toxics

Review
Clean-Up of Heavy Metals from Contaminated Soil
by Phytoremediation: A Multidisciplinary and
Eco-Friendly Approach
A. K. Priya 1,2, * , Muthiah Muruganandam 2 , Sameh S. Ali 3,4 and Michael Kornaros 5, *

1 Department of Chemical Engineering, KPR Institute of Engineering and Technology, Coimbatore 641407, India
2 Project Prioritization, Monitoring & Evaluation and Knowledge Management Unit, ICAR-Indian Institute of
Soil & Water Conservation (ICAR-IISWC), Dehradun 248195, India; [email protected]
3 Biofuels Institute, School of the Environment and Safety Engineering, Jiangsu University,
Zhenjiang 212013, China; [email protected]
4 Botany Department, Faculty of Science, Tanta University, Tanta 31527, Egypt
5 Department of Chemical Engineering, University of Patras, 1 Karatheodori Str., University Campus-Rio,
26504 Patras, Greece
* Correspondence: [email protected] (A.K.P.); [email protected] (M.K.)

Abstract: Pollution from heavy metals is one of the significant environmental concerns facing the
world today. Human activities, such as mining, farming, and manufacturing plant operations, can
allow them access to the environment. Heavy metals polluting soil can harm crops, change the food
chain, and endanger human health. Thus, the overarching goal for humans and the environment
should be the avoidance of soil contamination by heavy metals. Heavy metals persistently present in
the soil can be absorbed by plant tissues, enter the biosphere, and accumulate in the trophic levels
of the food chain. The removal of heavy metals from contaminated soil can be accomplished using
various physical, synthetic, and natural remediation techniques (both in situ and ex situ). The most
controllable (affordable and eco-friendly) method among these is phytoremediation. The removal
of heavy metal defilements can be accomplished using phytoremediation techniques, including
phytoextraction, phytovolatilization, phytostabilization, and phytofiltration. The bioavailability of
Citation: Priya, A.K.; heavy metals in soil and the biomass of plants are the two main factors affecting how effectively
Muruganandam, M.; Ali, S.S.; phytoremediation works. The focus in phytoremediation and phytomining is on new metal hyper-
Kornaros, M. Clean-Up of Heavy accumulators with high efficiency. Subsequently, this study comprehensively examines different
Metals from Contaminated Soil by frameworks and biotechnological techniques available for eliminating heavy metals according to
Phytoremediation: A Multidisciplinary environmental guidelines, underscoring the difficulties and limitations of phytoremediation and its
and Eco-Friendly Approach. Toxics potential application in the clean-up of other harmful pollutants. Additionally, we share in-depth
2023, 11, 422. https://doi.org/
experience of safe removing the plants used in phytoremediation—a factor frequently overlooked
10.3390/toxics11050422
when choosing plants to remove heavy metals in contaminated conditions.
Academic Editor: Agustin Probanza
Keywords: biotechnological methods; genetic modifications; heavy metal degradation; phytoremediation;
Received: 13 April 2023
remediation techniques
Revised: 26 April 2023
Accepted: 28 April 2023
Published: 2 May 2023

1. Introduction
Increasing industrialization and agricultural practices have led to the widespread
Copyright: © 2023 by the authors. contamination of soil with heavy metals (HMs), which has become a significant environ-
Licensee MDPI, Basel, Switzerland. mental concern globally [1,2]. HMs are exceptionally stable entities with half-lives that are
This article is an open access article more than 20 years long [3,4]. The extraction of minerals and associated various handling
distributed under the terms and
techniques influence the introduction of pollutants and HMs into the environment, which
conditions of the Creative Commons
largely determines the specific mobility of different metals in the environment. Due to the
Attribution (CC BY) license (https://
expansion in industrialization and the organic cycle’s unsettling influence, heavy metal
creativecommons.org/licenses/by/
contamination becomes a problematic issue that needs an effective solution to moderate its
4.0/).

