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Hazardous heavy metals contamination of vegetables and food chain: Role of sustainable remediation approaches - A review
Journal Pre-proof Hazardous heavy metals contamination of vegetables and food chain: Role of sustainable remediation approaches - A review Sandeep Kumar, Shiv Prasad, Krishna Kumar Yadav, Manoj Shrivastava, Neha Gupta, Shivani Nagar, Quang-Vu Bach, Hesam Kamyab, Shakeel A. Khan, Sunita Yadav, Lal Chand Malav PII:
S0013-9351(19)30589-4
DOI:
https://doi.org/10.1016/j.envres.2019.108792
Reference:
YENRS 108792
To appear in:
Environmental Research
Received Date: 23 June 2019 Revised Date:
12 September 2019
Accepted Date: 1 October 2019
Please cite this article as: Kumar, S., Prasad, S., Yadav, K.K., Shrivastava, M., Gupta, N., Nagar, S., Bach, Q.-V., Kamyab, H., Khan, S.A., Yadav, S., Malav, L.C., Hazardous heavy metals contamination of vegetables and food chain: Role of sustainable remediation approaches - A review, Environmental Research (2019), doi: https://doi.org/10.1016/j.envres.2019.108792. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2019 Published by Elsevier Inc.
Hazardous heavy metals contamination of vegetables and food chain: Role of sustainable remediation approaches - A review Sandeep Kumara*, Shiv Prasada, Krishna Kumar Yadavb*, Manoj Shrivastavaa, Neha Guptab, Shivani Nagarc, Quang-Vu Bachd, Hesam Kamyabe, Shakeel A. Khana, Sunita Yadava, Lal Chand Malavf a
Centre for Environment Science and Climate Resilient Agriculture, Indian Agricultural Research Institute, New Delhi 110012, India Email- [email protected]
b
Institute of Environment and Development Studies, Bundelkhand University, Kanpur Road, Jhansi 284128, India c
Division of Plant Physiology, Indian Agricultural Research Institute, New Delhi 110012, India d
e
Institute of Research and Development, Duy Tan University, Da Nang, Vietnam
UTM Razak School of Engineering and Advanced Technology, Universiti Teknologi Malaysia, Malaysia f
National Bureau of Soil Survey and Land Use Planning, Nagpur, India *Corresponding author: [email protected]
1
Graphical Abstract
Abstract This review emphasizes the role of toxic metal remediation approaches due to their broad sustainability and applicability. The rapid developmental processes can incorporate a large quantity of hazardous and unseen heavy metals in all the segments of the environment, including soil, water, air and plants. The released hazardous heavy metals (HHMs) entered into the food chain and biomagnified into living beings via food and vegetable consumption and originate potentially health-threatening effects. The physical and chemical remediation approaches are restricted and localized and, mainly applied to wastewater and soils and not the plant. The nanotechnological, biotechnological and genetical approaches required to more rectification and sustainability. A cellular, molecular and nano-level understanding of the pathways and reactions 2
are responsible for potentially toxic metals (TMs) accumulation. These approaches can enable the development of crop varieties with highly reduced concentrations of TMs in their consumable foods and vegetables. As a critical analysis by authors observed that nanoparticles could provide very high adaptability for both in-situ and ex-situ remediation of hazardous heavy metals (HHMs) in the environment. These methods could be used for the improvement of the inbuilt genetic potential and phytoremediation ability of plants by developing transgenic. These biological processes involve the transfer of gene of interest, which plays a role in hazardous metal uptake, transport, stabilization, inactivation and accumulation to increased host tolerance. This review identified that use of nanoremediation and combined biotechnological and, transgenic could help to enhance phytoremediation efficiency in a sustainable way. Keywords: bioaccumulation; biotechnology; nanotechnology; toxicity, transgenic approach. 1. Introduction Worldwide, more than 10 million sites covering more than 20 million ha of land are considered soil polluted sites, of which >50% are contaminated with hazardous heavy metals (HHMs) and/or metalloids (He et al., 2015). The combined worldwide economic impact of heavy metals (HMs) pollution is estimated to be in excess of US $10 billion per year (He et al., 2015). A study by the Ministry of Environmental Protection (MEP), China, reported that the total area of arable land contaminated with heavy metals had reached near to 20 mha, estimating that almost 16.1% of the total arable land, and 19.4% of recognized cropland locations were above the normal range of heavy metals accumulation. Furthermore, 13.7%, 2.8%, 1.8% and 1.1% of arable land contained slight, mild, moderate and heavy pollution levels, respectively (Zhao et al., 2015; Sodango et al., 2018). According to the Central Water Commission (CWC) of India, 42 3
rivers have at least two HHMs beyond the permissible limit (CWC, 2018). As per Central Ground Water Board (CGWB), India, groundwater of more than 718 districts is affected by heavy metal toxicity with cadmium (Cd), chromium (Cr), arsenic (As), lead (Pb) and iron (Fe). The heavy metals in contaminated soils impair the natural ecosystem services and eventually damage human health via the food chain (Jaishankar et al., 2014; Yadav et al., 2018a; Maurya et al., 2019). The primary sources of heavy-metal pollution are industrialization, mining, milling, fossil fuel burning, agrochemicals that discharge a variety of HHMs such as As, Cr, mercury (Hg), Cd, copper (Cu), nickel (Ni), cobalt (Co), zinc (Zn) and Pb into the agricultural soils and water bodies (Kumar et al., 2019a; Kumar et al., 2019b; Kumar et al., 2019c; Gupta et al., 2018). Vegetables are an important part of the human diet due to the richness of beneficial and essential minerals and nutrients (Nankishore, 2014). Unfortunately, vegetables can uptake and accumulate HHMs beyond recommended limits in their entire body including both edible and inedible parts (Tasrina et al., 2015). In the last few years, the concentration of HHMs in vegetables (leafy, root and fruit), has been observed at high levels (Wai et al., 2017). Eventually, the build-up of HHMs in vegetables and edible parts of crops in contaminated soils, is a matter of serious concern due to the harmful and irreversible effects of metals impacting both humans as well as animal’s overall health (Malik, 2004). The removal of HHMs from industrial wastewaters and contaminated soils has been studied for many years, including the implementation of several physicochemical approaches of removal that include filtration, evaporation, reverse osmosis, ion-exchange, redox reactions (oxidation and reduction), precipitation, and electrochemical removal. However, hazardous metal contamination in vegetables and plants and their subsequent decontamination fall under the
4
exploration stage of research and are not considered important enough to lay out a concrete remediation plan to move forward by local community governments. The physical and chemical remediation approaches are restricted and localized and mainly applied to wastewater and contaminated soils and not the plant life that may reside there. Some phytoremediation methods are well explored but not suitable for edible crops and vegetables (Ali et al., 2013; Sharma et al., 2015). To move past these issues, the biotechnological and nanotechnological approaches can open a path ahead to remove the metals from contaminated vegetables and plants (Mani and Kumar, 2014; Zeng et al., 2015; Dixit et al., 2015; Singh et al., 2015; Mosa et al., 2016; Ali et al., 2018; Srivastav et al., 2018) by successfully superseding traditional methods (Singh and Prasad, 2015). Certain microorganisms, for example, can respond to heavy-metal stress through transport across the cell membrane, entrapment in extracellular capsules, precipitation, biosorption to cell walls, complexation and redox reactions (Malik, 2004). Microorganisms can also counter heavy metal stress using diverse defensive systems, such as compartmentalization, exclusion, formation of complexes and the synthesis of binding proteins, i.e. metallothioneins (MTs) or phytochelatins (PCs) (Mejare and Bulow, 2001). The application of nanomaterials (NMs) in plants for removal of HMs is still under investigation (Okuo et al., 2018; Srivastav et al., 2018). This review identified advanced approaches such as nanoremediation and use of combined biotechnological and transgenic that can help in a better way to enhance phytoremediation efficiency in a sustainable way. 2. Search strategy for quality of the articles applied in the study
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The method used in the literature review involves of three steps: (i) Collection and identification of relevant literature for the study, and (ii) Extraction of data and diagraming representation, and (iii) Applicability of sustainable remedial approaches for this study. We searched and collected the relevant literature in the Scopus, Science Direct and Google Scholar databases, in March and April of 2018, using the following Boolean search string: ( “heavy metals” OR “Heavy metal contamination” OR “Heavy metals toxicity” OR “Heavy metals contamination of food chain” OR “Heavy metals remediation sustainable methods” OR “nanotechnology for heavy metals remediation” OR Biotechnological advances for heavy metals remediation” OR “Genetic approaches of remediation” OR “Heavy metals guidelines and permissible limits” OR “Current status of remedial approaches”. We collected all the well cited and high impacts literature and screened them as per requirement. To select most relevant and manageable set of studies among the identified pieces of literature, we set up the following selection rules as followed by Sandin and Peters (2017). 2.1. Collection and identification of relevant literature for the study a) Search all type relevant findings and included in study (mostly peer-reviewed) b) All type material related to heavy metal toxicity and contamination were carefully studied and selected the suitable one. c) Included the study throughout the World. d) Excluded the studies which do not include quantitative results. e) Excluded almost all the studies which are more than 15 years old. f) Excluded the studies from other languages like Chinese, French, German and Swedish. g) Exclusion of studies on physical and chemical remediation of heavy metals. h) Included only nanotechnological, biotechnological and genetical approaches.
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i) Exclusion of duplicates and copying of studies. 2.2. Extraction of data and diagraming representation a) Data was extracted mostly in tabular manner and provided in supplementary files. b) A huge number of studies were read thoroughly and collected the data in systematic and captureable manner. c) Diagrammatic representation of processes was keep in mind and try to represent in ease to access manner. d) Collected all the permissible limits of many countries in tabular manner for easy access. 2.3. Applicability of sustainable remedial approaches for this study a) Sustainable methods of remediation were studied and layout the new concept with wide applicability in the review. b) Try to incorporate the possible new outcomes of sustainable approaches of heavy metals remediation c) Sustainable methods were selected as per several assumptions like why, applicability and final outcome. 3. Sources of heavy metals in agricultural soil Heavy metals (HMs) are omnipresent in the environment due to both natural (geogenic) as well as anthropologic (human induced) sources found in agricultural soils (Rahimi et al., 2017; Ratul et al., 2018). The contamination of TMs in soil, water and plants in several regions of the world are summarized in Table 1. Soil pollution by heavy metals is a universal problem for food production and human health (Liu et al., 2018). The most important natural sources for heavy metal introduction into soils are weathering of rocks, erosion and volcanic activity and the anthropogenic sources of ore mining operations, smelting, electroplating, industries’ 7
effluents, landfills, warfare and military training, use of pesticides and phosphate fertilizer, application of biosolids (e.g., livestock manures, composts, and municipal sewage sludge) and atmospheric deposition (Fulekar et al., 2009; Herrero et al., 2019) (Fig. S1). The heavy metals are a key component of rocks and soils in the environment, introduced through weathering, erosion and anthropogenically. Heavy metals can reach into the soilplant-human atmosphere and accumulate there. The total concentration of heavy metals in soil is the sum of all these variables minus the losses through off-take in harvested crops, erosion of soil particles by wind or water, leaching down the soil profile in solution and losses by volatilization of some elements in gaseous forms. This balance of the heavy metals in the soil can be represented by the equation 1 (Lombi and Gerzabek, 1998): Mtotal = [Mp + Ma + Mf + Mag + Mow + Mip] – [Mcr + Ml]………..eq (1) where, Mtotal is the total heavy metal in soil, Mp is the heavy metals in the parent material, Ma is the heavy metal concentration in atmospheric deposition, Mf are the heavy metals in fertilizer sources, Mag are the heavy metals in agrochemical sources, Mow are the heavy metal concentrations in organic waste sources, Mip are other inorganic pollutants, Mcr is the heavy metal in crop removal, and Ml is the heavy metal losses by leaching, volatilization, and other extraction processes. Agricultural land and irrigation water contamination has become a harsh environmental problem in several developed and developing countries in the last decade due to scarcity of irrigation water availability (Fan et al., 2017). In agricultural soil, soil quality is an indicator of heavy metal contamination arising from on-farm activities (Liu et al., 2012). As mentioned previously, the heavy metals that accumulate in soil significantly add to the pollution of agricultural commodities and indirectly become the leading component of health risks (Sawut
8
et al., 2018). Heavy metals contamination of soil, water, crop and vegetables is one of the most severe environmental predicaments globally (Ahmad and Goni, 2010). It creates possible threats to the ecological soil-food chain that can impair with soil fertility, quality of drinking water and human health, direct ingestion, dermal contact, inhalation and oral consumption (Khan et al., 2008; Lu et al., 2011). The contamination of agricultural soil occurs through irrigation with wastewater (Hajjami et al., 2013), fertilizers application, pesticides dosing, erosion and sedimentation of mined or contaminated soils, heavy farm machinery operations, municipal solid-waste compost incorporation, and leaching from landfill site, dry and wet deposition of industrial pollutants, and volcanic activities (Gupta et al., 2015; Sodango et al., 2018). In addition, fly ash deposition from coal power plants are the notable sources of soil contamination, accumulation and pollution of heavy metals in soil, water and crops (Nagajyoti et al., 2010; (Kanchan et al., 2015). Long-term application of wastewater results in build-up of heavy metals in soil and crops that can limit soil functioning, reduce the nutritional quality of vegetables, toxicity to crops and contamination of the food chain (Chen et al., 2010; Singh et al., 2010). Due to continuous intake, the bioaccumulation of heavy metals takes place in vegetables, crops and humans. Crop species differ in their ability to absorb heavy metals from soil and water (Mapanda et al., 2005). The immense growth of industries has remarkably increased the discharge of effluents to the environment, particularly in soil and water, which has led to the contamination of HHMs in soil and now finally accumulated in living beings. The chaotic discharge of heavy metals into the soil and waters is a significant health concern, as they cannot be broken down to non9
toxic forms and therefore have long-lasting influences on the ecosystem (Dixit et al., 2015). Mining and milling works, along with grinding, gathering ores, extraction and purification of minerals and disposal of tailings provide apparent sources of contamination in the environment, i.e. soil, water and plants, along with the discharge of mining wastewater (Table S1). Kumar et al. (2019) used regression modeling, principal component analysis and accumulation nutrient elements to predict the heavy metal concentrations in Brassica oleracea tissues grown in integrated industrial effluent.
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Table 1. Heavy metal contamination in agricultural soils, crops or vegetables and water in different countries Source of HM contamination
HM Species
Contamination
Wastewater of Shitalakhya river
Cu, Ni, Cd, Cr, Pb, Zn
Soil and Vegetables
Wastewater treatment plant
Zn, Cu, Pb, Cd
Soil, water and crops
Soil
Hg
vegetables
Mining activities
Pb, As, Hg, Cd, Cr, Ni
Soil and sediment samples
Vegetable/Crop Basella alba, Cucurbita moschata, Amaranthus lividus, Trichosanthes cucumerina and Spinacia oleracea Vicia faba, Triticum turgidum, Triticum æstivum, Eruca. sativa, Urtica dioica, Madia sativa and Malus sylvestris Piper nigrum, Spinacia oleracea, Brassica oleracea, Brassica rapa, Raphanus raphanistrum, Phaseolus vulgaris, Vigna unguiculata and Solnum melongena Phaseolus vulgaris, Solanum melongena, Piper nigrum, Ipomoea aquatic, Ipomoea batatas, Amaranthus dubius and Solanum lycopersicum
Mine affected area
Cu, Pb, As, Cd
Soil and vegetable
Industrial and municipal sewage water
Cd, Pb, Ni, Zn
Soil and crop
Oryza sativa
Human Activities
Fe, Mn, Pb, Cu, Cd, Zn, Cr, Ni
Soil and Sediment
-
Agricultural field and urban settlements
Cu, Cr, Zn, Ni, Cd, Pb
Water samples, sediments
Lemna minor
Urbanization
As, Zn, Cd, Cr, Hg, and Pb
Soil, water and vegetables
Solanum lycopersicum, Phaseolus vulgaris, Triticum aestivum, Raphanus raphanistrum, Momordica charantia and Brassica oleracea
11
Region
Reference
Narayangonj, Bangladesh
Ratul et al. (2018)
Marrakech, Morocco
Chaoua et al. (2018)
China
Yu et al. (2018)
Zacatecas, Mexico
Covarrubias et al. (2018)
Daye, China
Yang et al. (2018)
Lenjan, Iran
Rahimi et al. (2017)
Liaohe River Delta, North China Anchar Lake, Kashmir, India
Urumqi, Xinjiang, China
Yan et al. (2018)
Showqi et al. (2018)
Sawut et al. (2018)
Geogenic and anthropogenic sources Human induced activities
As, Cd, Cr, Cu, Hg, Ni, Pb, Se, and Zn As, Cd, Cu, Ni, Pb, Zn
Human activities in river area
Cd, Mn, Cr, Cu, Ni, Pb, Zn, Fe
Geogenic and anthropogenic sources
Pb, Zn, Cu, Cd, As, Hg, Cr, Ni Cr, Ni, Cu, As, Cd and Pb Pb, Cd, and Cu
Industrialization Fertilizers, pesticides and other farm inputs Industries Soil Erosion
Cd, As, Pb, Cu, Zn, Ni, Cr Cr, Cu, Pb, and Ni
Glass industry
Cd, Cr, Cu, Fe, Mn, Pb, Zn
Coal Fired Thermal Power Plant
Pb, Cd, Cr As. Cu, Zn, Ni and Fe
Industrial area
Cu, Zn, Pb, Cr, Cd, Fe, and Ni
Soil Soil Soil and vegetables
Spinacia oleracea, Lagenaria siceraria, Cucurbita maxima and Solanum melongena
Agricultural soil
-
Agricultural soil
-
Agricultural soil
-
Agricultural soil
-
Agricultural Fields Soil and Agricultural Crops
Brassica juncea, Triticum aestivum and Hordeum vulgare
Agricultural soil
water, soil, and vegetables
Solanum melongena, Capsicum frutescence, , Raphanus sativus, Abelmoschus esculentus, Solanum lycopersicum and Brassica oleracea
12
Hainan Island, China
Liao et al. (2018)
Azerbaijan Province, Iran
Mohammadi et al. (2018)
Dera Ghazi Khan, Pakistan
Latif et al. (2018)
Hunan province, China Tangail, Bangladesh Semarang, Indonesia
Proshad et al. (2018)
Hunan, China
Zhang et al. (2018)
Bedfordshire, UK
Quinton and Catt (2007)
Jhabrera, India
Kumar and Chopra (2015)
Farakka, India
Sengupta et al. (2010)
Dhaka, Bangladesh
Ahmad and Goni (2010)
Li et al. (2018)
Hindarwati et al. (2018)
4. Heavy metal toxicity and bioaccumulation through food chain contamination The physical, chemical, and biological processes as well as anthropogenic activities, can release heavy metals in the environment and cause the accumulation of heavy metal toxins within living beings participating in the food chain (Koivula et al., 2011). As previously discussed, the HHMs disperse into the soil, air and water bodies from where they can be taken up or ingested by crops/plants, bio-accumulated into top consumers, and finally biomagnified (Hossain et al., 2008; Pollard et al., 2014). Once HHMs enter into food chain, they can not be removed easily from the top of food chain and thereby become circulated into the whole food web. Many hyperaccumulated plants serve as food for human beings and animals. Hence, the cycle from soil to humans via plants and again into the soil after death of top consumers, provide a path for HHMs to remain sustained within the environment for long periods of time inducing many harmful effects (Fig. S2). The contamination in crops depends on the efficiency of transfer from soil to aboveground portions of plants. The toxic metal bioaccumulation in vegetables is explained in Table 2. Consumption of contaminated crops containing HHMs can create conceivably deleterious health hazards in living beings (Clemens and Ma, 2016). The cycle of heavy metals in the food chain begins with various sources. To illustrate, Cd is taken up from soil via roots to the plant body. In the case of Pb, the heave metal is absorbed from the air dust into plants, and As and Hg may be obtained from sewage water. During the transfer from one section to another in the food chain, some heavy metals have tendency of accumulation in the tissues (liver, feathers, muscles, kidney and other organs) of top consumers. Table 2. Bioaccumulation of HHMs in different organs of vegetables Region
HM Species
Plant Part Analyzed
Vegetable
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*Concentration of HM (mg/kg)
Reference
Basella alba, Cucurbita moschata, Anolis lividus, Trichosanthes cucumerina, Spinacia oleracea
Edible parts
Lepidium sativum, Coriandrum sativum, Spinacia olarecea
Leaves
Zn - 19.762 Cu - 9.373 Pb - 3.699 Ni - 2.92 Cr - 1.127 Cd - 0.168 Pb – 0.2-4.7 Zn – 1.7-6.7 Cu – 0.59-2.23 Cd – 0.02-0.52 Ni – 0.04-0.81 As – 0.018-0.126 Co – 0.005-0.21 Cr – 0.1-1.87 Zn – 33.8-77.2 Cu – 2.9-7.0 Pb – 18.3-45.7 Cd – 6.0-12.0 Cd – 0.01-0.07, Pb – BDL-0.05
Narayangonj, Bangladesh
Cu, Ni, Cd, Cr, Pb and Zn
Kahrizak, South of Tehran, Iran
Pb, Zn, Cu, Cd, Ni, As, Cr and Co
Marrakech, Morocco
Zn, Cu, Pb and Cd
Vicia faba
Root, Leaves, Pod and seeds
Tamale Metropolis, Ghana
Pb and Cd
Brassica oleracea, Solanum lycopersicum, Daucus carota, Capsicum annuum, Allium cepa
Edible parts
Assiut, Egypt
Cd, Pb and Ni
Solanum melongena
Edible parts
Egypt
Pb, Cd, Cu, Ni and Cr
Solanum tuberosum, Solanum lycopersicum, Cucurbita maxima
Edible parts
Nevsehir Province, Turkey
Cd, Pb, Zn, Cr, Cu, Ni and Fe
Gazipur district, Bangladesh
Pb, Ni, Co, Cr and Cd
Ethiopia
Fe, Zn, Pb, Cr and Cd
Temeke district, Tanzania
Fe, Zn, Pb and Cu
Daye, China
Cu, Pb, As and Cd
Solanum lycopersicum, Solanum cepa, Capsicum annuum
Edible parts
Leaves, roots and stem
Spinacia oleracea, Agelaius tricolor, Sonchus oleraseus
Spinacia oleracea
Leaves
Ipomoea batatas, Amaranthus hybridus, Abelmoschus esculentus, Solanum melongena Vigna unguiculata, Ipomoea aquatic, Agelaius tricolor,
14
Edible parts Edible parts
Cd – 0.07-11.14 Pb – 0.88-42.7 Ni – 0.01-4.82 Pb – up to 0.96 Cd – up to 0.16 Cu – up to 2.39 Ni – up to 0.49 Cr – up to 2.17 Cd – 0.001-0.004 Pb – 0.02-0.03 Zn – 0.50-1.16 Cr – 0.001-0.02 Cu – 0.14-0.25 Ni – 0.02-0.48 Fe – 0.74-4.37 Pb - 0.64−5.97 Ni - 4.02–46.5 Co - 0.39–2.62 Cr - 1.71–6.99 Cd - 0.22–1.28 Fe - 483-612 Zn - 109-219 Pb - 2.56-3.97 Cr - 8.42-13.4 Cd - 1.62-1.91 Fe – 4.84-13.64 Zn – 2.64-10.29 Pb – 0.32-2.46 Cu - 0.55-1.04 Cu – 0.46 to 6.67 Pb – 0.00 to 1.47 As – 0.00 to 0.94
Ratul et al. (2018)
Souri et al. (2018)
