plants

Review
Assisting Phytoremediation of Heavy Metals Using
Chemical Amendments
Md. Mahadi Hasan 1 , Md. Nashir Uddin 2 , Iffat Ara-Sharmeen 3 , Hesham F. Alharby 4 ,
Yahya Alzahrani 4 , Khalid Rehman Hakeem 4 and Li Zhang 5, *
1 State Key Laboratory of Grassland Agro-Ecosystems, School of Life Sciences, Lanzhou University,
Lanzhou 730000, China
2 Department of Biochemistry and Microbiology, School of Health and Life Sciences, North South University,
Dhaka 1229, Bangladesh
3 Department of Biochemistry, School of Life Science, Independent University, Dhaka 1229, Bangladesh
4 Department of Biological Sciences, Faculty of Science, King Abdulaziz University,
Jeddah 21577, Saudi Arabia
5 Institute of Cell Biology, School of Life Sciences, Lanzhou University, No.222 South TianShui Road,
Lanzhou 730000, China
* Correspondence: [email protected]; Tel.: +86-182-9841-7508




Received: 29 July 2019; Accepted: 16 August 2019; Published: 21 August 2019


Abstract: Phytoremediation is one of the safer, economical, and environment-friendly techniques in

which plants are used to recover polluted soils, particularly those containing toxic organic substances
and heavy metals. However, it is considered as a slow form of remediation, as plants take time to
grow and flourish. Various amendments, including the augmentation of certain chemical substances
i.e., ethylenediamine tetraacetic acid (EDTA), ethylene glycol tetra acetic acid (EGTA), and sodium
dodecyl sulfate (SDS) have been used to induce and enhance the phytoextraction capacity in plants.
Several reports show that chemical amendments can improve the metal accumulation in different
plant parts without actually affecting the growth of the plant. This raises a question about the amount
and mechanisms of chemical amendments that may be needed for potentially good plant growth and
metal phytoremediation. This review provides a detailed discussion on the mechanisms undertaken
by three important chemical amendments that are widely used in enhancing phytoremediation (i.e.,
EDTA, EGTA, and SDS) to support plant growth as well as soil phytoremediation. A core part of this
review focuses on the recent advances that have been made using chemical amendments in assisting
metal phytoremediation.

Keywords: environmental pollution; phytoextraction; cadmium; biostimulation; oxidative damage

1. Introduction
Heavy metal pollution is regarded as a serious problem for crop production [1]. In soil ecosystems,
the gradual increase in heavy metal levels is a major concern throughout the world [2]. Heavy metal
pollution is a vital issue for environmental management due to the rapid increase in anthropogenic
activities, including industrialization, transportation, and urbanization. Several sources of heavy metals
include medical waste, the combustion of coal, petrol, mining, fertilizers, smelting, and pesticides,
which are adding heavy metals to the environment [3,4]. Among these heavy metals, cadmium (Cd),
lead (Pb), aluminum (Al), zinc (Zn), manganese (Mn), chromium (Cr), and copper (Cu) are considered
as common toxic heavy metals [1].
Toxic heavy metals considered as phytotoxic agents to plants that affect the plant morphological
and physiological processes such as lower growth rate, stomatal movement and nutrient imbalance,

