Chemosphere 303 (2022) 134788

Contents lists available at ScienceDirect

Chemosphere
journal homepage: www.elsevier.com/locate/chemosphere

Phytoremediation of heavy metals in soil and water: An eco-friendly,

sustainable and multidisciplinary approach
Shakeel Ahmad Bhat a, Omar Bashir b, Syed Anam Ul Haq c, Tawheed Amin d, Asif Rafiq e,
Mudasir Ali a, Juliana Heloisa Pinê Américo-Pinheiro f, g, Farooq Sher h, *
a
College of Agricultural Engineering and Technology, Sher-e-Kashmir University of Agricultural Sciences and Technology of Kashmir, Srinagar, Jammu and Kashmir,
190025, India
b
Department of Food Technology and Nutrition, Lovely Professional University, Punjab, 144402, India
c
Division of Plant Biotechnology, Sher-e-Kashmir University of Agricultural Sciences and Technology of Kashmir, Srinagar, Jammu and Kashmir, 190025, India
d
Division of Food Science and Technology, Sher-e-Kashmir University of Agricultural Sciences and Technology of Kashmir, Srinagar, Jammu and Kashmir, 190025, India
e
College of Temperate Sericulture, Sher-e-Kashmir University of Agricultural Sciences and Technology of Kashmir, Mirgund, Baramulla, Jammu and Kashmir, 193121,
India
f
School of Engineering, São Paulo State University (UNESP), Ave. Brasil Sul, Number 56, 15385-000, Ilha Solteira, SP, Brazil
g
Brazil University, Street Carolina Fonseca, Number 584, 08230-030, São Paulo, SP, Brazil
h
Department of Engineering, School of Science and Technology, Nottingham Trent University, Nottingham, NG11 8NS, United Kingdom

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• Rapid industrialization, increased waste

production and surge in water treatment
activities.
• Industrial effluents contribute to
contamination and water sources due to
heavy metal accumulation.
• Different strategies and approaches for
the removal of various heavy metal
containments are explored.
• Various plants and related soil organ­
isms could be employed in phytor­
emediation to lower the pollutants.
• For heavy metal cleaning from contam­
inated regions, phytoremediation is a
viable and ecologically friendly
technique.

A R T I C L E I N F O A B S T R A C T

Handling editor: Pau-Loke Show Rapid industrialization, increased waste production and surge in agricultural activities, mining, contaminated
irrigation water and industrial effluents contribute to the contamination of water resources due to heavy metal
Keywords: (HM) accumulation. Humans employ HM-contaminated resources to produce food, which eventually accumu­
Nanotechnology lates in the food chain. Decontamination of these valuable resources, as well as avoidance of additional
Sustainability
contamination has long been needed to avoid detrimental health impacts. Phytoremediation is a realistic and
Waste management
promising strategy for heavy metal removal from polluted areas, based on the employment of hyper-accumulator
Heavy metals
Phytoremediation plant species that are extremely tolerant to HMs present in the environment/soil. Green plants are used to
Phytoextraction and genetic engineering remove, decompose, or detoxify hazardous metals in this technique. For soil decontamination, five types of

* Corresponding author.
E-mail address: Farooq.Sher@ntu.ac.uk (F. Sher).

https://doi.org/10.1016/j.chemosphere.2022.134788
Received 27 January 2022; Received in revised form 16 April 2022; Accepted 27 April 2022
Available online 30 April 2022
0045-6535/© 2022 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
S.A. Bhat et al. Chemosphere 303 (2022) 134788

phytoremediation methods have been used viz. phytostabilization, phytodegradation, rhizofiltration, phytoex­
traction and phytovolatilization. Traditional phytoremediation methods, on the other hand, have significant
limits in terms of large-scale application, thus biotechnological efforts to modify plants for HM phytoremediation
ways are being explored to improve the efficacy of plants as HM decontamination candidates. It is relatively a
new technology that is widely regarded as economic, efficient and unique besides being environment friendly.
New metal hyperaccumulators with high efficiency are being explored and employed for their use in phytor­
emediation and phytomining. Therefore, this review comprehensively discusses different strategies and
biotechnological approaches for the removal of various HM containments from the environment, with emphasis
on the advancements and implications of phytoremediation, along with their applications in cleaning up various
toxic pollutants. Moreover, sources, effects of HMs and factors affecting phytoremediation of HMs metals have
also been discussed.

1. Introduction have an atomic density of >41 g/cm3, citing Cd, Cr, Co, Cu, Pb, Hg, Zn
and other metals as examples. Even the trace amounts of HMs in the
Owing to increasingly growing industrialization combined with system have an intensive effect on ecosystems (terrestrial and aquatic)
agricultural practices, soil contamination with heavy metals (HMs) has (Bansod et al., 2017). This could be due to diffuse factors like air
evolved as a severe environmental concern on global level (Chaoua emissions, which has been recognized as the foremost reason for soil and
et al., 2019; Sandeep et al., 2019). HMs have a half-life of greater than water pollution (Kelly et al., 1996). For ecological environments as well
twenty years and are very persistent in nature (Asati et al., 2016; as human health, these are the most dangerous and harmful water
Hadia-e-Fatima, 2018; Kapoor and Singh, 2021). Elements with den­ pollutants (Kim et al., 2012).
sities >5 g/cm3 are described as heavy metals and are therefore Volcanoes, soil erosion and rock disintegration are examples of
considered to be universal pollutants (Saif and Khan, 2017; Prieto et al., natural sources, while incomplete fossil burning, mineral extraction,
2018). HMs are apportioned into two categories viz. necessary and landfilling, metal refining, electronic goods manufacturing, dyes, agri­
in-essential. Various elements like cobalt (Co), copper (Cu), chromium cultural chemicals, military operations and vehicular emissions are ex­
(Cr), iron (Fe), nickel (Ni), manganese (Mn) and zinc (Zn) are basic HMs amples of anthropogenic activities. Toxic HMs like As, Cd, Cr, Cu, Hg, Pb
that are considered micronutrients but become toxic when consumed in and others are widely found in wastewater from mines, sewage, dyes,
large amounts. Cadmium (Cd), mercury (Hg) and lead (Pb) are alloys etc. (Ene et al., 2010). Anthropogenic practices, on the other
non-essential HMs that are extremely lethal to living organisms (San­ hand, lead more to environmental pollution than natural sources (Dur­
deep et al., 2019). uibe et al., 2007). Many HMs, as per (Kumar et al., 2017), are extremely
HMs exist naturally in rocks, but human activity has increased their reactive in nature, resulting in negative consequences for both the
accumulation. Excessive use of sewage sludge, agrochemicals, waste­ environment and humans. Fig. 1 summarizes the major anthropogenic
water, biosolids and manure are all HM sources in soil (de Figueiredo behaviours that can lead to higher levels of toxic HMs in the environ­
et al., 2019; Haroon et al., 2019). HMs build up in the soil and trigger ment; As, Cd, Pb, Hg, Ni, Zn and U metals may be added during mining
serious health issues for plants, livestock and humans (Srivastava et al., or smelting or during agrochemical activities.
2017; Alizadeh-Kouskuie et al., 2020). As per literature, approximately Furthermore, some bacterial activities subsidize the buildup of toxic
10 million people worldwide have been affected by HM contaminated Hg (monomethyl mercury or dimethyl mercury) in soil and water
soil (Ashraf et al., 2019). Thus, HMs buildup in crops via soil-root thereby, lowering the water quality (Kumar et al., 2017). Smelting and
interface, thereby posing a serious threat (Sakizadeh and Ghorbani,
2017). Water and soil are the two most significant natural resource
foundations for a long-term viability of agriculture and survival of the
civilizations (Ul Zaman et al., 2018; Kumar et al., 2016). Further,
anthropogenic and natural activities have also lead to the contamination
of soil and water (Ali et al., 2013).
These practices produce waste and put the public health, natural
habitat,or the environment at risk (Yadav et al., 2017a; Yadav et al.,
2017bYadav et al., 2018; Bhat et al., 2022). The organic components
from the waste are biodegradable however, HMs and metalloids pose a
new challenge as a consequence of their prolonged tenacity in the
environment (Ahmadpour et al., 2012; Saha et al., 2017). Due to useful
effect some of these HMs in biological systems, it is necessary to exist a
specific range of concentration. HMs for a number of physiological and
biochemical functions, humans require Fe, Co Mn, Mo and Zn (Zoroddu
et al., 2019), however, excessive amounts can have negative conse­
quences. Some HMs such as Hg, Pu, Cd and Pb have no beneficial impact
on organisms (Kumar et al., 2017). Pollution because of HMs in the soil
is a worldwide issue.

2. Heavy metal sources in soil and water

HM contamination has piqued the world’s attention due to its

toxicity to living organisms through bioaccumulation (Ekmekyapar
et al., 2012). HMs are typically classified as metals or metalloids with a
higher elemental density. These are subdivided on basis of density,
weight or atomic number (Kumar et al., 2017; Ali and Khan, 2018). Ali
et al. (Ali et al., 2019) proposed a new standard, stating that HM should Fig. 1. Different sources responsible for HM accumulation in water and soil.