Chaoua et al. (2018)
Ametepey et al. (2018)
Youssef and ElGawad (2018)
Abdel-Rahman et al. (2018)
Leblebici and Kar (2018)
Naser et al. (2018)
Gebreyohannes and Gebrekidan (2018)
Kacholi and Sahu (2018)
Yang et al. (2018)
Ipomoea batatas, Lycopersicon esculentum, Solanum melongena, Capsicum annuum Jordan
Cu
Lactuca sativa
Golestan province, Iran
Zn, Cd, Pb, and Cu
Solanum lycopersicum, Cucurbita maxima
Dera Ghazi Khan District, Pakistan
Cd, Mn, Cr, Cu, Fe, Ni, Pb and Zn
Cd - 0.00 to 0.71
Root, shoot and leaf Fruits
Spinacia oleracea, Solanum melongena, Cucumis melo
Edible parts
Solanum lycopersicum, Solanum tuberosum, Allium cepa, Spinacia oleracea, Daucus carota, Piper nigrum, Berberis vulgaris, Brassica oleracea, Brassica oleracea var. italic, Petroselinum crispum, Pastinaca sativa
Vojvodina Province, Serbia
Cr, Ni, Cd and Pb
Khyber Pakhtunkhwa Province, Pakistan
Pb, Ni, Cr, Cd and Zn
Abelmoschus esculentus, Lycopersicon esculentum
Fruits
Zhejiang, China
As, Cd, Cr, Pb, Ni and Hg
28 species of different vegetables**
Edible parts
Korba, Chhattisgarh, India
Cr, Mn, Fe, Ni, Cu, Zn, Cd, Pb and Hg
Solanum lycopersicum, Solanum melongena, Agelaius tricolor, Polygonia album, Spinacia oleracea, Coriandrum sativum
Edible parts
Bologna, Italy
As, Cd, Cr, Cu, Hg and Pb
Edible parts
Lycopersicon esculentum
15
Fruit
Cu – 0.5-2.3 Zn – 1.1-128.5 Cd – up to 2.2 Pb –up to 14.2 Cu – 0.38-7.7 Cd – 0.05-0.39 Mn – 18.7-137 Cr – 2.7-3.7 Cu – 22.2-65 Fe – 129-968 Ni – 1.8-5.05 Pb - BDL Zn – 19.5-41
Cd – up to 0.89 Pb – up to 3.56 Cr – up to 2.3 Ni – up to 2.2
Pb – 0.53-1.39 Cd – 0.01-0.05 Ni – 0.31-0.86 Zn – 0.02-0.09 Cr – 1.02-18.95 As – up to 0.013 Cd – up to 0.017 Cr – up to 0.057 Ni – up to 0.002 Hg – up to 0.094 Pb – up to 0.034 As – 0.56-2.08 Fe – 192-2255 Cr – 1-17 Mn – 17-676 Cu – 25-71 Zn – 24-121 Cd – 0.25-1.57 Pb – 0.7-4.7 Hg – 0.07-0.18 As - BDL Cd – 0.2 Cr – 0.1-0.8 Cu – up to 13.1 Hg - BDL Pb – up to 0.28
Shiyab (2018) Zafarzadeh et al. (2018)
Latif et al. (2018)
Pajević et al. (2018)
Ali et al. (2017)
Pan et al. (2016)
Ramteke et al. (2016)
Antisari et al. (2015)
Sri Ganganagar, Rajasthan, India
Hyderabad
Fe, Mn, Cu and Zn
Zn, Cr, Cu, Ni, Pb and Co
Raphanus sativus, Spinacia oleracea, Brassica rapa, Solanum melogena, Brassica oleracea, Coriandrum sativum, Trigonella foenumgraecum, Daucus carota Spinacia oleracea, Amaranthus graecizans, Coriandrum sativum, Mentha spicata, Abelmoschus esculentus, Solanum melengina
Edible parts
Fe – 111-333 Mn – 20.7-50.7 Cu – 10-73.8 Zn – 4.8-22.5
Arora et al. (2008)
Edible parts
Zn – 1.1-11.2 Cr – 0.10-3.1 Cu – 0.1-1.7 Ni – 0.1-3.6 Co – up to-0.17 Pb – 0.60-4.1
Chary et al. (2007)
* Represents the average value of metals in all vegetable samples collected in particulate study **Chinese cabbage, cabbage, spinach, wax gourd, zucchini squash, cauliflower, cucumber, cowpea, water bamboo shoot, Chinese chive, swamp cabbage, radish, pumpkin, eggplant, celery, brassica chinensis, sweet pepper, romaine lettuce, sponge gourd, kidney bean, crown daisy, potato, lettuce, tomato, broccoli, amaranth, coriander, pakchoi
The quantification of heavy metals accumulated in the food chain are assessed by using several factors or indices such as trophic transfer factor (TTF), biota-sediments accumulation factor (BSAF), transfer factor (TF), metal transfer factor (MTF), accumulation factor (AF), bioaccumulation factor (BAF) and bio-concentration factor (BCF) (Table 3). The BCF and BAF of HHMs are usually tissue-specific factorsthat provide a significant inverse correlation with concentrations of contaminated HHMs (Kumar et al., 2010). BAF and TTF values alone cannot be used for the expression of bioaccumulation and trophic transfer without considering the contaminated concentration (DeForest et al., 2007). In the case of plants, the soil-to-plant TF and, BAF in animals, are more relevant for the trophic transfer of HHMs. In plants, poisonous metals are transferred to the plant from the abiotic environment only (mainly soil), while in animals, metals are obtained from both the biotic and abiotic environments (Ali and Khan, 2018; Mehmood et al., 2019). The bioaccumulation load of HHMs can be calculated by the equation 2 (Yarsan and Yipel, 2013): Bioaccumulation = (Bioconcentration + Food chain transfer) – (Elimination + Growth dilution)…………eq (2). 16
Table 3. Quantification of
HHMs at trophic levels in food chain
Factor
Equation
Trophic transfer factor (TTF) Transfer factor (TF) Metal transfer factor (MTF) Accumulation factor (AF)
TTF = Metal conc. in organism tissue/ Metal conc. in the organism food TF = Conc. of metal in plant tissue/ Conc. of metal in soil MTF = Metal concentrations in plant/ Metal concentrations in soil AF = Conc. of metal in plant edible part/ Conc. of metal in soil BAF = Conc. of metal in organism tissue/ Conc. of metal in abiotic medium BSAF = (Metal conc. in experimental organism tissues - Metal conc. in the control organism tissues)/ Metal conc. in water BSAF = Metal conc. in the organism/ Metal conc. in sediments BMF = Metal conc. in the organism/ Metal conc. in the organism’s diet TMF is calculated from the slope of logarithmically transformed metal concentrations in organisms plotted against the trophic levels of the organisms in the food web
Bioaccumulation factor (BAF) Bio-concentration factor (BCF) Biota-sediments AF (BSAF) Biomagnification factor (BMF) Trophic magnification factor (TMF)
Reference DeForest et al. (2007) Cui et al. (2004) Jan et al. (2010) Balkhair and Ashraf (2016) Mortuza and AlMisned (2015) Chalkiadaki et al. (2014) Ziyaadini et al. (2017) Yarsan and Yipel (2013)
Conder et al. (2012)
It is well known that most of the heavy metals are toxic to living beings (Peralta-Videa et al., 2009; Gupta et al., 2018). The metals from their parent material are released into soil, water and air. In soil, these HHMs are present in soluble, non-soluble and partially soluble forms, where the soluble forms are particularly toxic because they are easily absorbed by plants via roots before distribution throughout the entire plant body. Toxic effects of metals are due to the interruption of cellular biochemical pathways (Table 4) (Onakpa et al., 2018). When poisonous metals are ingested in the stomach via contaminated foods, they are converted to their stable oxidation states in the acid medium and fuse with certain proteins and enzymes. The stabilized metallic compounds react with the sulphydryl groups (-SH) of cysteine and sulphur atoms of methionine (-SCH3) in amino acids thereby prompting the degeneration of protein molecules (Ogwuegbu and Ijioma, 2003). Humans can take up As in various ways including inhalation, smoking, water and food. When the direct exposure of toxic elements is not present, these elements can have poisonous 17
effects on the population of a particular region due to accumulation in the food chain. In humans, crops plants are primary sources for the entrance of HHMs. The mobility and availability of HHMs in the environment primarily depends on speciation and its chemical form. The arsenite, As(III) form of As is less mobile but has been recognized as more toxic than the arsenate, As(V) form (Caruso et al., 2001; Yadav et al., 2019b). Arsenite binds to sulfur-containing enzymes and proteins and the thiol groups from phytochelatins in plants, whereas arsenate attaches to the amino or reduced nitrogen groups (Kumaresan and Riyazuddin, 2001). Detoxification of As happens through methylation of As(III) which is highly metabolized by humans and originates from some organo-arsenic compounds like monomethylarsonic acid (MMA), dimethylarsinic acid (DMA), and trimethylarsine. These compounds are recognised to be cancer promoters (Zhou et al., 2003). Arsenic uptake by plants from soil solution in As(V) form occurs via phosphate transport channels because of its similarity to phosphate ions (Tripathi et al., 2007). After uptake, it affects oxidative phosphorylation and ATP synthesis and forms complex compounds with sulphur containing molecules (Tripathi et al., 2007). Arsonate is converted into As(III) inside plant tissues and becomes transformed into less toxic compounds like MMA, DMA and other complexes. Dhanker and co-workers (Dhanker et al., 2006) found that many plants can produce enough arsenate reductase enzyme, which reduces most of the arsonate to arsonite. Arsenic was mobilized within plant compartments as the soluble fraction and chelated with cyclohexylenedinitrotetraacetic acid, or As-sulfur complexes (Lopez et al., 2008). The principal source of Cd intake in humans is through smoking and food (Jarup, 2003). Cd can pose dangerous environmental risks because it can be absorbed via the digestive tract,
18
penetration through the placenta during pregnancy, and imparting damage to cellular membranes and DNA (Kabata-Pendias, 2004). Another consideration is that HHMs might be harmful to humans and animals but not phytotoxic within plant tissues (Peijnenburg et al., 2000). The differences between the electrochemical potential gradient of the plasma membrane in plant roots and concentrations of HHMs provide the passage for entry of these toxins into plant root cells (Blaylock and Huang, 2000). Cd is transported in mammals as a Cd-metallothionein, a Cdprotein complex which is stored in liver, intestinal mucosa and kidneys (Cooke and Johnson, 1996) with a retention time of 10 years (Pokorny and Ribaric-Lasnik, 2000). The absorption of Cr from soil takes place by reduction and complexation with root exudates, like organic acids, which enhance the solubility and mobility of Cr through the root xylem tissues (Bluskov et al., 2005). However, Cr is poorly translocated in aerial plant fractions (James and Barlett, 1983). The most stable and common oxidation states of Cr are Cr+3 and Cr+6. Cr+6 is the most toxic species because it has high solubility, higher oxidizing potential, and effective mobility (Marqués et al., 1998). Cr+6 increases the formation of reactive oxygen species (ROS) which cause damage to several metabolites. In crops, Cr at low concentrations (0.05-1mg/L) was found to promote growth and increase yield. Conversely, when the Cr level is increased to 15mg/L, alterations in metabolic processes occurs including growth inhibition, decrease of chlorophyll synthesis, and chlorosis (Dube et al., 2003). Table 4. Toxic form of metals and their harmful effects on plants and humans HMs
As
Cd
Toxic Form +3
As+3, DMA, MMA, As2S3 and As2O5
+2
Cd+2-deoxymugineic acid, Cd–phytochelatins
As
Cd
Form Present in Plants
Major Effects
Human
Plant
Cardiovascular, neurologic and developmental anomalies, portal fibrosis, hematologic disorders and carcinoma Bone demineralization, renal dysfunction, impair lung function and increase
Stunted growth, reduction in seed germination, seedling height, leaf area and dry matter production Reduction in seed germination, plant nutrient content and
19
Reference Abbas et al. (2018); SignesPastor et al. (2019) Loi et al. (2018)
the risk of lung cancer
Cr
Cr+6
Chromium acetate, Chromium phosphate, Chromium nitrate
Pb
Pb+2
Pb-phytochelatins, Pb-acetate, Pbnitrate, Pb-sulfide
Hg
Methylmerc ury (MeHg)
Hg , MeHg
Gastrointestinal, neurotoxicity, carcinogenesis and nephrotoxicity
Ni
Ni salts and dust
Chelated Ni compounds
Vomiting, diarrhea, dermatitis, risk of lung and nasal cancers
Cu
Cu salts, dust and fumes
Chelated Cu compounds
Zn
Zn
+2
+2
Chelated Zn compounds
Multi-organ toxicity, nose ulcers and cancer of the respiratory tract
Kidney failure, affect CNS and PNS, damage to the reproductive systems
Damage the liver and kidneys, hematemesis, hypotension, melena and gastrointestinal discomfort Cytotoxicity, haematological change, harmful effect on growth, neuronal development and immunity
reduced shoot and root length Decrease in plant nutrient acquisition, inhibition of germination process and reduction of plant biomass Decrease in plant protein content and inhibition of enzymes activity Reduction in germination percentage, plant height, flowering and fruit weight, chlorosis and reduced tiller and panicle formation Impede shoot and root growth, injure various plant parts, induce leaf spotting and produce Fe deficiency
Medda and Mondal (2017)
Zhou et al. (2018)
Azevedo et al. (2018); Gardner et al. (2010)
Ahmad, and Ashraf (2012)
Injury to plant roots and deformation of root structure
Sheldon and Menzies (2004)
Adverse effect on enzymatic activities, stunted growth and reduced yield
Plum et al. (2010), Maurya et al. (2019)
The mechanism of Pb mobility in plants is less understood (Clemens and Ma, 2016). Pb enters the food chain primarily through the discharge of metal smelting industries (Caussy et al., 2003), agriculture and urban developmental activities (Marchiol et al., 2004). Plants do not have any specific routes for Pb intake. For examples in soil, Pb can be bound to complex compounds such as carboxylic groups of mucilage uronic acids in the rhizosphere (Sharma and Dubey, 2005). Plant roots are the first barrier for Pb uptake via translocation to upper portions of plant bodies (Blaylock and Huang, 2000). After crossing the root cell membranes, Pb binds to ionexchangeable sites within the cell walls and extracellular precipitation occurs resulting in
20
phosphate and carbonate compound formation (Blaylock and Huang, 2000; Sharma and Dubey, 2005). The free or unbound Pb is passed in Ca channels accumulating near the endodermis (Antosiewicz, 2005). In humans and mammals, the primary route of exposure to lead is via the contaminated food chain (Ma, 1996). The toxicity of Pb is determined by its complexation with other compounds within tissues (ATSDR, 2007). In blood serum for example, Pb is bound to proteins or low molecular weight sulfhydryl compounds such as cysteine and homocysteine, citrate, cysteamine, ergothioneine and glutathione (ATSDR, 2007). In Hg exposure, plant-derived food plays only an insignificant role, except in regions with high Hg contamination of agricultural soils (Rothenberg et al., 2014). The primary source of Hg exposure risk to humans and animals is through ingestion of contaminated food and agricultural products (Doty, 2008). Methylmercury is more toxic and more bioavailable than inorganic Hg, and is taken up by humans and animals dominantly through seafood, because methylmercury readily bioaccumulates through aquatic food chains (Moore et al., 2014). Guzzi and La Porta (2008) observed that approximately 95% of methylmercury ingested by fish is absorbed into the gastrointestinal tract. In some plants, like corn, Hg binds to root tissues and reduces the translocation in the plant body and reduces bioaccumulation and toxic effects on human health. Fig. 1 shows the toxic metal transfer and bio-accumulation through the food chain. This study was demonstrated in a garden used for crop production nearby Ori-Ile battery waste dumpsite, Omilende Area, Olodo, Nigeria. A high concentration of Pb and Cd was observed in the garden topsoil that ultimately bio-accumulated in roots, stems, grains and leaves of maize via the food chain. The contaminated maize grains consumed by humans and animals finally biomagnified in fatty tissues and created health problems (Afolayan, 2018). 21
Fig. 1. Heavy metal transfer and bio-accumulation through food chain (The study was carried out in a garden nearby Ori-Ile battery waste dumpsite, Omilende Area, Olodo, Nigeria, Afolayan, 2018
22
5. Mechanistic approach of hazardous heavy metals transportation in vegetables The HHMs present in soil organic matter are taken up by vegetables and become critical in the form of cations when bonded to short chains of carbon atoms (Manzoor et al., 2018). The mechanism of heavy metal transfer from soil to plant is depicted in Fig. 2. The uptake of toxic metal from the soil depends on the soluble cations and anions, soil pH, plant species, pesticides, fertilizers and soil type. Vegetables and/or other plants act as accumulators and indicators of survivability despite a high concentration of HHMs in their aerial tissues and excluders. Plant survival increases when biodegradation or biotransformation of the contaminants into inert forms occurs effectively within their tissues. HHMs are actively mobilized from the soil or the apoplast to the plasma membrane of root cells in root hairs. Translocation of the uptaken metals to the shoot is dependent on barriers, vacuoles, and the upward mobility in the xylem and phloem (Meng et al., 2011). Distribution in different plant organs is a function of phloem loading and unloading, and mobility and the efficiency of xylem-to-phloem transfer of elements (Mendoza et al., 2011). Bacteria produce MMA (monomethylarsonic acid) and DMA (dimethylarsinic acid) in the rhizosphere, however, that is not enough to initiate methylation of As in plants. Particular enzymes like Sadenosylmethionine-dependent arsenite methyltransferase catalyze As and also play an essential role in the biogeochemical cycling of As. Both toxic nonessential and essential elements move into a plant through the same pathways (Zhu et al., 2014). For the mobilization and transfer of metals from one compartment to another compartment of cells and plant parts, several metal transporters are involved: OsNramp5, OsHMA2, OsHMA3, NIP, Lsi1, Lsi2, PT, ABC, HAC1, MMA and DMA (Clemens and Ma, 2016). To illustrate, in rice plants, OsNramp5 confined at the distal side of both the exodermis 23
and endodermis, is responsible for the transport of Cd from the apoplast to the rice root cells (Sasaki et al., 2012). In vacuoles of a tonoplast, OsHMA3 sequesters Cd, and OsHMA2 sequesters Cd at the plasma membrane of pericycle cells (Clemens et al., 2013). In rice fields, under anaerobic conditions, As(III) is the dominant form in the soil. Arsenate is taken up through phosphate transporters (PTs) and then reduced to arsenite by As(V) reductases such as HAC1 in Arabidopsis thaliana (Chao et al., 2014). In the rice plant, Oryza sativa, arsenite uptake occurs by the aquaporin Lsi1, and in Arabidopsis thaliana uptake is facilitated by nodulin 26–like intrinsic proteins (NIPs) (Ma et al., 2008; Li et al., 2009, Zhao et al., 2010). Some other metal transporters like ABC transporters (AtABCC1 and AtABCC2) in A. thaliana and OsABCC1 in O. sativa, sequester As and form phytochelatins complexes (As-PCs) in the vacuole. The Lsi2 transporter in rice effluxes the remaining As(III) in the xylem. In rice additionally, arsenate is transported towards the stele by two Si transporters like Lsi1 and Lsi2, and these are located at the distal and proximal sides of the exodermis and endodermis. Arsenic forms phytochelatins with OsABCC1 transporters in the tonoplast and sequesters toxins as As-phytochelatins (As-PCs) complexes in the vacuoles restricting the availability of As(III). The sequestration of HHMs can restrict the movement in the root toward the xylem. This was confirmed by the badge of P1B-type ATPase in rice (OsHMA3) as the primary determinant of Cd root-to-shoot translocation (Miyadate et al., 2010). Long distance transfer of HHMs between plant organs takes place via the xylem and phloem loading (Ma et al., 2007; Ma et al., 2008). The accumulation of HHMs in leaves occurs mainly through uptake by xylem-loading and in seeds and fruits by phloem-loading. More investigation is required to elucidate more obvious pathways of metal transport in plants (Khan et al., 2014; Olsen and Palmgren, 2014).
24
Fig. 2. Transfer and bio-accumulation of HHMs in different plant parts (modified from Clemens and Ma, 2016; Peralta-Videa et al., 2009) *OsNramp5, OsHMA2, OsHMA3, NIP, Lsi1, Lsi2, PT, ABC, HAC1, MMA and DMA are metal transporters in plants for the transport of plant parts, vacuoles and cells.
25
HHMs in different
6. Hazardous heavy metal management by nanotechnological approaches With the accelerated advanced development in nanoscience, unique possibilities have arose to develop more cost-effective, environmentally safe and sustainable remediation processes (Adeleye et al., 2016). In the last few years, nanotechnological tools have been increasingly used in soil, soil sediments, solid waste and wastewater remediation. Nanoparticles ranging from 1100 nm in size, known are applied in several remediation processes that allow nanotubes, nanosheets and nanolayers to be utilized as treatment material. Nanoparticles, (NPs) nanomaterials (NMs) or nanoadsorbents could provide very high adaptability for both in situ and ex situ remediation of pollutants. Nanotechnology can help clean up polluted water by employing nanoscale biosensors to detect contaminants in surface and groundwater, and improving the efficiency of chemical and photo-catalytic processes. Nanosized compounds come in a variety of forms such as NPs, nanofilms, nanowires, quantum dots, nanotubes and various colloids (Anjum et al., 2016; ). NM characterization is listed in Table 5. Recently researchers focused on the synthesis and surface functionalization of nanoparticles (sizes less than 50 nm) which have a huge potential as adsorbents of contaminants like heavy metals, organic pollutants and dyes from polluted waters (Bobik et al., 2017). Iron oxide NPs have been synthesized in top-down and bottom-up approaches. The seldom used “top-down” approach is based on crushing or grinding of hostmaterial in ball mills. The “bottom-up” approach is more prevalent and based on the chemical syntheses of nanomaterials such as pyrolysis, chemical precipitation, the sol-gel method, co-precipitation, reverse micelles, magnetic nanocomposites, micro-emulsion, polyols method, sonolysis, gas-aerosols, electrochemical decomposition, flow injection syntheses, electrospray syntheses and thermolysis of precursors or hydrothermal reactions (Khan et al., 2011; Cui et al., 2013; Li et al., 2013; Fajaroh et al., 2008;
26
Wu et al., 2008; Ahmad et al., 2017). Amongst the several emerging technologies, the progress and versatility in nanotechnology has confirmed an incredible potential for the remediation of pollutants and HHMs in the environment (Gupta et al., 2015). These methods are dynamic, require less time, possess broad applicability, and pose good economic expediency (Wernisch et al., 2013). The categoris of nanomaterial are classified in Table 6. The application of NMs or nanoparticles has gained enormous attention due to their size and large surface area to unit mass ratios, short intra-particle diffusion distance, magnetic properties, surface modifiability, biocompatibility, tunable surface chemistry, increased adsorption sites, reusability, increased porosity, higher gas permeability, ease of separation, enhanced catalytic activity, greater dispersion degree, and comparatively low cost of manufacturing (Ali, 2012). Nanoremediation methods involve the use of potential NMs for transformation, treatment, stabilization and detoxification of contaminants. Various nanomaterials have been tested to remediate metal concentrations like nano catalysts, CNTs, graphenes, nanoscale metal oxides, nanomembranes, carbon nanotubes, nanobiological processes, and zero-valent iron (FeO), Fe2O3, Fe3O4, TiO2, SiO2, and Al2O3 (Anjum et al., 2016; Saad et al., 2018; Hosseini et al., 2019). Several adsorbents such as activated carbon, silica, clay materials, metal oxides, magnetic iron oxide nanoparticles (MNPs), nano-titanates, alginate biopolymer and their composites have all been utilized to remove the harmful heavy metal ions (Yong-Mei et al., 2010; Yadav et al., 2017a; Yadav et al., 2019). Nano-adsorbence can be performed using atoms of certainelements which are chemically active with a high surface adsorption capacity (Kyzas and Matis, 2015).
27
Table 5. Characterizations of nanoparticles/nanoadsorbents and their removal efficiencies of heavy metals Nanoparticle Species
Iron oxides NPs
Fe3O4 Synthetic Fe7S8 nanoparticles
Property
NP Synthesis
HM Species Remediated
Absorbent Dose (g/L)
Optimum pH
Magnetite nanoparticles
Co-precipitation from a mixture of Fe(II) and (III) salts with aqueous NH3 and KOH
Cr(VI), Pb(II), Cr(III), Cu(II), Zn(II), Ni(II) and Cd(II).