Plants 2019, 8, 295; doi:10.3390/plants8090295 www.mdpi.com/journal/plants

Plants 2019, 8, 295 2 of 14

and photosynthetic processes result in the oxidative damage [5]. Due to increased contamination of
soil by toxic metal components, it is important to use necessary techniques for cleaning up heavy
metals from contaminated soil, which requires an effective and reasonable solution. Some modern
techniques that have been used for the remediation of heavy metals are based on the biological,
chemical, and physical approaches [6]. Phytoremediation is one of the biological approaches used
for the remediation of soils. Phytoremediation is preferable due to its safety and lower cost as
compared to physical and chemical remediation [6]. The technologies of metal phytoremediation
include phytoextraction, phytostabilization, and phytovolatilization [7]. Among these, phytoextraction
is one of the promising techniques being used for reclaiming the metal polluted soils [1].
However, the heavy metal extraction by plants is usually limited by the availability of heavy
metals in soils. The application of chemical enhanced technology is one of the prevalent approaches,
which helps the uptake of heavy metals and their translocation in the aboveground parts of plants [4,8].
Several chemical amendments have been used for the enhancement of phytoextraction processes.
In recent years, chemical amendments including ethylenediamine tetraacetic acid (EDTA), ethylene
glycol tetraacetic acid (EGTA), and sodium dodecyl sulfate (SDS) are widely used for soil remediation
applications, which can bring potential metal leaching risk. EDTA is considered as having the most
potential and most studied chemical amendment, and is used to increase the phytoextraction of metals
from contaminated soils [9].
Therefore, it is important to increase phytoremediation efficiency through the phytoextraction
processes of heavy metals. The phytoremediation of heavy metals in plants may be enhanced through
an emerging chemical amendments technology. Our present review attempts to describe the potential
benefits of chemical amendments in phytoremediation research.

2. Source of Heavy Metal Pollution, Ecotoxicity, and Approaches for Remediation

In general, heavy metals originate from anthropogenic and natural sources. Different sources
of heavy metals were identified such as (a) industrial sources, (b) domestic effluent, (c) agricultural
sources, and (d) natural sources such as the atmosphere (Figure 1). It has been reported that most of
the areas in the world such as China, Japan, and Indonesia have been contaminated by Cd, Cu, and Zn
due to mining and agricultural operations [6].
In terrestrial ecosystems, the heavy metal contaminations are increasing due to anthropogenic
activities, which are known to be liable for ecotoxicity. The largest availability of heavy metals toxicity
occurs in soil and aquatic ecosystems, whereas the smaller portion of metals available in the atmosphere
form of vapors or particulate. In soil, the major heavy metal ranges vary from 0.01 to 0.7 ppm dw of
Cd, 2 to 200 ppm dw of Pb, 10 to 300 ppm dw of Zn, 5 to 3000 ppm dw of Cr, and 7000 to 55,000 ppm
dw of Fe etc. [10]. Heavy metal pollution in soils is becoming increasingly common in the agricultural
sector, and affects food safety and crop growth. The metal toxicity in plants is not the same; it varies
with plant species, metal concentration, soil pH, soil composition, specific metal and chemical form,
etc. According to Misra and Mani [11], the range of vital heavy metal in plants is 0.1 to 2.4 µg−1 dw for
Cd, 1 to 13 µg−1 dw for Pb, 0.02 to 7 µg−1 dw for As, 8 to 100 µg−1 dw for Zn, 0.2 to 1 µg−1 dw for Cr,
140 µg−1 dw for Fe, etc.
Toxic heavy metal is hazardous to the environment. Therefore, heavy metal remediation in the
soil is very important [12]. Over the past few decades, various techniques were employed for the
remediation of toxic heavy metals. The preferred strategies were selected for the remediation of heavy
metal from the environment based on their technical complexity and cost [13]. The techniques include
physical, chemical, and biological methods [14].
Plants 2019, 8, 295 3 of 14
Plants 2019, 8, x FOR PEER REVIEW 3 of 14

Sources of heavy metals, and foliar, root uptake of heavy metals in plants.
Figure 1. Sources plants.

Traditionally,
Traditionally, the
the contaminated
contaminated soils
soils are
are cleaned
cleaned upup byby excavation
excavation or or removing
removing thethe soils
soils from
from
the
the land
land sites. The toxic
sites. The toxic metals
metals problems
problems in in the
the soil
soil may
may also
also arise
arise due
due to
to the
the transportation
transportation ofof
contaminants that are closely adjacent to the soils [15]. Soil washing is another strategy to eliminate
contaminants that are closely adjacent to the soils [15]. Soil washing is another strategy to eliminate soil
metal contaminants,
soil metal but it has
contaminants, but been reported
it has that this isthat
been reported unsuitable
this is for plant growth
unsuitable and development
for plant growth and
due to the hindrance
development of biological
due to the hindranceand chemical activities
of biological [16]. Chemical
and chemical methods
activities [16]. are not
Chemical preferable
methods are
due to alterations in the soil texture and structure, expense, and the generation of high quantities
not preferable due to alterations in the soil texture and structure, expense, and the generation of high of
sludge [16,17].
quantities of sludge [16,17].

