A. Arsenic phytovolatilization and epigenetic modifications in Arundo donax L. assisted by a PGPR consortium. Chemosphere. 2020 Jul 1;251:126310 - 59.
Simmons ZD, Suleiman AA, Theegala CS. Phytoremediation of arsenic and lead using alligator weed ( Alternathera philoxeroides ). Transactions of the ASABE. 2007;50(5):1895-900 - 60.
Sharma P, Tripathi S, Chandra R. Highly efficient phytoremediation potential of metal and metalloids from the pulp paper industry waste employing Eclipta alba (L) andAlternanthera philoxeroide (L): Biosorption and pollution reduction. Bioresource Technology. 2021 Jan 1;319:124147 - 61.
Ghassemzadeh F, Yousefzadeh H, Arbab-Zavar MH. Arsenic phytoremediation by Phragmites australis : green technology. International journal of environmental studies. 2008 Aug 1;65(4):587-94 - 62.
Caporale AG, Sarkar D, Datta R, Punamiya P, Violante A. Effect of arbuscular mycorrhizal fungi ( Glomus spp.) on growth and arsenic uptake of vetiver grass (Chrysopogon zizanioides L.) from contaminated soil and water systems. Journal of soil science and plant nutrition. 2014 Dec;14(4):955-72 - 63.
Tripathi RD, Srivastava S, Mishra S, Singh N, Tuli R, Gupta DK, Maathuis FJ. Arsenic hazards: strategies for tolerance and remediation by plants. Trends in biotechnology. 2007 Apr 1;25(4):158-65 - 64.
Zhao FJ, Ma JF, Meharg AA, McGrath SP. Arsenic uptake and metabolism in plants. New Phytologist. 2009 Mar;181(4):777-94 - 65.
Mkandawire M, Lyubun YV, Kosterin PV, Dudel EG. Toxicity of arsenic species to Lemna gibba L. and the influence of phosphate on arsenic bioavailability. Environmental Toxicology: An International Journal. 2004 Feb;19(1):26-34 - 66.
Abedin MJ, Feldmann J, Meharg AA. Uptake kinetics of arsenic species in rice plants. Plant physiology. 2002 Mar 1;128(3):1120-8 - 67.
Meharg AA, Jardine L. Arsenite transport into paddy rice ( Oryza sativa ) roots. New phytologist. 2003 Jan;157(1):39-44 - 68.
Ma JF, Yamaji N, Mitani N, Xu XY, Su YH, McGrath SP, Zhao FJ. Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proceedings of the National Academy of Sciences. 2008 Jul 22;105(29):9931-5 - 69.
Benga G. Water channel proteins (later called aquaporins) and relatives: past, present, and future. IUBMB life. 2009 Feb;61(2):112-33 - 70.
Robinson B, Kim N, Marchetti M, Moni C, Schroeter L, van den Dijssel C, Milne G, Clothier B. Arsenic hyperaccumulation by aquatic macrophytes in the Taupo Volcanic Zone, New Zealand. Environmental and Experimental Botany. 2006 Dec 1;58(1-3):206-15 - 71.
Srivastava S, Mishra S, Tripathi RD, Dwivedi S, Trivedi PK, Tandon PK. Phytochelatins and antioxidant systems respond differentially during arsenite and arsenate stress in Hydrilla verticillata (Lf) Royle. Environmental science & technology. 2007 Apr 15;41(8):2930-6 - 72.
Raab A, Ferreira K, Meharg AA, Feldmann J. Can arsenic–phytochelatin complex formation be used as an indicator for toxicity in Helianthus annuus ?. Journal of Experimental Botany. 2007 Apr 1;58(6):1333-8 - 73.
Delnomdedieu M, Basti MM, Otvos JD, Thomas DJ. Reduction and binding of arsenate and dimethylarsinate by glutathione: a magnetic resonance study. Chemico-biological interactions. 1994 Feb 1;90(2):139-55 - 74.
Bleeker PM, Hakvoort HW, Bliek M, Souer E, Schat H. Enhanced arsenate reduction by a CDC25-like tyrosine phosphatase explains increased phytochelatin accumulation in arsenate-tolerant Holcus lanatus . The Plant Journal. 2006 Mar;45(6):917-29 - 75.