2
S.A. Bhat et al. Chemosphere 303 (2022) 134788

mineral mining, according to some researchers, are the main sources of number of health issues (Table 1).
Heavy Metal Concentration (HMC) in China, as a large amount of
wastewater is produced in these activities, posing significant health risks 4. Phytoremediation of HMs in soil and water
to society on a large scale (Sun et al., 2010). Cosmetics and chemical
fertilizers, in addition to the above, contribute to heavy metal pollution Phytoremediation exploits metal-accumulating plants to restore
(Callender, 2004). Intriguingly, heavy metals released by vehicles have contaminated main sources; soil and water (Muthusaravanan et al.,
been found to be deposited on plant leaves and the surface of soil 2018). HMs uptake through phytoremediation technology involves
(Harrison et al., 1981). Studies have demonstrated the occurrence of several processes like phytostabilization, rhizodegradation, phytoex­
different hazardous HMs in the soil or farm areas (Turer and Maynard, traction, phytodegradation, phytoaccumulation and phytovolatilization
2003). As per recent studies, untreated effluent water has been proven to (Tangahu et al., 2011) (Fig. 2) (Table 2).
be a substantial source of HM polluted water and other areas of the Specific plants for phytoremediation have the potential to extract
world (arsenic, cadmium, mercury, and so on). Sewage water has been high levels of HMs into their roots, tolerate different metals and have the
linked to the presence of potentially harmful elements like Cd, Cu, Ni, physiological conditions to adapt to different environments (Prieto
Cr, Pb and Zn in soil, plants and foods. et al., 2018). The capability of some aquatic hydrophytes, E. crassipes, E.
Moreover, HM is a significant hazard to the planet’s living creatures stagnina, L. stolonifera and P. australis to accumulate Cd, Ni, Pb and use
(Cao et al., 2019; Dumont et al., 2019; Nanda et al., 2019; Zhang et al., these species for indicating and phytoremediation polluted wetlands
2020). HMC in soil samples can come from diffused sources such as from HMs, was estimated by (Eid et al., 2020). The esults showed that
vehicles, untreated wastewater disposal, paint and varnishes, and so on Phragmites australis has the ability to accumulate the highest concen­
(Alloway, 2012). Fossil fuel combustion, agrochemicals and soil texture trations of Cd and Ni, while Echinochloa stagnina accumulated a high
(rocks) are the substantial causes of HMs in crop soils (Peralta et al., level of Pb in the tissues. Furthermore, except for Ni in Echinochloa
2020). used a portable ED-XRF to detect HMs in 40-year-old vineyard stagnina and Cd in Ludwigia stolonifera, suitable for phytoextraction of
soil containing Bordeaux mixture. The upper soil was found to contain these metals-these studied species are capable of phytostabilizing these
70–128 mg/Kg of Cu, much higher than the Spain government’s rec­ tested HMs. Thus, phytoremediation is an economic and effective
ommended minimum (90 mg/Kg). HM contaminated soil sites were technique for the elimination of HMs from water and soil (Eid et al.,
found in 1.7 million (mn), 0.6 mn, and >20 mn ha of agricultural land in 2020).
Europe, the United States, and China, according to (Shah and Daverey,
2020). Volcanoes and rock disintegration are natural sources of HMs in
soils, while industrial discharge, urban growth, the automotive industry 4.1. Phytoremediation techniques
and extensive use of agrochemicals are anthropic sources of HMC in soils
(Pan et al., 2016; Ali et al., 2019; Ali et al., 2019). 4.1.1. Phytoextraction
Soil is contaminated with HMs via some activities such as urban The uptake and transport of toxins by plant roots into shoots is
waste, mining and industrial sludge (Ye et al., 2017; Bello et al., 2019; termed as phytoextraction, sometimes known as phytoaccumulation,
Vardhan et al., 2019). According to (Wang et al., 2020), the soil HM photoabsorption or phytosequestration. In order to remove soil toxins,
contamination is predominantly caused by the rapid development of the roots and shoots are harvested (Ali et al., 2013). (Chandra and
manufacturing and metropolitan fields. Cd and Ni are often applied to Kumar 2017) demonstrated that, twelve suitable native plants growing
the soil in the southwest part of China (Sun et al., 2013). Apart from on sludge observed their ability to accumulate Fe. A. spinosus L. was
these, several studies have stated a rise in heavy metal concentrations in discovered to be Zn and Mn shoot accumulator. Except for A. spinosus L.
soil that has caused degradation in crop quality, soil health and yield and Ricinus communis, all plants were found to be leaf accumulators for
(Ahmad et al., 2016; Shah and Daverey, 2020). Zhang et al. (2020)
calculated the Sb, As, Pb, Cd, Cr, Hg, Mn, Ni and Ti concentrations in tea Table 1
leaves. HM levels have also been found to be higher in soils produced Various hazardous impacts of different HMs on human health.
from carbonate-bearing rocks (Jia et al., 2020). Heavy Related hazardous effects Reference
Reduction of the HM content of water is difficult therefore, only metal
oxidation state transformation is applicable (Singh et al., 2018), As Interferes with key cellular functions in Tripathi et al. (2007)
resulting in significant disruptions in aquatic life metabolism as well as human body
ecological instability (Baby et al., 2010). According to (Marella et al., Cd Chronic anemia, mutagenic, renal failure (Degraeve, 1981; Salem
2020), a number of behaviours are responsible for the presence of HMs and carcinogenic etc. et al., 2000)
Cr Hair loss Salem et al. (2000)
(Pb, Cd, Cr, Hg and Zn) in the aquatic environment (Rizwan et al., 2019).
Cu Brain and kidney injury, liver cirrhosis, Wuana and Okieimen
HMs in soil can cause surface and groundwater contamination, the stomach and intestinal inflammation have (2011)
extinction of agricultural-useful microbes, poor soil health, and a all been linked to elevated levels.
decrease in crop yield (Sarkar et al., 2017; Singh et al., 2018). Hg Anxiety, autoimmune disorders, (Ainza et al., 2010;
Furthermore, the metals accumulate in crops, posing a danger to depression, trouble with coordination, Verma et al., 2021)
exhaustion, loss of hair, insomnia,
ecological systems, including humans (Chai et al., 2018; Wang et al., irritability, ulcers, and brain, kidney, and
2020b). lung damage are just a few of the
symptoms.
3. Effect of heavy metals on human health Ni Nickel itch is allergic dermatitis; (Khan et al., 2007; Das
inhalation can cause lung, nose, and sinus et al., 2008)
cancers; throat and/or stomach cancers.
HMs pose harmful effects on human health and thus, many HMs and Causes hair loss by being hematotoxin,
metalloids are hazardous even at lower concentrations (Kara, 2005; neurotoxic, genotoxic, nephrotoxic, and
Haferburg and Kothe, 2007; Arora et al., 2008). By forming free radicals, hepatotoxic.
Pb Its poisoning causes developmental delays, (Mishra et al., 2010;
HMs induce oxidative stress (Mudipalli, 2008). Further, they may act as
decreased intelligence, learning Wuana and Okieimen,
a replacement for main metals in pigments and enzymes (Malayeri et al., difficulties, and balance issues in infants, 2011)
2008). HMs like As, Hg, Cd, Cr, Cu, Pb, Sn and Zn are the most toxic in as well as renal failure, cardiovascular
terms of their toxicity (Ghosh, 2010). HMs like Hg, Cd, Pb and As are disease.
non-essential, whereas Cu and Zn are (trace elements). Depending on the Zn Overdosing will result in dizziness and Hess and Schmid (2002)
exhaustion.
HM, its concentration, and oxidation state, toxic HMs may result in a

3
S.A. Bhat et al. Chemosphere 303 (2022) 134788

et al., 2019) investigated the suitability of using four woody plants in

combination with organic amendments to phytostabilize zinc smelting
slag. The results showed that planting vegetation directly in zinc
smelting waste slag increased nutrient accumulation and decreased
heavy metal bioavailability (Cu, Zn and Cd). (Saran et al., 2020) per­
formed a phytostabilization demonstration to determine the capacity of
growing Helianthus petiolaris (an aromatic plant) in HMC soils. In terms
of phytostabilization, H. petiolaris could develop in soils with up to 500
mg/Kg Pb2 and 50 mg/Kg Cd2, accumulating >3 times the soil Cd
content in the aerial parts and translocating large amounts of Pb to the
aerial parts. (Galal et al., 2017) investigated the ability of Vossia cuspi­
date (emergent macrophytes) as a phytoremediator to absorb HM from
contaminated water sources in another analysis. The results revealed
substantial seasonal variation in the concentrations of the investigated
HMs in the various plant tissues of V. cuspidate, with HMs accumulating
in higher concentrations in below-ground sections than in above-ground
shoots.