2.1. Physiochemical Techniques

2.1. Physiochemical Techniques
The
The physiochemical
physiochemical technique
technique includes
includes excavation,
excavation, leaching,
leaching, landfill,
landfill, and
and thermal
thermal treatment
treatment
(bioreactor) approaches. Nevertheless, these processes are fast but costly, and have detrimental
(bioreactor) approaches. Nevertheless, these processes are fast but costly, and have detrimental effects
on the soil properties [13,18]. These techniques are not completely suitable for heavy metal remediation,
effects on the soil properties [13,18]. These techniques are not completely suitable for heavy metal
and only change
remediation, andthe
onlyform of the
change theproblem without
form of the remediating
problem the pollutants
without remediating thethoroughly
pollutants [19].
thoroughly
[19].Biological Approaches
2.2.
Heavy metals
2.2. Biological are removed from the environment through natural remediation coordinated
Approaches
by microorganisms and plants [14]. Biological remediation is a preferable method as it is natural,
Heavy metals are removed from the environment through natural remediation coordinated by
cost-effective, environmentally friendly, and has wider public support [20]. There are several approaches,
microorganisms and plants [14]. Biological remediation is a preferable method as it is natural, cost-
such as bioaugmentation, biostimulation, bioleaching, composting, bioreactors, bioremediation,
effective, environmentally friendly, and has wider public support [20]. There are several approaches,
and phytoremediation [21]. Biological approaches are considered superior to physiological approaches,
such as bioaugmentation, biostimulation, bioleaching, composting, bioreactors, bioremediation, and
because these processes use solar energy and ensure that the soil properties are conserved [20].
phytoremediation [21]. Biological approaches are considered superior to physiological approaches,
Bioremediation is a technique by which heavy metals are removed from the environment [19,22].
because these processes use solar energy and ensure that the soil properties are conserved [20].
Bacterial strains such as P. aeruginosa and Bacillus spp. can remediate metals such as zinc and
Bioremediation is a technique by which heavy metals are removed from the environment [19,22].
copper in this context [23]. Bioremediation can be done using biostimulation, biofilters, treated and
Bacterial strains such as P. aeruginosa and Bacillus spp. can remediate metals such as zinc and copper
pumped methods, bioventing, bioreactors, composting, land forming, bioaugmentation, and intrinsic
in this context [23]. Bioremediation can be done using biostimulation, biofilters, treated and pumped
bioremediation [24]. The efficiency of phytoremediation can be increased if microbes are used [25].
methods, bioventing, bioreactors, composting, land forming, bioaugmentation, and intrinsic
bioremediation
2.2.1. [24]. Theof
Phytoremediation efficiency of phytoremediation can be increased if microbes are used [25].
Heavy Metals

2.2.1.Phytoremediation
Phytoremediationisof
a part
Heavyof the emerging green technology being used for the uptake of various
Metals
heavy metals in different amounts from the soil and storage of them in parts of the plant that can be
Phytoremediation is a part of the emerging green technology being used for the uptake of
various heavy metals in different amounts from the soil and storage of them in parts of the plant that
Plants 2019, 8, 295 4 of 14