Toxics 2023, 11, 422. https://doi.org/10.3390/toxics11050422 https://www.mdpi.com/journal/toxics

Toxics 2023, 11, 422 2 of 24

effects. Heavy metals are essentially large, non-biodegradable metals that accumulate in
the environment and pose a risk to human and environmental health by contaminating
soil and water, for example [5]. In a living organic entity, these elements accumulate in the
body tissue through a process known as bioaccumulation, and they move from a lower to a
higher trophic level with an elevated concentration—a phenomenon known as biomagnifi-
cation. Due to the negative effects of heavy metals, there are fewer soil organisms in the
soil [6].
Due to the fundamental role of soils in biological solidity and horticultural creation,
they are considered as essential components of earthly environments [7,8]. However,
excessive mining operations, rapidly expanding modern activities, waste removal, and
careless use of engineered composts and pesticides have made soil tainting by potentially
toxic elements (PTEs) a significant natural issue globally [9–11]. Heavy metals are often
defined as metals or metalloids with a higher atomic number and atomic weight than
lighter elements, such as carbon, nitrogen, and oxygen. They are typically characterized by
a density greater than 5 g/cm3 and a thickness that exceeds a certain threshold [12,13]. Ali
et al. (2019) proposed an alternative definition of heavy metals based on nuclear density,
specifically a nuclear density of more than 41 g/cm3 [14]. They used specific metals,
including Cd, Cr, Co, Cu, Pb, Hg, and Zn, as examples of heavy metals based on their
nuclear density. Heavy metals can also accumulate in the food chain, potentially leading
to health problems in animals and humans who consume contaminated food. Heavy
metal contamination is a widespread issue affecting millions of hectares of land worldwide.
Expanded persistence through varying rates, land degradation, and geological cycles are
the leading recurring causes of soil contamination or depletion [15]. The effects of excessive
exposure to soil toxins, such as heavy metals, on plant development and physiological
cycles include reducing seed germination [16], limiting plant growth [17], disrupting
nutrient uptake [18], stifling photosynthesis [19], and adjusting enzymatic activities [20].
PTEs cause higher plants to become more susceptible to oxidative damage by producing
excess reactive oxygen species (ROS) [21]. In addition, soil PTEs can increase risks to human
health as they rise in the food chain [22–24].
Studies have shown that the primary source of lead and cadmium in the local air
is the release of gases from gas fuel, brakes, and tires [25]. Subsequently, HMs, such as
Copper (Cu), Lead (Pb), Zinc (Zn), Nickel (Ni), Cadmium (Cd), Chromium (Cr), Iron (Fe),
Manganese (Mn), and natural toxins, such as hydrocarbons, sweet-smelling compounds,
phenols, organo-chlorinated compounds, and pesticides, have been found at higher levels
in contaminated soil [26]. The first category, which focuses on improving the ability of
plants to remediate heavy-metal-polluted soils, highlights the importance of identifying
plant species and genetic traits that effectively remove heavy metals from the soil. This
research is essential for developing efficient and sustainable phytoremediation strategies.
The second category, which analyses the effects of heavy metals on plants from a molecular
perspective, is necessary for understanding the mechanisms underlying plant responses
to heavy metal stress. This knowledge is essential for identifying molecular targets that
can be manipulated to enhance plant tolerance and phytoremediation efficiency. The
third category, which focuses on the progress of the plant remediation effect on heavy
metal pollution, is critical for evaluating the effectiveness of phytoremediation in the field.
These studies provide important insights into the factors that influence the success of
phytoremediation, such as soil properties, plant species, and environmental conditions [27].
Food crops contaminated with HMs have the potential to bioaccumulate HMs, and the
ensuing biomagnification along the higher trophic levels in the established pecking order
can potentially harm the prosperity of both living things and people [5]. HM development
in the body can bring about unexpected severe problems, for example, itai sickness due
to diligent disc openness; kidney harm and ailment because of Zn; mucosa disintegration,
hepatic structure disappointment, and central tactile framework harm because of Cu; and
skin aggravation and tangible framework entrapments because of Ni [28].
Toxics 2023, 11, x FOR PEER REVIEW 3 of 24