Meharg AA, Hartley-Whitaker J. Arsenic uptake and metabolism in arsenic resistant and nonresistant plant species. New Phytologist. 2002 Apr;154(1):29-43 - 76.
Mittler R. Oxidative stress, antioxidants and stress tolerance. Trends in plant science. 2002 Sep 1;7(9):405-10 - 77.
Dhankher OP, Pilon-Smits EA, Meagher RB, Doty S. Biotechnological approaches for phytoremediation. InPlant biotechnology and agriculture 2012 Jan 1 (pp. 309-328). Academic Press - 78.
Kotrba P, Najmanova J, Macek T, Ruml T, Mackova M. Genetically modified plants in phytoremediation of heavy metal and metalloid soil and sediment pollution. Biotechnology advances. 2009 Nov 1;27(6):799-810 - 79.
Sunkar R, Kaplan B, Bouché N, Arazi T, Dolev D, Talke IN, Maathuis FJ, Sanders D, Bouchez D, Fromm H. Expression of a truncated tobacco NtCBP4 channel in transgenic plants and disruption of the homologous Arabidopsis CNGC1 gene confer Pb2+ tolerance. The Plant Journal. 2000 Nov;24(4):533-42 - 80.
Hirschi KD, Korenkov VD, Wilganowski NL, Wagner GJ. Expression of Arabidopsis CAX2 in tobacco. Altered metal accumulation and increased manganese tolerance. Plant physiology. 2000 Sep 1;124(1):125-34 - 81.
Zeng H, Xu L, Singh A, Wang H, Du L, Poovaiah BW. Involvement of calmodulin and calmodulin-like proteins in plant responses to abiotic stresses. Frontiers in plant science. 2015 Aug 11;6:600 - 82.
Song WY, Sohn EJ, Martinoia E, Lee YJ, Yang YY, Jasinski M, Forestier C, Hwang I, Lee Y. Engineering tolerance and accumulation of lead and cadmium in transgenic plants. Nature biotechnology. 2003 Aug;21(8):914-9 - 83.
Bienert GP, Thorsen M, Schüssler MD, Nilsson HR, Wagner A, Tamás MJ, Jahn TP. A subgroup of plant aquaporins facilitate the bi-directional diffusion of As (OH) 3 and Sb (OH) 3 across membranes. BMC biology. 2008 Dec;6(1):1-5 - 84.
Mosa KA, Kumar K, Chhikara S, Mcdermott J, Liu Z, Musante C, White JC, Dhankher OP. Members of rice plasma membrane intrinsic proteins subfamily are involved in arsenite permeability and tolerance in plants. Transgenic research. 2012 Dec 1;21(6):1265-77 - 85.
Xu XY, McGrath SP, Zhao FJ. Rapid reduction of arsenate in the medium mediated by plant roots. New Phytologist. 2007 Nov;176(3):590-9 - 86.
Duan GL, Zhu YG, Tong YP, Cai C, Kneer R. Characterization of arsenate reductase in the extract of roots and fronds of Chinese brake fern, an arsenic hyperaccumulator. Plant Physiology. 2005 May 1;138(1):461-9 - 87.
Ma JF, Tamai K, Ichii M, Wu GF. A rice mutant defective in Si uptake. Plant Physiology. 2002 Dec 1;130(4):2111-7 - 88.
Ma JF, Tamai K, Yamaji N, Mitani N, Konishi S, Katsuhara M, Ishiguro M, Murata Y, Yano M. A silicon transporter in rice. Nature. 2006 Mar;440(7084):688-91 - 89.
Meng YL, Liu Z, Rosen BP. As (III) and Sb (III) uptake by GlpF and efflux by ArsB in Escherichia coli . Journal of Biological Chemistry. 2004 Apr 30;279(18):18334-41 - 90.
Dubey S, Shri M, Misra P, Lakhwani D, Bag SK, Asif MH, Trivedi PK, Tripathi RD, Chakrabarty D. Heavy metals induce oxidative stress and genome-wide modulation in transcriptome of rice root. Functional & integrative genomics. 2014 Jun;14(2):401-17 - 91.