harvested [26]. With changes in soil properties, plants can tolerate pollutants [27]. Soils containing
heavy metals can be easily treated through phytoremediation, and the biomass that is formed during the
process can be further applied in biodiesel production. Thus, bioenergy crops such as Brassica species,
which are known to accumulate toxic metals, are increasingly suitable for this purpose. Some plants
can accumulate pollutants in tissues [28]. The Jerusalem artichoke (Helianthus tuberosus L.) is known to
be an energy crop that is used for the phytoremediation of soils contaminated by heavy metals. It is
more suitable for the phytoextraction of heavy metals among the energy crops. The highest heavy
metal uptake was observed at a dose of 60 Mg DMha−1 in the Jerusalem artichoke [29].
Hyperaccumulating plants are fit to grow on soils contaminated with heavy metals and can be
used to remove pollutants [19]. Plants that contain greater than 10,000 mg/kg dry weight of Zn or
Mn or more than 1000 mg/kg dry weight of Ni, Cu, or Pb or greater than 100 mg/kg dry weight of
Cd in contaminated areas are considered as hyperaccumulating plants. There are several families of
plants that are known to hyperaccumulate toxic heavy metals. Some such important plant families
are Lamiaceae, Fabaceae, Scrophulariaceae, Asteraceae, Euphorbiaceae, and Brassicaceae, which are
usually used in the phytoremediation processes. Other than that, there have been reports of heavy
metal hyperaccumulation in about 500 plant species [30]. Plants with greater hyperaccumulating
abilities include Alyssum bertolonii, Thlaspi caerulescens, Calendula officinalis, and Tagetes erecta [31].
Higher concentrations of Ni, Zn, and Cd are best gathered by Thlaspi caerulescens [32]. This plant
can accumulate 500–52,000 mg kg−1 of Zn and 0.3–1020 mg kg−1 of Cd. Trees are more suitable for
phytoremediation because of their greater root systems and biomass [19], although trees take more time
in accumulating metals, even in low quantities. This issue could be solved by using fast-growing plants
instead of trees [33]. For an example, the Poplus alba is a deciduous tree, which can accumulate zinc (Zn)
in different plant parts such as leaves, stems, and roots. An increasing trend of Zn accumulation was
observed in the leaves of Poplus alba with the application of SDS [34]. Phytoremediation depends on
the ability of the plants to gather increased levels of toxic metals within their tissues [35]. Some plants
contain enzymes that can break down a number of organic compounds. However, pollutants that
are inorganic cannot be degraded with these enzymes. Thus, there is a need to ensure that inorganic
pollutants be less available in soils or extracted and accumulated in different parts of the plants and also
reduce volatile versions of inorganic pollutants [36]. Energy recovery strategies can be used to produce
bioenergy from plant biomass, such as to form biodiesel. Fuel gas, char, and bio-oil can be produced via
pyrolysis, during which the biomass undergoes thermal degradation without oxygen [37]. Soils greatly
polluted with toxic heavy metals can be remediated easily by growing plants that are tolerant to more
than one heavy metal, can produce a good amount of harvestable biomass with enhanced growth rates,
and are highly competitive [30].

2.2.2. Problems with Heavy Metals of Remediation with Phytoremediation

Phytoremediation performance could be affected by several processes such as the rate of
contaminant uptake by plant roots, the availability of toxic metal ions in the soil, and the root-to-shoot
movement of the metal ions [38]. Plants store the heavy metals in the different parts of the plant such
as in the leaf, stem, and root [26]. Although phytoremediation is considered as a green technology,
it has some problems or limitations in the case of remediation of soils. According to Koptsik [39],
there are some problems or limitations of phytoremediation as follows:

• It depends on the local climate, weather, and seasonal conditions.

• It requires more time to remediate pollutants from the soil.
• It is suitable only for low-polluted territories.
• It depends on the depth of the root system and solubility of the pollutants.
• Pollutants may enter the trophic chains and adjacent media.
Plants 2019, 8, 295 5 of 14

Plants 2019, 8, x FOR

3. Assistance PEER REVIEW
of Chemical Amendments to Increase the Efficiency of Phytoremediation 5 of 14

High heavy
High heavy metal
metal concentrations
concentrations inin plant
plant tissues
tissues and
and biomass
biomass areare considered
considered asas aa key
key factor
factor for
for
the successful phytoremediation of heavy metal polluted soils [40]. The natural levels of
the successful phytoremediation of heavy metal polluted soils [40]. The natural levels of heavy metals heavy metals
are relatively
are high in
relatively high in the
the Earth’s
Earth’s crust,
crust, and
and most
most ofof these
these are
are phytoavailable
phytoavailable and and low
low soluble
soluble [41].
[41].
Chemical amendments have a key role to compensate for relatively low heavy metal availabilitysoil,
Chemical amendments have a key role to compensate for relatively low heavy metal availability in in
and itand
soil, helps the plants
it helps uptakeuptake
the plants and translocate metals toward
and translocate the shoot
metals toward [42].
the Different
shoot kinds of chemical
[42]. Different kinds of
amendments
chemical or chelating
amendments or agents have
chelating been have
agents used and
beentested
used to increase
and tested the bioavailability
to increase of metals in
the bioavailability
plants
of metals in plants and facilitate the transport of metals between the roots and shoots. The of
and facilitate the transport of metals between the roots and shoots. The most important the
most
three chemical amendments are EDTA, EGTA, and SDS, which have been widely
important of the three chemical amendments are EDTA, EGTA, and SDS, which have been widely used in recent years
(Figure
used in 2).
recent years (Figure 2).