4.1.3. Rhizofiltration
Rhizofiltration is a technique in which plant roots are employed to
eliminate pollutants from wastewater. Root exudates can absorb HMs,
thus altering the pH of rhizosphere (Yan et al., 2020). A study (Bena­
vides et al., 2018) revealed that Zea mays has a higher potential for
uptake and bioaccumulation of Hg. In a sewage treatment plant of
KwaZulu-Natal (a province of South Africa), a rhizofiltration device was
planted with two species (Phragmites australis and Kyllinga nemoralis),
was tested for its efficiency in extracting HMs from municipal waste­
water. HMs were deposited in the planted and reference parts of the
rhizofilter in varying concentrations. Cd levels were also found to have
risen by 33% and 21% on of K nemoralis root system, indicating that the
system is effective at extracting HMs from wastewater (Odinga et al.,
Fig. 2. Heavy metal uptake mechanisms of phytoremediation technology 2019).
(Tangahu et al., 2011).
4.1.4. Phytovolatilization
Plants are used to convert different pollutants into less hazardous
Table 2 volatiles, which are then released into the atmosphere through the foliar
Different phytoremediation processes for HM uptake (Bian et al., 2018). system. This concept may be used to remove organic pollutants as well
Types of Scope of Mechanism Contaminant as heavy metals including Se, Hg and As (Yan et al., 2020). According to
phytoremediation application prior research, Astragalus racemosus may convert Se into dimethyl dis­
Phytovolatilization Volatile Volatilization by Organics/ elenide by phytovolatilization, whereas Arabidopsis thaliana can
contaminants leaves Inorganics convert Hg2+ to Hg0, hence boosting Hg volatility (Awa and Hadibarata,
Phytostabilization Mining Complexation Inorganics
2020). Moreover, Sakakibara et al. (2010) observed the ability of Pteris
contamination
Phytoextraction Low-to-medium- Hyper- Inorganics
vittate to metabolize arsenic into volatile arsenic forms. In phytovolati­
contaminated sites accumulation lization, harvesting or disposing of HM pollutants are collected from the
Rhizofiltration Wastewater Rhizosphere Organics/ soil and spread as gaseous compounds (Yan et al., 2020).
accumulation Inorganics

5. Potential biotechnological approaches for phytoremediation

Fe, Mn and Zn. Lajayer et al., 2019 have demonstrated the promising
potential of ornamental plants for phytoextraction of HMs from polluted
environments. When compared to traditional cleanup techniques, this
strategy appears to be more ecologically friendly. Ugya et al. (2019)
looked at the phytoextraction capacity of certain vegetables as well as
the possible health risks related to eating vegetables that are grown in
agricultural soils irrigated with refinery wastewater. For Cd and Hg, the
results revealed a strong accumulation pattern in the vegetable.
Makarova et al. (Makarova et al., 2021) studied the possibility to
enhance the phytoextraction process by Trifolium repens of Cd, Ni and
Cu. The results showed the efficiency of the potassium salt of K2HEDP,
plant growth regulators and iron chelate for the phytoextraction of Cd.
4.1.2. Phytostabilization
Phytostabilization uses the metal-tolerant plants for HM immobili­
zation in contaminated soils thereby, decreasing their bioavailability in
the environment (Yan et al., 2020). As a result, they are unable to
migrate to groundwater or join the food cycle (Ali et al., 2013). (Luo
Plants are being employed for remediation of hazardous metals,
however, due to HM phytotoxicity, this process has been sluggish and
generally unsuccessful (Dhankher et al., 2012). Phytoremediation has a
lot of promise using genetic engineering methods to improve plant
tolerance and hazardous metal buildup. In addition, a slew of new
studies has been done utilizing omics technologies to decipher the ge­
netic factors and underlying mechanisms in HM tolerance in plants.
HM’s viz. As, Cd, Cu, Hg, Pb and Se are now being phytoremediation
using biotechnological methods. Plants are being engineered for phy­
toremediation of HMs using three primary biotechnological methods
(Fig. 3). These methods involve the modification of HM transporter
genes and their uptake systems; improvement of the HM ligand synthesis
and conversion of the HM into less hazardous and volatile forms (Mosa
et al., 2016).
5.1. Modifying HM transporter genes and their uptake systems
Modification of different HM transporters has led to improved

4
S.A. Bhat et al.
Fig. 3. Schematic representation of biotechnological approaches to engineer plants for HM phytoremediation (Dhankher et al., 2012; Mosa et al., 2016).
tolerance and buildup of HMs in several plant species (Fig. 3). In Ara­
bidopsis thaliana, over-expression of YCF1 gene leads to improved
tolerance to Pb and Cd as well as larger buildup of HMs in plants (Song
et al., 2003). Improved Pb hypersensitivity and accumulation were
observed in transgenic plants overexpressing NtCBP4 protein from
Nicotiana tabacum. Moreover, enhanced expression of a truncated
variant of NtCBP4 improved Pb tolerance but decreased its accumula­
tion (Sunkar et al., 2000). Pb tolerance was also shown in T-DNA mu­
tants of the Arabidopsis CNGC1 gene, which produces a protein that is
similar to NtCBP4. According to these findings, NtCBP4 and AtCNGC1
are involved in the transfer of Pb2+ (Zeng et al. 2015). Expression of
CAX2 gene in Nicotiana tabacum resulted in higher Ca, Cd, and Mn ion
accumulation. CAX2 overexpression also boosted the transport of Cd and
Mn ions in isolated root tonoplast vesicles. (Hirschi et al., 2000). Rice
roots subjected to HM like As(V), Cd, Cr (VI), and Pb increased the
expression of both common and unique genes (Dubey et al., 2014).
Furthermore, utilizing a de novo transcriptome sequencing method, Cu
tolerant genes in the Paeonia ostii plant were discovered (Wang et al.,
2016).
5.2. Increasing heavy metal ligand synthesis
For HM detoxification or accumulation, cystine-rich peptides like
metallothioneins (MTs), phytochelatins and GSH are utilized as metal-
binding ligands. Over-expression of pea MT gene PsMTA, for example,
led to increased Cu ion accumulation in roots (Evans et al., 1992).
Transgenic plants with the E. coli GSH synthetase (GS) gene overex­
pressed in the Brassica juncea showed improved Cd tolerance (Liang Zhu,
Pilon-Smits et al., 1999). Over-expression of wheat TaPCS1 gene in
shrub tobacco seedlings cultivated in soil with 1572 ppm Pb acquired
twice as much Pb as WT plants (Gisbert et al., 2003). Plant species can
also be altered to improve their tolerance to Cd, Pb and As. When two
bacterial genes were co-expressed in Arabidopsis and cultivated in the
medium containing sodium arsenate (125 M), the double transgenic
plants accumulated three times more As in above-ground biomass
(Dhankher et al., 2002). Modifying genes to increase metal chelation
agent synthesis has a lot of potential for enhancing HM and metalloid
tolerance (reviewed by (Mosa et al., 2016). In A. thaliana and B. juncea,
constitutive overexpression of AtPCS1 enhanced arsenate resistance but
5
Chemosphere 303 (2022) 134788
did not increase shoot As accumulation (Li et al., 2004).
5.3. Converting heavy metals into less hazardous and volatile forms
Selenium (Se) is required as a micronutrient but its higher concen­
trations lead to its toxicity and it, therefore is considered a global
pollutant (Zwolak and Zaporowska, 2012). Plants take Se and convert
them into volatile forms like dimethyl selenide (DMSe). The goal of
biotechnological Se phytoremediation has been to improve Se tolerance,
bioaccumulation, and volatilization. (Pilon-Smits and LeDuc, 2009). In
Brassica juncea, over-expression APS gene from Arabidopsis increased
the reduction of selenate to organic Se forms, whereas WT plants
accumulated mostly selenate (Pilon-Smits et al., 1999).
6. Factors affecting phytoremediation of HMs
Plant types, root region, environmental conditions, root composition
and elemental species, as well as the soil physio-chemical and biological
properties, all have an effect on HM buildup and distribution in plants.
To improve remediation, agronomic practices have been introduced (pH
adjustments, chelators and fertilizers are some of the things that can be
done). The pH of soil, organic matter and phosphorus content are also
important factors to consider. To minimize Pb absorption by plants, the
soil pH can be changed with lime to between 6.5 and 7.0. (Traunfeld and
Clement, 2001). Moreover, plant’s ability to absorb HMs is influenced
by a number of factors as discussed below.
6.1. Phytoremediation friendly plant species
As previously mentioned, several characteristics of the affected plant
species influence the absorption of a metal. A contaminant-specific
hyper-accumulator is also needed for phytoremediation (Lorestani
et al., 2012). In this context, (Tariq and Ashraf, 2016) investigated the
phytoremediation capacity of different plant species viz., common
sunflower (Helianthus annuus), field mustard (Brassica campestris), corn
(Zea mays) and pea (Pisum sativum). They came to the conclusion that
hyperaccumulators had a variety of metal accumulation potentials. After
being treated with EDTA, zea mays was shown to be a hyperaccumulator
of Co and chrome, but common sunflower exhibited an affinity for Cd
S.A. Bhat et al. Chemosphere 303 (2022) 134788

under the same circumstances, and Brassica campestris showed hyper­
accumulating capabilities for Chrome. In the absence of EDTA, Pisum
sativum was shown to be the most efficient Pb accumulator. As a result,
a region-specific cropping method with the highest potential for HMs
accumulation should be studied and proposed. The species needs to be
chosen according to the type of contaminant present at the time of
transplantation. Table 3 lists plant species based on their ability to
accumulate HMs and their resistance to HMs.
metal tolerance genetic engineering, shoot translocation, aggregation
and sequestration to increase metal bioavailability, will all help to
improve phytoremediation efficiency. Table 4 shows the effects of
different factors on heavy metal bioexistency or/and accumulation
strength.
6.3. Phytoremediation in the root zone