50mg/20cm3
5.31-9.37
Coating
Zn(II)
0.80
6
>94%
solvothermal synthetic method Modified co-precipitation synthesis Hydrothermal method
As (III) and As (V)
-
4
Up to 98%
Cd(II), Cu(II) and Pb(II)
0.008
-
Cd(II) up to 32.3% Cu(II) up to 23.8% Pb(II) up to 38.1%
Klekotka et al. (2018)
Cr(VI)
0.80
2
93%
Lu et al. (2017)
Co-precipitation
Cu(II), Fe(III), As(III)
0.15
6.5
Cu(II)-100% Fe(III)-100% As(III)-98%
Esmat et al. (2017)
-
Cr(VI)
0.10
3-9
100%
Huang et al. (2015)
V (vanadium)
0.15
-
73%
Mthombeni et al. (2015)
Cr(VI) and Hg(II)
-
-
Cr(VI)-92% Hg(II)-upto 80%
Stefaniuk et al. (2016)
Magnetite nanoparticles High binding capacity
Ferrite nanoparticles MoS2/Fe3O4/nZVI nanocomposites Cobalt ferrite nanoparticles Magnetic multi-wall carbon nanotubes
Synergistic effect for adsorption High surface area and greater adsorption capacity Large specific surface area and high reaction activity
Magnetic zeolite-polymer composite
Monolayer adsorption
Chemical co-precipitation of Fe3+ and Fe2+ ions at a ratio of 2:1 in the presence of zeolite
Zero-valent iron (ZVI)
Reducing agent and good adsorbent
Abrasion and grinding
28
HM Removal Efficiency (%) Cr(III)-66-77%, Cr(VI)- >90%, Cu(II)-26%, Pb(II)76-92%, Zn(II)26%, Ni(II)-14%, Cd(II)-21%
Reference
Bobik et al. (2017)
Helal et al. (2010) Cantu et al. (2016)
Magnetic nano-particles coated zeolite
High adsorbing capacity
Using magnetic nanoparticle (Fe2O3)-coated zeolite (MNCZ)
As(III)
0.50
2.5
95.6%
Attia et al. (2014)
Titanate nanotubes
High surface area and greater adsorption capacity
Co-precipitation
Cu(II), Fe(III), As(III)
0.15
6.5
Cu(II)- 99.9% Fe(III)-100% As(III)- 98%
Esmat et al. (2017)
Hydrolysis of titanium sulfate solution
As(III)
0.20
9.5
>98%
Pena et al. (2006)
Multifunctional flexible freestandingNa-TNB membrane by vacuum filtration
Sr(II), Cs(II)
25-50
-
Sr(II)-97.5% Cs(II)-57.7%
Wen et al. (2016)
Nanocrystalline titanium dioxide
Sodium titanate nanobelt membrane (Na-TNB)
Negatively charged inner-sphere surface complexes Ion-exchange properties with greater selectivity for target cations and higher adsorption capacity due to large surface area
TiO2 Engineered Nanoparticles (ENs)
Surface adsorption and internalization
Polyacrylatecoated TiO2-EN
Cd(II)
0.10
2
Activated carbon NPs
High surface area and greater adsorption capacity
-
Fe, Pb and Ni,
0.02
2-10
Fe up to 99%, Pb up to 87%, Ni up to 96%
Hegazi (2013)
Nano sized ZVI (NZVI)
High adsorbing capacity
Reduction of ferric chloride by sodium borohydride
As(III)
1.0
7
99.9%
Rahmani et al. (2011)
Nano scale zero valent iron (nZVI)
High surface area and cation exchange capacity
Reduction of Fe (II) using borohydride
Cd(II) and Pb(II)
-
-
-
Mohammed et al. (2018)
29
> 20%
Yang et al. (2012)
Starch stabilized zerovalent iron nanoparticles (nZVI-Starch)
Larger surface area for sorption reactions
Chemical reduction method
Pb(II)
1g/kg soil
4.2
100%
Okuo et al. (2018)
ZnS nanocrystals
High cation exchange capacity
Direct coating ZnS NCs on the surface of the αAl2O3nanoparticles
Hg(II)
10
1-6
99.99%
Qu et al. (2014)
ZIF-8 nanoparticles
Ultrahigh surface area, tunable pore structures, high crystallinity and designable organic ligands
Rapid synthesis in aqueous solution
As
0.20
7
60%
Jian et al. (2015)
Graphene nanosheets (GNS)/d-MnO2
Chemical exfoliation
Ni (II)
5.0
-
77.04%
Varma et al. (2013)
Zeolite materials obtained from fly ash Pyromellitic acid dianhydride/ N-(3(trimethoxysilyl) propyl ethylene diamine (PMDA/TMSPEDA) Chitosan-modified multi-walled carbon nanotube composite
Greater specific area Bound heavy metal ions via co-ordinate and electrostatic interactions Chitosan is a cationic biopolymer, high hydrophilicity
Pb(II)
6.0
5.6-6.6
>80%
Visa (2016)
Ring opening polymerization and sol-gel reaction
Pd(II), Cu(II), Zn(II)
0.01
7
Pd(II)-79.60% Cu(II)-72.36% Zn(II)-66.80%
Alsohaimi et al. (2015)
Heating and mixing
Cr(VI)
0.05
2
98-100%
Huang et al. (2018)
Modification macro-particles of Jordanian raw kaolin clay by hydrochloric acid and hydrogen peroxide
As(V)
0.5
8
98.45%
Amer and Awwad (2018)
Nanocrystalline kaolinite
High adsorption efficiency
Nanocomposite of MnO2 loaded on graphene nanosheet Hydrothermal process
30
Ag and Zn nanoparticles functionalized cellulose
High catalytic activity, great biocompatibility, high adsorption capacity, high surface-area, reusability and greater dispersion degree
Co-precipitation method
Hg(II), Cr(III), Co(II), Pb(II), and Ni(II)
0.5 and 1.0
5.5
Hg(II) >Ni(II) >Cr(III) >Co(II) > Pb(II)
Ali et al. (2018)
ZnO@Chitosancoreshell Nanocomposite (ZOCS)
Hydrophilicity, biocompatibility, biodegradability, non-toxicity and High adsorption capacity
Direct precipitation followedby thermal decarbonation
Pb(II), Cd(II) and Cu(II)
0.02
4 (Cu), 6 (Pb) and 6.5 (Cd)
Pb(II) up to 99%, Cd(II) up to 98%, Cu(II) up to 96%
Saad et al. (2018)
ZnO-Fe3O4 nanocomposites
High adsorption capacity and surface area
Chemical co-precipitation
Pb(II) and Cu(II)
0.50
5.5
Pb(II) up to 39.2%, Cu(II) up to 37.66%
Goyal et al. (2018)
Polymer functionalized nanocomposites PS – (HFO)(Polystyrene sulfone supported Hydrated Iron (III) Oxide)
High surface area
grafting NPs into polymer structures
As(V)
0.01
3
95%
Nie et al. (2013)
31
Table 6. Categories of nanomaterials (NMs) and their applications for HM remediation Nanomaterial (NM)
NM Species
Composition of NM
Oxides NPs
Metallic and mixed
Multi-wall CNT and modified magnetic CNTs
Carbon nanosheets (CNSs)
CNSs combined with metal ions or metal oxides
Nanofibers
Aminated polyacrylonitrile nanofiber mats
Surface modification of e-spun PAN with DETA (diethylenetriamine)
Nano clays
hydrous aluminosilicates
Kaolinite and montmorillonite
Graphene NM
Carbon NPs
Graphene oxide (GO)
Adsorption of HMs
Magnetic NPs (MNPs)
Iron oxide NPs Polymer-functionalized nanocomposites (PFNCs)
Fe3O4-gum-arabic S-PFNCs and B-PFNCs (Polymer-functionalized nanocomposites) SiOx layers on beryllium deposition
Removal of Cr(VI)
Polymer NMs
Aerogels NM NMs as photocatalyst Photocatalysts as antimicrobial agent Nano-catalysts NMs as electrocatalysts Nano-material based Fenton catalyst Fouling and membrane modification
Au hydrogel with Au nanoparticles Semiconductor metals with NPs
Feng et al. (2012) Ren et al. (2011) Wang et al. (2012) Kampalanonwat and Supaphol (2014) Bhattacharyya and Sen Gupta (2006) Lingamdinne et al., 2016 Elfeky et al. (2017) Lofrano et al. (2016)
Wastewater treatment
Castrucci et al., 2006
Nanoscale Si grown on Ag
Wastewater treatment
Grazianetti et al. (2017)
Au aerogels
Adsorption of HHMs
Gurav et al. (2010)
ZnO:Co, ZnS:Mn, ZnS:Cu, ZnSe:Mn, ZnS:Pb
(Fe2O3/SiO2)
Removal of POPsand HMs from wastewater Biological wastewater treatment (mainly bacteria) Wastewater treatment and electricity generation Oxidation of organic pollutants
-
Wastewater treatment
Silicon nanotubes Silicon nanosheets
Reference
Removal of HMs from wastewater
Silicon NMs
Nano-membranes
Applications HM removal from wastewater RemovalHMs organic contaminants from wastewater Removal of HMs from wastewater Removal of Ag(I), Cu(II), Pb(II) and Fe(II) from aqueous solution Removal of Co, CU, Fe and Pb
Carbon nanotubes (CNTs)
Carbon NMs
Nano-adsorbents
Functions Tioxides, Zn oxides,Mg oxide, Mn oxidesand Fe oxides
Ag nano-particles on TiO2 films
Ag/TiO2
Pt nanocatalyst supported by carbon black XC72 Heterogeneous MFe2O4 NM Mixed matrix membranes (MMMs)
Microbial fuel cells
32
Adeleye et al. (2016) Akhavan (2009)
Chen et al. (2015) Ferroudj et al. (2013) Rajabi et al. (2013)
Carbon nanotube membranes
Electrospun nano-fiber membranes
with carbon nanotubes (CNTs) Polyether urethane (PEU) membranes filledwith isophorone diisocyanate grafted with multi wall carbon nanotubes (MWCNT-IPDI) Polymer composite membranes,single and multi-walled carbon nanotubes (SWCNTs/MWCNTs) Electrospuning of natural and synthetic polymers like PVC, PS, PVDF (Polyvinylidene Fluoride) and PBI (Polybenzimidazole) Impregnated polysulfone (PSF) with zeolite nano-particle membrane
-
Wastewater treatment
Deng et al. (2007)
Carboxyl multi-walled carbon nanotubes/calciumalginate (CMWCNT/CA)
Treatment of contaminated water
Liu et al. (2016)
Graphene doped polyacrylonitrile/polyvinylidene fluoride electrospun nanofiber
Cr removal and wastewater treatment
Qu et al. (2013) Yadav et al. (2019a)
Zeolite NP-PSf
Removal of Pb and Ni form wastewater
Yurekli (2016)
Na-TNBM
Sr2+ removal
Wen et al. (2016)
Hybrid nanomembranes Sodium titanate nanobelt membrane (Na-TNB)
Nano-Biotechnological processes
Composites of NPs
Algal membrane bioreactor (A-MBR) with NP
Algae with nano fibers and NP
CNTs with TiO2 NP and Polysulfone (PSF) fibre
HM removal from wastewater
Abou-Shanab et al. (2013)
Aerobic digestion with NPs
Aerobic degradation with ZVI NPs
-
Municipal and industrial wastewater treatment
Ma and Zhang (2008)
-
-
HM removal from wastewater
Anjum et al. (2016)
ZVI NPs with
CMC/Fe2+
Removal of Cr (VI)
He et al. (2007)
Titanium oxide/dendrimers composites Composites of
33
stabilized ZVI Nanoparticles Bentonite clay iron oxide composite Chitosan montmorillonite-Na Calcined kaolin and bentonite Mixed clay fluoroapatite
carboxymethyl cellulose (CMC) and polyacrylate (PAA) -
-
Removal of Cu, Cd and Zn
Etci et al. (2010)
-
-
Removal of Cr
Pandey and Mishra (2011)
-
Removal of As
Dousov et al. (2009)
-
Removal of Cd, Cr, Zn, Cu, Hg and Pb
Sajidu et al. (2006)
Pretreated with Fe2+, Fe3+, Al3+ and Mn2+ Illite, kaolinite, mixed layer minerals and nonclay mineral carbonate
Bentonite polyacrylamide composite
-
-
Removal of Cu
Zhao et al. (2010a)
Dendrimer-based nanocomposite
Dendrimer-based magnetic nanoparticles
Magnetic hyperbranched polyol-modified graphene oxide (GO)
Removal of Zn(II) and Pb(II)
Hu et al. (2016)
34
6.1. Nanomaterial induced phytoremediation of hazardous heavy metal Many remediation processes can convert the hazardous heavy metals into less hazardous heavy metals or stabilize in the soil over a time period. But phytoremediation coupled with NMs is a novel technology that can separate the extract, degrade, modify, sequester, and stabilize a broad category of soil contaminants (Ali et al., 2013; Gong et al., 2017; Yadav et al., 2018). The synergistic and antagonistic influences of merged remediation techniques have been exhibited as an efficient process to decontaminant of pollutants due to the diverse responses of plants to NPs and the variable influence of NMs on soil contaminants (Mahar et al., 2016). The effects of NMs on the phytoremediation of heavy metals and organic pollutants contaminated soils were given in Table 7. The removal of toxic material from soil occurs due to co-uptake between NMs and the contaminants. The NPs suitability for particular plants should also be considered because when NPs enter into plants through absorption, they can damage the cell membrane and cell walls, resulting in the loss of membrane integrity or turgidity and cell function, consequently promoting the introduction of contaminants from soils into plants body (Gong et al., 2017). Researchers have shown NMs can enhance the accumulation of metals by three approaches: (i) improvment in the permeability of the cell wall, (ii) co-transportation of NMs and heavy metals, and (iii) regulation of transporter gene expression. Graphene oxide (GO) is a nanomaterial that has been studied in the removal of heavy metals from soil to enhance the uptake of As in wheat. GO can enhance the reduction of plant biomass, the number of roots exposed to toxins, disturbing the urea cycle and fat metabolism, by transforming arsenate to arsenite thereby reducing oxidative stress in wheat seedlings as compared to the exposure of heavy metals without remediation alone (Hu et al., 2014). Gil-Dıaz and co-workers (Gil-Diaz et
35
al., 2016) found that the use of 10% nano-zerovalent iron (nZVI) decreases the uptake of As in plant parts (root and shoot), and raises the height and dry weight of barley plants under metal stress. The application of titanium dioxide (TiO2) NPs improved Cd accumulation from polluted soils, and reduced Cd toxicity by enhancing photosynthesis rate and plant growth in soybeans (Singh et al., 2016). The uptake of iron oxide NMs by wheat plants mitigated the toxicity of Cd(II) and Cr(VI) in the crops (Lopez-Luna et al., 2016). The efficient remediation process depends on the types of metal contaminattion, and levels of contamination, which nanomaterial used and on what plant species. 6.2. Heavy metal removal mechanism of nano material Nanomaterials exhibit particular properties due to their large number of particles, high surface area to volume ratio, specificity for particular toxic metal, magnetic separation, surface chemistry and surface interactions (Lakshmanan, 2013). Several NMs such as carbon nanotubes (CNTs), nanocages, nanocrystals, nanowires, nanoflakes, silica NPs, cellulose nanocrystals and nanofibrils, fullerenes, hydroxyfullerenes and heterofullerenes are depicted in Fig. 3. As discussed previously, NMs can be manufactured using the bottom-up approach to form polymers and biopolymers, metals and their oxides and hydroxides, ceramics and derivatives of carbon (Heimann et al., 2015) by several processes we listed earlier (Chen and Mao, 2007). Adsorption processes using nanoadsorbents on oxides of Zn, Cu and Fe, are highly dependent on pH. To illustrate, enhanced elimination of HHMs from aqueous solutions occurred with increased pH levels due to electrostatic interplays, precipitation and formation of covalent bonds to different functional groups. A raise in the pH supports the deprotonation of nanosorbent surfaces, thereby increasing the concentration of the negatively charged sites on and
36
nanoadsorbent material. This further increases the attractive forces between positively charged ions and the negative sites on the nanoadsorbents (Mahdavi et al., 2012). Superparamagnetic iron oxide nanoparticles (SPIONs) have large surface area-to-volume ratios, are less toxic, chemically inert, can be rendered biocompatible, allow small diffusion resistance, and their surfaces can be modified with organic/inorganic functional groups rendering their surfaces biocompatible and possessing increased potential for eliminating HHMs. The functional groups –COOH, -NH2, -OH and –SH provide active active sites for the replacement of toxic metal ions. Physical interactions (such as electrostatic and Vander Waal’s forces) and chemical interactions (such as chemical binding, complex formation and modified ligand combination) are responsible for the adsorption of toxic metal ions onto the nanoadsorbant (Wang et al., 2012; Patwardhan, 2012). CNTs express novel properties due to their high porosity, light mass density, large specific area, the hollow structure and active interactions with HHMs (Dresselhaus et al., 2001). The adsorption mechanism is mainly governed by the chemical interactions between the surface functional groups (–OH, –C=O and –COOH) and the toxic metal ions (Gadhave and Waghmare, 2014). Chitosan also exhibits unique characteristics, such as being chemically stable, biodegradable, biocompatible and hydrophilic. The adsorption capacity of HHMs is due to the presence of amine groups (–NH2), which attract metal ionsin solution (Jassal et al., 2015). Si coating stimulates the surface functional groups on the NPs due to the abundant presence of silanol groups on the silica layer (Patwardhan, 2012).
37
Table 7. NP-induced phytoremediation of heavy metal contaminated soils
NMs
Suitable Dose of NPs for Plants
Plant Species
HM Remediated
Interaction of NMs
With HMs
Graphene oxide (GO)
0.1-10 mg/L
Triticum aestivum
As
Enhanced As uptake
GO
5 mg/l
Microcystis aeruginosa
Cd
Enhanced Cd toxicity
As
Reduced As availability and decreased As uptake Reduced Cr leachability
nZVI
14-18 g/kg (10%)
Hordeum vulgare
CMC-stabilized nZVI (Carboxymethyl cellulose)
-
Brassica rapa
Cr
TiO2 NPs
100-300 mg/kg
Glycine max
Cd
TiO2 NPs
100 mg/L
Chlamydomonas reinhardtii
Cd
Citrate-coated magnetite NPs
1 g/kg
Triticum aestivum
Cd and Cr
Reducedmetal phytoavailability
Silicon NPs
-
Pisum sativum
Cr
Decreased Cr accumulation
38
Increased Cd uptake Reduced free Cd ion contents, loweredCd bioavailability
Reference
On Plants Decrease plant biomassand root numbers, disrupted fatty acid metabolism and the urea cycle and increase the oxidativestress Increased ROS production and MDA contents and suppressed plant growth Increased plant growth rate and the biomass
Hu et al. (2014)
Tang et al. (2015)
Gil-Díaz et al. (2016)
Reduced bioaccumulation and bioavailabilityand suppressedCr uptake Decreased Cd stress in the plants
Singh and Lee (2016)
Mitigated Cd-induced growth inhibition
Yang et al. (2012)
Reduced the concentration of Cd and Cr Improved plant growth, protein, carotenoids and chlorophyll contents, and decrease ROS production
Wang et al. (2014)
López-Luna et al. (2016)
Tripathi et al. (2015)
Fig. 3. Different nanomaterials and their removal mechanisms
39
7. Biotechnological and genetic approaches of remediation Heavy metal contamination in soil has led to contamination of food and fodder grown on such soils. Through plants, these heavy metals enter the food chain endangering human and animal health. Increases in reports of such contaminants found in foods are proof (Bald et al., 2005). However, when we look for the solution to this problem we have very few options and most of them are uneconomical. Therefore, phytoremediation is emerging as a tool for reclamation of heavy metal contaminated soil by growing metal hyperacumulators in contaminated soils. One argument for phytoremediation states that this technique is economical and eco-friendly but its field application is limited by slow growth and low biomass production ability of the hyperaccumulators (Yadav et al., 2018). During the remediation of HHMs, plants extract heavy metals from soil followed by their stabilization and accumulation in their inactive states. If these HHMs become accumulated above their threshold limit in plant tissue, then these toxins disturb physiological and biochemical processes such as photosynthesis, respiration, membrane integrity and antioxidant defense system. All perturbations of healthy and natural growth and homeostasis have deleterious effects. Research has shown that the most suitable plant for phytoremediation will have an increased heavy metal accumulation rate coupled with rapid growth and greater biomass production ability. The capacity of any plant to extract and accumulate heavy metals is highly governed by its genetic potential as no plant can store heavy metals more than its threshold capacity (Kawashima et al., 2004; Shah et al., 2007; Ovecka et al., 2014). Genetic engineering/manipulation can be used as tools for improvements of the inbuilt genetic potential and phytoremediation ability of any plants according to the needs of the
40
community. Recent biotechnological research in the field of heavy metal remediation has developed transgenic plants possessing improved heavy metal accumulation or remediation capacity compared to their host thus making them more suitable for /phytomining (Duan et al., 2011). This process involves the transfer of genes-of-interest which play a role in heavy metal uptake, transport and accumulation from its efficient donor to host leading to increased tolerance of the host. Phytomining can improve the ability of plants to sense, uptake and accumulate heavy metals. Many studies have been investigated on Arabidopsis, tobacco, Indian mustard, and sugar beets resulting in these plants possessing improved tolerance for heavy metal stress with greater biomass accumulation. However, the success of transgenic modifications in heavy metal remediation is highly dependent on availability of gene sequences. Heavy metal accumulation efficiency is highly dependent on the mechanisms of uptake, translocation, detoxification, sequestration and storage efficiency of plants. In 1989, a Cd-tolerant Nicotiana tabacum transgenic plant was developed by the introduction of a human metallothionein gene by Misra and Gedamu (1989). Table 8 gives details about phytoremediations exploited for the development of heavy metal tolerance with the associated genes governing that trait. Uptake of heavy metals is dependent on root traits since roots are the first and formost directly exposed organ to heavy metal stress and contaminated soils (Hossain et al., 2012) which adversely affects the ability of roots to take up water and nutrients from the soil (Poschenrieder and Barcelo, 1999). Rhizosphere pH determines the mobilization of heavy metals. In acidic PH heavy metals get dissolved in soil water which increases their mobility to plants. Organic acids secreted by roots, however, bind with heavy metals and improve their mobilization and absorption by roots (Singh et al., 2016).
41
Genetic manipulation in uptake, transport and accumulation ability of heavy metals can be made resulting in the overexpression of uptake and mobilization transporter proteins of the plasma membrane such as NRAMP, HMA4, aquaporin, YCF1, ZIP4, IRT1, and CAX4 and the tonoplast can improve metal absorption capacity of the root. Lee and co-workers (Lee et al., 2010) observed that in certain Saccharomyces cerevisiae yeast cadmium factor 1Protein (YCF1) is involved in pumping cadmium (Cd(II)) into vacuoles thereby conferring resistance to Cd and Pb. YCF1 is a vacuolar glutathione S-conjugate transporter, related to the ATP-binding cassette superfamily where it enhances uptake and storage of the HHMs in yeast vacuoles. On overexpression of the YCF1 gene in Arabidopsis thaliana, transgenic lines were able to increase uptake and accumulation efficiency of transgenic plants (Song et al., 2003; Lee et al., 2010). Transporter proteins coded by the AtMRP2 gene have similar functions as the yeast YCF1 gene and also confers Cd tolerance by transporting Cd/glutathione complexes to the vacuole (Li et al., 1996). Arabidopsis ATP-binding cassette (ABC) transporter proteins are vacuolar GS-x pumps involved in transport of metal conjugates of glutathione to vacuoles for detoxification or maintenance of homeostasis (Bovet et al., 2005). In Schizosaccharomyces pombe, toxic metal tolerance is linked with the action of an ABC-type transporter protein at the vacuolar membrane. In another example, transgenic Brassica juncea possesses the gene for the expression of selenocysteine methyltransferase (SMT) shifts into a Se hyperaccumulator while A. bisulcatus exhibits greater uptake of Se and enhanced Se tolerance than the wild types (Pilon-Smits, et al., 1999; Huysen et al., 2004). In overexpressed lines, root growth was better with higher accumulation of Zn and Cd (Verret et al., 2004). Overexpression of CAX2 (calcium exchanger 2) in tomato plants results in the accumulation of more Ca2C compounds and antioxidant (Xie et al., 2015). Nicotiana tabacum plasma membrane channels the protein NtCBP4 and Arabidopsis
42
cyclic nucleotide gated ion channel (AtCNGC1) also plays a role in the Pb2C transport pathway which imparts Pb tolerance in its overexpressing plant lines (Sunkar et al., 2000; Zeng et al., 2015). As stated before, heavy metal detoxification and sequestration is accomplished with the help of many heavy-metal-binding peptides such as phytochelatins, glutathione and metalothionones. The binding of toxic metal ions to organic or sulfur-rich peptide complexes (HM-PC/GS/MT) produces carriers of the toxins to the vacuole for storage or detoxification. Overexpression of E. coli GSH1 and GSH2 genes in Brassica juncea and Populus canescens enhanced its Cd and Zn tolerance ability, respectively, due to higher accumulation of glutathione and phytochelatines in transgenics (Zhu et al., 1999). γ-glutamyl cysteine synthetase-glutathione synthetase (StGCS-GS) involved in glutathione was isolated from Streptococcus thermophiles. This gene is not redox-regulated and has limited feedback inhibition ability. It is overexpressed in tobacco and sugar beet and their transgenic lines have yielded plants with enhanced tolerance to individual/combinations of heavy metals (Cd, Zn, Cu) thus producing increased biomass wild-type plants (Liedschulte et al., 2010). Three transgenic lines overproducing γ-glutamylcysteinesynthetase (ECS), GS and adenosine triphosphate sulfurylase (APS), expressed increased levels of metal-binding peptides such as phytochelatins and glutathione when grown in metal-contaminated soil in green houses. These transgenics lines accumulated 1.5-3-fold higher heavy metal content as compared to wild type which led to significant decreases in heavy metal content in soil and produced enhanced Cd tolerance and accumulation in above ground biomass. Metallothioneins are cysteine rich metal binding proteins that play a role in metal detoxification by ROS scavenging mechanisms (Leszczyszyn et al., 2013). Over expression of
43
Arabidopsis metallothioneins (AtMT2a and AtMT3) in Vicia faba can reduce chloroplast degradation in guard cells and Brasicca rapa metallothionein 1 (BrMT1) in Arabidopsis has been shown to reduce oxidative stress under Cd toxicity (Lee et al., 2004; Kim et al., 2007). These metallothioneins were found to be helpful in heavy metal accumulation of Zn in OsMT1A-overexpressing rice (Yang et al., 2009) and for both Cu and Zn accumulation by means of the seed-specific AtMT4A gene in Arabidopsis (Rodríguez-Llorente et al., 2012). In one study, yeast metallothionein biosynthesis gene CUP1 was overexpressed and evaluated in the callus of sunflower. The transgenic calli of several strains showed high triphenyl tetrazolium chloride reducing activity after its treatment with Cd for 10 days (Watanabe et al., 2001). Zinc tolerance of Populuscanescens was enhanced by overexpression of bacterial genes encoding γ-glutamyl cysteine synthetase (GCS) in the cytosol (11ggs) and in chloroplasts (6LgI) (Bittsanszkya et al., 2005). The transformed poplar tree line had more glutathione as compared to non-transformed poplar trees. Phytochelatins are metal-binding proteins that chelate heavy metals utilizing their thiolgroups and the resulting in the formation of metal-phytochelatin complexes that become further sequestered into vacuoles. The overexpression of phytochelatin synthase gene from Ceratophyllum demersum L. (CdPCS1) in tobacco, E. coli, or Arabidopsis (Shukla et al., 2012; Shukla et al., 2013), and the Nelumbo nucifera (NnPCS1) gene in Arabidopsis thaliana (Liu et al., 2012) enhanced phytochelatine accumulation and stress tolerance in plants. Further, overexpression of Arabidopsis PC synthase (AtPCS1) in transgenic Arabidopsis increased phytochelatine synthesis, metal accumulation, and Cd and Zn tolerance in transformed plants (Lee et al., 2003).