Figure 2.2.Chemical
Chemical structure
structure ofethylene
of (A) (A) ethylene
diaminediamine
tetraacetictetraacetic acid
acid (EDTA), (B) (EDTA), (B) ethylene
ethylene glycol tetraaceticglycol
tetraacetic
acid (EGTA),acid
(C)(EGTA),
sodium (C) sodium
dodecyl dodecyl
sulfate (SDS),sulfate (SDS), with
and binding and binding 2+ (Cd
with
metals, M 2+ , PbM
metals, 2+2+etc.).
(Cd2+, Pb2+etc.).
3.1. Assisting of Phytoremediation by EDTA
3.1. Assisting of Phytoremediation by EDTA
Ethylenediamine tetraacetic acid, also known as EDTA, is used frequently in the agricultural
sectorEthylenediamine
due to its ability to mobilizeacid,
tetraacetic heavyalso
metals.
knownEDTA enhances
as EDTA, metalfrequently
is used uptake through
in thethe roots and
agricultural
also supports metal xylem loading (Figure 3).
sector due to its ability to mobilize heavy metals. EDTA enhances metal uptake through the roots and
also supports metal xylem loading (Figure 3).
This has also been reported in previous studies [44]. The increased uptake occurs due to the
production of soluble metal–EDTA complexes [45]. Most plants are able to take up metal–EDTA
complexes [46], especially hyperaccumulator species [47]. The effect of EDTA depends on the plant
species, heavy metal, and type of soil, ranging from 0 to 200-fold higher accumulations [42]. Cu, Zn,
Pb, Ni, and Cd uptake was enhanced by EDTA in Zea mays and Lolium perenne [48]. Lead accumulation
increased fourfold in the Sedum alfredii roots [49] and twofold in Vicia faba seedlings in a 24-h
experiment [50].
 Figure 2. Chemical structure of (A) ethylene diamine tetraacetic acid (EDTA), (B) ethylene glycol
tetraacetic acid (EGTA), (C) sodium dodecyl sulfate (SDS), and binding with metals, M2+(Cd2+, Pb2+etc.).
3.1. Assisting of Phytoremediation by EDTA
Ethylenediamine tetraacetic acid, also known as EDTA, is used frequently in the agricultural
sector2019,
Plants due8,to
295its ability to mobilize heavy metals. EDTA enhances metal uptake through the roots and
6 of 14
also supports metal xylem loading (Figure 3).

Figure 3. Chemical amendments assisting the heavy metal uptake in the plants, adapted from Souza
et al. [43]. Figure (A) depicts that a hyperaccumulator plant accumulates the heavy metal gradually
and constantly during the entire life cycle of the plant, whereas Figure (B) shows that the heavy metal
behavior of a non-hyperaccumulator plant is relatively slow, but the metal uptake increases quickly
after the application of chemical amendments along with metals.