In phytoremediation, plant root zone is particularly important

6.2. Medium properties
The characteristics and bioavailability of hazardous HMs to plants
are influenced by soil pH, texture, cation exchange capacity, tempera­
ture and nutrient content etc.(Zhou et al., 2014; Rosenfeld et al., 2018).
Soil properties and pH, which are the most important variables regu­
lating element availability in the soil for plant absorption, impact sol­
ubility and availability of metals. By minimizing HM adsorption by plant
tissues, a lower soil pH raises MM concentrations in the solution. If the
pH of the soil falls, the volume of H+ ions rises, increasing the cation
exchange efficiency for HMs. At low PH values, the desorption process
increases the penetration of HM’s from colloids and particles of minerals
into the earth (Sheoran et al., 2016). Thlaspi caerulescens is a Cd and Zn
hyperaccumulator that demonstrates the effectiveness of increased
metal uptake by lowering pH of the soil (Rosenfeld et al., 2018).
HMs are divided into two groups depending on their mobility in
common soil pH ranges: those with high mobility, such as Cd, Ni, Zn and
those with low mobility, such as Cu, Cr, and Pb (Kim et al., 2015). The
activation of all HMs is not uniformly caused by a decrease in soil pH
(Sun et al., 2010; Sheoran et al., 2016). HM mobilization increases with
more organic matter in the soil, which stimulates chelate formation,
enhances nutrient supply and enhances cation exchange capacity, both
of which increase metal availability in plants (Zeng et al., 2011; Her­
nandez-Soriano and Jimenez-Lopez, 2012; Sheoran et al., 2016).
Increased pH in organic matter also dissociates the functional groups
viz. alcoholic, carbonyl, carboxyl and phenolic, raising the affinity of
ligand ions to metal cations. Adding cattle manure to Glycine max soil
has been shown to improve Zn and Pb aggregation as it contains het­
erogeneous materials that can have both mobilizing and stabilizing
impacts (Chu et al., 2017).
Organic amendments of metal-contaminated soils with peat,
compost and biochar increase the soil’s cation-exchange potential
(CEC), provide sorption sites, minimize metal mobility, and encourage
higher binding affinity (Beiyuan, 2016; Egene et al., 2018). Metal ion
abundance decreases as soil CEC levels rise, while metal ion availability
decreases. Rhizo-biological activity, root exudation, moisture, pH,
temperature, competing ions (concentration), and metal content in soil
solution all affect root absorption factor (Ma et al., 2016). Recent
agronomic activities, which include the management of crop and soil,
Table 3
The propensity of different plant species to accumulate HMs.
Characteristics Heavy Plant species References
metal
(Elekes, 2014a,b; Elekes, 2014a,b), as it provides entry points through
metabolic pathways for pollutants to be absorbed, stored or metabolized
within plant tissue (Tangahu et al., 2011). The reduction of pollutants
into simpler or basic forms via some enzymes secreted from the root
system is another phytoremediation process (Merkl et al., 2005). By
transforming HMs and chemical speciation in soils, these proteins assist
in HM uptake (Laghlimi et al., 2015). Acidification/alkalinization, redox
potential changes, metal chelate, organic ligand and exudation in plant
roots can all influence HM speciation, and these processes can increase
metal solubility potential in the plant root system (Ma et al., 2016).
Precipitation, temperature, drought and soil moisture are all local
environmental variables that have an effect on root properties, these
influence root growth rate and length (Montagnoli et al., 2012;
McCormack and Guo, 2014). In addition to the dry soil’s reduced
permeability, morphological adaptations to drought stress include a rise
in root diameter and a decrease in root elongation (Brunner et al., 2015).
Land conditions vary from greenhouse conditions in terms of root
structure (Merkl et al., 2005). As a result, the study of root zone char­
acteristics and enzyme exudate composition may be the most efficient
screening approach for finding more accumulator plant species.
6.4. Phytoremediation promoters
These are factors or management strategies that increase related
phenomena such as phosphate-solubilizing bacteria as plant growth
promoters, growth hormone concentrations, and osmolytes, possibly
speeding up or raising the overall rate of HM buildup. Gibberellic acid,
for example, raises plant height by intermodal elongation. Plant meri­
stem activity and morphogenesis are regulated by phytohormones,
auxins and cytokinin, which play opposing roles in roots as well as in
shoots. The effective control on the phytoremediation accelerators, as
well as their optimal integration, can help to boost the final phytor­
emediation result. The major techniques to demonstrate phytor­
emediation’s relevance are to understand studies of biomass balance and
the metabolic fate of pollutants in plants (Arthur et al., 2005; Mwegoha,
2008).
Table 4
Effect of environmental factors on hHM supply and deposition potential on
different plant species.
Factor Heavy Plant species Condition Effect References
Metal
(HM)

A and S species Cd, Cr, Ni, Lemna minor Al-Khafaji et al. SM Ni A. murale, B. coddii ▴ SM ↑ Angle et al.
Pb (2018) (2003)
A and T species Cr, Cu Eichhornia crassipes Sarkar et al. (2017) pH Cd, Zn T. caerulescens ▾pH ↑ Wang et al.
MA and T species Zn, Pb P. australis Bernardini et al. (soil) (2006)
(2016) CEC Pb, Cd, Oryza sativa ▴CEC ↓ Zhou et al.
NA and T species Cu, Zn, Cd E. canadensis Török et al. (2015) Cu, Zn (2014)
MA and MS Zn, Cd, Pb Typha angustifolia Sricoth et al. (2018) Soil and Cu, Zn, Elodea canadensis, ▴T ↑ Fritioff et al.
species water Cd, Pb Potamogeton natans (2005)
A and MS species Pb (II), Hg Azolla filiculoides Arshadi et al. SOM Cr, Cu, Oryza sativa ▴ SOM ↑ Zeng et al.
(II) (2017) Fe, Mn, (2011)
S species Cd, Pb Ceratophyllum Dogan et al. (2018) Zn
demersum L.
Where T = temperature. CEC= Cation exchange capacity, SOM= Soil organic
Whereas; A = Accumulator, S = sensitive, T = tolerant NA= Non_Accumulator matter, SM= Soil moisture, ↑ = Enhance the metal accumulation, ↓ = Reduces
M = moderately, MA = Moderately accumulator, MS = Moderately sensitive. the metal uptake, ▴ = Increase, ▾ = Decrease.