44
Heavy metal accumulation generates redox reactions because of increases in production of ROS and reduced efficiency of ROS scavengers’ simultaniously (Mittler et al., 2004). ROS production takes places in chloroplasts, mitochondria and peroxisomes by electron transport to oxygen. Redox active metals such as Cu, Cd, Fe and Zn forms ROS by participating in Haber– Weiss and Fenton reactions. Heavy metals are inhibitory to antioxidant enzymes which reduce efficiency of scavenging mechanisms. Additionally, ROS are highly reactive and inactivate macromolecules such as lipids, proteins, carbohydrates and nucleic acids thus inducing chain reactions of macromolecule oxidative damage. One strategy exploited by researchers is the development of genetically engineered plants with more effective antioxidant defense systems and increased capacities to accumulate and/or tolerate heavy metals. Metal toxicity and gene expression levels of superoxide dismutase and peroxidase, catalase, glutathione-S-transferase involved in antioxidant defense systems is well reported (Tahara et al., 2008). Effects of Al toxicity in Arabidopsis was ameliorated by overexpression of four Al-induced genes: Arabidopsis blue-copper-bindingprotein, N. tabacum glutathione S-transferase (parB), N. tabacum GDP-dissociation inhibitor gene (NtGDl1) and N. tabacum peroxidase gene (NtPox) (Ezaki et al. 2000). Overexpression of Cu-Zn superoxide dismutase and ascorbate peroxidase in transgenic tall fescue plants improved abiotic stress tolerance. Overexpression of MnSOD gene encoding superoxide dismutase in canola also improved Al tolerance (Basu et al., 2001). Ascorbate acts as a scavenger of ROS in its reduced state and possesses the abilities to reduce H2O2 production and lipid peroxidation resulting in lower levels of oxidative DNA damage. Overexpression of dehydroascorbate reductase could maintain high levels of reduced ascorbate while conferring aluminum tolerance (Yin et al., 2010). RsMYB1 transcription factor of radishes
45
(Raphanus sativus) could enhance anthocyanin production in vegetative (leaves, stems, roots) and floral (petals) tissues by transcriptional activation of anthocyanin biosynthetic genes and endogenous antocyanin regulatory genes (Ai et al., 2018). Overexpression of RsMYB1 gene in tobacco and petunias was shown to enhance anthocyanin production (Ai et al., 2017). It was also reported that plants with these overexpressed genes had enhanced metal detoxification capacities. Glutathione S-transferase, phytochelatin synthase, superoxide dismutase, catalase, and peroxidase improved metal detoxification abilities and antioxidant enzyme activity imparting stress tolerance. For elements such as Hg and Se, volatilization is preferred over accumulation. Se is first taken up by plants from water, soil, or sediment, and then accumulated in their tissues (Banuelos et al., 1997, Berken et al., 2002), and finally volatilized as dimethylselenide (Wilber, 1980). Se is taken up via S transporters and gets volatilzed through S assimilation pathways into dimethylselenide (DMSe) a non-toxic form. ATP sulfurylase has a high substrate/product ratio, a Km (where Km is the concentration of substrates when the reaction reaches half of Vmax [or the maximum rate achieved by the system reaction]) for sulfate and ATP in the millimolar range, and is subject to powerful inhibition by adenosine phosphosulfate (Ki = 0.04 µM, where Ki is the inhibitory constant) (Schwenn, 1994). Adenosine phosphosulfate acts as the rate limiting step for enzymatic reactions in sulphur and selenium assimilation by restricting the production of sulfate and selenate in plants. Indian mustard transformed with the plastid-localized ATP sulfurylase gene (APS1) from Arabidopsis, had a higher selenate reduction, accumulation, and tolerance ability as compared to nontrasformed Indian mustard plants (Leustek et al., 1994). One group (Pilon-Smits et al., 1999) overexpressed Arabidopsis thaliana ATP sulfurylase (APS) in Brassica juncea. Wild type plants
46
had higher selenate accumulation as compared to transgenic plants because of the APSconversion of sellenate to selenite. Se-cysmethyltransferase and lyase enzymes increase Se volatilization. Various strategies have been employed for mercury phytoremediation using two bacterial genes: merA (mercuric ion reductase), and merB (organomercuriallyase). These enzymes are involved in the conversion of Hg into less toxic forms (Dhankher et al., 2012). Constitutive overexpression of either of these genes in plant species such as A. thaliana (Bizily et al., 1999, 2000, 2003), yellow poplar (Rugh et al., 1998), cotton wood (Lyyra et al., 2007), rice (Heaton et al., 2003), and tobacco (Heaton et al., 2005) increased Hg resistance up to higher levels of HgCl2. Transgenic plants have shown more Hg volatilization of both forms, Hg(0) and organic mercury, as compared to control plants. From the data we can conclude that transgenic technology has the potential to improve reclamation of heavy metal contaminated soil through phytoremediation. We need to engineer plants with better heavy metals uptake, tolerance and accumulation abilities thereby achieving higher phytoextraction potential. Looking at the complexity of the phytoremediation mechanisms, it appears that this field of ecology requires better understading of functions and regulations of plant genes involved in metal hyperaccumulation, improved uptake, root-to-shoot translocation, as well as detoxification and sequestration mechanisms. Better understanding on all aspects will help in solving the phytoremediation of HHMs through transgenic approaches. Most of the progress in development of genetically modified plants with improved phytoremediation ability, has been acheived in Arabidopsis thaliana and Nicotiana spp.. Other plant species undergoing current research include Oryza sativa, Brassica juncea, and Populus species. There are both pros and cons in the development of transgenic crop plants with
47
improved metal accumulation. On one end it provides an easy and fast way for reclamation of heavy metal contaminated soil but at the same time it increases the risk of the entry of heavy metals into food chains. Many such plants produce seeds and fruits which are highly attractive for birds and other animals thus increasing the risk factor for food chain heavy metal contamination. Moreover, genetically modified crops are not accepted easily by the public because of the peoples’ lack of complete scientific/technological knowledge and negative perceptions about the technology and failure of biotechnology companies to ‘educate’ the community about the risks and benefits of transgenic technology. Transgenic plants developed for phytoetraxtion are likely to face more challenges as they have a double risk of GM and toxic metal. There is a need to work on the development of such transgenic plants which have no food uses and can be used for production of energy and biofuels after its phytoremediation uses and thus, providing sustainable postharvest management options (Mench et al., 2009). Further, to improve the understanding of heavy metals phytoremediation, it is imperative to gain public trust on GM phytoremediation transgenic technology since there is need for risk analysis studies to be done in parallel for the application of transgenic technology on phytoremediation (Linacre et al., 2003).
48
Table 8. Transgenic plants for heavy metal tolerance Host
Gene Source
Gene
Gene Function
B. juncea
Escherichia coli
GSH2
Glutathione synthetase
B. juncea
Escherichia coli
GSHII
Glutathione synthetase
B. juncea
Escherichia coli
GSH1
γ-glutamyl cysteine synthetase
B. juncea
Arabidopsis
APS1
ATP sulfurylase
L. esculentum
Bacteria
ACC
Bacterial gene 1aminocyclopropane-1carboxylic acid (ACC) deaminase
Arabidopsis
Bacteria
Mer A and Mer B
Mercury detoxification
B. napus
T. aestivum
Sunflower callus
Yeast
Arabidopsis, Yeast
Arabidopsis
A. thaliana
A. thaliana
MnSOD CUP1
AtPcrs AtHMA4
Superoxide dismutase
Metallothionein Cys-rich membrane protein Plasma membrane localized P1B-ATPase
49
Phytoremediation Mechanism Transgenic seedling and mature plants had Cd tolerance with up to 25% higher shoot Cd accumulation and higher concentrations of glutathione, phytochelatin, thiol compunds and Ca than wild-type plants Transgenic plants had higher level of glutathione, phytochelatin and thiols and thus showed enhanced Cd tolerance Transgenic had 40-90% higher accumulation of Cd and high PCs, γGluCys, glutathione, and total nonprotein thiols compared with wild-type Increased Se uptake and reduction in both the root and shoot tissues Transgenic plants had better ability to grow under high Cd, Co, Cu, Ni, Pb, Zn and higher ACC-deaminase gene activity Double gene transgenic had 50-fold and up to 10-fold higher methylmercury concentrations in merB alone overexpressing plants than wildtype plants due to higher volatilization of mercury SOD activity was 1.5-2.5-fold greater than wild type and enhanced Al tolerance Transgenic sunflower calli had high TTC-reducing activity and increased metallothionein synthesis after 10 days Cd treatment Reduced Cd uptake of Arabidopsis and yeast protoplast Overexpression of AtHMA4 improved the root growth in the presence higher
Reference
Zhu et al. (1999)
Zhu et al. (1999)
Zhu et al. (1999) Pilon-Smits et al. (1999) Grichko et al. (2000)
Bizily et al. (2000)
Basu et al. (2001)
Watanabe et al. (2001) Song et al. (2004) Verret et al. (2004)
transporter
Bacteria
11ggs (cytosol), 6LgI (chlopoplas ts)
N. tabacum
E. coli and S. pombe
CYSE, GSHA and PCS
Serine acetyl transferase, -glutamyl cysteine synthetase, phytochelatin synthase
N. tabacum
Arabidopsis
AtPCS1
Phytochelatine synthatase
B. campestris
Z. mays
Cu/ZnSOD and CAT
Superoxide dismutase and catalase
IAAM and ACC
1-amino cyclo propane-1carboxylic acid deaminase and tryptophan monooxygenase
P. canescens
N. tabacum
P. hybrida
N. tabacum
B. juncea
CAT3 and CAT
A. palustris
P. australis
PaGCS
A. thaliana
Garlic and baker's yeast
GSH1 and AsPCS1
N. tabacum
S. thermophilus
StGCL‐GS
N. tabacum
Arabidopsis
MDHAR/ DHAR
γ -glutamylcysteinsesynthetase
Catalase
γ-glutamylcysteine synthetase Glutathione synthetase and phytochelatin synthase γ‐glutamylcysteine ligase-glutathione synthetase enzyme Mono/ De-hydro ascorbate reductase
50
Zn, Cd and Co concentration Leaf disc of transgenic poplar lines had higher Cd (~4.5-8.5 ppm), Cr (~8-35 ppm), Cu (~30-90 ppm), and Zn (~5000 ppm)
Bittsánszkya et al. (2005)
122-167% higher accumulation of Cd
Wawrzynski et al. (2006)
Transgenic seedlings had 2-fold increase in Cd+2 and higher production of PCs Less reduction in photosynthetic activity and more active antioxidant enzymes than wild type under SO2 stress Transgenic tobacco had better growth, higher biomass and more extensive root system, and accumulated a greater amount of heavy metals (Cu and Co) CAT activity of transgenics was approximately 2-fold higher with lower H2O2 accumulation than that of wild type plants High gutathione, phytochelatines and thiol compound accumulation and antioxidant enzyme activity Transgenic lines had elevated Cd and As tolerance and accumulation due to increased total PC production
Pomponi et al. (2006)
Tseng et al. (2007)
Zhang et al. (2008)
Guan et al. (2009)
Zhao et al. (2010b)
Guo et al. (2010)
20 to 30 fold higher glutathione levels as compared to wild-type
Liedschulte et al. (2010)
MDHAR accumulation enhanced Al tolerance by maintaining ascorbate level
Yin et al. (2010)
S. cerevisiae and N.tabacum
T. caerulescens
TcPCS1
Phytochelatine synthatase
N. tabacum
T. virens
GST
Glutathione-S transferase
N. tabacum
M. musculus
MT1
Metallothionein
A. thaliana
N. nucifera
NnPCS1
Phytochelatine synthatase
N. tabacum
C. demersum
CdPCS1
Phytochelatin synthase
Arabidopsis
B. oleracea
BoCAT1 and BoCAT2
Catalase
E. coli, Arabidopsis
C. demersum
CdPCS1
Phytochelatin synthase
B. vulgaris
S. thermophilus
StGCS-GS
γ-glutamyl cysteine synthetase-glutathione synthetase
N. tabacum var. Sumsun
A. thaliana
AtACR2
Arsenic reductase 2
51
Increased tolerance to Cd due to the decreased lipid peroxidation and enhanced activities of SOD, POD, CAT and PCs content Enhanced Cd tolerance simultaneously, increased activity of SOD, CAT, GST, APX, and GPX than wild type Enhanced Hg accumulation Under high Cd exposure transgenics had 1.4-2.3-fold higher Cd content, 1.3-1.5-fold non-protein thiols, 1.51.9-fold greater phytochelatines than wild-type Transgenic tobacco plants several-fold increased PCs content (up to 100-600 nmol/g FW), Cd (up to 1500 µg/g DW) and As (up to 6000 µg/g DW) accumulation without significant decrease in plant growth 6-fold higher catalase activity and low H2O2 content in transgenic line under heat stress Transformed E. coli had higher accumulation of Cd up to 17 ppm Transgenic B. vulgaris accumulated more Cd, Zn and Cu ions in shoots (3fold ) than wild-type As content in the roots of transgenics was significantly higher (2400µg/g DW) than that of wild type roots
Liu et al. (2011)
Dixit et al. (2011) Ruiz et al. (2011)
Liu et al. (2012)
Shukla et al. (2012)
Chiang et al. (2013) Shukla et al. (2013) Liu et al. (2015)
Nahar et al. (2017)
8.
Human health effects due to consumption of vegetables contaminated with HHMs Heavy metals are critical environmental pollutants that rapidly accumulate in vegetables
mainly in peri-urban areas by natural as well as anthropogenic means (Li et al., 2014). Heavy metals are indispensable in minute quantities to sustain various physiological and biochemical functions in living beings, though they can pose harmful effects when they exceed the specified safe threshold levels (Jaishankar et al., 2014). Fig. 4 explains that most of the vegetables get contaminated by absorbing heavy metals from polluted water, soil, and air (Kacholi and Sahu, 2018; Wongsasuluk et al., 2018). For decades, vegetables have been important diet constituents that fulfil the required needs of essential nutrients. Mainly leafy vegetables may be more harmful to human consumption due to greater accumulation capacity. HHMs penetrate cell membranes and produce ROS that ultimately affect functions of cells and cellular organelles (SanchezChardi et al., 2009). As we have discussed earlier, several heavy metals like As, Pb, Cd, Cr, and Hg are unusually toxic (hematotoxic, immunotoxic, neurotoxic, genotoxic, reproductive toxic, pulmonary toxic, nephrotoxic, and hepatotoxic) and hazardous to the environment and living-beings (Ametepey et al., 2018; 2018, Domingo et al., 2017; Mari et al., 2018). The ingestion of toxic heavy metal concentrations from vegetables may lead to several short-term as well as long-term adverse health effects such as vomiting, stomach irritation, headache, diarrhea, fatigue, weakness, drowsiness, confusion, muscular pain, pricking sensation in hands and legs, skin manifestations, unusual pigmentation and keratosis, hypertension, cardiovascular disease, lung edema, destruction of mucous membranes, hair and memory losses, difficulty with balance, damage to brain, kidney and lungs, changes in vision and/or hearing (Carrington et al., 2019).
52
On the cellular level, toxic metal poisoning can have deleterious affects on oxidative phosphorylation and ATP synthesis (Yan et al., 2017; Yang et al., 2018; Lai et al., 2018; Zafarzadeh et al., 2018; Rehman et al., 2018). Furthermore, HHMs can produce both acute and chronic toxicity symptoms in pregnant women, fetuses, young children and adults (Table 9).
53
Fig. 4. Health effects of heavy metals on humans
54
Table 9. Acute and chronic effects of HHMs before and after nativity in humans Toxic metal
Toxicity
Acute As Chronic
Acute Cd
Before nativity effect Neurotoxic to brain development and pose behavioral changes Increase in fetal loss, detrimental effects on embryo, mutagenesis and reduction in birth weight -
Chronic
Embryotoxic and teratogenic, reduced size and weights of embryo
Acute
Premature birth risk and babies with low birth weight
Pb Chronic
Cr
Reduced the cognitive capacity of children and birth defects
Acute
Detrimental effects on fetus developmental
Chronic
Embryotoxic and fetotoxic,
After nativity effect Weakness, drowsiness and confusion, muscular pain, flusking skin, abnormal changes in heartbeats and pricking sensation in hands and legs Affect oxidative phosphorylation and ATP synthesis, reduced production of erythrocytes and leukocytes, skin manifestations, pigmentation and keratosis, neurological disorders and cardiovascular disease Lung edema and destruction of mucous membranes, stomach irritation, vomiting, diarrhea and fatigue Disturbances in Ca+2 metabolism, renal dysfunction, formation of kidney stones and hypercalciuria, mutagenic, carcinogenic and teratogenic Affect central nervous system and the gastrointestinal tract, loss of appetite, kidney disease, fragile bones, renal dysfunction and abdominal pain Mental retardation, autism, birth defects, allergies, psychosis, dyslexia, weight loss, hyperactivity, paralysis, muscular weakness, brain and kidney damage and IQ reduction Ulcers, hair loss, inhibition of erythrocyte glutathione reductase and reduce the conversion of methemoglobin to hemoglobin Chromosomal aberrations and mutation,
55
Affected system &/or organelle
Reference
Lungs, liver, bladder and skin
Yang et al. (2018); Tripathi et al. (2007); José Zocche et al. (2010)
kidney
Neuromuscular system
Digestive tract
Lai et al. (2018); Salem et al. (2000); Trzcinka-Ochocka et al. (2010)
Yan et al. (2017); Salem et al. (2000); Iqbal (2012);
Salem et al. (2000); Matsumoto et al. (2006)
low birth weight and preterm birth, and congenital malformations
Acute
Affect growth and development
Hg
Chronic
Acute Cu Chronic
Affect brain and nervous systems development in unborn infants' Affects fetal growth, induces behavioral changes and neurotoxic Neurological changes in newborn and preeclampsia in mother
Acute
-
Chronic
-
Ni
Chronic
Musculoskeletal defects
alterations in replication and transcription of DNA process Anxiety, depression, drowsiness, hair and memory loss, difficulty with balance, insomnia, irritability, memory loss, damage to brain, kidney and lungs, and changes in vision or hearing
Nervous system
Zafarzadeh et al. (2018);
Lung damage, skin rashes, vomiting, diarrhea, nausea, increased blood pressure Stomach and intestinal irritation Damage to brain and kidney, liver cirrhosis and chronic anemia Headache, spinning dizziness, insomnia, nausea, vomiting, irritability, itching and hair loss Hematotoxic, immunotoxic, neurotoxic, genotoxic, nephrotoxic, and hepatotoxic, cancer of the lungs and nose, and respiratory disorders Risk of lung cancer
56
Neurological and enzymatic systems
Mitochondria
Salem et al. (2000);
Rehman et al. (2018); Salem et al. (2000); Khan et al. (2007); Mishra et al. (2010)
9. Permissible limits of HHMs in the environment HHMs may adversely affect soil ecology, agricultural soil, food quality, and the health of living organism, in addition to air and groundwater quality (Kacholi and Sahu, 2018). Long-term applications of sewage treatment plant (STP) effluents for irrigation, also contaminates soil, water and vegetables resulting in deterioration of soil and water resources (Sharma et al., 2008). Presently in peri-urban areas, vegetable production is on the rise and remains at highly maintained levels throughout the year. Health-conscious citizens include more vegetables in their diets, and specifically their green leafy vegetable consumption is increasing (Gupta et al., 2013). Many researchers, institutes, organizations and countries have set their particular maximum permissible limits of heavy metals in vegetables, plants, soil and water (drinking and irrigation) to get a broad idea about the contamination and intake levels Therefore, it has become important, to generate these new guidelines for HHMs levels, that focus on implementing scientific guidance on the assessment of the quality of vegetables and foods based on technical improvements and novel developments. In many countries, however, the permissible standards are still higher than the World Health Organizatin (WHO) or the Food and Agricultural Association (FAO) standards allow. The maximum permissible limits of HHMs in vegetables and plants, soil, drinking and irrigation waters are given in Tables S2, S3, S4 and S5, respectively. 10.
Challenges, issues and prospects for further applications
All the remedial approaches, such as physical, chemical, biological, genetic, physiological, biotechnological, and nanotechnological are doing well to some extent but are restricted due to environmental as well as biological limitations that are site- and contaminant-specific and require optimum running conditions. The cocktails of pollutants in the environment can obviously
57
decrease the efficiency of these methods. When the food chain gets contaminated, plants first accumulate a high amount of HHMs in their storage organs that ultimately create hazards to human and animal health. The contamination pathways of HHMs in plants are still not fully understood and require a more intensive focus in the future. Contamination mechanisms should be well understood to identify the load of a poisonous element that can enter in our food and become biomagnified. The physiological, genetic and biotechnological approaches based on microbial and plant interventions, can modify the required suitable changes needed in organisms and genes to better resist heavy metal intake. Present methods are mostly focused on a particular single pollutant even though background environments contain a mixture of various pollutants. On a large scale, financial and technical problems have made soil remediation/intervention a challenging responsibility. Biological remediation approaches have shown to produce better and more effective responses as compared to physico-chemical methods with respect to environmental safety, small-scale applications, public acceptability and cost. Advanced approaches such as nanoremediation and the use of combined biotechnological and transgenic technologies can better help to promote bioremediation efficiency and effectiveness. By introducing foreign genes into plant genomes to improve the adaptability to withstand high HHMs concentrations and hyperaccumulators, capacities for tolerances can be managed effectively due to the overexpression of particular proteins and natural chelators in transgenic plants cells (Yadav et al., 2017b). Transgenetic and nanotechnological approaches of remediation are well studied in the laboratory,
however,
field
applicability
requires
more
extensive
investigation.
In
nanotechnological remediation approaches, carbonaceous NMs possess large specific surface
58
areas, outstanding electrical, optical, thermal and chemical potentials and broad applications so as to be considered one of the most highly prospective candidates to remove chemical/biological contaminants from wastewater. Nevertheless, future development and full-scale applications of these remedial tactics still face a wide variety of challenges and more thorough studies are certainly required. The following challenges are offered as remedial processes: •
The comprehensive understanding of HHMs accumulation in the food chain and bioaccumulation requires comprehension of the toxicity, mobility, function and reaction of metal transporters and ligands of plant cell mechanisms and metabolism.
•
More advanced and detailed knowledge of metal transporters is necessary for all toxic elements found in contaminated plants.
•
The complex passage/transference of toxic metal transporters across apoplastic barriers into plant seeds is largely unexplained and necessitates investigation to aid in plant tolerances.
•
The mechanisms of toxic element uptake into plant leaves and fruits, seeds and tubers should be classified.
•
Source reduction strategies should be focused in the future as part of preventive measurements for food chain incorporation that have been identified.
•
The commercial large-scale production of carbonaceous nanomaterials is still challenging and requires intervention of production methods for scale-up in larger numbers of plants.
•
The modern synthesis techniques for carbonaceous nanomaterials are still complicated with less efficiency compared to standard genetic methods, hence simple and efficient nanodesign methods are essentially needed.
59
•
CNTs and graphene-based NMs in the liquid phase currently do not perform properly for the removal of HHMs. The applications of nanomaterials coupled with several functional groups and surface modifications have been applied to overcome present problems.
•
Phytoremediation processes are not permanent solutions for removal or stabilization of HHMs. The suitability of phytoremediation procedures mainly depends on the site of uptake in the plant, the tolerance level of the plant, bioavailability of metals, climate and weather conditions. Hence a wide applicability of phytoremediation should be concentrated on improving the utilization of recent biotechnological and genetic approaches.
•
Rhizospheric chemistry and interactions of HHMs and microbes should be more elucidated to better understand the transport mechanism in plants.
•
Physical methods require large working volumes, are costly, generate toxic waste and build up negative effects on soil fertility. These procedures must be rendered more safe to the environment and plants while simultaneously studying other new remediation methods such as nanotechnological processes.
•
Chemical methods are not stable solutions of remediation and require permanent monitoring. In addition, extractants necessitate washing steps to remove unbound toxins that can cause environmental issues later on.
For the sustainability and broad applicability of future generations and resources, to overcome and reduce the contamination of HHMs in the food chain, intensive studies at the field level with the optimization of processes and improvments in the suitability of materials/methods in specific environments must be carried out effectively. 11. Conclusions
60
In this review, we mainly focused on nanotechnological and phyto-bio-genetic approaches for remediation. This review has revealed that heavy metal sources, food chain contamination with them, the mechanisms of metal transport in plants, and the physicochemical, phytoremediation, nanotechnological and genetic approaches in heavy metal removal, all possess constraints to effective phytoremediation. The entire environmental compartments including soil, water, air and food have been contaminated by HHMs around the world. This severe problem is rising in industrial towns and rapidly developing cities. In the periphery of cities, cultivated soils are polluted with deposition or discharge of HHMs thereby increasing the levels of hazardous substances in food chains. Food chain contamination is one of the main routes for the entry of HHMs into the human body and intake of contaminated foods may contribute to the development of several disorders in living beings. Among the modified and advanced technologies of remediation such as nanoabsorbents, phytoremediation and genetic approaches are highly effective, efficient and can be economically viable. Nevertheless, the applicability of these methods is still restricted, and more intensive investigation at the field level is undoubtedly necessary. Conflict of interest The authors declare no conflict of interest. Acknowledgements The authors are very grateful to Lisa M. Reece, with the University of Texas Medical Branch, Galveston, TX, USA for her consistent support and guidance. The authors are also thankful to the editor and anonymous reviewers for their valuable suggestions to improve the manuscript.