The metal uptake rate or concentration in plants depends on the chemical amendments dose
during the application of chemical amendments. The uptake of toxic metals rate may reach a maximum
in plants at a certain amendments dose level. Before treatment, the lead (Pb) concentration was
0.025 mg/g in Typha sp. The concentration was increased to 0.846 mg/g, while 1 mL of EDTA was
added along with 1 ppm of lead. Similarly, the copper (Cu) was increased 0.030 mg/g to 0.522 mg/g,
when 1 mL of EDTA was added in combination with 1 ppm of Cu. Cd concentration was increased by
51.98% in the shoot during the application of EDTA with Cd [45].
In another study, EDTA caused a 15-fold increased uptake of lead in the roots of Vetiveria
zizanioides. The concentrations of EDTA solution (0–10 mmol·kg−1 soil) were added under the exposure
of 1000 mg·kg−1 of Pb in the form of Pb(NO3 )2 for 14 days. They concluded that 10 mmol·kg−1 of
EDTA treatment was best regarding the lead (Pb) uptake in Vetiveria zizanioides [51]. The maximum Pb
concentrations in the shoot were found in Canavalia ensiformis L. when 0.5 g·kg−1 of EDTA was used
for 40 days with the application of 1800 mg·kg−1 of Pb as Pb(NO3 )2 [52]. A study showed a higher
uptake of lead, but no other heavy metals from contaminated soils [53]. Under the exposure of Cd as
CdCl2 (50 mg·kg−1 ), the shoot concentrations of Cd significantly increased at a rate of 0.5 g·kg−1 EDTA
in Helianthus annuus [54] (Table 1).
Phytoextraction using EDTA can be made more efficient with the proper mix of organic chelators,
metals, and appropriate plant species [70].
The mechanism of EDTA increasing metal uptake is not fully understood yet. There are various
steps involved in the entrance of metals from the soil to the roots, which determines the rate of uptake
and also the capability of a plant to take in heavy metals. The uptake of metals into the roots involves:
(i) the movement of soluble metals to plant roots through mass flow or diffusion [71], (ii) adsorption on
roots, and (iii) attachment to functional groups within the rhizoderm cell surface [72]. The adsorption
of metals into the plant root surface has been observed in various studies [73]. The metal–EDTA
complexes form affects almost all of the steps previously mentioned of metals uptaking through
plant roots. Initially, EDTA allows the diffusion of metals through the roots by (i) increasing their
concentration in soil by desorbing metals and (ii) lowering the apparent diffusion coefficient of metals
in metal–EDTA complex forms [71]. Since metal–EDTA complexes carry a neutral charge, they are
not attached or blocked by polysaccharides or carboxyl groups in the rhizoderm cell surface. In this
way, EDTA allows the movement of metals directly into the roots. However, there have been various
hypotheses about whether metal–EDTA complexes dissociate just before entering the plant roots or
Plants 2019, 8, 295 7 of 14

enter as they are [74]. In some studies, it was shown that EDTA form complexes in solution, then enter
plants [61]. A study involving 14C-labeling showed that indeed, the full metal–EDTA complex is
absorbed, with particular selectivity toward lower charged complexes in Swiss chard. Sarret et al. [75]
mentioned that these metal–EDTA complexes are nontoxic and break down after entering the roots,
forming free heavy metal ions that could induce phytotoxicity. Inductively coupled plasma mass
spectrometry (ICP-MS) analysis of xylem sap showed the presence of metal–EDTA complexes and the
absence of EDTA individually in Hordeum vulgare grown in contaminated soil amended with EDTA.
Schaider et al. [76] showed the presence of complexes in xylem sap such as Cd–EDTA, Pb–EDTA,
and Fe–EDTA.

Table 1. Effects of heavy metals on the plants with different growing conditions along with
chemical amendments.

Heavy Growing Chemical References

Scientific Name Metals Conditions Amendments
Calendula Cd Pot EDTA, EGTA, [55]
officinalis SDS
Tagetes erecta Pb Pot EDTA [56]
Impatiens Cd Pot EDTA [57]
walleriana
Medicago sativa Cr Pot EDTA [58]
Tribulus terrestris Cd, Pb Pot EDTA [59]
Helianthus annuus Cd, Ni Pot EDTA [54]
Dianthus chinensis Cd, Zn, Pb Pot EDTA [60]
Vetiver zizanioides Cd, Zn, Pb Pot EDTA [60]
Canavalia ensiformis L. Pb Pot EDTA [52]
Brassica carinata Cd, Cr, Pb Pot EDTA [44]
Brassica juncea Cd, Cr, Pb Pot EDTA [44]
Brassica juncea Pb Pot EDTA [61]
Phaseolus vulgaris L. Pb, Zn, Cu Pot EDTA [62]
Zea mays L. cv. Pb, Zn, Cu Pot EDTA [62]
Nongda 108
Brassica juncea L. Pb, Zn Pot EDTA [63]
Czern.
Triticum aestivum Pb, Zn Pot EDTA [63]
Mirabilis jalapa L. Cd Pot EDTA, EGTA [64]
Althaea rosea Cd Pot EDTA, EGTA, SDS [65]
Mirabilis jalapa Cd Pot EDTA, EGTA [64]
Cicer arietinum Cd Pot EGTA [66]
Sesbania exaltata Pb Pot EDTA, EGTA [67]
Calendula officinalis Cd Pot EGTA, SDS [68]
Althaea rosea Cd Pot EGTA, SDS [68]
Halimione portulacoides Cu Field SDS [69]
Populus alba Zn Pot SDS [34]