6
S.A. Bhat et al.
6.5. Phytoremediation and environmental constraints
The most important and evident drawback to the applicability of
phytoremediation is the environment at a given place. Temperature
affects both pollutant absorption and removal as it regulates transpira­
tion, plant growth and metabolism (Bhargava et al., 2012). As the
temperature rises, the rate of metal removal via plants rises linearly (Yu
et al., 2010; Ali et al., 2016). (Fritioff et al., 2005), for example, looked
into the impact of salinity and temperature of the water on harmful
metal absorption in two submerged plant organisms, Elodea canadensis
(Michx.) and Potamogeton natans. Cu, Zn, Cd and Pb were added to the
plants and were grown at 5, 11 and 20 ◦ C with salinities of 0, 0.5 and 5%.
According to (Pourghasemian et al., 2013), the Carthamus tinctorius
(Safflower), absorbs more Cd at high temperatures than plants culti­
vated at lower temperatures. The soil moisture content (SMC), vapour
pressure deficit (VPD), relative humidity (RH) and soil heat fluxes (SHF)
all impact the distinct metabolic pathways of accumulators. When soil
moisture levels are greater, plants produce more biomass, which in­
creases the number of metal compounds that can be collected from the
soil (Shen et al., 2002; Schmidt, 2003; Marchiol et al., 2004).
The effects of high SMC on growth and Ni hyper-accumulation in 3
species: Berkheya coddii, Alyssum murale and Thlaspi caerulescens culti­
vars AB300 and AB336 have been investigated by Angle et al., (Angle
et al., 2003). According to their findings, hyperaccumulators flourish in
high-moisture soils, whereas biomass of all studied species was shown to
be higher at greater SMC levels and inhibited at lower SMC levels. The
physio-chemical qualities of the accumulates have an impact on plant
metabolism. Because plant roots absorb HMs from soils and air, aerosols
reach plants via the surface of leaves, emissions can have a complex
impact on mineral accumulation. Only a small percentage of the
microscopic metal particles adhere to the leaves and are absorbed. Cu,
Cd and Zn only enter the leaves to a limited amount, but Pb persists as a
surface deposit (Bhargava et al., 2012). As a result, standardization of
growing procedures to generate the maximum amounts of accumulators
and bioavailability of accumulates should be examined and examined
for every particular context. Physio-chemical and biological parameters
impact the HM phytoremediation rate based on the features of
contaminated areas as well as the organism (species) utilized for phy­
toremediation. As a result, future research should concentrate on easy,
chief site-specific phytoremediation techniques. In addition, plans for
potential polluted sites should be created.
7. Conclusion
Heavy metals (HMs) are one of the serious dangers to soil, water and
humans. The use of low-cost and environmentally-safe strategies seems
to be a potential approach to remediate these pollutants. As a result,
phytoremediation is among the most popular and effective plant-based
approaches for removing contaminants from contaminated areas while
causing minimal damage to water bodies or soil structure. The need to
intensify and accelerate phytoremediation emerged from research and
applications not only because of the benefits it provides as an ecological
process but also because of the drawbacks associated with the long time
it takes to remove HMs as well as threats HM toxicity poses to plant
integrity, heavy metals. The research examines the origins of HM
pollution, HM contamination of soil and water, and their harmful effects
on human health in this environment. The full study assists us in
determining how to choose a technique for a certain metal-bearing
effluent based on time consumption and efficiency, as well as identi­
fying commonly utilized plants for phytoremediation. Moreover, some
of the possibilities and strategies for enhancing phytoremediation viz.,
different phytoremediation techniques, biotechnological approaches,
plants used in various approaches, and variables impacting phytor­
emediation have been discussed thus creating perspectives for the
development of new strategies. In nutshell, phytoremediation may be
utilized as an economical, effective, environmentally and eco-friendly
7
Chemosphere 303 (2022) 134788
method related to the usage of metal-accumulating plants as an alter­
native method for HM cleanup. Novel plant species suitable for
extracting heavy metals from polluted soils must be introduced to
improve the process. Metal bioavailability-increasing strategies, such as
using bio-augmented acidified manure, can be used to lower the pH of
polluted soil and thereby increase heavy metal availability to plants.
Furthermore, genetic engineering and molecular science research can
make significant and innovative contributions to increasing the impact
of phytoremediation as a beneficial technique for improving and
increasing soil quality, as well as a method of recovering critical metals
from heavily polluted areas. Chelating agents and microbes can be
employed in conjunction with this technique to boost HM bioavail­
ability, allowing for greater heavy metal accumulation in plants and soil
cleanup. Further, more research is needed to better understand the im­
pacts of different types of catalysts on phytoremediation effectiveness in
order to increase the practicability of phytoremediation for environ­
mental restoration.
Credit author statement
Shakeel Ahmad Bhat, Omar Bashir: Data Curation, Investigation,
Formal Analysis, Methodology, Software, Resources, Writing-Original
Draft. Syed Anam Ul Haq, Tawheed Amin, Asif Rafiq, Mudasir Ali:
Conceptualization, Visualization, Resources, Validation, Supervision.
Juliana Heloisa Pinê Américo-Pinheiro: Visualization, Software,
Writing-Original Draft, Resources. Farooq Sher: Formal Analysis, Soft­
ware, Resources, Administration, Funding Acquisition, Supervision,
Submission, Reviewing and Editing.
Declaration of competing interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Acknowledgement
The authors are grateful for the financial support from the Engi­
neering and Physical Sciences Research Council (EPSRC) UK.
References
Ahmad, R., Tehsin, Z., Malik, S.T., Asad, S.A., Shahzad, M., Bilal, M., Shah, M.M.,
Khan, S.A., 2016. Phytoremediation potential of hemp (Cannabis sativa L.):
identification and characterization of heavy metals responsive genes. Clean 44 (2),
195–201.
Ahmadpour, P., Ahmadpour, F., Mahmud, T., Abdu, A., Soleimani, M., Tayefeh, F.H.,
2012. Phytoremediation of heavy metals: a green technology. Afr. J. Biotechnol. 11
(76), 14036–14043.
Ainza, C., Trevors, J., Saier, M., 2010. Environmental mercury rising. Water Air Soil
Pollut. 205 (1), 47–48.
Al-Khafaji, M.S., Al-Ani, F.H., Ibrahim, A.F., 2018. Removal of some heavy metals from
industrial wastewater by Lemmna minor. KSCE J. Civ. Eng. 22 (4), 1077–1082.
Ali, H., Khan, E., 2018. What are heavy metals? Long-standing controversy over the
scientific use of the term ‘heavy metals’–proposal of a comprehensive definition.
Toxicol. Environ. Chem. 100 (1), 6–19.
Ali, H., Khan, E., Ilahi, I., 2019. Environmental chemistry and ecotoxicology of
hazardous heavy metals: environmental persistence, toxicity, and bioaccumulation.
J. Chem. 2019.
Ali, H., Khan, E., Sajad, M.A., 2013. Phytoremediation of heavy metals—concepts and
applications. Chemosphere 91 (7), 869–881.
Ali, I., Mbianda, X., Burakov, A., Galunin, E., Burakova, I., Mkrtchyan, E., Tkachev, A.,
Grachev, V., 2019. Graphene based adsorbents for remediation of noxious pollutants
from wastewater. Environ. Int. 127, 160–180.
Ali, R.M., Hamad, H.A., Hussein, M.M., Malash, G.F., 2016. Potential of using green
adsorbent of heavy metal removal from aqueous solutions: adsorption kinetics,
isotherm, thermodynamic, mechanism and economic analysis. Ecol. Eng. 91,
317–332.
Alizadeh-Kouskuie, A., Atapour, H., Rahmani, F., 2020. Assessing the geochemical and
environmental baseline of heavy metals in soils around hydrothermal
hematite–barite–galena veins in Baghin area, Kerman, Iran. Environ. Geochem.
Health 42 (11), 4011–4036.
S.A. Bhat et al.
Alloway, B.J., 2012. Heavy Metals in Soils: Trace Metals and Metalloids in Soils and
Their Bioavailability. Springer Science & Business Media.
Angle, J.S., Baker, A.J., Whiting, S.N., Chaney, R.L., 2003. Soil moisture effects on uptake
of metals by Thlaspi, Alyssum, and Berkheya. Plant Soil 256 (2), 325–332.
Arora, M., Kiran, B., Rani, S., Rani, A., Kaur, B., Mittal, N., 2008. Heavy metal
accumulation in vegetables irrigated with water from different sources. Food Chem.
111 (4), 811–815.