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S0013-9351(19)30589-4
DOI:
https://doi.org/10.1016/j.envres.2019.108792
Reference:
YENRS 108792
To appear in:
Environmental Research
Received Date: 23 June 2019 Revised Date:
12 September 2019
Accepted Date: 1 October 2019
Please cite this article as: Kumar, S., Prasad, S., Yadav, K.K., Shrivastava, M., Gupta, N., Nagar, S., Bach, Q.-V., Kamyab, H., Khan, S.A., Yadav, S., Malav, L.C., Hazardous heavy metals contamination of vegetables and food chain: Role of sustainable remediation approaches - A review, Environmental Research (2019), doi: https://doi.org/10.1016/j.envres.2019.108792. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2019 Published by Elsevier Inc.
Hazardous heavy metals contamination of vegetables and food chain: Role of sustainable remediation approaches - A review Sandeep Kumara*, Shiv Prasada, Krishna Kumar Yadavb*, Manoj Shrivastavaa, Neha Guptab, Shivani Nagarc, Quang-Vu Bachd, Hesam Kamyabe, Shakeel A. Khana, Sunita Yadava, Lal Chand Malavf a
Centre for Environment Science and Climate Resilient Agriculture, Indian Agricultural Research Institute, New Delhi 110012, India Email- [email protected]
b
Institute of Environment and Development Studies, Bundelkhand University, Kanpur Road, Jhansi 284128, India c
Division of Plant Physiology, Indian Agricultural Research Institute, New Delhi 110012, India d
e
Institute of Research and Development, Duy Tan University, Da Nang, Vietnam
UTM Razak School of Engineering and Advanced Technology, Universiti Teknologi Malaysia, Malaysia f
National Bureau of Soil Survey and Land Use Planning, Nagpur, India *Corresponding author: [email protected]
1
Graphical Abstract
Abstract This review emphasizes the role of toxic metal remediation approaches due to their broad sustainability and applicability. The rapid developmental processes can incorporate a large quantity of hazardous and unseen heavy metals in all the segments of the environment, including soil, water, air and plants. The released hazardous heavy metals (HHMs) entered into the food chain and biomagnified into living beings via food and vegetable consumption and originate potentially health-threatening effects. The physical and chemical remediation approaches are restricted and localized and, mainly applied to wastewater and soils and not the plant. The nanotechnological, biotechnological and genetical approaches required to more rectification and sustainability. A cellular, molecular and nano-level understanding of the pathways and reactions 2
are responsible for potentially toxic metals (TMs) accumulation. These approaches can enable the development of crop varieties with highly reduced concentrations of TMs in their consumable foods and vegetables. As a critical analysis by authors observed that nanoparticles could provide very high adaptability for both in-situ and ex-situ remediation of hazardous heavy metals (HHMs) in the environment. These methods could be used for the improvement of the inbuilt genetic potential and phytoremediation ability of plants by developing transgenic. These biological processes involve the transfer of gene of interest, which plays a role in hazardous metal uptake, transport, stabilization, inactivation and accumulation to increased host tolerance. This review identified that use of nanoremediation and combined biotechnological and, transgenic could help to enhance phytoremediation efficiency in a sustainable way. Keywords: bioaccumulation; biotechnology; nanotechnology; toxicity, transgenic approach. 1. Introduction Worldwide, more than 10 million sites covering more than 20 million ha of land are considered soil polluted sites, of which >50% are contaminated with hazardous heavy metals (HHMs) and/or metalloids (He et al., 2015). The combined worldwide economic impact of heavy metals (HMs) pollution is estimated to be in excess of US $10 billion per year (He et al., 2015). A study by the Ministry of Environmental Protection (MEP), China, reported that the total area of arable land contaminated with heavy metals had reached near to 20 mha, estimating that almost 16.1% of the total arable land, and 19.4% of recognized cropland locations were above the normal range of heavy metals accumulation. Furthermore, 13.7%, 2.8%, 1.8% and 1.1% of arable land contained slight, mild, moderate and heavy pollution levels, respectively (Zhao et al., 2015; Sodango et al., 2018). According to the Central Water Commission (CWC) of India, 42 3
rivers have at least two HHMs beyond the permissible limit (CWC, 2018). As per Central Ground Water Board (CGWB), India, groundwater of more than 718 districts is affected by heavy metal toxicity with cadmium (Cd), chromium (Cr), arsenic (As), lead (Pb) and iron (Fe). The heavy metals in contaminated soils impair the natural ecosystem services and eventually damage human health via the food chain (Jaishankar et al., 2014; Yadav et al., 2018a; Maurya et al., 2019). The primary sources of heavy-metal pollution are industrialization, mining, milling, fossil fuel burning, agrochemicals that discharge a variety of HHMs such as As, Cr, mercury (Hg), Cd, copper (Cu), nickel (Ni), cobalt (Co), zinc (Zn) and Pb into the agricultural soils and water bodies (Kumar et al., 2019a; Kumar et al., 2019b; Kumar et al., 2019c; Gupta et al., 2018). Vegetables are an important part of the human diet due to the richness of beneficial and essential minerals and nutrients (Nankishore, 2014). Unfortunately, vegetables can uptake and accumulate HHMs beyond recommended limits in their entire body including both edible and inedible parts (Tasrina et al., 2015). In the last few years, the concentration of HHMs in vegetables (leafy, root and fruit), has been observed at high levels (Wai et al., 2017). Eventually, the build-up of HHMs in vegetables and edible parts of crops in contaminated soils, is a matter of serious concern due to the harmful and irreversible effects of metals impacting both humans as well as animal’s overall health (Malik, 2004). The removal of HHMs from industrial wastewaters and contaminated soils has been studied for many years, including the implementation of several physicochemical approaches of removal that include filtration, evaporation, reverse osmosis, ion-exchange, redox reactions (oxidation and reduction), precipitation, and electrochemical removal. However, hazardous metal contamination in vegetables and plants and their subsequent decontamination fall under the
4
exploration stage of research and are not considered important enough to lay out a concrete remediation plan to move forward by local community governments. The physical and chemical remediation approaches are restricted and localized and mainly applied to wastewater and contaminated soils and not the plant life that may reside there. Some phytoremediation methods are well explored but not suitable for edible crops and vegetables (Ali et al., 2013; Sharma et al., 2015). To move past these issues, the biotechnological and nanotechnological approaches can open a path ahead to remove the metals from contaminated vegetables and plants (Mani and Kumar, 2014; Zeng et al., 2015; Dixit et al., 2015; Singh et al., 2015; Mosa et al., 2016; Ali et al., 2018; Srivastav et al., 2018) by successfully superseding traditional methods (Singh and Prasad, 2015). Certain microorganisms, for example, can respond to heavy-metal stress through transport across the cell membrane, entrapment in extracellular capsules, precipitation, biosorption to cell walls, complexation and redox reactions (Malik, 2004). Microorganisms can also counter heavy metal stress using diverse defensive systems, such as compartmentalization, exclusion, formation of complexes and the synthesis of binding proteins, i.e. metallothioneins (MTs) or phytochelatins (PCs) (Mejare and Bulow, 2001). The application of nanomaterials (NMs) in plants for removal of HMs is still under investigation (Okuo et al., 2018; Srivastav et al., 2018). This review identified advanced approaches such as nanoremediation and use of combined biotechnological and transgenic that can help in a better way to enhance phytoremediation efficiency in a sustainable way. 2. Search strategy for quality of the articles applied in the study
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The method used in the literature review involves of three steps: (i) Collection and identification of relevant literature for the study, and (ii) Extraction of data and diagraming representation, and (iii) Applicability of sustainable remedial approaches for this study. We searched and collected the relevant literature in the Scopus, Science Direct and Google Scholar databases, in March and April of 2018, using the following Boolean search string: ( “heavy metals” OR “Heavy metal contamination” OR “Heavy metals toxicity” OR “Heavy metals contamination of food chain” OR “Heavy metals remediation sustainable methods” OR “nanotechnology for heavy metals remediation” OR Biotechnological advances for heavy metals remediation” OR “Genetic approaches of remediation” OR “Heavy metals guidelines and permissible limits” OR “Current status of remedial approaches”. We collected all the well cited and high impacts literature and screened them as per requirement. To select most relevant and manageable set of studies among the identified pieces of literature, we set up the following selection rules as followed by Sandin and Peters (2017). 2.1. Collection and identification of relevant literature for the study a) Search all type relevant findings and included in study (mostly peer-reviewed) b) All type material related to heavy metal toxicity and contamination were carefully studied and selected the suitable one. c) Included the study throughout the World. d) Excluded the studies which do not include quantitative results. e) Excluded almost all the studies which are more than 15 years old. f) Excluded the studies from other languages like Chinese, French, German and Swedish. g) Exclusion of studies on physical and chemical remediation of heavy metals. h) Included only nanotechnological, biotechnological and genetical approaches.
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i) Exclusion of duplicates and copying of studies. 2.2. Extraction of data and diagraming representation a) Data was extracted mostly in tabular manner and provided in supplementary files. b) A huge number of studies were read thoroughly and collected the data in systematic and captureable manner. c) Diagrammatic representation of processes was keep in mind and try to represent in ease to access manner. d) Collected all the permissible limits of many countries in tabular manner for easy access. 2.3. Applicability of sustainable remedial approaches for this study a) Sustainable methods of remediation were studied and layout the new concept with wide applicability in the review. b) Try to incorporate the possible new outcomes of sustainable approaches of heavy metals remediation c) Sustainable methods were selected as per several assumptions like why, applicability and final outcome. 3. Sources of heavy metals in agricultural soil Heavy metals (HMs) are omnipresent in the environment due to both natural (geogenic) as well as anthropologic (human induced) sources found in agricultural soils (Rahimi et al., 2017; Ratul et al., 2018). The contamination of TMs in soil, water and plants in several regions of the world are summarized in Table 1. Soil pollution by heavy metals is a universal problem for food production and human health (Liu et al., 2018). The most important natural sources for heavy metal introduction into soils are weathering of rocks, erosion and volcanic activity and the anthropogenic sources of ore mining operations, smelting, electroplating, industries’ 7
effluents, landfills, warfare and military training, use of pesticides and phosphate fertilizer, application of biosolids (e.g., livestock manures, composts, and municipal sewage sludge) and atmospheric deposition (Fulekar et al., 2009; Herrero et al., 2019) (Fig. S1). The heavy metals are a key component of rocks and soils in the environment, introduced through weathering, erosion and anthropogenically. Heavy metals can reach into the soilplant-human atmosphere and accumulate there. The total concentration of heavy metals in soil is the sum of all these variables minus the losses through off-take in harvested crops, erosion of soil particles by wind or water, leaching down the soil profile in solution and losses by volatilization of some elements in gaseous forms. This balance of the heavy metals in the soil can be represented by the equation 1 (Lombi and Gerzabek, 1998): Mtotal = [Mp + Ma + Mf + Mag + Mow + Mip] – [Mcr + Ml]………..eq (1) where, Mtotal is the total heavy metal in soil, Mp is the heavy metals in the parent material, Ma is the heavy metal concentration in atmospheric deposition, Mf are the heavy metals in fertilizer sources, Mag are the heavy metals in agrochemical sources, Mow are the heavy metal concentrations in organic waste sources, Mip are other inorganic pollutants, Mcr is the heavy metal in crop removal, and Ml is the heavy metal losses by leaching, volatilization, and other extraction processes. Agricultural land and irrigation water contamination has become a harsh environmental problem in several developed and developing countries in the last decade due to scarcity of irrigation water availability (Fan et al., 2017). In agricultural soil, soil quality is an indicator of heavy metal contamination arising from on-farm activities (Liu et al., 2012). As mentioned previously, the heavy metals that accumulate in soil significantly add to the pollution of agricultural commodities and indirectly become the leading component of health risks (Sawut
8
et al., 2018). Heavy metals contamination of soil, water, crop and vegetables is one of the most severe environmental predicaments globally (Ahmad and Goni, 2010). It creates possible threats to the ecological soil-food chain that can impair with soil fertility, quality of drinking water and human health, direct ingestion, dermal contact, inhalation and oral consumption (Khan et al., 2008; Lu et al., 2011). The contamination of agricultural soil occurs through irrigation with wastewater (Hajjami et al., 2013), fertilizers application, pesticides dosing, erosion and sedimentation of mined or contaminated soils, heavy farm machinery operations, municipal solid-waste compost incorporation, and leaching from landfill site, dry and wet deposition of industrial pollutants, and volcanic activities (Gupta et al., 2015; Sodango et al., 2018). In addition, fly ash deposition from coal power plants are the notable sources of soil contamination, accumulation and pollution of heavy metals in soil, water and crops (Nagajyoti et al., 2010; (Kanchan et al., 2015). Long-term application of wastewater results in build-up of heavy metals in soil and crops that can limit soil functioning, reduce the nutritional quality of vegetables, toxicity to crops and contamination of the food chain (Chen et al., 2010; Singh et al., 2010). Due to continuous intake, the bioaccumulation of heavy metals takes place in vegetables, crops and humans. Crop species differ in their ability to absorb heavy metals from soil and water (Mapanda et al., 2005). The immense growth of industries has remarkably increased the discharge of effluents to the environment, particularly in soil and water, which has led to the contamination of HHMs in soil and now finally accumulated in living beings. The chaotic discharge of heavy metals into the soil and waters is a significant health concern, as they cannot be broken down to non9
toxic forms and therefore have long-lasting influences on the ecosystem (Dixit et al., 2015). Mining and milling works, along with grinding, gathering ores, extraction and purification of minerals and disposal of tailings provide apparent sources of contamination in the environment, i.e. soil, water and plants, along with the discharge of mining wastewater (Table S1). Kumar et al. (2019) used regression modeling, principal component analysis and accumulation nutrient elements to predict the heavy metal concentrations in Brassica oleracea tissues grown in integrated industrial effluent.
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Table 1. Heavy metal contamination in agricultural soils, crops or vegetables and water in different countries Source of HM contamination
HM Species
Contamination
Wastewater of Shitalakhya river
Cu, Ni, Cd, Cr, Pb, Zn
Soil and Vegetables
Wastewater treatment plant
Zn, Cu, Pb, Cd
Soil, water and crops
Soil
Hg
vegetables
Mining activities
Pb, As, Hg, Cd, Cr, Ni
Soil and sediment samples
Vegetable/Crop Basella alba, Cucurbita moschata, Amaranthus lividus, Trichosanthes cucumerina and Spinacia oleracea Vicia faba, Triticum turgidum, Triticum æstivum, Eruca. sativa, Urtica dioica, Madia sativa and Malus sylvestris Piper nigrum, Spinacia oleracea, Brassica oleracea, Brassica rapa, Raphanus raphanistrum, Phaseolus vulgaris, Vigna unguiculata and Solnum melongena Phaseolus vulgaris, Solanum melongena, Piper nigrum, Ipomoea aquatic, Ipomoea batatas, Amaranthus dubius and Solanum lycopersicum
Mine affected area
Cu, Pb, As, Cd
Soil and vegetable
Industrial and municipal sewage water
Cd, Pb, Ni, Zn
Soil and crop
Oryza sativa
Human Activities
Fe, Mn, Pb, Cu, Cd, Zn, Cr, Ni
Soil and Sediment
-
Agricultural field and urban settlements
Cu, Cr, Zn, Ni, Cd, Pb
Water samples, sediments
Lemna minor
Urbanization
As, Zn, Cd, Cr, Hg, and Pb
Soil, water and vegetables
Solanum lycopersicum, Phaseolus vulgaris, Triticum aestivum, Raphanus raphanistrum, Momordica charantia and Brassica oleracea
11
Region
Reference
Narayangonj, Bangladesh
Ratul et al. (2018)
Marrakech, Morocco
Chaoua et al. (2018)
China
Yu et al. (2018)
Zacatecas, Mexico
Covarrubias et al. (2018)
Daye, China
Yang et al. (2018)
Lenjan, Iran
Rahimi et al. (2017)
Liaohe River Delta, North China Anchar Lake, Kashmir, India
Urumqi, Xinjiang, China
Yan et al. (2018)
Showqi et al. (2018)
Sawut et al. (2018)
Geogenic and anthropogenic sources Human induced activities
As, Cd, Cr, Cu, Hg, Ni, Pb, Se, and Zn As, Cd, Cu, Ni, Pb, Zn
Human activities in river area
Cd, Mn, Cr, Cu, Ni, Pb, Zn, Fe
Geogenic and anthropogenic sources
Pb, Zn, Cu, Cd, As, Hg, Cr, Ni Cr, Ni, Cu, As, Cd and Pb Pb, Cd, and Cu
Industrialization Fertilizers, pesticides and other farm inputs Industries Soil Erosion
Cd, As, Pb, Cu, Zn, Ni, Cr Cr, Cu, Pb, and Ni
Glass industry
Cd, Cr, Cu, Fe, Mn, Pb, Zn
Coal Fired Thermal Power Plant
Pb, Cd, Cr As. Cu, Zn, Ni and Fe
Industrial area
Cu, Zn, Pb, Cr, Cd, Fe, and Ni
Soil Soil Soil and vegetables
Spinacia oleracea, Lagenaria siceraria, Cucurbita maxima and Solanum melongena
Agricultural soil
-
Agricultural soil
-
Agricultural soil
-
Agricultural soil
-
Agricultural Fields Soil and Agricultural Crops
Brassica juncea, Triticum aestivum and Hordeum vulgare
Agricultural soil
water, soil, and vegetables
Solanum melongena, Capsicum frutescence, , Raphanus sativus, Abelmoschus esculentus, Solanum lycopersicum and Brassica oleracea
12
Hainan Island, China
Liao et al. (2018)
Azerbaijan Province, Iran
Mohammadi et al. (2018)
Dera Ghazi Khan, Pakistan
Latif et al. (2018)
Hunan province, China Tangail, Bangladesh Semarang, Indonesia
Proshad et al. (2018)
Hunan, China
Zhang et al. (2018)
Bedfordshire, UK
Quinton and Catt (2007)
Jhabrera, India
Kumar and Chopra (2015)
Farakka, India
Sengupta et al. (2010)
Dhaka, Bangladesh
Ahmad and Goni (2010)
Li et al. (2018)
Hindarwati et al. (2018)
4. Heavy metal toxicity and bioaccumulation through food chain contamination The physical, chemical, and biological processes as well as anthropogenic activities, can release heavy metals in the environment and cause the accumulation of heavy metal toxins within living beings participating in the food chain (Koivula et al., 2011). As previously discussed, the HHMs disperse into the soil, air and water bodies from where they can be taken up or ingested by crops/plants, bio-accumulated into top consumers, and finally biomagnified (Hossain et al., 2008; Pollard et al., 2014). Once HHMs enter into food chain, they can not be removed easily from the top of food chain and thereby become circulated into the whole food web. Many hyperaccumulated plants serve as food for human beings and animals. Hence, the cycle from soil to humans via plants and again into the soil after death of top consumers, provide a path for HHMs to remain sustained within the environment for long periods of time inducing many harmful effects (Fig. S2). The contamination in crops depends on the efficiency of transfer from soil to aboveground portions of plants. The toxic metal bioaccumulation in vegetables is explained in Table 2. Consumption of contaminated crops containing HHMs can create conceivably deleterious health hazards in living beings (Clemens and Ma, 2016). The cycle of heavy metals in the food chain begins with various sources. To illustrate, Cd is taken up from soil via roots to the plant body. In the case of Pb, the heave metal is absorbed from the air dust into plants, and As and Hg may be obtained from sewage water. During the transfer from one section to another in the food chain, some heavy metals have tendency of accumulation in the tissues (liver, feathers, muscles, kidney and other organs) of top consumers. Table 2. Bioaccumulation of HHMs in different organs of vegetables Region
HM Species
Plant Part Analyzed
Vegetable
13
*Concentration of HM (mg/kg)
Reference
Basella alba, Cucurbita moschata, Anolis lividus, Trichosanthes cucumerina, Spinacia oleracea
Edible parts
Lepidium sativum, Coriandrum sativum, Spinacia olarecea
Leaves
Zn - 19.762 Cu - 9.373 Pb - 3.699 Ni - 2.92 Cr - 1.127 Cd - 0.168 Pb – 0.2-4.7 Zn – 1.7-6.7 Cu – 0.59-2.23 Cd – 0.02-0.52 Ni – 0.04-0.81 As – 0.018-0.126 Co – 0.005-0.21 Cr – 0.1-1.87 Zn – 33.8-77.2 Cu – 2.9-7.0 Pb – 18.3-45.7 Cd – 6.0-12.0 Cd – 0.01-0.07, Pb – BDL-0.05
Narayangonj, Bangladesh
Cu, Ni, Cd, Cr, Pb and Zn
Kahrizak, South of Tehran, Iran
Pb, Zn, Cu, Cd, Ni, As, Cr and Co
Marrakech, Morocco
Zn, Cu, Pb and Cd
Vicia faba
Root, Leaves, Pod and seeds
Tamale Metropolis, Ghana
Pb and Cd
Brassica oleracea, Solanum lycopersicum, Daucus carota, Capsicum annuum, Allium cepa
Edible parts
Assiut, Egypt
Cd, Pb and Ni
Solanum melongena
Edible parts
Egypt
Pb, Cd, Cu, Ni and Cr
Solanum tuberosum, Solanum lycopersicum, Cucurbita maxima
Edible parts
Nevsehir Province, Turkey
Cd, Pb, Zn, Cr, Cu, Ni and Fe
Gazipur district, Bangladesh
Pb, Ni, Co, Cr and Cd
Ethiopia
Fe, Zn, Pb, Cr and Cd
Temeke district, Tanzania
Fe, Zn, Pb and Cu
Daye, China
Cu, Pb, As and Cd
Solanum lycopersicum, Solanum cepa, Capsicum annuum
Edible parts
Leaves, roots and stem
Spinacia oleracea, Agelaius tricolor, Sonchus oleraseus
Spinacia oleracea
Leaves
Ipomoea batatas, Amaranthus hybridus, Abelmoschus esculentus, Solanum melongena Vigna unguiculata, Ipomoea aquatic, Agelaius tricolor,
14
Edible parts Edible parts
Cd – 0.07-11.14 Pb – 0.88-42.7 Ni – 0.01-4.82 Pb – up to 0.96 Cd – up to 0.16 Cu – up to 2.39 Ni – up to 0.49 Cr – up to 2.17 Cd – 0.001-0.004 Pb – 0.02-0.03 Zn – 0.50-1.16 Cr – 0.001-0.02 Cu – 0.14-0.25 Ni – 0.02-0.48 Fe – 0.74-4.37 Pb - 0.64−5.97 Ni - 4.02–46.5 Co - 0.39–2.62 Cr - 1.71–6.99 Cd - 0.22–1.28 Fe - 483-612 Zn - 109-219 Pb - 2.56-3.97 Cr - 8.42-13.4 Cd - 1.62-1.91 Fe – 4.84-13.64 Zn – 2.64-10.29 Pb – 0.32-2.46 Cu - 0.55-1.04 Cu – 0.46 to 6.67 Pb – 0.00 to 1.47 As – 0.00 to 0.94
Ratul et al. (2018)
Souri et al. (2018)
Chaoua et al. (2018)
Ametepey et al. (2018)
Youssef and ElGawad (2018)
Abdel-Rahman et al. (2018)
Leblebici and Kar (2018)
Naser et al. (2018)
Gebreyohannes and Gebrekidan (2018)
Kacholi and Sahu (2018)
Yang et al. (2018)