3.2. Assisting of Phytoremediation by EGTA

EGTA, or ethylene glycol tetraacetic acid, is a widely used chelating agent. Similar to EDTA,
the four carboxyl groups dissociate and produce four protons (Figure 2). The two N atoms of the two
amino groups have unshared pairs of electrons each. EGTA has been shown to have more affinity
for Ca ions, but less affinity toward Mg ions. Such synthetic chelators have been successfully used
for phytoextraction [77]. The factor to consider for using EGTA is that it increases the uptake of
heavy metals by plants more efficiently. Sakouhi et al. [66] reported that applying EGTA increased Pb
accumulation by more than 80% in parts of Cicer arietinum plants above ground. After the application
of 1 mmol kg−1 of EGTA in A. rosea, the maximum total Cd content was observed, which was increased
by 72% [68]. In Mirabilis Jalapa, Cd concentration was increased by 43.27% in the shoot under EGTA
Plants 2019, 8, 295 8 of 14

treatment along with Cd (25 mg·kg−1 ) [64]. The Cd concentration was at a maximum in the shoots
when 1.0 mmol·kg−1 was used. In Calendula officinalis, 30–100 mg·kg−1 of Cd as CdCl2 was added
to the soil, and it was observed that the total Cd increases up to 217% with the application of EGTA
alone. They concluded that the use of 1.0 mmol kg−1 EGTA showed the greatest effect among the
treatments [55] (Table 1).

3.3. Assisting of Phytoremediation by SDS

SDS is a surfactant that is most commonly used in detergents, but it can also be used for heavy
metal and organic contaminant remediation from soil [34]. SDS can ameliorate solubilities of various
hydrocarbons and heavy metals such as zinc, cadmium, lead, and copper, making their removal easier,
both in phytoremediation trails involving herbaceous species [78] and soil flushing [79]. Surfactants
contain a hydrophobic portion that has less affinity for aqueous solutions, and the hydrophilic
polar portion, which has a higher affinity for aqueous solutions. Thus, surfactants are amphiphilic.
Anionic surfactants such as SDS are amphipathic, as they can interact with both non-polar and polar
macromolecules, causing membrane damage and even oxidative stress [80]. However, the direct
involvement of SDS in plant remediation trials has not yet been widely investigated, because some
strains of Pseudomonas can degrade SDS by using it as a carbon source [81,82] and photoelectrochemical
reactions [83]. It has been observed that SDS can increase the dry biomass of plants such as Althaea
rosea, and also promote Cd accumulation in roots and shoots [65]. Calendula and Althaea rosea provide
some evidence that Zn accumulation changes with the presence of SDS [34]. When 1 mM of Zn was
added in combination with 0.5 mM of SDS, the Zn translocation was increased toward basal leaves in
Poplus alba [34]. The maximum Cd concentration was observed in the shoots and roots in Althaea rosea,
when 1.0 mmol kg−1 was added among the single SDS treatments (0.5 mmol·kg−1 to 2 mmol·kg−1 ) [68].
In Calendula officinalis, when the applied soil Cd contamination was 30 mgkg−1 , the Cd concentrations in
the shoot increased significantly under 0.5–2.0 mmolkg−1 SDS treatments. For the higher concentration
of 100 mg·kg−1 Cd as CdCl2 , the application of SDS (0.5–2.0 mmol·kg−1 ) was observed to increase
the Cd concentrations in the shoot. They concluded that the maximal shoot Cd concentrations were
observed when 2.0 mmol·kg−1 SDS were used [55] (Table 1).