Arshadi, M., Abdolmaleki, M., Mousavinia, F., Foroughifard, S., Karimzadeh, A., 2017.
Nano modification of NZVI with an aquatic plant Azolla filiculoides to remove Pb (II)
and Hg (II) from water: aging time and mechanism study. J. Colloid Interface Sci.
486, 296–308.
Arthur, E.L., Rice, P.J., Rice, P.J., Anderson, T.A., Baladi, S.M., Henderson, K.L., Coats, J.
R., 2005. Phytoremediation—an overview. Crit. Rev. Plant Sci. 24 (2), 109–122.
Asati, A., Pichhode, M., Nikhil, K., 2016. Effect of heavy metals on plants: an overview.
Int. J. Appl. Innov. Eng. Manag. 5 (3), 56–66.
Ashraf, S., Ali, Q., Zahir, Z.A., Ashraf, S., Asghar, H.N., 2019. Phytoremediation:
environmentally sustainable way for reclamation of heavy metal polluted soils.
Ecotoxicol. Environ. Saf. 174, 714–727.
Awa, S.H., Hadibarata, T., 2020. Removal of heavy metals in contaminated soil by
phytoremediation mechanism: a review. Water, Air, Soil Pollut. 231 (2), 1–15.
Baby, J., Raj, J.S., Biby, E.T., Sankarganesh, P., Jeevitha, M., Ajisha, S., Rajan, S.S., 2010.
Toxic effect of heavy metals on aquatic environment. Int. J. Brain Cognit. Sci. 4 (4).
Bansod, B., Kumar, T., Thakur, R., Rana, S., Singh, I., 2017. A review on various
electrochemical techniques for heavy metal ions detection with different sensing
platforms. Biosens. Bioelectron. 94, 443–455.
Beiyuan, J., 2016. Integrated Remediation of Metal-Contaminated Soils: Biodegradable
Chelant-Enhanced Extraction and In-Situ Stabilization.
Bello, S., Nasiru, R., Garba, N., Adeyemo, D., 2019. Carcinogenic and non-carcinogenic
health risk assessment of heavy metals exposure from Shanono and Bagwai artisanal
gold mines, Kano state, Nigeria. Sci. Afr. 6, e00197.
Benavides, L.C.L., Pinilla, L.A.C., Serrezuela, R.R., Serrezuela, W.F.R., 2018. Extraction
in laboratory of heavy metals through rhizofiltration using the plant Zea mays
(maize). Int. J. Appl. Environ. Sci. 13 (1), 9–26.
Bernardini, A., Salvatori, E., Guerrini, V., Fusaro, L., Canepari, S., Manes, F., 2016.
Effects of high Zn and Pb concentrations on Phragmites australis (Cav.) Trin. Ex.
Steudel: photosynthetic performance and metal accumulation capacity under
controlled conditions. Int. J. Phytoremediation 18 (1), 16–24.
Bhargava, A., Carmona, F.F., Bhargava, M., Srivastava, S., 2012. Approaches for
enhanced phytoextraction of heavy metals. J. Environ. Manag. 105, 103–120.
Bhat, R.A., Singh, D.V., Qadri, H., Dar, G.H., Dervash, M.A., Bhat, S.A., Unal, B.T.,
Ozturk, M., Hakeem, K.R., Yousaf, B., 2022. Vulnerability of municipal solid waste:
An emerging threat to aquatic ecosystems. Chemosphere 287. https://doi.org/
10.1016/j.chemosphere.2021.132223.
Bian, X., Cui, J., Tang, B., Yang, L., 2018. Chelant-induced phytoextraction of heavy
metals from contaminated soils: a review. Pol. J. Environ. Stud. 27 (6), 2417–2424.
Brunner, I., Herzog, C., Dawes, M.A., Arend, M., Sperisen, C., 2015. How tree roots
respond to drought. Front. Plant Sci. 6, 547.
Callender, E., 2004. Heavy metals in environment-historical trends. Treatise Geochem 9,
67–105.
Cao, J., Wang, G., Wang, T., Chen, J., Wenjing, G., Wu, P., He, X., Xie, L., 2019. Copper
caused reproductive endocrine disruption in zebrafish (Danio rerio). Aquat. Toxicol.
211, 124–136.
Chai, L., Ding, C., Tang, C., Yang, W., Yang, Z., Wang, Y., Liao, Q., Li, J., 2018.
Discerning three novel chromate reduce and transport genes of highly efficient
Pannonibacter phragmitetus BB: from genome to gene and protein. Ecotoxicol.
Environ. Saf. 162, 139–146.
Chandra, R., Kumar, V., 2017. Phytoextraction of heavy metals by potential native plants
and their microscopic observation of root growing on stabilised distillery sludge as a
prospective tool for in situ phytoremediation of industrial waste. Environ. Sci. Pollut.
Control Ser. 24 (3), 2605–2619.
Chaoua, S., Boussaa, S., El Gharmali, A., Boumezzough, A., 2019. Impact of irrigation
with wastewater on accumulation of heavy metals in soil and crops in the region of
Marrakech in Morocco. J. Saudi Soc. Agri. Sci. 18 (4), 429–436.
Chu, Q., Sha, Z., Osaki, M., Watanabe, T., 2017. Contrasting effects of cattle manure
applications and root-induced changes on heavy metal dynamics in the rhizosphere
of soybean in an acidic haplic fluvisol: a chronological pot experiment. J. Agric. Food
Chem. 65 (15), 3085–3095.
Das, K., Das, S., Dhundasi, S., 2008. Nickel, its adverse health effects & oxidative stress.
Indian J. Med. Res. 128 (4), 412.
de Figueiredo, C.C., Chagas, J.K.M., da Silva, J., Paz-Ferreiro, J., 2019. Short-term effects
of a sewage sludge biochar amendment on total and available heavy metal content of
a tropical soil. Geoderma 344, 31–39.
Degraeve, N., 1981. Carcinogenic, teratogenic and mutagenic effects of cadmium. Mutat.
Res. Rev. Genet. Toxicol. 86 (1), 115–135.
Dhankher, O.P., Li, Y., Rosen, B.P., Shi, J., Salt, D., Senecoff, J.F., Sashti, N.A.,
Meagher, R.B., 2002. Engineering tolerance and hyperaccumulation of arsenic in
plants by combining arsenate reductase and γ-glutamylcysteine synthetase
expression. Nat. Biotechnol. 20 (11), 1140–1145.
Dhankher, O.P., Pilon-Smits, E.A., Meagher, R.B., Doty, S., 2012. Biotechnological
Approaches for Phytoremediation. Plant Biotechnology and Agriculture. Elsevier,
pp. 309–328.
Dogan, M., Karatas, M., Aasim, M., 2018. Cadmium and lead bioaccumulation potentials
of an aquatic macrophyte Ceratophyllum demersum L.: a laboratory study.
Ecotoxicol. Environ. Saf. 148, 431–440.
Dubey, S., Shri, M., Misra, P., Lakhwani, D., Bag, S.K., Asif, M.H., Trivedi, P.K.,
Tripathi, R.D., Chakrabarty, D., 2014. Heavy metals induce oxidative stress and
8
Chemosphere 303 (2022) 134788
genome-wide modulation in transcriptome of rice root. Funct. Integr. Genom. 14 (2),
401–417.
Dumont, E.R., Larue, C., Lorber, S., Gryta, H., Billoir, E., Gross, E.M., Elger, A., 2019.
Does intraspecific variability matter in ecological risk assessment? Investigation of
genotypic variations in three macrophyte species exposed to copper. Aquat. Toxicol.
211, 29–37.
Duruibe, J.O., Ogwuegbu, M., Egwurugwu, J., 2007. Heavy metal pollution and human
biotoxic effects. Int. J. Phys. Sci. 2 (5), 112–118.
Egene, C.E., Van Poucke, R., Ok, Y.S., Meers, E., Tack, F., 2018. Impact of organic
amendments (biochar, compost and peat) on Cd and Zn mobility and solubility in
contaminated soil of the Campine region after three years. Sci. Total Environ. 626,
195–202.
Eid, E.M., Galal, T.M., Sewelam, N.A., Talha, N.I., Abdallah, S.M., 2020.
Phytoremediation of heavy metals by four aquatic macrophytes and their potential
use as contamination indicators: a comparative assessment. Environ. Sci. Pollut.
Control Ser. 27 (11), 12138–12151.
Ekmekyapar, F., Sabudak, T., Seren, G., 2012. Assessment of heavy metal contamination
in soil and wheat (Triticum aestivum L.) plant around the Çorlu–Çerkezkoy highway
in Thrace region. Glob. NEST J. 14 (4), 496–504.
Elekes, C.C., 2014a. Assessment of Historical Heavy Metal Pollution of Land in the
Proximity of Industrial Area of Targoviste, Romania. Environmental Risk Assessment
of Soil Contamination, p. 257.
Elekes, C.C., 2014b. "Eco-technological Solutions for the Remediation of Polluted Soil
and Heavy Metal recovery." Environmental Risk Assessment of Soil Contamination.
InTech, Rijeka, pp. 309–335.
Ene, A., Bosneaga, A., Georgescu, L., 2010. Determination of heavy metals in soils using
XRF technique. Rom. J. Phys. 55 (7–8), 815–820.
Evans, K.M., Gatehouse, J.A., Lindsay, W.P., Shi, J., Tommey, A.M., Robinson, N.J.,
1992. Expression of the pea metallothionein-like gene PsMT A in Escherichia coli
and Arabidopsis thaliana and analysis of trace metal ion accumulation: implications
for PsMT A function. Plant Mol. Biol. 20 (6), 1019–1028.
Fritioff, Å., Kautsky, L., Greger, M., 2005. Influence of temperature and salinity on heavy
metal uptake by submersed plants. Environ. Pollut. 133 (2), 265–274.
Galal, T.M., Gharib, F.A., Ghazi, S.M., Mansour, K.H., 2017. Phytostabilization of heavy
metals by the emergent macrophyte Vossia cuspidata (Roxb.) Griff.: a
phytoremediation approach. Int. J. Phytoremediation 19 (11), 992–999.
Ghosh, S., 2010. Wetland macrophytes as toxic metal accumulators. Int. J. Environ. Sci. 1
(4), 523.
Gisbert, C., Ros, R., De Haro, A., Walker, D.J., Bernal, M.P., Serrano, R., Navarro-
Aviñó, J., 2003. A plant genetically modified that accumulates Pb is especially
promising for phytoremediation. Biochem. Biophys. Res. Commun. 303 (2),
440–445.
Hadia-e-Fatima, A.A., 2018. Heavy metal pollution–A mini review. J. Bacteriol. Mycol.
Open. Access 6 (3), 179–181.
Haferburg, G., Kothe, E., 2007. Microbes and metals: interactions in the environment.
J. Basic Microbiol. 47 (6), 453–467.