Toxics 2023, 11, 422 3 of 24

because of Cu; and skin aggravation and tangible framework entrapments because of Ni
[28].
These heavy metals have toxicological effects that can reduce the number of living
thingsThese
and theirheavy metals have
productivity toxicological
in the soil whereeffects that
they are can reduce
found the number
on Earth’s surface. Theof living
use
things and their productivity in the soil where they are found
of vegetation for natural remediation is an ancient practice that cannot be pinned down on Earth’s surface. The use
to a single institution; however, a line of fascinating logical developments combined withto
of vegetation for natural remediation is an ancient practice that cannot be pinned down
ana single institution; however,
interdisciplinary a line of fascinating
review methodology logicalthe
has allowed developments
extension ofcombined with an
this knowledge
interdisciplinary review methodology has allowed the extension
into powerful biological hardware, known as phytoremediation. In which, green vegeta- of this knowledge into
powerful biological hardware, known as phytoremediation.
tion is suitably used to remove impurities, rendering the contaminants in the environment In which, green vegetation
is suitablyorused
innocuous to remove
consolidated forimpurities, rendering the
their easy elimination [29].contaminants in the environment
innocuous or consolidated for their easy elimination [29].
Soil recovery from heavy metal pollution is possible, but the methods used depend
Soil recovery from heavy metal pollution is possible, but the methods used depend
on the specific metals present, their speciation, and the degree of contamination. Possible
on the specific metals present, their speciation, and the degree of contamination. Possible
approaches include physical and chemical treatments, such as soil washing, electrokinetic
approaches include physical and chemical treatments, such as soil washing, electrokinetic
remediation, and phytoremediation. The effectiveness of these methods will depend on
remediation, and phytoremediation. The effectiveness of these methods will depend on
factors such as the type of soil, the nature of the contaminants, and the desired end-use of
factors such as the type of soil, the nature of the contaminants, and the desired end-use of
the remediated soil. Risk assessment, which contributes to the modest protection of the
the remediated soil. Risk assessment, which contributes to the modest protection of the
environment and general wellbeing, is an effective tool that enables strategists and deci-
environment and general wellbeing, is an effective tool that enables strategists and decision
sion makers to manage heavy-metal-polluted regions [11]. If soils polluted with pesticides
makers to manage heavy-metal-polluted regions [11]. If soils polluted with pesticides are
are used to grow food crops, there is a risk that these pollutants will enter the food chain
used to grow food crops, there is a risk that these pollutants will enter the food chain and
and potentially harm humans and animals that consume the contaminated crops. Pesti-
potentially harm humans and animals that consume the contaminated crops. Pesticides
cides can persist in the soil for long periods, especially if natural processes do not break
can persist in the soil for long periods, especially if natural processes do not break them
them
down down
or if or if they
they are continuously
are continuously applied.applied. The pesticides
The pesticides can then
can then be taken
be taken upthe
up by byroots
the
roots of food crops and accumulate in the edible parts of plants, such
of food crops and accumulate in the edible parts of plants, such as fruits, vegetables, and as fruits, vegetables,
and grains
grains [30].[30].
Phytoremediation,
Phytoremediation,impurity impurityimmobilization,
immobilization,and andsoil
soilwashing
washingare arecommonly
commonlyknown known
techniques
techniques that are effective for the remediation of metal-contaminatedsoil
that are effective for the remediation of metal-contaminated soil[31].
[31].Despite
Despite
their
theirefficiency
efficiencyand andeco-friendly
eco-friendlynature,nature,these theseinnovations
innovationshave havenotnotyet
yetbeenbeenwidely
widelyusedused
ininnon-industrial
non-industrial nations due to inadequate knowledge or awareness. However,major
nations due to inadequate knowledge or awareness. However, major
realistic
realisticapplications
applicationsof of these
these advancements
advancements have have been
been considered
consideredeffective
effectiveand andapplied
appliedin
indeveloped
developed nations.
nations. Additionally,
Additionally, effective
effective communication
communication and community
and community engage-
engagement are
ment are crucial for ensuring the success of soil remediation efforts.
crucial for ensuring the success of soil remediation efforts. It is essential to involve local It is essential to in-
volve local communities
communities in designing in designing
and implementing and implementing soil remediation
soil remediation strategies strategies and
and to provide
tothem
provide them with information about the risks associated with
with information about the risks associated with contaminated soil and the poten- contaminated soil and
the
tialpotential
benefits benefits of remediation
of remediation [32]. The [32].
mainTheeffects
main effects
of soil of soil contamination
contamination on sus-
on sustainable
tainable
developmentdevelopment
goals are goals
shownare inshown
Figure in1.Figure 1.