4. Challenges with Chemical Amendments

Chemical amendments are useful in phytoremediation methods used to phytoextract heavy metals
from contaminated soil; however, adding EDTA, EGTA, and SDS also have a few limitations [84],
such as toxic effects toward soil microbes [85], soil enzyme activities, and on cultivated plant species [86].
Due to metal mobilization during extended periods, the chemical-assisted phytoextraction increases
the risk of adverse environmental effects. Chemical amendments can disrupt chemical properties and
the physical structures of soil by dissolving minerals.
EDTA and its metal complexes are not just highly toxic, but also non-biodegradable and could
persist for many weeks [87]. EDTA is an exogenous substance that has adverse environmental effects
on soils. EDTA is said to persist within the soil for six months or more [86]. EDTA-facilitated metal
movement through soil could occur post-growing season. A monitoring study conducted by [88]
mentioned a similar movement of metals such as Zn, Cu, Pb, and Cd using EDTA post-treatment while
observing the behavior of heavy metals. Grcman et al. [89] observed that EDTA could leave phytotoxic
effects on plants such as red clover. Luo et al. [90] reported similar phytotoxic effects by EDTA even
after six months since addition to the soil.
A recent study by Krujatz [91] found that EDTA reduced the toxicity of Ni2+ and Cd2+ within
the stoichiometric ratio, but still inhibited the growth of Pseudomonas brassicacearum above the ratio.
EDTA also has potentially toxic effects on fungi and bacteria living in soil [88] and plants [84].
Ruley et al. [92] observed lower photosynthetic activity in seedlings of Sesbania drummondii that
were exposed to EDTA solutions. The toxicity of metals induced by EDTA is due to increased metal
uptake [93]. Other phytotoxic effects caused by EDTA may occur due to enhanced metal uptake
Plants 2019, 8, 295 9 of 14

by plants [94]. Other authors reported results of lower plant biomass when EDTA is present [95].
The toxicity symptom seen in Brassica juncea and Lolium perenne showed a significant decrease in
their biomass [87]. In Typha angustifolia, there was a significant decrease in biomass and plant height,
resulting in stunted growth [96].
Metal leaching enhanced by chemical amendments depends on various factors, such as:

• Plant-related: root type, species, type and amount of root exudates, age [52,97];
• Soil related: soil texture, pH, organic contents, competing ions, carbonates, biological and microbial
conditions, soil water holding capacity, cation exchange capacity (CEC), soil redox potential,
soil-buffering capacity [98];
• Metal related: concentration and type of metal, EDTA, EGTA, and SDS-binding capacity to a
specific metal, whether single or more than one metal contamination [61,99].

5. Conclusions and Future Direction

Heavy metals can cause serious environmental pollution, as they can accumulate in soils and persist
for a long time, and even possibly enter the food chain. The chemical amendment-induced remediation
of heavy metals by plant species is an effective technique, because it has high binding capacities toward
the majority of the heavy metals. Among the three chemical amendments, EDTA is known to be
the most efficient organic ligand that can increase metal uptake, solubilization, and translocation,
as it can form highly stable and soluble metal–EDTA complexes. Most probably, iron (Fe) is the best
metal to bind with EDTA due to its high affinity to ferric ions. Metal phytoremediation enhanced
by EDTA, EGTA, and SDS can be affected depending on various biogeochemical processes found in
plants, metal, and the soil. Chemical amendment capacity is an important aspect, in order to reduce
the time and cost needed for heavy metal contaminated soil. This can be done by increasing the heavy
metal bioaccumulation index in plants.

Author Contributions: M.M.H. wrote the initial draft of the manuscript, M.N.U. modified and edited the figure
and table, I.A.-S., H.F.A., K.R.H. and Y.A. were involved in the compilation of the final draft, and L.Z. revised the
final manuscript.
Funding: This research did not receive any external funding.
Acknowledgments: The authors are thankful to the School of Life Sciences, Lanzhou University, China, for the
financial support in the form of a postdoctorate fellowship to M.M.H. We thank Mirza Hasanuzzaman, Department
of Agronomy, Sher-e-Bangla Agricultural University, and Katherine Li, Director of the office of external affairs,
North South University for the critical reading and formatting of the final manuscript.
Conflicts of Interest: The authors declare no conflict of interest.

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