Ipomoea batatas, Lycopersicon esculentum, Solanum melongena, Capsicum annuum Jordan
Cu
Lactuca sativa
Golestan province, Iran
Zn, Cd, Pb, and Cu
Solanum lycopersicum, Cucurbita maxima
Dera Ghazi Khan District, Pakistan
Cd, Mn, Cr, Cu, Fe, Ni, Pb and Zn
Cd - 0.00 to 0.71
Root, shoot and leaf Fruits
Spinacia oleracea, Solanum melongena, Cucumis melo
Edible parts
Solanum lycopersicum, Solanum tuberosum, Allium cepa, Spinacia oleracea, Daucus carota, Piper nigrum, Berberis vulgaris, Brassica oleracea, Brassica oleracea var. italic, Petroselinum crispum, Pastinaca sativa
Vojvodina Province, Serbia
Cr, Ni, Cd and Pb
Khyber Pakhtunkhwa Province, Pakistan
Pb, Ni, Cr, Cd and Zn
Abelmoschus esculentus, Lycopersicon esculentum
Fruits
Zhejiang, China
As, Cd, Cr, Pb, Ni and Hg
28 species of different vegetables**
Edible parts
Korba, Chhattisgarh, India
Cr, Mn, Fe, Ni, Cu, Zn, Cd, Pb and Hg
Solanum lycopersicum, Solanum melongena, Agelaius tricolor, Polygonia album, Spinacia oleracea, Coriandrum sativum
Edible parts
Bologna, Italy
As, Cd, Cr, Cu, Hg and Pb
Edible parts
Lycopersicon esculentum
15
Fruit
Cu – 0.5-2.3 Zn – 1.1-128.5 Cd – up to 2.2 Pb –up to 14.2 Cu – 0.38-7.7 Cd – 0.05-0.39 Mn – 18.7-137 Cr – 2.7-3.7 Cu – 22.2-65 Fe – 129-968 Ni – 1.8-5.05 Pb - BDL Zn – 19.5-41
Cd – up to 0.89 Pb – up to 3.56 Cr – up to 2.3 Ni – up to 2.2
Pb – 0.53-1.39 Cd – 0.01-0.05 Ni – 0.31-0.86 Zn – 0.02-0.09 Cr – 1.02-18.95 As – up to 0.013 Cd – up to 0.017 Cr – up to 0.057 Ni – up to 0.002 Hg – up to 0.094 Pb – up to 0.034 As – 0.56-2.08 Fe – 192-2255 Cr – 1-17 Mn – 17-676 Cu – 25-71 Zn – 24-121 Cd – 0.25-1.57 Pb – 0.7-4.7 Hg – 0.07-0.18 As - BDL Cd – 0.2 Cr – 0.1-0.8 Cu – up to 13.1 Hg - BDL Pb – up to 0.28
Shiyab (2018) Zafarzadeh et al. (2018)
Latif et al. (2018)
Pajević et al. (2018)
Ali et al. (2017)
Pan et al. (2016)
Ramteke et al. (2016)
Antisari et al. (2015)
Sri Ganganagar, Rajasthan, India
Hyderabad
Fe, Mn, Cu and Zn
Zn, Cr, Cu, Ni, Pb and Co
Raphanus sativus, Spinacia oleracea, Brassica rapa, Solanum melogena, Brassica oleracea, Coriandrum sativum, Trigonella foenumgraecum, Daucus carota Spinacia oleracea, Amaranthus graecizans, Coriandrum sativum, Mentha spicata, Abelmoschus esculentus, Solanum melengina
Edible parts
Fe – 111-333 Mn – 20.7-50.7 Cu – 10-73.8 Zn – 4.8-22.5
Arora et al. (2008)
Edible parts
Zn – 1.1-11.2 Cr – 0.10-3.1 Cu – 0.1-1.7 Ni – 0.1-3.6 Co – up to-0.17 Pb – 0.60-4.1
Chary et al. (2007)
* Represents the average value of metals in all vegetable samples collected in particulate study **Chinese cabbage, cabbage, spinach, wax gourd, zucchini squash, cauliflower, cucumber, cowpea, water bamboo shoot, Chinese chive, swamp cabbage, radish, pumpkin, eggplant, celery, brassica chinensis, sweet pepper, romaine lettuce, sponge gourd, kidney bean, crown daisy, potato, lettuce, tomato, broccoli, amaranth, coriander, pakchoi
The quantification of heavy metals accumulated in the food chain are assessed by using several factors or indices such as trophic transfer factor (TTF), biota-sediments accumulation factor (BSAF), transfer factor (TF), metal transfer factor (MTF), accumulation factor (AF), bioaccumulation factor (BAF) and bio-concentration factor (BCF) (Table 3). The BCF and BAF of HHMs are usually tissue-specific factorsthat provide a significant inverse correlation with concentrations of contaminated HHMs (Kumar et al., 2010). BAF and TTF values alone cannot be used for the expression of bioaccumulation and trophic transfer without considering the contaminated concentration (DeForest et al., 2007). In the case of plants, the soil-to-plant TF and, BAF in animals, are more relevant for the trophic transfer of HHMs. In plants, poisonous metals are transferred to the plant from the abiotic environment only (mainly soil), while in animals, metals are obtained from both the biotic and abiotic environments (Ali and Khan, 2018; Mehmood et al., 2019). The bioaccumulation load of HHMs can be calculated by the equation 2 (Yarsan and Yipel, 2013): Bioaccumulation = (Bioconcentration + Food chain transfer) – (Elimination + Growth dilution)…………eq (2). 16
Table 3. Quantification of
HHMs at trophic levels in food chain
Factor
Equation
Trophic transfer factor (TTF) Transfer factor (TF) Metal transfer factor (MTF) Accumulation factor (AF)
TTF = Metal conc. in organism tissue/ Metal conc. in the organism food TF = Conc. of metal in plant tissue/ Conc. of metal in soil MTF = Metal concentrations in plant/ Metal concentrations in soil AF = Conc. of metal in plant edible part/ Conc. of metal in soil BAF = Conc. of metal in organism tissue/ Conc. of metal in abiotic medium BSAF = (Metal conc. in experimental organism tissues - Metal conc. in the control organism tissues)/ Metal conc. in water BSAF = Metal conc. in the organism/ Metal conc. in sediments BMF = Metal conc. in the organism/ Metal conc. in the organism’s diet TMF is calculated from the slope of logarithmically transformed metal concentrations in organisms plotted against the trophic levels of the organisms in the food web
Bioaccumulation factor (BAF) Bio-concentration factor (BCF) Biota-sediments AF (BSAF) Biomagnification factor (BMF) Trophic magnification factor (TMF)
Reference DeForest et al. (2007) Cui et al. (2004) Jan et al. (2010) Balkhair and Ashraf (2016) Mortuza and AlMisned (2015) Chalkiadaki et al. (2014) Ziyaadini et al. (2017) Yarsan and Yipel (2013)
Conder et al. (2012)
It is well known that most of the heavy metals are toxic to living beings (Peralta-Videa et al., 2009; Gupta et al., 2018). The metals from their parent material are released into soil, water and air. In soil, these HHMs are present in soluble, non-soluble and partially soluble forms, where the soluble forms are particularly toxic because they are easily absorbed by plants via roots before distribution throughout the entire plant body. Toxic effects of metals are due to the interruption of cellular biochemical pathways (Table 4) (Onakpa et al., 2018). When poisonous metals are ingested in the stomach via contaminated foods, they are converted to their stable oxidation states in the acid medium and fuse with certain proteins and enzymes. The stabilized metallic compounds react with the sulphydryl groups (-SH) of cysteine and sulphur atoms of methionine (-SCH3) in amino acids thereby prompting the degeneration of protein molecules (Ogwuegbu and Ijioma, 2003). Humans can take up As in various ways including inhalation, smoking, water and food. When the direct exposure of toxic elements is not present, these elements can have poisonous 17
effects on the population of a particular region due to accumulation in the food chain. In humans, crops plants are primary sources for the entrance of HHMs. The mobility and availability of HHMs in the environment primarily depends on speciation and its chemical form. The arsenite, As(III) form of As is less mobile but has been recognized as more toxic than the arsenate, As(V) form (Caruso et al., 2001; Yadav et al., 2019b). Arsenite binds to sulfur-containing enzymes and proteins and the thiol groups from phytochelatins in plants, whereas arsenate attaches to the amino or reduced nitrogen groups (Kumaresan and Riyazuddin, 2001). Detoxification of As happens through methylation of As(III) which is highly metabolized by humans and originates from some organo-arsenic compounds like monomethylarsonic acid (MMA), dimethylarsinic acid (DMA), and trimethylarsine. These compounds are recognised to be cancer promoters (Zhou et al., 2003). Arsenic uptake by plants from soil solution in As(V) form occurs via phosphate transport channels because of its similarity to phosphate ions (Tripathi et al., 2007). After uptake, it affects oxidative phosphorylation and ATP synthesis and forms complex compounds with sulphur containing molecules (Tripathi et al., 2007). Arsonate is converted into As(III) inside plant tissues and becomes transformed into less toxic compounds like MMA, DMA and other complexes. Dhanker and co-workers (Dhanker et al., 2006) found that many plants can produce enough arsenate reductase enzyme, which reduces most of the arsonate to arsonite. Arsenic was mobilized within plant compartments as the soluble fraction and chelated with cyclohexylenedinitrotetraacetic acid, or As-sulfur complexes (Lopez et al., 2008). The principal source of Cd intake in humans is through smoking and food (Jarup, 2003). Cd can pose dangerous environmental risks because it can be absorbed via the digestive tract,
18
penetration through the placenta during pregnancy, and imparting damage to cellular membranes and DNA (Kabata-Pendias, 2004). Another consideration is that HHMs might be harmful to humans and animals but not phytotoxic within plant tissues (Peijnenburg et al., 2000). The differences between the electrochemical potential gradient of the plasma membrane in plant roots and concentrations of HHMs provide the passage for entry of these toxins into plant root cells (Blaylock and Huang, 2000). Cd is transported in mammals as a Cd-metallothionein, a Cdprotein complex which is stored in liver, intestinal mucosa and kidneys (Cooke and Johnson, 1996) with a retention time of 10 years (Pokorny and Ribaric-Lasnik, 2000). The absorption of Cr from soil takes place by reduction and complexation with root exudates, like organic acids, which enhance the solubility and mobility of Cr through the root xylem tissues (Bluskov et al., 2005). However, Cr is poorly translocated in aerial plant fractions (James and Barlett, 1983). The most stable and common oxidation states of Cr are Cr+3 and Cr+6. Cr+6 is the most toxic species because it has high solubility, higher oxidizing potential, and effective mobility (Marqués et al., 1998). Cr+6 increases the formation of reactive oxygen species (ROS) which cause damage to several metabolites. In crops, Cr at low concentrations (0.05-1mg/L) was found to promote growth and increase yield. Conversely, when the Cr level is increased to 15mg/L, alterations in metabolic processes occurs including growth inhibition, decrease of chlorophyll synthesis, and chlorosis (Dube et al., 2003). Table 4. Toxic form of metals and their harmful effects on plants and humans HMs
As
Cd
Toxic Form +3
As+3, DMA, MMA, As2S3 and As2O5
+2
Cd+2-deoxymugineic acid, Cd–phytochelatins
As
Cd
Form Present in Plants
Major Effects
Human
Plant
Cardiovascular, neurologic and developmental anomalies, portal fibrosis, hematologic disorders and carcinoma Bone demineralization, renal dysfunction, impair lung function and increase
Stunted growth, reduction in seed germination, seedling height, leaf area and dry matter production Reduction in seed germination, plant nutrient content and
19
Reference Abbas et al. (2018); SignesPastor et al. (2019) Loi et al. (2018)
the risk of lung cancer
Cr
Cr+6
Chromium acetate, Chromium phosphate, Chromium nitrate
Pb
Pb+2
Pb-phytochelatins, Pb-acetate, Pbnitrate, Pb-sulfide
Hg
Methylmerc ury (MeHg)
Hg , MeHg
Gastrointestinal, neurotoxicity, carcinogenesis and nephrotoxicity
Ni
Ni salts and dust
Chelated Ni compounds
Vomiting, diarrhea, dermatitis, risk of lung and nasal cancers
Cu
Cu salts, dust and fumes
Chelated Cu compounds
Zn
Zn
+2
+2
Chelated Zn compounds
Multi-organ toxicity, nose ulcers and cancer of the respiratory tract
Kidney failure, affect CNS and PNS, damage to the reproductive systems
Damage the liver and kidneys, hematemesis, hypotension, melena and gastrointestinal discomfort Cytotoxicity, haematological change, harmful effect on growth, neuronal development and immunity
reduced shoot and root length Decrease in plant nutrient acquisition, inhibition of germination process and reduction of plant biomass Decrease in plant protein content and inhibition of enzymes activity Reduction in germination percentage, plant height, flowering and fruit weight, chlorosis and reduced tiller and panicle formation Impede shoot and root growth, injure various plant parts, induce leaf spotting and produce Fe deficiency
Medda and Mondal (2017)
Zhou et al. (2018)
Azevedo et al. (2018); Gardner et al. (2010)
Ahmad, and Ashraf (2012)
Injury to plant roots and deformation of root structure
Sheldon and Menzies (2004)
Adverse effect on enzymatic activities, stunted growth and reduced yield
Plum et al. (2010), Maurya et al. (2019)
The mechanism of Pb mobility in plants is less understood (Clemens and Ma, 2016). Pb enters the food chain primarily through the discharge of metal smelting industries (Caussy et al., 2003), agriculture and urban developmental activities (Marchiol et al., 2004). Plants do not have any specific routes for Pb intake. For examples in soil, Pb can be bound to complex compounds such as carboxylic groups of mucilage uronic acids in the rhizosphere (Sharma and Dubey, 2005). Plant roots are the first barrier for Pb uptake via translocation to upper portions of plant bodies (Blaylock and Huang, 2000). After crossing the root cell membranes, Pb binds to ionexchangeable sites within the cell walls and extracellular precipitation occurs resulting in
20
phosphate and carbonate compound formation (Blaylock and Huang, 2000; Sharma and Dubey, 2005). The free or unbound Pb is passed in Ca channels accumulating near the endodermis (Antosiewicz, 2005). In humans and mammals, the primary route of exposure to lead is via the contaminated food chain (Ma, 1996). The toxicity of Pb is determined by its complexation with other compounds within tissues (ATSDR, 2007). In blood serum for example, Pb is bound to proteins or low molecular weight sulfhydryl compounds such as cysteine and homocysteine, citrate, cysteamine, ergothioneine and glutathione (ATSDR, 2007). In Hg exposure, plant-derived food plays only an insignificant role, except in regions with high Hg contamination of agricultural soils (Rothenberg et al., 2014). The primary source of Hg exposure risk to humans and animals is through ingestion of contaminated food and agricultural products (Doty, 2008). Methylmercury is more toxic and more bioavailable than inorganic Hg, and is taken up by humans and animals dominantly through seafood, because methylmercury readily bioaccumulates through aquatic food chains (Moore et al., 2014). Guzzi and La Porta (2008) observed that approximately 95% of methylmercury ingested by fish is absorbed into the gastrointestinal tract. In some plants, like corn, Hg binds to root tissues and reduces the translocation in the plant body and reduces bioaccumulation and toxic effects on human health. Fig. 1 shows the toxic metal transfer and bio-accumulation through the food chain. This study was demonstrated in a garden used for crop production nearby Ori-Ile battery waste dumpsite, Omilende Area, Olodo, Nigeria. A high concentration of Pb and Cd was observed in the garden topsoil that ultimately bio-accumulated in roots, stems, grains and leaves of maize via the food chain. The contaminated maize grains consumed by humans and animals finally biomagnified in fatty tissues and created health problems (Afolayan, 2018). 21
Fig. 1. Heavy metal transfer and bio-accumulation through food chain (The study was carried out in a garden nearby Ori-Ile battery waste dumpsite, Omilende Area, Olodo, Nigeria, Afolayan, 2018
22
5. Mechanistic approach of hazardous heavy metals transportation in vegetables The HHMs present in soil organic matter are taken up by vegetables and become critical in the form of cations when bonded to short chains of carbon atoms (Manzoor et al., 2018). The mechanism of heavy metal transfer from soil to plant is depicted in Fig. 2. The uptake of toxic metal from the soil depends on the soluble cations and anions, soil pH, plant species, pesticides, fertilizers and soil type. Vegetables and/or other plants act as accumulators and indicators of survivability despite a high concentration of HHMs in their aerial tissues and excluders. Plant survival increases when biodegradation or biotransformation of the contaminants into inert forms occurs effectively within their tissues. HHMs are actively mobilized from the soil or the apoplast to the plasma membrane of root cells in root hairs. Translocation of the uptaken metals to the shoot is dependent on barriers, vacuoles, and the upward mobility in the xylem and phloem (Meng et al., 2011). Distribution in different plant organs is a function of phloem loading and unloading, and mobility and the efficiency of xylem-to-phloem transfer of elements (Mendoza et al., 2011). Bacteria produce MMA (monomethylarsonic acid) and DMA (dimethylarsinic acid) in the rhizosphere, however, that is not enough to initiate methylation of As in plants. Particular enzymes like Sadenosylmethionine-dependent arsenite methyltransferase catalyze As and also play an essential role in the biogeochemical cycling of As. Both toxic nonessential and essential elements move into a plant through the same pathways (Zhu et al., 2014). For the mobilization and transfer of metals from one compartment to another compartment of cells and plant parts, several metal transporters are involved: OsNramp5, OsHMA2, OsHMA3, NIP, Lsi1, Lsi2, PT, ABC, HAC1, MMA and DMA (Clemens and Ma, 2016). To illustrate, in rice plants, OsNramp5 confined at the distal side of both the exodermis 23
and endodermis, is responsible for the transport of Cd from the apoplast to the rice root cells (Sasaki et al., 2012). In vacuoles of a tonoplast, OsHMA3 sequesters Cd, and OsHMA2 sequesters Cd at the plasma membrane of pericycle cells (Clemens et al., 2013). In rice fields, under anaerobic conditions, As(III) is the dominant form in the soil. Arsenate is taken up through phosphate transporters (PTs) and then reduced to arsenite by As(V) reductases such as HAC1 in Arabidopsis thaliana (Chao et al., 2014). In the rice plant, Oryza sativa, arsenite uptake occurs by the aquaporin Lsi1, and in Arabidopsis thaliana uptake is facilitated by nodulin 26–like intrinsic proteins (NIPs) (Ma et al., 2008; Li et al., 2009, Zhao et al., 2010). Some other metal transporters like ABC transporters (AtABCC1 and AtABCC2) in A. thaliana and OsABCC1 in O. sativa, sequester As and form phytochelatins complexes (As-PCs) in the vacuole. The Lsi2 transporter in rice effluxes the remaining As(III) in the xylem. In rice additionally, arsenate is transported towards the stele by two Si transporters like Lsi1 and Lsi2, and these are located at the distal and proximal sides of the exodermis and endodermis. Arsenic forms phytochelatins with OsABCC1 transporters in the tonoplast and sequesters toxins as As-phytochelatins (As-PCs) complexes in the vacuoles restricting the availability of As(III). The sequestration of HHMs can restrict the movement in the root toward the xylem. This was confirmed by the badge of P1B-type ATPase in rice (OsHMA3) as the primary determinant of Cd root-to-shoot translocation (Miyadate et al., 2010). Long distance transfer of HHMs between plant organs takes place via the xylem and phloem loading (Ma et al., 2007; Ma et al., 2008). The accumulation of HHMs in leaves occurs mainly through uptake by xylem-loading and in seeds and fruits by phloem-loading. More investigation is required to elucidate more obvious pathways of metal transport in plants (Khan et al., 2014; Olsen and Palmgren, 2014).
24
Fig. 2. Transfer and bio-accumulation of HHMs in different plant parts (modified from Clemens and Ma, 2016; Peralta-Videa et al., 2009) *OsNramp5, OsHMA2, OsHMA3, NIP, Lsi1, Lsi2, PT, ABC, HAC1, MMA and DMA are metal transporters in plants for the transport of plant parts, vacuoles and cells.
25
HHMs in different
6. Hazardous heavy metal management by nanotechnological approaches With the accelerated advanced development in nanoscience, unique possibilities have arose to develop more cost-effective, environmentally safe and sustainable remediation processes (Adeleye et al., 2016). In the last few years, nanotechnological tools have been increasingly used in soil, soil sediments, solid waste and wastewater remediation. Nanoparticles ranging from 1100 nm in size, known are applied in several remediation processes that allow nanotubes, nanosheets and nanolayers to be utilized as treatment material. Nanoparticles, (NPs) nanomaterials (NMs) or nanoadsorbents could provide very high adaptability for both in situ and ex situ remediation of pollutants. Nanotechnology can help clean up polluted water by employing nanoscale biosensors to detect contaminants in surface and groundwater, and improving the efficiency of chemical and photo-catalytic processes. Nanosized compounds come in a variety of forms such as NPs, nanofilms, nanowires, quantum dots, nanotubes and various colloids (Anjum et al., 2016; ). NM characterization is listed in Table 5. Recently researchers focused on the synthesis and surface functionalization of nanoparticles (sizes less than 50 nm) which have a huge potential as adsorbents of contaminants like heavy metals, organic pollutants and dyes from polluted waters (Bobik et al., 2017). Iron oxide NPs have been synthesized in top-down and bottom-up approaches. The seldom used “top-down” approach is based on crushing or grinding of hostmaterial in ball mills. The “bottom-up” approach is more prevalent and based on the chemical syntheses of nanomaterials such as pyrolysis, chemical precipitation, the sol-gel method, co-precipitation, reverse micelles, magnetic nanocomposites, micro-emulsion, polyols method, sonolysis, gas-aerosols, electrochemical decomposition, flow injection syntheses, electrospray syntheses and thermolysis of precursors or hydrothermal reactions (Khan et al., 2011; Cui et al., 2013; Li et al., 2013; Fajaroh et al., 2008;
26
Wu et al., 2008; Ahmad et al., 2017). Amongst the several emerging technologies, the progress and versatility in nanotechnology has confirmed an incredible potential for the remediation of pollutants and HHMs in the environment (Gupta et al., 2015). These methods are dynamic, require less time, possess broad applicability, and pose good economic expediency (Wernisch et al., 2013). The categoris of nanomaterial are classified in Table 6. The application of NMs or nanoparticles has gained enormous attention due to their size and large surface area to unit mass ratios, short intra-particle diffusion distance, magnetic properties, surface modifiability, biocompatibility, tunable surface chemistry, increased adsorption sites, reusability, increased porosity, higher gas permeability, ease of separation, enhanced catalytic activity, greater dispersion degree, and comparatively low cost of manufacturing (Ali, 2012). Nanoremediation methods involve the use of potential NMs for transformation, treatment, stabilization and detoxification of contaminants. Various nanomaterials have been tested to remediate metal concentrations like nano catalysts, CNTs, graphenes, nanoscale metal oxides, nanomembranes, carbon nanotubes, nanobiological processes, and zero-valent iron (FeO), Fe2O3, Fe3O4, TiO2, SiO2, and Al2O3 (Anjum et al., 2016; Saad et al., 2018; Hosseini et al., 2019). Several adsorbents such as activated carbon, silica, clay materials, metal oxides, magnetic iron oxide nanoparticles (MNPs), nano-titanates, alginate biopolymer and their composites have all been utilized to remove the harmful heavy metal ions (Yong-Mei et al., 2010; Yadav et al., 2017a; Yadav et al., 2019). Nano-adsorbence can be performed using atoms of certainelements which are chemically active with a high surface adsorption capacity (Kyzas and Matis, 2015).
27
Table 5. Characterizations of nanoparticles/nanoadsorbents and their removal efficiencies of heavy metals Nanoparticle Species
Iron oxides NPs
Fe3O4 Synthetic Fe7S8 nanoparticles
Property
NP Synthesis
HM Species Remediated
Absorbent Dose (g/L)
Optimum pH
Magnetite nanoparticles
Co-precipitation from a mixture of Fe(II) and (III) salts with aqueous NH3 and KOH
Cr(VI), Pb(II), Cr(III), Cu(II), Zn(II), Ni(II) and Cd(II).