Haroon, B., Ping, A., Pervez, A., Faridullah, F., Irshad, M., 2019. Characterization of
heavy metal in soils as affected by long-term irrigation with industrial wastewater.
J. Water Reuse Desalin. 9 (1), 47–56.
Harrison, R.M., Laxen, D.P., Wilson, S.J., 1981. Chemical associations of lead, cadmium,
copper, and zinc in street dusts and roadside soils. Environ. Sci. Technol. 15 (11),
1378–1383.
Hernandez-Soriano, M.C., Jimenez-Lopez, J.C., 2012. Effects of soil water content and
organic matter addition on the speciation and bioavailability of heavy metals. Sci.
Total Environ. 423, 55–61.
Hess, R., Schmid, B., 2002. Zinc supplement overdose can have toxic effects. J. Paediatr.
Haematol./Oncol 24, 582–584.
Hirschi, K.D., Korenkov, V.D., Wilganowski, N.L., Wagner, G.J., 2000. Expression of
Arabidopsis CAX2 in tobacco. Altered metal accumulation and increased manganese
tolerance. Plant physiology 124 (1), 125–134.
Jia, Z., Wang, J., Zhou, X., Zhou, Y., Li, Y., Li, B., Zhou, S., 2020. Identification of the
sources and influencing factors of potentially toxic elements accumulation in the soil
from a typical karst region in Guangxi, Southwest China. Environ. Pollut. 256,
113505.
Kapoor, D., Singh, M.P., 2021. Heavy Metal Contamination in Water and its Possible
Sources. Heavy Metals in the Environment. Elsevier, pp. 179–189.
Kara, Y., 2005. Bioaccumulation of Cu, Zn and Ni from the wastewater by treated
Nasturtium officinale. Int. J. Environ. Sci. Technol. 2 (1), 63–67.
Kelly, J., Thornton, I., Simpson, P., 1996. Urban geochemistry: a study of the influence of
anthropogenic activity on the heavy metal content of soils in traditionally industrial
and non-industrial areas of Britain. Appl. Geochem. 11 (1–2), 363–370.
Khan, M.A., Ahmad, I., Rahman, I.U., 2007. Effect of environmental pollution on heavy
metals content of Withania somnifera. J. Chin. Chem. Soc. 54 (2), 339–343.
Kim, H.N., Ren, W.X., Kim, J.S., Yoon, J., 2012. Fluorescent and colorimetric sensors for
detection of lead, cadmium, and mercury ions. Chem. Soc. Rev. 41 (8), 3210–3244.
Kim, R.-Y., Yoon, J.-K., Kim, T.-S., Yang, J.E., Owens, G., Kim, K.-R., 2015.
Bioavailability of heavy metals in soils: definitions and practical implementation—a
critical review. Environ. Geochem. Health 37 (6), 1041–1061.
Kumar, S.S., Kadier, A., Malyan, S.K., Ahmad, A., Bishnoi, N.R., 2017. "Phytoremediation
and Rhizoremediation: Uptake, Mobilization and Sequestration of Heavy Metals by
plants." Plant-Microbe Interactions in Agro-Ecological Perspectives, pp. 367–394.
Laghlimi, M., Baghdad, B., El Hadi, H., Bouabdli, A., 2015. Phytoremediation
mechanisms of heavy metal contaminated soils: a review. Open J. Ecol. 5 (8), 375.
Lajayer, B.A., Moghadam, N.K., Maghsoodi, M.R., Ghorbanpour, M., Kariman, K., 2019.
Phytoextraction of heavy metals from contaminated soil, water and atmosphere
S.A. Bhat et al.
using ornamental plants: mechanisms and efficiency improvement strategies.
Environ. Sci. Pollut. Control Ser. 26 (9), 8468–8484.
Li, Y., Dhankher, O.P., Carreira, L., Lee, D., Chen, A., Schroeder, J.I., Balish, R.S.,
Meagher, R.B., 2004. Overexpression of phytochelatin synthase in Arabidopsis leads
to enhanced arsenic tolerance and cadmium hypersensitivity. Plant Cell Physiol. 45
(12), 1787–1797.
Liang Zhu, Y., Pilon-Smits, E.A., Jouanin, L., Terry, N., 1999. Overexpression of
glutathione synthetase in Indian mustard enhances cadmium accumulation and
tolerance. Plant physiology 119 (1), 73–80.
Lorestani, B., Cheraghi, M., Yousefi, N., 2012. The potential of phytoremediation using
hyperaccumulator plants: a case study at a lead-zinc mine site. Int. J.
Phytoremediation 14 (8), 786–795.
Luo, Y., Wu, Y., Qiu, J., Wang, H., Yang, L., 2019. Suitability of four woody plant species
for the phytostabilization of a zinc smelting slag site after 5 years of assisted
revegetation. J. Soils Sediments 19 (2), 702–715.
Ma, Y., Oliveira, R.S., Freitas, H., Zhang, C., 2016. Biochemical and molecular
mechanisms of plant-microbe-metal interactions: relevance for phytoremediation.
Front. Plant Sci. 7, 918.
Makarova, A., Nikulina, E., Avdeenkova, T., Pishaeva, K., 2021. The improved
phytoextraction of heavy metals and the growth of Trifolium repens L.: the role of
K2HEDP and plant growth regulators alone and in combination. Sustainability 13
(5), 2432.
Malayeri, B.E., Chehregani, A., Yousefi, N., Lorestani, B., 2008. Identification of the
hyper accumulator plants in copper and iron mine in Iran. Pakistan J. Biol. Sci.: PJBS
11 (3), 490–492.
Marchiol, L., Assolari, S., Sacco, P., Zerbi, G., 2004. Phytoextraction of heavy metals by
canola (Brassica napus) and radish (Raphanus sativus) grown on multicontaminated
soil. Environ. Pollut. 132 (1), 21–27.
Marella, T.K., Saxena, A., Tiwari, A., 2020. Diatom mediated heavy metal remediation: a
review. Bioresour. Technol. 305, 123068.
McCormack, M.L., Guo, D., 2014. Impacts of environmental factors on fine root lifespan.
Front. Plant Sci. 5, 205.
Merkl, N., Schultze-Kraft, R., Infante, C., 2005. Phytoremediation in the
tropics–influence of heavy crude oil on root morphological characteristics of
graminoids. Environ. Pollut. 138 (1), 86–91.
Mishra, S., Dwivedi, S.P., Singh, R., 2010. A review on epigenetic effect of heavy metal
carcinogens on human health. Open Nutraceuticals J. 3 (1).
Montagnoli, A., Terzaghi, M., Di Iorio, A., Scippa, G.S., Chiatante, D., 2012. Fine-root
morphological and growth traits in a Turkey-oak stand in relation to seasonal
changes in soil moisture in the Southern Apennines, Italy. Ecol. Res. 27 (6),
1015–1025.
Mosa, K.A., Saadoun, I., Kumar, K., Helmy, M., Dhankher, O.P., 2016. Potential
biotechnological strategies for the cleanup of heavy metals and metalloids. Front.
Plant Sci. 7, 303.
Mudipalli, A., 2008. Metals (micro nutrients or toxicants) & Global Health. Indian J.
Med. Res. 128 (4), 331.
Muthusaravanan, S., Sivarajasekar, N., Vivek, J., Paramasivan, T., Naushad, M.,
Prakashmaran, J., Gayathri, V., Al-Duaij, O.K., 2018. Phytoremediation of heavy
metals: mechanisms, methods and enhancements. Environ. Chem. Lett. 16 (4),
1339–1359.
Mwegoha, W.J., 2008. The use of phytoremediation technology for abatement soil and
groundwater pollution in Tanzania: opportunities and challenges. J. Sustain. Dev.
Afr. 10 (1), 140–156.
Nanda, M., Kumar, V., Sharma, D., 2019. Multimetal tolerance mechanisms in bacteria:
the resistance strategies acquired by bacteria that can be exploited to ‘clean-
up’heavy metal contaminants from water. Aquat. Toxicol. 212, 1–10.
Odinga, C.A., Kumar, A., Mthembu, M.S., Bux, F., Swalaha, F.M., 2019. Rhizofiltration
system consisting of Phragmites australis and Kyllinga nemoralis: evaluation of
efficient removal of metals and pathogenic microorganisms. Desalination Water
Treat. 169, 120–132.
Pan, L.-b., Ma, J., Wang, X.-l., Hou, H., 2016. Heavy metals in soils from a typical county
in Shanxi Province, China: levels, sources and spatial distribution. Chemosphere
148, 248–254.
Peralta, E., Pérez, G., Ojeda, G., Alcañiz, J.M., Valiente, M., López-Mesas, M., Sánchez-
Martín, M.-J., 2020. Heavy metal availability assessment using portable X-ray
fluorescence and single extraction procedures on former vineyard polluted soils. Sci.
Total Environ. 726, 138670.
Pilon-Smits, E.A., Hwang, S., Mel Lytle, C., Zhu, Y., Tai, J.C., Bravo, R.C., Chen, Y.,
Leustek, T., Terry, N., 1999. Overexpression of ATP sulfurylase in Indian mustard
leads to increased selenate uptake, reduction, and tolerance. Plant physiology 119
(1), 123–132.
Pilon-Smits, E.A., LeDuc, D.L., 2009. Phytoremediation of selenium using transgenic
plants. Curr. Opin. Biotechnol. 20 (2), 207–212.
Pourghasemian, N., Ehsanzadeh, P., Greger, M., 2013. Genotypic variation in safflower
(Carthamus spp.) cadmium accumulation and tolerance affected by temperature and
cadmium levels. Environ. Exp. Bot. 87, 218–226.
Prieto, M., Acevedo, S., Prieto, G., González, N., 2018. Phytoremediation of soils
contaminated with heavy metals. Biodiversity Int. J 2, 362–376.
Rizwan, M., Ali, S., ur Rehman, M.Z., Maqbool, A., 2019. A critical review on the effects
of zinc at toxic levels of cadmium in plants. Environ. Sci. Pollut. Control Ser. 26 (7),
6279–6289.
Rosenfeld, C.E., Chaney, R.L., Martínez, C.E., 2018. Soil geochemical factors regulate Cd
accumulation by metal hyperaccumulating Noccaea caerulescens (J. Presl & C. Presl)
FK Mey in field-contaminated soils. Sci. Total Environ. 616, 279–287.
9
Chemosphere 303 (2022) 134788
Saha, S., Saha, B.N., Pati, S., Pal, B., Hazra, G.C., 2017. Agricultural use of sewage sludge
in India: benefits and potential risk of heavy metals contamination and possible