Wang Y, Dong C, Xue Z, Jin Q, Xu Y. De novo transcriptome sequencing and discovery of genes related to copper tolerance in Paeonia ostii. Gene. 2016 Jan 15;576(1):126-35 - 92.
Lu YP, Li ZS, Rea PA. AtMRP1 gene of Arabidopsis encodes a glutathione S-conjugate pump: isolation and functional definition of a plant ATP-binding cassette transporter gene. Proceedings of the National Academy of Sciences. 1997 Jul 22;94(15):8243-8 - 93.
Tommasini R, Vogt E, Fromenteau M, Hörtensteiner S, Matile P, Amrhein N, Martinoia E. An ABC-transporter of Arabidopsis thaliana has both glutathione-conjugate and chlorophyll catabolite transport activity. The Plant Journal. 1998 Mar;13(6):773-80 - 94.
Gasic K, Korban SS. Transgenic Indian mustard ( Brassica juncea ) plants expressing an Arabidopsis phytochelatin synthase (AtPCS1 ) exhibit enhanced As and Cd tolerance. Plant molecular biology. 2007 Jul;64(4):361-9 - 95.
Guo J, Dai X, Xu W, Ma M. Overexpressing GSH1 andAsPCS1 simultaneously increases the tolerance and accumulation of cadmium and arsenic inArabidopsis thaliana . Chemosphere. 2008 Jul 1;72(7):1020-6 - 96.
Dhankher OP, Li Y, Rosen BP, Shi J, Salt D, Senecoff JF, Sashti NA, Meagher RB. Engineering tolerance and hyperaccumulation of arsenic in plants by combining arsenate reductase and γ-glutamylcysteine synthetase expression. Nature biotechnology. 2002 Nov;20(11):1140-5 - 97.
Li Y, Dhankher OP, Carreira L, Lee D, Chen A, Schroeder JI, Balish RS, Meagher RB. Overexpression of phytochelatin synthase in Arabidopsis leads to enhanced arsenic tolerance and cadmium hypersensitivity. Plant and Cell Physiology. 2004 Dec 15;45(12):1787-97 - 98.
Xu L, Wang Y, Liu W, Wang J, Zhu X, Zhang K, Yu R, Wang R, Xie Y, Zhang W, Gong Y. De novo sequencing of root transcriptome reveals complex cadmium-responsive regulatory networks in radish ( Raphanus sativus L.). Plant Science. 2015 Jul 1;236:313-23 - 99.
Xie Y, Ye S, Wang Y, Xu L, Zhu X, Yang J, Feng H, Yu R, Karanja B, Gong Y, Liu L. Transcriptome-based gene profiling provides novel insights into the characteristics of radish root response to Cr stress with next-generation sequencing. Frontiers in plant science. 2015 Mar 31;6:202 - 100.
Williams PN, Price AH, Raab A, Hossain SA, Feldmann J, Meharg AA. Variation in arsenic speciation and concentration in paddy rice related to dietary exposure. Environmental science & technology. 2005 Aug 1;39(15):5531-40 - 101.
Zhu YG, Sun GX, Lei M, Teng M, Liu YX, Chen NC, Wang LH, Carey AM, Deacon C, Raab A, Meharg AA. High percentage inorganic arsenic content of mining impacted and nonimpacted Chinese rice. Environmental science & technology. 2008 Jul 1;42(13):5008-13 - 102.
Qin J, Rosen BP, Zhang Y, Wang G, Franke S, Rensing C. Arsenic detoxification and evolution of trimethylarsine gas by a microbial arsenite S-adenosylmethionine methyltransferase. Proceedings of the National Academy of Sciences. 2006 Feb 14;103(7):2075-80 - 103.
Qin J, Lehr CR, Yuan C, Le XC, McDermott TR, Rosen BP. Biotransformation of arsenic by a Yellowstone thermoacidophilic eukaryotic alga. Proceedings of the National Academy of Sciences. 2009 Mar 31;106 (13):5213-7 - 104.
Norton GJ, Lou-Hing DE, Meharg AA, Price AH. Rice–arsenate interactions in hydroponics: whole genome transcriptional analysis. Journal of experimental botany. 2008 May 1;59(8):2267-76