50mg/20cm3
5.31-9.37
Coating
Zn(II)
0.80
6
>94%
solvothermal synthetic method Modified co-precipitation synthesis Hydrothermal method
As (III) and As (V)
-
4
Up to 98%
Cd(II), Cu(II) and Pb(II)
0.008
-
Cd(II) up to 32.3% Cu(II) up to 23.8% Pb(II) up to 38.1%
Klekotka et al. (2018)
Cr(VI)
0.80
2
93%
Lu et al. (2017)
Co-precipitation
Cu(II), Fe(III), As(III)
0.15
6.5
Cu(II)-100% Fe(III)-100% As(III)-98%
Esmat et al. (2017)
-
Cr(VI)
0.10
3-9
100%
Huang et al. (2015)
V (vanadium)
0.15
-
73%
Mthombeni et al. (2015)
Cr(VI) and Hg(II)
-
-
Cr(VI)-92% Hg(II)-upto 80%
Stefaniuk et al. (2016)
Magnetite nanoparticles High binding capacity
Ferrite nanoparticles MoS2/Fe3O4/nZVI nanocomposites Cobalt ferrite nanoparticles Magnetic multi-wall carbon nanotubes
Synergistic effect for adsorption High surface area and greater adsorption capacity Large specific surface area and high reaction activity
Magnetic zeolite-polymer composite
Monolayer adsorption
Chemical co-precipitation of Fe3+ and Fe2+ ions at a ratio of 2:1 in the presence of zeolite
Zero-valent iron (ZVI)
Reducing agent and good adsorbent
Abrasion and grinding
28
HM Removal Efficiency (%) Cr(III)-66-77%, Cr(VI)- >90%, Cu(II)-26%, Pb(II)76-92%, Zn(II)26%, Ni(II)-14%, Cd(II)-21%
Reference
Bobik et al. (2017)
Helal et al. (2010) Cantu et al. (2016)
Magnetic nano-particles coated zeolite
High adsorbing capacity
Using magnetic nanoparticle (Fe2O3)-coated zeolite (MNCZ)
As(III)
0.50
2.5
95.6%
Attia et al. (2014)
Titanate nanotubes
High surface area and greater adsorption capacity
Co-precipitation
Cu(II), Fe(III), As(III)
0.15
6.5
Cu(II)- 99.9% Fe(III)-100% As(III)- 98%
Esmat et al. (2017)
Hydrolysis of titanium sulfate solution
As(III)
0.20
9.5
>98%
Pena et al. (2006)
Multifunctional flexible freestandingNa-TNB membrane by vacuum filtration
Sr(II), Cs(II)
25-50
-
Sr(II)-97.5% Cs(II)-57.7%
Wen et al. (2016)
Nanocrystalline titanium dioxide
Sodium titanate nanobelt membrane (Na-TNB)
Negatively charged inner-sphere surface complexes Ion-exchange properties with greater selectivity for target cations and higher adsorption capacity due to large surface area
TiO2 Engineered Nanoparticles (ENs)
Surface adsorption and internalization
Polyacrylatecoated TiO2-EN
Cd(II)
0.10
2
Activated carbon NPs
High surface area and greater adsorption capacity
-
Fe, Pb and Ni,
0.02
2-10
Fe up to 99%, Pb up to 87%, Ni up to 96%
Hegazi (2013)
Nano sized ZVI (NZVI)
High adsorbing capacity
Reduction of ferric chloride by sodium borohydride
As(III)
1.0
7
99.9%
Rahmani et al. (2011)
Nano scale zero valent iron (nZVI)
High surface area and cation exchange capacity
Reduction of Fe (II) using borohydride
Cd(II) and Pb(II)
-
-
-
Mohammed et al. (2018)
29
> 20%
Yang et al. (2012)
Starch stabilized zerovalent iron nanoparticles (nZVI-Starch)
Larger surface area for sorption reactions
Chemical reduction method
Pb(II)
1g/kg soil
4.2
100%
Okuo et al. (2018)
ZnS nanocrystals
High cation exchange capacity
Direct coating ZnS NCs on the surface of the αAl2O3nanoparticles
Hg(II)
10
1-6
99.99%
Qu et al. (2014)
ZIF-8 nanoparticles
Ultrahigh surface area, tunable pore structures, high crystallinity and designable organic ligands
Rapid synthesis in aqueous solution
As
0.20
7
60%
Jian et al. (2015)
Graphene nanosheets (GNS)/d-MnO2
Chemical exfoliation
Ni (II)
5.0
-
77.04%
Varma et al. (2013)
Zeolite materials obtained from fly ash Pyromellitic acid dianhydride/ N-(3(trimethoxysilyl) propyl ethylene diamine (PMDA/TMSPEDA) Chitosan-modified multi-walled carbon nanotube composite
Greater specific area Bound heavy metal ions via co-ordinate and electrostatic interactions Chitosan is a cationic biopolymer, high hydrophilicity
Pb(II)
6.0
5.6-6.6
>80%
Visa (2016)
Ring opening polymerization and sol-gel reaction
Pd(II), Cu(II), Zn(II)
0.01
7
Pd(II)-79.60% Cu(II)-72.36% Zn(II)-66.80%
Alsohaimi et al. (2015)
Heating and mixing
Cr(VI)
0.05
2
98-100%
Huang et al. (2018)
Modification macro-particles of Jordanian raw kaolin clay by hydrochloric acid and hydrogen peroxide
As(V)
0.5
8
98.45%
Amer and Awwad (2018)
Nanocrystalline kaolinite
High adsorption efficiency
Nanocomposite of MnO2 loaded on graphene nanosheet Hydrothermal process
30
Ag and Zn nanoparticles functionalized cellulose
High catalytic activity, great biocompatibility, high adsorption capacity, high surface-area, reusability and greater dispersion degree
Co-precipitation method
Hg(II), Cr(III), Co(II), Pb(II), and Ni(II)
0.5 and 1.0
5.5
Hg(II) >Ni(II) >Cr(III) >Co(II) > Pb(II)
Ali et al. (2018)
ZnO@Chitosancoreshell Nanocomposite (ZOCS)
Hydrophilicity, biocompatibility, biodegradability, non-toxicity and High adsorption capacity
Direct precipitation followedby thermal decarbonation
Pb(II), Cd(II) and Cu(II)
0.02
4 (Cu), 6 (Pb) and 6.5 (Cd)
Pb(II) up to 99%, Cd(II) up to 98%, Cu(II) up to 96%
Saad et al. (2018)
ZnO-Fe3O4 nanocomposites
High adsorption capacity and surface area
Chemical co-precipitation
Pb(II) and Cu(II)
0.50
5.5
Pb(II) up to 39.2%, Cu(II) up to 37.66%
Goyal et al. (2018)
Polymer functionalized nanocomposites PS – (HFO)(Polystyrene sulfone supported Hydrated Iron (III) Oxide)
High surface area
grafting NPs into polymer structures
As(V)
0.01
3
95%
Nie et al. (2013)
31
Table 6. Categories of nanomaterials (NMs) and their applications for HM remediation Nanomaterial (NM)
NM Species
Composition of NM
Oxides NPs
Metallic and mixed
Multi-wall CNT and modified magnetic CNTs
Carbon nanosheets (CNSs)
CNSs combined with metal ions or metal oxides
Nanofibers
Aminated polyacrylonitrile nanofiber mats
Surface modification of e-spun PAN with DETA (diethylenetriamine)
Nano clays
hydrous aluminosilicates
Kaolinite and montmorillonite
Graphene NM
Carbon NPs
Graphene oxide (GO)
Adsorption of HMs
Magnetic NPs (MNPs)
Iron oxide NPs Polymer-functionalized nanocomposites (PFNCs)
Fe3O4-gum-arabic S-PFNCs and B-PFNCs (Polymer-functionalized nanocomposites) SiOx layers on beryllium deposition
Removal of Cr(VI)
Polymer NMs
Aerogels NM NMs as photocatalyst Photocatalysts as antimicrobial agent Nano-catalysts NMs as electrocatalysts Nano-material based Fenton catalyst Fouling and membrane modification
Au hydrogel with Au nanoparticles Semiconductor metals with NPs
Feng et al. (2012) Ren et al. (2011) Wang et al. (2012) Kampalanonwat and Supaphol (2014) Bhattacharyya and Sen Gupta (2006) Lingamdinne et al., 2016 Elfeky et al. (2017) Lofrano et al. (2016)
Wastewater treatment
Castrucci et al., 2006
Nanoscale Si grown on Ag
Wastewater treatment
Grazianetti et al. (2017)
Au aerogels
Adsorption of HHMs
Gurav et al. (2010)
ZnO:Co, ZnS:Mn, ZnS:Cu, ZnSe:Mn, ZnS:Pb
(Fe2O3/SiO2)
Removal of POPsand HMs from wastewater Biological wastewater treatment (mainly bacteria) Wastewater treatment and electricity generation Oxidation of organic pollutants
-
Wastewater treatment
Silicon nanotubes Silicon nanosheets
Reference
Removal of HMs from wastewater
Silicon NMs
Nano-membranes
Applications HM removal from wastewater RemovalHMs organic contaminants from wastewater Removal of HMs from wastewater Removal of Ag(I), Cu(II), Pb(II) and Fe(II) from aqueous solution Removal of Co, CU, Fe and Pb
Carbon nanotubes (CNTs)
Carbon NMs
Nano-adsorbents
Functions Tioxides, Zn oxides,Mg oxide, Mn oxidesand Fe oxides
Ag nano-particles on TiO2 films
Ag/TiO2
Pt nanocatalyst supported by carbon black XC72 Heterogeneous MFe2O4 NM Mixed matrix membranes (MMMs)
Microbial fuel cells
32
Adeleye et al. (2016) Akhavan (2009)
Chen et al. (2015) Ferroudj et al. (2013) Rajabi et al. (2013)
Carbon nanotube membranes
Electrospun nano-fiber membranes
with carbon nanotubes (CNTs) Polyether urethane (PEU) membranes filledwith isophorone diisocyanate grafted with multi wall carbon nanotubes (MWCNT-IPDI) Polymer composite membranes,single and multi-walled carbon nanotubes (SWCNTs/MWCNTs) Electrospuning of natural and synthetic polymers like PVC, PS, PVDF (Polyvinylidene Fluoride) and PBI (Polybenzimidazole) Impregnated polysulfone (PSF) with zeolite nano-particle membrane
-
Wastewater treatment
Deng et al. (2007)
Carboxyl multi-walled carbon nanotubes/calciumalginate (CMWCNT/CA)
Treatment of contaminated water
Liu et al. (2016)
Graphene doped polyacrylonitrile/polyvinylidene fluoride electrospun nanofiber
Cr removal and wastewater treatment
Qu et al. (2013) Yadav et al. (2019a)
Zeolite NP-PSf
Removal of Pb and Ni form wastewater
Yurekli (2016)
Na-TNBM
Sr2+ removal
Wen et al. (2016)
Hybrid nanomembranes Sodium titanate nanobelt membrane (Na-TNB)
Nano-Biotechnological processes
Composites of NPs
Algal membrane bioreactor (A-MBR) with NP
Algae with nano fibers and NP
CNTs with TiO2 NP and Polysulfone (PSF) fibre
HM removal from wastewater
Abou-Shanab et al. (2013)
Aerobic digestion with NPs
Aerobic degradation with ZVI NPs
-
Municipal and industrial wastewater treatment
Ma and Zhang (2008)
-
-
HM removal from wastewater
Anjum et al. (2016)
ZVI NPs with
CMC/Fe2+
Removal of Cr (VI)
He et al. (2007)
Titanium oxide/dendrimers composites Composites of
33
stabilized ZVI Nanoparticles Bentonite clay iron oxide composite Chitosan montmorillonite-Na Calcined kaolin and bentonite Mixed clay fluoroapatite
carboxymethyl cellulose (CMC) and polyacrylate (PAA) -
-
Removal of Cu, Cd and Zn
Etci et al. (2010)
-
-
Removal of Cr
Pandey and Mishra (2011)
-
Removal of As
Dousov et al. (2009)
-
Removal of Cd, Cr, Zn, Cu, Hg and Pb
Sajidu et al. (2006)
Pretreated with Fe2+, Fe3+, Al3+ and Mn2+ Illite, kaolinite, mixed layer minerals and nonclay mineral carbonate
Bentonite polyacrylamide composite
-
-
Removal of Cu
Zhao et al. (2010a)
Dendrimer-based nanocomposite
Dendrimer-based magnetic nanoparticles
Magnetic hyperbranched polyol-modified graphene oxide (GO)
Removal of Zn(II) and Pb(II)
Hu et al. (2016)
34
6.1. Nanomaterial induced phytoremediation of hazardous heavy metal Many remediation processes can convert the hazardous heavy metals into less hazardous heavy metals or stabilize in the soil over a time period. But phytoremediation coupled with NMs is a novel technology that can separate the extract, degrade, modify, sequester, and stabilize a broad category of soil contaminants (Ali et al., 2013; Gong et al., 2017; Yadav et al., 2018). The synergistic and antagonistic influences of merged remediation techniques have been exhibited as an efficient process to decontaminant of pollutants due to the diverse responses of plants to NPs and the variable influence of NMs on soil contaminants (Mahar et al., 2016). The effects of NMs on the phytoremediation of heavy metals and organic pollutants contaminated soils were given in Table 7. The removal of toxic material from soil occurs due to co-uptake between NMs and the contaminants. The NPs suitability for particular plants should also be considered because when NPs enter into plants through absorption, they can damage the cell membrane and cell walls, resulting in the loss of membrane integrity or turgidity and cell function, consequently promoting the introduction of contaminants from soils into plants body (Gong et al., 2017). Researchers have shown NMs can enhance the accumulation of metals by three approaches: (i) improvment in the permeability of the cell wall, (ii) co-transportation of NMs and heavy metals, and (iii) regulation of transporter gene expression. Graphene oxide (GO) is a nanomaterial that has been studied in the removal of heavy metals from soil to enhance the uptake of As in wheat. GO can enhance the reduction of plant biomass, the number of roots exposed to toxins, disturbing the urea cycle and fat metabolism, by transforming arsenate to arsenite thereby reducing oxidative stress in wheat seedlings as compared to the exposure of heavy metals without remediation alone (Hu et al., 2014). Gil-Dıaz and co-workers (Gil-Diaz et
35
al., 2016) found that the use of 10% nano-zerovalent iron (nZVI) decreases the uptake of As in plant parts (root and shoot), and raises the height and dry weight of barley plants under metal stress. The application of titanium dioxide (TiO2) NPs improved Cd accumulation from polluted soils, and reduced Cd toxicity by enhancing photosynthesis rate and plant growth in soybeans (Singh et al., 2016). The uptake of iron oxide NMs by wheat plants mitigated the toxicity of Cd(II) and Cr(VI) in the crops (Lopez-Luna et al., 2016). The efficient remediation process depends on the types of metal contaminattion, and levels of contamination, which nanomaterial used and on what plant species. 6.2. Heavy metal removal mechanism of nano material Nanomaterials exhibit particular properties due to their large number of particles, high surface area to volume ratio, specificity for particular toxic metal, magnetic separation, surface chemistry and surface interactions (Lakshmanan, 2013). Several NMs such as carbon nanotubes (CNTs), nanocages, nanocrystals, nanowires, nanoflakes, silica NPs, cellulose nanocrystals and nanofibrils, fullerenes, hydroxyfullerenes and heterofullerenes are depicted in Fig. 3. As discussed previously, NMs can be manufactured using the bottom-up approach to form polymers and biopolymers, metals and their oxides and hydroxides, ceramics and derivatives of carbon (Heimann et al., 2015) by several processes we listed earlier (Chen and Mao, 2007). Adsorption processes using nanoadsorbents on oxides of Zn, Cu and Fe, are highly dependent on pH. To illustrate, enhanced elimination of HHMs from aqueous solutions occurred with increased pH levels due to electrostatic interplays, precipitation and formation of covalent bonds to different functional groups. A raise in the pH supports the deprotonation of nanosorbent surfaces, thereby increasing the concentration of the negatively charged sites on and
36
nanoadsorbent material. This further increases the attractive forces between positively charged ions and the negative sites on the nanoadsorbents (Mahdavi et al., 2012). Superparamagnetic iron oxide nanoparticles (SPIONs) have large surface area-to-volume ratios, are less toxic, chemically inert, can be rendered biocompatible, allow small diffusion resistance, and their surfaces can be modified with organic/inorganic functional groups rendering their surfaces biocompatible and possessing increased potential for eliminating HHMs. The functional groups –COOH, -NH2, -OH and –SH provide active active sites for the replacement of toxic metal ions. Physical interactions (such as electrostatic and Vander Waal’s forces) and chemical interactions (such as chemical binding, complex formation and modified ligand combination) are responsible for the adsorption of toxic metal ions onto the nanoadsorbant (Wang et al., 2012; Patwardhan, 2012). CNTs express novel properties due to their high porosity, light mass density, large specific area, the hollow structure and active interactions with HHMs (Dresselhaus et al., 2001). The adsorption mechanism is mainly governed by the chemical interactions between the surface functional groups (–OH, –C=O and –COOH) and the toxic metal ions (Gadhave and Waghmare, 2014). Chitosan also exhibits unique characteristics, such as being chemically stable, biodegradable, biocompatible and hydrophilic. The adsorption capacity of HHMs is due to the presence of amine groups (–NH2), which attract metal ionsin solution (Jassal et al., 2015). Si coating stimulates the surface functional groups on the NPs due to the abundant presence of silanol groups on the silica layer (Patwardhan, 2012).
37
Table 7. NP-induced phytoremediation of heavy metal contaminated soils
NMs
Suitable Dose of NPs for Plants
Plant Species
HM Remediated
Interaction of NMs
With HMs
Graphene oxide (GO)
0.1-10 mg/L
Triticum aestivum
As
Enhanced As uptake
GO
5 mg/l
Microcystis aeruginosa
Cd
Enhanced Cd toxicity
As
Reduced As availability and decreased As uptake Reduced Cr leachability
nZVI
14-18 g/kg (10%)
Hordeum vulgare
CMC-stabilized nZVI (Carboxymethyl cellulose)
-
Brassica rapa
Cr
TiO2 NPs
100-300 mg/kg
Glycine max
Cd
TiO2 NPs
100 mg/L
Chlamydomonas reinhardtii
Cd
Citrate-coated magnetite NPs
1 g/kg
Triticum aestivum
Cd and Cr
Reducedmetal phytoavailability
Silicon NPs
-
Pisum sativum
Cr
Decreased Cr accumulation
38
Increased Cd uptake Reduced free Cd ion contents, loweredCd bioavailability
Reference
On Plants Decrease plant biomassand root numbers, disrupted fatty acid metabolism and the urea cycle and increase the oxidativestress Increased ROS production and MDA contents and suppressed plant growth Increased plant growth rate and the biomass
Hu et al. (2014)
Tang et al. (2015)
Gil-Díaz et al. (2016)
Reduced bioaccumulation and bioavailabilityand suppressedCr uptake Decreased Cd stress in the plants
Singh and Lee (2016)
Mitigated Cd-induced growth inhibition
Yang et al. (2012)
Reduced the concentration of Cd and Cr Improved plant growth, protein, carotenoids and chlorophyll contents, and decrease ROS production
Wang et al. (2014)
López-Luna et al. (2016)
Tripathi et al. (2015)
Fig. 3. Different nanomaterials and their removal mechanisms
39
7. Biotechnological and genetic approaches of remediation Heavy metal contamination in soil has led to contamination of food and fodder grown on such soils. Through plants, these heavy metals enter the food chain endangering human and animal health. Increases in reports of such contaminants found in foods are proof (Bald et al., 2005). However, when we look for the solution to this problem we have very few options and most of them are uneconomical. Therefore, phytoremediation is emerging as a tool for reclamation of heavy metal contaminated soil by growing metal hyperacumulators in contaminated soils. One argument for phytoremediation states that this technique is economical and eco-friendly but its field application is limited by slow growth and low biomass production ability of the hyperaccumulators (Yadav et al., 2018). During the remediation of HHMs, plants extract heavy metals from soil followed by their stabilization and accumulation in their inactive states. If these HHMs become accumulated above their threshold limit in plant tissue, then these toxins disturb physiological and biochemical processes such as photosynthesis, respiration, membrane integrity and antioxidant defense system. All perturbations of healthy and natural growth and homeostasis have deleterious effects. Research has shown that the most suitable plant for phytoremediation will have an increased heavy metal accumulation rate coupled with rapid growth and greater biomass production ability. The capacity of any plant to extract and accumulate heavy metals is highly governed by its genetic potential as no plant can store heavy metals more than its threshold capacity (Kawashima et al., 2004; Shah et al., 2007; Ovecka et al., 2014). Genetic engineering/manipulation can be used as tools for improvements of the inbuilt genetic potential and phytoremediation ability of any plants according to the needs of the
40
community. Recent biotechnological research in the field of heavy metal remediation has developed transgenic plants possessing improved heavy metal accumulation or remediation capacity compared to their host thus making them more suitable for /phytomining (Duan et al., 2011). This process involves the transfer of genes-of-interest which play a role in heavy metal uptake, transport and accumulation from its efficient donor to host leading to increased tolerance of the host. Phytomining can improve the ability of plants to sense, uptake and accumulate heavy metals. Many studies have been investigated on Arabidopsis, tobacco, Indian mustard, and sugar beets resulting in these plants possessing improved tolerance for heavy metal stress with greater biomass accumulation. However, the success of transgenic modifications in heavy metal remediation is highly dependent on availability of gene sequences. Heavy metal accumulation efficiency is highly dependent on the mechanisms of uptake, translocation, detoxification, sequestration and storage efficiency of plants. In 1989, a Cd-tolerant Nicotiana tabacum transgenic plant was developed by the introduction of a human metallothionein gene by Misra and Gedamu (1989). Table 8 gives details about phytoremediations exploited for the development of heavy metal tolerance with the associated genes governing that trait. Uptake of heavy metals is dependent on root traits since roots are the first and formost directly exposed organ to heavy metal stress and contaminated soils (Hossain et al., 2012) which adversely affects the ability of roots to take up water and nutrients from the soil (Poschenrieder and Barcelo, 1999). Rhizosphere pH determines the mobilization of heavy metals. In acidic PH heavy metals get dissolved in soil water which increases their mobility to plants. Organic acids secreted by roots, however, bind with heavy metals and improve their mobilization and absorption by roots (Singh et al., 2016).
41
Genetic manipulation in uptake, transport and accumulation ability of heavy metals can be made resulting in the overexpression of uptake and mobilization transporter proteins of the plasma membrane such as NRAMP, HMA4, aquaporin, YCF1, ZIP4, IRT1, and CAX4 and the tonoplast can improve metal absorption capacity of the root. Lee and co-workers (Lee et al., 2010) observed that in certain Saccharomyces cerevisiae yeast cadmium factor 1Protein (YCF1) is involved in pumping cadmium (Cd(II)) into vacuoles thereby conferring resistance to Cd and Pb. YCF1 is a vacuolar glutathione S-conjugate transporter, related to the ATP-binding cassette superfamily where it enhances uptake and storage of the HHMs in yeast vacuoles. On overexpression of the YCF1 gene in Arabidopsis thaliana, transgenic lines were able to increase uptake and accumulation efficiency of transgenic plants (Song et al., 2003; Lee et al., 2010). Transporter proteins coded by the AtMRP2 gene have similar functions as the yeast YCF1 gene and also confers Cd tolerance by transporting Cd/glutathione complexes to the vacuole (Li et al., 1996). Arabidopsis ATP-binding cassette (ABC) transporter proteins are vacuolar GS-x pumps involved in transport of metal conjugates of glutathione to vacuoles for detoxification or maintenance of homeostasis (Bovet et al., 2005). In Schizosaccharomyces pombe, toxic metal tolerance is linked with the action of an ABC-type transporter protein at the vacuolar membrane. In another example, transgenic Brassica juncea possesses the gene for the expression of selenocysteine methyltransferase (SMT) shifts into a Se hyperaccumulator while A. bisulcatus exhibits greater uptake of Se and enhanced Se tolerance than the wild types (Pilon-Smits, et al., 1999; Huysen et al., 2004). In overexpressed lines, root growth was better with higher accumulation of Zn and Cd (Verret et al., 2004). Overexpression of CAX2 (calcium exchanger 2) in tomato plants results in the accumulation of more Ca2C compounds and antioxidant (Xie et al., 2015). Nicotiana tabacum plasma membrane channels the protein NtCBP4 and Arabidopsis
42
cyclic nucleotide gated ion channel (AtCNGC1) also plays a role in the Pb2C transport pathway which imparts Pb tolerance in its overexpressing plant lines (Sunkar et al., 2000; Zeng et al., 2015). As stated before, heavy metal detoxification and sequestration is accomplished with the help of many heavy-metal-binding peptides such as phytochelatins, glutathione and metalothionones. The binding of toxic metal ions to organic or sulfur-rich peptide complexes (HM-PC/GS/MT) produces carriers of the toxins to the vacuole for storage or detoxification. Overexpression of E. coli GSH1 and GSH2 genes in Brassica juncea and Populus canescens enhanced its Cd and Zn tolerance ability, respectively, due to higher accumulation of glutathione and phytochelatines in transgenics (Zhu et al., 1999). γ-glutamyl cysteine synthetase-glutathione synthetase (StGCS-GS) involved in glutathione was isolated from Streptococcus thermophiles. This gene is not redox-regulated and has limited feedback inhibition ability. It is overexpressed in tobacco and sugar beet and their transgenic lines have yielded plants with enhanced tolerance to individual/combinations of heavy metals (Cd, Zn, Cu) thus producing increased biomass wild-type plants (Liedschulte et al., 2010). Three transgenic lines overproducing γ-glutamylcysteinesynthetase (ECS), GS and adenosine triphosphate sulfurylase (APS), expressed increased levels of metal-binding peptides such as phytochelatins and glutathione when grown in metal-contaminated soil in green houses. These transgenics lines accumulated 1.5-3-fold higher heavy metal content as compared to wild type which led to significant decreases in heavy metal content in soil and produced enhanced Cd tolerance and accumulation in above ground biomass. Metallothioneins are cysteine rich metal binding proteins that play a role in metal detoxification by ROS scavenging mechanisms (Leszczyszyn et al., 2013). Over expression of
43
Arabidopsis metallothioneins (AtMT2a and AtMT3) in Vicia faba can reduce chloroplast degradation in guard cells and Brasicca rapa metallothionein 1 (BrMT1) in Arabidopsis has been shown to reduce oxidative stress under Cd toxicity (Lee et al., 2004; Kim et al., 2007). These metallothioneins were found to be helpful in heavy metal accumulation of Zn in OsMT1A-overexpressing rice (Yang et al., 2009) and for both Cu and Zn accumulation by means of the seed-specific AtMT4A gene in Arabidopsis (Rodríguez-Llorente et al., 2012). In one study, yeast metallothionein biosynthesis gene CUP1 was overexpressed and evaluated in the callus of sunflower. The transgenic calli of several strains showed high triphenyl tetrazolium chloride reducing activity after its treatment with Cd for 10 days (Watanabe et al., 2001). Zinc tolerance of Populuscanescens was enhanced by overexpression of bacterial genes encoding γ-glutamyl cysteine synthetase (GCS) in the cytosol (11ggs) and in chloroplasts (6LgI) (Bittsanszkya et al., 2005). The transformed poplar tree line had more glutathione as compared to non-transformed poplar trees. Phytochelatins are metal-binding proteins that chelate heavy metals utilizing their thiolgroups and the resulting in the formation of metal-phytochelatin complexes that become further sequestered into vacuoles. The overexpression of phytochelatin synthase gene from Ceratophyllum demersum L. (CdPCS1) in tobacco, E. coli, or Arabidopsis (Shukla et al., 2012; Shukla et al., 2013), and the Nelumbo nucifera (NnPCS1) gene in Arabidopsis thaliana (Liu et al., 2012) enhanced phytochelatine accumulation and stress tolerance in plants. Further, overexpression of Arabidopsis PC synthase (AtPCS1) in transgenic Arabidopsis increased phytochelatine synthesis, metal accumulation, and Cd and Zn tolerance in transformed plants (Lee et al., 2003).