remediation options–a review. Int. J. Environ. Technol. Manag. 20 (3–4), 183–199.
Saif, S., Khan, M., 2017. Assessment of heavy metals toxicity on plant growth promoting
rhizobacteria and seedling characteristics of Pseudomonas putida SFB3 inoculated
greengram. Acta Sci. Agric 1, 47–56.
Sakakibara, M., Watanabe, A., Inoue, M., Sano, S., Kaise, T., 2010. Phytoextraction and
phytovolatilization of arsenic from As-contaminated soils by Pteris vittata. In:
Proceedings of the Annual International Conference on Soils, Sediments, Water and
Energy.
Sakizadeh, M., Ghorbani, H., 2017. Concentration of heavy metals in soil and staple
crops and the associated health risk. Archive. Hygine Sci. 6 (4), 303–313.
Salem, H.M., Eweida, E.A., Farag, A., 2000. Heavy metals in drinking water and their
environmental impact on human health. Int. Conf. Environ. Hazard. Mitigat. (Cairo
Univ Egypt).
Sandeep, G., Vijayalatha, K., Anitha, T., 2019. Heavy metals and its impact in vegetable
crops. Int. J. Chem. Stud. 7 (1), 1612–1621.
Saran, A., Fernandez, L., Cora, F., Savio, M., Thijs, S., Vangronsveld, J., Merini, L.J.,
2020. Phytostabilization of Pb and Cd polluted soils using Helianthus petiolaris as
pioneer aromatic plant species. Int. J. Phytoremediation 22 (5), 459–467.
Sarkar, M., Rahman, A., Bhoumik, N., 2017. Remediation of chromium and copper on
water hyacinth (E. crassipes) shoot powder. Water Resour. Ind. 17, 1–6.
Schmidt, U., 2003. Enhancing phytoextraction: the effect of chemical soil manipulation
on mobility, plant accumulation, and leaching of heavy metals. J. Environ. Qual. 32
(6), 1939–1954.
Shah, V., Daverey, A., 2020. Phytoremediation: a multidisciplinary approach to clean up
heavy metal contaminated soil. Environ. Technol. Innovat. 18, 100774.
Shen, Z.G., Li, X.D., Wang, C.C., Chen, H.M., Chua, H., 2002. Lead phytoextraction from
contaminated soil with high-biomass plant species. J. Environ. Qual. 31 (6),
1893–1900.
Sheoran, V., Sheoran, A.S., Poonia, P., 2016. Factors affecting phytoextraction: a review.
Pedosphere 26 (2), 148–166.
Singh, P.K., Wang, W., Shrivastava, A.K., 2018. Cadmium-mediated morphological,
biochemical and physiological tuning in three different Anabaena species. Aquat.
Toxicol. 202, 36–45.
Song Y, W, Sohn J, E, Martinoia, E, Lee J, Y, Yang Y, Y, Jasinski, M, Forstier, C, Hwang, I,
Lee, Y, et al., 2003. Engineering tolerance and accumulation of lead and camium in
transgenic plants. Nature Biotech 21, 914–919. In this issue.
Sricoth, T., Meeinkuirt, W., Pichtel, J., Taeprayoon, P., Saengwilai, P., 2018. Synergistic
phytoremediation of wastewater by two aquatic plants (Typha angustifolia and
Eichhornia crassipes) and potential as biomass fuel. Environ. Sci. Pollut. Control Ser.
25 (6), 5344–5358.
Srivastava, V., Sarkar, A., Singh, S., Singh, P., de Araujo, A.S., Singh, R.P., 2017.
Agroecological responses of heavy metal pollution with special emphasis on soil
health and plant performances. Front. Environ. Sci. 5, 64.
Sun, C., Liu, J., Wang, Y., Sun, L., Yu, H., 2013. Multivariate and geostatistical analyses
of the spatial distribution and sources of heavy metals in agricultural soil in Dehui,
Northeast China. Chemosphere 92 (5), 517–523.
Sun, H.-F., Li, Y.-H., Ji, Y.-F., Yang, L.-S., Wang, W.-Y., Li, H.-R., 2010. Environmental
contamination and health hazard of lead and cadmium around Chatian mercury
mining deposit in western Hunan Province, China. Trans. Nonferrous Metals Soc.
China 20 (2), 308–314.
Sunkar, R., Kaplan, B., Bouché, N., Arazi, T., Dolev, D., Talke, I.N., Maathuis, F.J.,
Sanders, D., Bouchez, D., Fromm, H., 2000. Expression of a truncated tobacco
NtCBP4 channel in transgenic plants and disruption of the homologous Arabidopsis
CNGC1 gene confer Pb2+ tolerance. Plant J. 24 (4), 533–542.
Tangahu, B.V., Sheikh Abdullah, S.R., Basri, H., Idris, M., Anuar, N., Mukhlisin, M., 2011.
A review on heavy metals (As, Pb, and Hg) uptake by plants through
phytoremediation. Int. J. Chem. Eng. 2011.
Tariq, S.R., Ashraf, A., 2016. Comparative evaluation of phytoremediation of metal
contaminated soil of firing range by four different plant species. Arab. J. Chem. 9 (6),
806–814.
Török, A., Gulyás, Z., Szalai, G., Kocsy, G., Majdik, C., 2015. Phytoremediation capacity
of aquatic plants is associated with the degree of phytochelatin polymerization.
J. Hazard Mater. 299, 371–378.
Traunfeld, J., Clement, D., 2001. Lead in Garden Soils. Home and Garden. Maryland
Cooperative Extention, University of Maryland, pp. 333–336.
Tripathi, R.D., Srivastava, S., Mishra, S., Singh, N., Tuli, R., Gupta, D.K., Maathuis, F.J.,
2007. Arsenic hazards: strategies for tolerance and remediation by plants. Trends
Biotechnol. 25 (4), 158–165.
Turer, D.G., Maynard, B.J., 2003. Heavy metal contamination in highway soils.
Comparison of Corpus Christi, Texas and Cincinnati, Ohio shows organic matter is
key to mobility. Clean Technol. Environ. Policy 4 (4), 235–245.
Ugya, A., Ahmad, A., Adamu, H., Giwa, S., Imam, T., 2019. Phytoextraction of heavy
metals and risk associated with vegetables grown from soil irrigated with refinery
wastewater. J. Appl. Biol. Biotechnol. 7 (2), 14–19.
Vardhan, K.H., Kumar, P.S., Panda, R.C., 2019. A review on heavy metal pollution,
toxicity and remedial measures: current trends and future perspectives. J. Mol. Liq.
290, 111197.
Verma, A., Roy, A., Bharadvaja, N., 2021. Remediation of Heavy Metals Using
Nanophytoremediation. Advanced Oxidation Processes for Effluent Treatment
Plants. Elsevier, pp. 273–296.
Wang, A.S., Angle, J.S., Chaney, R.L., Delorme, T.A., Reeves, R.D., 2006. Soil pH effects
on uptake of Cd and Zn by Thlaspi caerulescens. Plant Soil 281 (1), 325–337.
S.A. Bhat et al.
Wang, Y., Dong, C., Xue, Z., Jin, Q., Xu, Y., 2016. De novo transcriptome sequencing and
discovery of genes related to copper tolerance in Paeonia ostii. Gene 576 (1),
126–135.
Wang, Y., Liu, Y., Zhan, W., Zheng, K., Wang, J., Zhang, C., Chen, R., 2020a. Stabilization
of heavy metal-contaminated soils by biochar: challenges and recommendations. Sci.
Total Environ. 729, 139060.
Wang, Y., Luo, Y., Zeng, G., Wu, X., Wu, B., Li, X., Xu, H., 2020b. Characteristics and in
situ remediation effects of heavy metal immobilizing bacteria on cadmium and
nickel co-contaminated soil. Ecotoxicol. Environ. Saf. 192, 110294.
Wuana, R.A., Okieimen, F.E., 2011. Heavy metals in contaminated soils: a review of
sources, chemistry, risks and best available strategies for remediation. Int. Sch. Res.
Notices 2011.
Yadav, K.K., Gupta, N., Kumar, A., Reece, L.M., Singh, N., Rezania, S., Khan, S.A., 2018.
Mechanistic understanding and holistic approach of phytoremediation: a review on
application and future prospects. Ecol. Eng. 120, 274–298.
Yadav, K.K., Gupta, N., Kumar, V., Singh, J.K., 2017a. Bioremediation of heavy metals
from contaminated sites using potential species: a review. Indian J. Environ. Protect.
37 (1), 65.
Yadav, K., Singh, J., Gupta, N., Kumar, V., 2017b. A review of nanobioremediation
technologies for environmental cleanup: a novel biological approach. J. Mater.
Environ. Sci. 8 (2), 740–757.
10
Chemosphere 303 (2022) 134788
Yan, A., Wang, Y., Tan, S.N., Yusof, M.L.M., Ghosh, S., Chen, Z., 2020. Phytoremediation:
a promising approach for revegetation of heavy metal-polluted land. Front. Plant Sci.
11.
Ye, S., Zeng, G., Wu, H., Zhang, C., Dai, J., Liang, J., Yu, J., Ren, X., Yi, H., Cheng, M.,
2017. Biological technologies for the remediation of co-contaminated soil. Crit. Rev.
Biotechnol. 37 (8), 1062–1076.
Yu, X.-Z., Peng, X.-Y., Xing, L.-Q., 2010. Effect of temperature on phytoextraction of
hexavalent and trivalent chromium by hybrid willows. Ecotoxicology 19 (1), 61–68.
Zeng, F., Ali, S., Zhang, H., Ouyang, Y., Qiu, B., Wu, F., Zhang, G., 2011. The influence of
pH and organic matter content in paddy soil on heavy metal availability and their
uptake by rice plants. Environ. Pollut. 159 (1), 84–91.
Zhang, J., Yang, R., Li, Y.C., Peng, Y., Wen, X., Ni, X., 2020. Distribution, accumulation,
and potential risks of heavy metals in soil and tea leaves from geologically different
plantations. Ecotoxicol. Environ. Saf. 195, 110475.
Zhou, H., Zhou, X., Zeng, M., Liao, B.-H., Liu, L., Yang, W.-T., Wu, Y.-M., Qiu, Q.-Y.,
Wang, Y.-J., 2014. Effects of combined amendments on heavy metal accumulation in
rice (Oryza sativa L.) planted on contaminated paddy soil. Ecotoxicol. Environ. Saf.
101, 226–232.
Zoroddu, M.A., Aaseth, J., Crisponi, G., Medici, S., Peana, M., Nurchi, V.M., 2019. The
essential metals for humans: a brief overview. J. Inorg. Biochem. 195, 120–129.
Zwolak, I., Zaporowska, H., 2012. Selenium interactions and toxicity: a review. Cell Biol.
Toxicol. 28 (1), 31–46.