44
Heavy metal accumulation generates redox reactions because of increases in production of ROS and reduced efficiency of ROS scavengers’ simultaniously (Mittler et al., 2004). ROS production takes places in chloroplasts, mitochondria and peroxisomes by electron transport to oxygen. Redox active metals such as Cu, Cd, Fe and Zn forms ROS by participating in Haber– Weiss and Fenton reactions. Heavy metals are inhibitory to antioxidant enzymes which reduce efficiency of scavenging mechanisms. Additionally, ROS are highly reactive and inactivate macromolecules such as lipids, proteins, carbohydrates and nucleic acids thus inducing chain reactions of macromolecule oxidative damage. One strategy exploited by researchers is the development of genetically engineered plants with more effective antioxidant defense systems and increased capacities to accumulate and/or tolerate heavy metals. Metal toxicity and gene expression levels of superoxide dismutase and peroxidase, catalase, glutathione-S-transferase involved in antioxidant defense systems is well reported (Tahara et al., 2008). Effects of Al toxicity in Arabidopsis was ameliorated by overexpression of four Al-induced genes: Arabidopsis blue-copper-bindingprotein, N. tabacum glutathione S-transferase (parB), N. tabacum GDP-dissociation inhibitor gene (NtGDl1) and N. tabacum peroxidase gene (NtPox) (Ezaki et al. 2000). Overexpression of Cu-Zn superoxide dismutase and ascorbate peroxidase in transgenic tall fescue plants improved abiotic stress tolerance. Overexpression of MnSOD gene encoding superoxide dismutase in canola also improved Al tolerance (Basu et al., 2001). Ascorbate acts as a scavenger of ROS in its reduced state and possesses the abilities to reduce H2O2 production and lipid peroxidation resulting in lower levels of oxidative DNA damage. Overexpression of dehydroascorbate reductase could maintain high levels of reduced ascorbate while conferring aluminum tolerance (Yin et al., 2010). RsMYB1 transcription factor of radishes
45
(Raphanus sativus) could enhance anthocyanin production in vegetative (leaves, stems, roots) and floral (petals) tissues by transcriptional activation of anthocyanin biosynthetic genes and endogenous antocyanin regulatory genes (Ai et al., 2018). Overexpression of RsMYB1 gene in tobacco and petunias was shown to enhance anthocyanin production (Ai et al., 2017). It was also reported that plants with these overexpressed genes had enhanced metal detoxification capacities. Glutathione S-transferase, phytochelatin synthase, superoxide dismutase, catalase, and peroxidase improved metal detoxification abilities and antioxidant enzyme activity imparting stress tolerance. For elements such as Hg and Se, volatilization is preferred over accumulation. Se is first taken up by plants from water, soil, or sediment, and then accumulated in their tissues (Banuelos et al., 1997, Berken et al., 2002), and finally volatilized as dimethylselenide (Wilber, 1980). Se is taken up via S transporters and gets volatilzed through S assimilation pathways into dimethylselenide (DMSe) a non-toxic form. ATP sulfurylase has a high substrate/product ratio, a Km (where Km is the concentration of substrates when the reaction reaches half of Vmax [or the maximum rate achieved by the system reaction]) for sulfate and ATP in the millimolar range, and is subject to powerful inhibition by adenosine phosphosulfate (Ki = 0.04 µM, where Ki is the inhibitory constant) (Schwenn, 1994). Adenosine phosphosulfate acts as the rate limiting step for enzymatic reactions in sulphur and selenium assimilation by restricting the production of sulfate and selenate in plants. Indian mustard transformed with the plastid-localized ATP sulfurylase gene (APS1) from Arabidopsis, had a higher selenate reduction, accumulation, and tolerance ability as compared to nontrasformed Indian mustard plants (Leustek et al., 1994). One group (Pilon-Smits et al., 1999) overexpressed Arabidopsis thaliana ATP sulfurylase (APS) in Brassica juncea. Wild type plants
46
had higher selenate accumulation as compared to transgenic plants because of the APSconversion of sellenate to selenite. Se-cysmethyltransferase and lyase enzymes increase Se volatilization. Various strategies have been employed for mercury phytoremediation using two bacterial genes: merA (mercuric ion reductase), and merB (organomercuriallyase). These enzymes are involved in the conversion of Hg into less toxic forms (Dhankher et al., 2012). Constitutive overexpression of either of these genes in plant species such as A. thaliana (Bizily et al., 1999, 2000, 2003), yellow poplar (Rugh et al., 1998), cotton wood (Lyyra et al., 2007), rice (Heaton et al., 2003), and tobacco (Heaton et al., 2005) increased Hg resistance up to higher levels of HgCl2. Transgenic plants have shown more Hg volatilization of both forms, Hg(0) and organic mercury, as compared to control plants. From the data we can conclude that transgenic technology has the potential to improve reclamation of heavy metal contaminated soil through phytoremediation. We need to engineer plants with better heavy metals uptake, tolerance and accumulation abilities thereby achieving higher phytoextraction potential. Looking at the complexity of the phytoremediation mechanisms, it appears that this field of ecology requires better understading of functions and regulations of plant genes involved in metal hyperaccumulation, improved uptake, root-to-shoot translocation, as well as detoxification and sequestration mechanisms. Better understanding on all aspects will help in solving the phytoremediation of HHMs through transgenic approaches. Most of the progress in development of genetically modified plants with improved phytoremediation ability, has been acheived in Arabidopsis thaliana and Nicotiana spp.. Other plant species undergoing current research include Oryza sativa, Brassica juncea, and Populus species. There are both pros and cons in the development of transgenic crop plants with
47
improved metal accumulation. On one end it provides an easy and fast way for reclamation of heavy metal contaminated soil but at the same time it increases the risk of the entry of heavy metals into food chains. Many such plants produce seeds and fruits which are highly attractive for birds and other animals thus increasing the risk factor for food chain heavy metal contamination. Moreover, genetically modified crops are not accepted easily by the public because of the peoples’ lack of complete scientific/technological knowledge and negative perceptions about the technology and failure of biotechnology companies to ‘educate’ the community about the risks and benefits of transgenic technology. Transgenic plants developed for phytoetraxtion are likely to face more challenges as they have a double risk of GM and toxic metal. There is a need to work on the development of such transgenic plants which have no food uses and can be used for production of energy and biofuels after its phytoremediation uses and thus, providing sustainable postharvest management options (Mench et al., 2009). Further, to improve the understanding of heavy metals phytoremediation, it is imperative to gain public trust on GM phytoremediation transgenic technology since there is need for risk analysis studies to be done in parallel for the application of transgenic technology on phytoremediation (Linacre et al., 2003).
48
Table 8. Transgenic plants for heavy metal tolerance Host
Gene Source
Gene
Gene Function
B. juncea
Escherichia coli
GSH2
Glutathione synthetase
B. juncea
Escherichia coli
GSHII
Glutathione synthetase
B. juncea
Escherichia coli
GSH1
γ-glutamyl cysteine synthetase
B. juncea
Arabidopsis
APS1
ATP sulfurylase
L. esculentum
Bacteria
ACC
Bacterial gene 1aminocyclopropane-1carboxylic acid (ACC) deaminase
Arabidopsis
Bacteria
Mer A and Mer B
Mercury detoxification
B. napus
T. aestivum
Sunflower callus
Yeast
Arabidopsis, Yeast
Arabidopsis
A. thaliana
A. thaliana
MnSOD CUP1
AtPcrs AtHMA4
Superoxide dismutase
Metallothionein Cys-rich membrane protein Plasma membrane localized P1B-ATPase
49
Phytoremediation Mechanism Transgenic seedling and mature plants had Cd tolerance with up to 25% higher shoot Cd accumulation and higher concentrations of glutathione, phytochelatin, thiol compunds and Ca than wild-type plants Transgenic plants had higher level of glutathione, phytochelatin and thiols and thus showed enhanced Cd tolerance Transgenic had 40-90% higher accumulation of Cd and high PCs, γGluCys, glutathione, and total nonprotein thiols compared with wild-type Increased Se uptake and reduction in both the root and shoot tissues Transgenic plants had better ability to grow under high Cd, Co, Cu, Ni, Pb, Zn and higher ACC-deaminase gene activity Double gene transgenic had 50-fold and up to 10-fold higher methylmercury concentrations in merB alone overexpressing plants than wildtype plants due to higher volatilization of mercury SOD activity was 1.5-2.5-fold greater than wild type and enhanced Al tolerance Transgenic sunflower calli had high TTC-reducing activity and increased metallothionein synthesis after 10 days Cd treatment Reduced Cd uptake of Arabidopsis and yeast protoplast Overexpression of AtHMA4 improved the root growth in the presence higher
Reference
Zhu et al. (1999)
Zhu et al. (1999)
Zhu et al. (1999) Pilon-Smits et al. (1999) Grichko et al. (2000)
Bizily et al. (2000)
Basu et al. (2001)
Watanabe et al. (2001) Song et al. (2004) Verret et al. (2004)
transporter
Bacteria
11ggs (cytosol), 6LgI (chlopoplas ts)
N. tabacum
E. coli and S. pombe
CYSE, GSHA and PCS
Serine acetyl transferase, -glutamyl cysteine synthetase, phytochelatin synthase
N. tabacum
Arabidopsis
AtPCS1
Phytochelatine synthatase
B. campestris
Z. mays
Cu/ZnSOD and CAT
Superoxide dismutase and catalase
IAAM and ACC
1-amino cyclo propane-1carboxylic acid deaminase and tryptophan monooxygenase
P. canescens
N. tabacum
P. hybrida
N. tabacum
B. juncea
CAT3 and CAT
A. palustris
P. australis
PaGCS
A. thaliana
Garlic and baker's yeast
GSH1 and AsPCS1
N. tabacum
S. thermophilus
StGCL‐GS
N. tabacum
Arabidopsis
MDHAR/ DHAR
γ -glutamylcysteinsesynthetase
Catalase
γ-glutamylcysteine synthetase Glutathione synthetase and phytochelatin synthase γ‐glutamylcysteine ligase-glutathione synthetase enzyme Mono/ De-hydro ascorbate reductase
50
Zn, Cd and Co concentration Leaf disc of transgenic poplar lines had higher Cd (~4.5-8.5 ppm), Cr (~8-35 ppm), Cu (~30-90 ppm), and Zn (~5000 ppm)
Bittsánszkya et al. (2005)
122-167% higher accumulation of Cd
Wawrzynski et al. (2006)
Transgenic seedlings had 2-fold increase in Cd+2 and higher production of PCs Less reduction in photosynthetic activity and more active antioxidant enzymes than wild type under SO2 stress Transgenic tobacco had better growth, higher biomass and more extensive root system, and accumulated a greater amount of heavy metals (Cu and Co) CAT activity of transgenics was approximately 2-fold higher with lower H2O2 accumulation than that of wild type plants High gutathione, phytochelatines and thiol compound accumulation and antioxidant enzyme activity Transgenic lines had elevated Cd and As tolerance and accumulation due to increased total PC production
Pomponi et al. (2006)
Tseng et al. (2007)
Zhang et al. (2008)
Guan et al. (2009)
Zhao et al. (2010b)
Guo et al. (2010)
20 to 30 fold higher glutathione levels as compared to wild-type
Liedschulte et al. (2010)
MDHAR accumulation enhanced Al tolerance by maintaining ascorbate level
Yin et al. (2010)
S. cerevisiae and N.tabacum
T. caerulescens
TcPCS1
Phytochelatine synthatase
N. tabacum
T. virens
GST
Glutathione-S transferase
N. tabacum
M. musculus
MT1
Metallothionein
A. thaliana
N. nucifera
NnPCS1
Phytochelatine synthatase
N. tabacum
C. demersum
CdPCS1
Phytochelatin synthase
Arabidopsis
B. oleracea
BoCAT1 and BoCAT2
Catalase
E. coli, Arabidopsis
C. demersum
CdPCS1
Phytochelatin synthase
B. vulgaris
S. thermophilus
StGCS-GS
γ-glutamyl cysteine synthetase-glutathione synthetase
N. tabacum var. Sumsun
A. thaliana
AtACR2
Arsenic reductase 2
51
Increased tolerance to Cd due to the decreased lipid peroxidation and enhanced activities of SOD, POD, CAT and PCs content Enhanced Cd tolerance simultaneously, increased activity of SOD, CAT, GST, APX, and GPX than wild type Enhanced Hg accumulation Under high Cd exposure transgenics had 1.4-2.3-fold higher Cd content, 1.3-1.5-fold non-protein thiols, 1.51.9-fold greater phytochelatines than wild-type Transgenic tobacco plants several-fold increased PCs content (up to 100-600 nmol/g FW), Cd (up to 1500 µg/g DW) and As (up to 6000 µg/g DW) accumulation without significant decrease in plant growth 6-fold higher catalase activity and low H2O2 content in transgenic line under heat stress Transformed E. coli had higher accumulation of Cd up to 17 ppm Transgenic B. vulgaris accumulated more Cd, Zn and Cu ions in shoots (3fold ) than wild-type As content in the roots of transgenics was significantly higher (2400µg/g DW) than that of wild type roots
Liu et al. (2011)
Dixit et al. (2011) Ruiz et al. (2011)
Liu et al. (2012)
Shukla et al. (2012)
Chiang et al. (2013) Shukla et al. (2013) Liu et al. (2015)
Nahar et al. (2017)
8.
Human health effects due to consumption of vegetables contaminated with HHMs Heavy metals are critical environmental pollutants that rapidly accumulate in vegetables
mainly in peri-urban areas by natural as well as anthropogenic means (Li et al., 2014). Heavy metals are indispensable in minute quantities to sustain various physiological and biochemical functions in living beings, though they can pose harmful effects when they exceed the specified safe threshold levels (Jaishankar et al., 2014). Fig. 4 explains that most of the vegetables get contaminated by absorbing heavy metals from polluted water, soil, and air (Kacholi and Sahu, 2018; Wongsasuluk et al., 2018). For decades, vegetables have been important diet constituents that fulfil the required needs of essential nutrients. Mainly leafy vegetables may be more harmful to human consumption due to greater accumulation capacity. HHMs penetrate cell membranes and produce ROS that ultimately affect functions of cells and cellular organelles (SanchezChardi et al., 2009). As we have discussed earlier, several heavy metals like As, Pb, Cd, Cr, and Hg are unusually toxic (hematotoxic, immunotoxic, neurotoxic, genotoxic, reproductive toxic, pulmonary toxic, nephrotoxic, and hepatotoxic) and hazardous to the environment and living-beings (Ametepey et al., 2018; 2018, Domingo et al., 2017; Mari et al., 2018). The ingestion of toxic heavy metal concentrations from vegetables may lead to several short-term as well as long-term adverse health effects such as vomiting, stomach irritation, headache, diarrhea, fatigue, weakness, drowsiness, confusion, muscular pain, pricking sensation in hands and legs, skin manifestations, unusual pigmentation and keratosis, hypertension, cardiovascular disease, lung edema, destruction of mucous membranes, hair and memory losses, difficulty with balance, damage to brain, kidney and lungs, changes in vision and/or hearing (Carrington et al., 2019).
52
On the cellular level, toxic metal poisoning can have deleterious affects on oxidative phosphorylation and ATP synthesis (Yan et al., 2017; Yang et al., 2018; Lai et al., 2018; Zafarzadeh et al., 2018; Rehman et al., 2018). Furthermore, HHMs can produce both acute and chronic toxicity symptoms in pregnant women, fetuses, young children and adults (Table 9).
53
Fig. 4. Health effects of heavy metals on humans
54
Table 9. Acute and chronic effects of HHMs before and after nativity in humans Toxic metal
Toxicity
Acute As Chronic
Acute Cd
Before nativity effect Neurotoxic to brain development and pose behavioral changes Increase in fetal loss, detrimental effects on embryo, mutagenesis and reduction in birth weight -
Chronic
Embryotoxic and teratogenic, reduced size and weights of embryo
Acute
Premature birth risk and babies with low birth weight
Pb Chronic
Cr
Reduced the cognitive capacity of children and birth defects
Acute
Detrimental effects on fetus developmental
Chronic
Embryotoxic and fetotoxic,
After nativity effect Weakness, drowsiness and confusion, muscular pain, flusking skin, abnormal changes in heartbeats and pricking sensation in hands and legs Affect oxidative phosphorylation and ATP synthesis, reduced production of erythrocytes and leukocytes, skin manifestations, pigmentation and keratosis, neurological disorders and cardiovascular disease Lung edema and destruction of mucous membranes, stomach irritation, vomiting, diarrhea and fatigue Disturbances in Ca+2 metabolism, renal dysfunction, formation of kidney stones and hypercalciuria, mutagenic, carcinogenic and teratogenic Affect central nervous system and the gastrointestinal tract, loss of appetite, kidney disease, fragile bones, renal dysfunction and abdominal pain Mental retardation, autism, birth defects, allergies, psychosis, dyslexia, weight loss, hyperactivity, paralysis, muscular weakness, brain and kidney damage and IQ reduction Ulcers, hair loss, inhibition of erythrocyte glutathione reductase and reduce the conversion of methemoglobin to hemoglobin Chromosomal aberrations and mutation,
55
Affected system &/or organelle
Reference
Lungs, liver, bladder and skin
Yang et al. (2018); Tripathi et al. (2007); José Zocche et al. (2010)
kidney
Neuromuscular system
Digestive tract
Lai et al. (2018); Salem et al. (2000); Trzcinka-Ochocka et al. (2010)
Yan et al. (2017); Salem et al. (2000); Iqbal (2012);
Salem et al. (2000); Matsumoto et al. (2006)
low birth weight and preterm birth, and congenital malformations
Acute
Affect growth and development
Hg
Chronic
Acute Cu Chronic
Affect brain and nervous systems development in unborn infants' Affects fetal growth, induces behavioral changes and neurotoxic Neurological changes in newborn and preeclampsia in mother
Acute
-
Chronic
-
Ni
Chronic
Musculoskeletal defects
alterations in replication and transcription of DNA process Anxiety, depression, drowsiness, hair and memory loss, difficulty with balance, insomnia, irritability, memory loss, damage to brain, kidney and lungs, and changes in vision or hearing
Nervous system
Zafarzadeh et al. (2018);
Lung damage, skin rashes, vomiting, diarrhea, nausea, increased blood pressure Stomach and intestinal irritation Damage to brain and kidney, liver cirrhosis and chronic anemia Headache, spinning dizziness, insomnia, nausea, vomiting, irritability, itching and hair loss Hematotoxic, immunotoxic, neurotoxic, genotoxic, nephrotoxic, and hepatotoxic, cancer of the lungs and nose, and respiratory disorders Risk of lung cancer
56
Neurological and enzymatic systems
Mitochondria
Salem et al. (2000);
Rehman et al. (2018); Salem et al. (2000); Khan et al. (2007); Mishra et al. (2010)
9. Permissible limits of HHMs in the environment HHMs may adversely affect soil ecology, agricultural soil, food quality, and the health of living organism, in addition to air and groundwater quality (Kacholi and Sahu, 2018). Long-term applications of sewage treatment plant (STP) effluents for irrigation, also contaminates soil, water and vegetables resulting in deterioration of soil and water resources (Sharma et al., 2008). Presently in peri-urban areas, vegetable production is on the rise and remains at highly maintained levels throughout the year. Health-conscious citizens include more vegetables in their diets, and specifically their green leafy vegetable consumption is increasing (Gupta et al., 2013). Many researchers, institutes, organizations and countries have set their particular maximum permissible limits of heavy metals in vegetables, plants, soil and water (drinking and irrigation) to get a broad idea about the contamination and intake levels Therefore, it has become important, to generate these new guidelines for HHMs levels, that focus on implementing scientific guidance on the assessment of the quality of vegetables and foods based on technical improvements and novel developments. In many countries, however, the permissible standards are still higher than the World Health Organizatin (WHO) or the Food and Agricultural Association (FAO) standards allow. The maximum permissible limits of HHMs in vegetables and plants, soil, drinking and irrigation waters are given in Tables S2, S3, S4 and S5, respectively. 10.
Challenges, issues and prospects for further applications
All the remedial approaches, such as physical, chemical, biological, genetic, physiological, biotechnological, and nanotechnological are doing well to some extent but are restricted due to environmental as well as biological limitations that are site- and contaminant-specific and require optimum running conditions. The cocktails of pollutants in the environment can obviously
57
decrease the efficiency of these methods. When the food chain gets contaminated, plants first accumulate a high amount of HHMs in their storage organs that ultimately create hazards to human and animal health. The contamination pathways of HHMs in plants are still not fully understood and require a more intensive focus in the future. Contamination mechanisms should be well understood to identify the load of a poisonous element that can enter in our food and become biomagnified. The physiological, genetic and biotechnological approaches based on microbial and plant interventions, can modify the required suitable changes needed in organisms and genes to better resist heavy metal intake. Present methods are mostly focused on a particular single pollutant even though background environments contain a mixture of various pollutants. On a large scale, financial and technical problems have made soil remediation/intervention a challenging responsibility. Biological remediation approaches have shown to produce better and more effective responses as compared to physico-chemical methods with respect to environmental safety, small-scale applications, public acceptability and cost. Advanced approaches such as nanoremediation and the use of combined biotechnological and transgenic technologies can better help to promote bioremediation efficiency and effectiveness. By introducing foreign genes into plant genomes to improve the adaptability to withstand high HHMs concentrations and hyperaccumulators, capacities for tolerances can be managed effectively due to the overexpression of particular proteins and natural chelators in transgenic plants cells (Yadav et al., 2017b). Transgenetic and nanotechnological approaches of remediation are well studied in the laboratory,
however,
field
applicability
requires
more
extensive
investigation.
In
nanotechnological remediation approaches, carbonaceous NMs possess large specific surface
58
areas, outstanding electrical, optical, thermal and chemical potentials and broad applications so as to be considered one of the most highly prospective candidates to remove chemical/biological contaminants from wastewater. Nevertheless, future development and full-scale applications of these remedial tactics still face a wide variety of challenges and more thorough studies are certainly required. The following challenges are offered as remedial processes: •
The comprehensive understanding of HHMs accumulation in the food chain and bioaccumulation requires comprehension of the toxicity, mobility, function and reaction of metal transporters and ligands of plant cell mechanisms and metabolism.
•
More advanced and detailed knowledge of metal transporters is necessary for all toxic elements found in contaminated plants.
•
The complex passage/transference of toxic metal transporters across apoplastic barriers into plant seeds is largely unexplained and necessitates investigation to aid in plant tolerances.
•
The mechanisms of toxic element uptake into plant leaves and fruits, seeds and tubers should be classified.
•
Source reduction strategies should be focused in the future as part of preventive measurements for food chain incorporation that have been identified.
•
The commercial large-scale production of carbonaceous nanomaterials is still challenging and requires intervention of production methods for scale-up in larger numbers of plants.
•
The modern synthesis techniques for carbonaceous nanomaterials are still complicated with less efficiency compared to standard genetic methods, hence simple and efficient nanodesign methods are essentially needed.
59
•
CNTs and graphene-based NMs in the liquid phase currently do not perform properly for the removal of HHMs. The applications of nanomaterials coupled with several functional groups and surface modifications have been applied to overcome present problems.
•
Phytoremediation processes are not permanent solutions for removal or stabilization of HHMs. The suitability of phytoremediation procedures mainly depends on the site of uptake in the plant, the tolerance level of the plant, bioavailability of metals, climate and weather conditions. Hence a wide applicability of phytoremediation should be concentrated on improving the utilization of recent biotechnological and genetic approaches.
•
Rhizospheric chemistry and interactions of HHMs and microbes should be more elucidated to better understand the transport mechanism in plants.
•
Physical methods require large working volumes, are costly, generate toxic waste and build up negative effects on soil fertility. These procedures must be rendered more safe to the environment and plants while simultaneously studying other new remediation methods such as nanotechnological processes.
•
Chemical methods are not stable solutions of remediation and require permanent monitoring. In addition, extractants necessitate washing steps to remove unbound toxins that can cause environmental issues later on.
For the sustainability and broad applicability of future generations and resources, to overcome and reduce the contamination of HHMs in the food chain, intensive studies at the field level with the optimization of processes and improvments in the suitability of materials/methods in specific environments must be carried out effectively. 11. Conclusions
60
In this review, we mainly focused on nanotechnological and phyto-bio-genetic approaches for remediation. This review has revealed that heavy metal sources, food chain contamination with them, the mechanisms of metal transport in plants, and the physicochemical, phytoremediation, nanotechnological and genetic approaches in heavy metal removal, all possess constraints to effective phytoremediation. The entire environmental compartments including soil, water, air and food have been contaminated by HHMs around the world. This severe problem is rising in industrial towns and rapidly developing cities. In the periphery of cities, cultivated soils are polluted with deposition or discharge of HHMs thereby increasing the levels of hazardous substances in food chains. Food chain contamination is one of the main routes for the entry of HHMs into the human body and intake of contaminated foods may contribute to the development of several disorders in living beings. Among the modified and advanced technologies of remediation such as nanoabsorbents, phytoremediation and genetic approaches are highly effective, efficient and can be economically viable. Nevertheless, the applicability of these methods is still restricted, and more intensive investigation at the field level is undoubtedly necessary. Conflict of interest The authors declare no conflict of interest. Acknowledgements The authors are very grateful to Lisa M. Reece, with the University of Texas Medical Branch, Galveston, TX, USA for her consistent support and guidance. The authors are also thankful to the editor and anonymous reviewers for their valuable suggestions to improve the manuscript.
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