Maineffects
Figure1.1.Main
Figure effectsofofsoil
soilcontamination
contaminationon
onsustainable
sustainabledevelopment
developmentgoals
goals[33].
[33].

This study examines both rural and urban soils and includes an overview of the po-
tential of plant species with capacity for accumulating contaminants, known as hyperaccu-
 study also explores potential ways of removing heavy metals from soil using phytoreme-
diation techniques and possible applications of the byproducts of phytoremediation. This
study provides a comprehensive overview of recent developments in removing heavy
metals from contaminated soil using phytoremediation techniques and the potential con-
Toxics 2023, 11, 422 sequences for food security and other human and ecological health aspects. The study4alsoof 24
explores possible uses of phytoremediation products and proposes ideas for future inno-
vations in this field. This study provides a comprehensive and forward-thinking analysis
of phytoremediation
mulator plants, tools and
and its potential required
approaches implications.
for phytoremediation, and biotechnological
strategies for removing heavy metals. Additionally, the study explores in situ and ex situ
2. Heavy Metal
remediation Sources in
approaches forthe Environment
heavy-metal-contaminated soil, focusing on phytoremediation
Due toAthe
methods. potential
critical aspectforof
bioaccumulation
the study is theand poisoning of living
examination organic
the effects entities,
of heavy HM
metals
contamination
on food security, hasincluding
drawn attention across for
their potential thebioaccumulation
world [28]. The effects of HM contamina-
and biotoxicity. The study
tion
alsoin the environment
explores significantly
potential ways impact
of removing biological
heavy metalssystems
from soil both
usingin terrestrial and ma-
phytoremediation
rine ecosystems [34]. In addition to diffuse sources, point sources
techniques and possible applications of the byproducts of phytoremediation. This study of contamination, such
as mining,asmelting,
provides and manufacturing,
comprehensive overview of recentcan also contribute toinheavy
developments removingmetalheavy
contamina-
metals
fromincontaminated
tion soil and water. soil usingactivities
These phytoremediation
can releasetechniques and the potential
high concentrations of heavy consequences
metals into
for food
the security and other
environment human
can result in and ecological
localized health aspects.
contamination Thewater,
of soil, study and
also air
explores
[31].
possible
These usescontaminations
water of phytoremediationare most products and proposes
dangerous and harmful ideas tofor future
human innovations
and natural en- in
this field. This
vironments study
[28]. provides
Various sourcesa comprehensive
of heavy metals andandforward-thinking
their environmental analysis of phytore-
pathways are
mediation
shown and its2.potential implications.
in Figure
Heavy metal contamination of soil can arise from both natural and anthropogenic
2. HeavyHeavy
sources. Metalmetals
Sources inin the Environment
contaminated areas can typically be obtained from parent soil,
Due to the
also referred to potential for bioaccumulation
as a lithogenic source. Numerous and poisoning
heavy metals of living
do not organic
existentities, HM
separately;
contamination
instead, has drawn
they exist attention
as synthetic across the
structures thatworld [28].
can be The effects
readily of HM contamination
and directly absorbed by
in the cells
living environment
and tissues significantly
[35]. Zn, Hg, impact biological
Cd, Pb, Cu, Ni,systems
As, and bothCr are in among
terrestrial
the and
mostmarine
com-
ecosystems [34]. In addition to diffuse sources, point sources
monly found heavy metals in soil. Other heavy metals, such as aluminum (Al), barium of contamination, such as
mining,
(Ba), smelting,
cobalt and manufacturing,
(Co), manganese can also(Se),
(Mn), selenium contribute
and silverto heavy
(Ag), metal
can alsocontamination
be present in in
soil at
soil and water. These
elevated levels activities
and can posecan release high concentrations
environmental of heavy
and health risks. metals
Natural into the
events, en-
such
vironment
as volcanic and can result
emissions, in localized
ocean contamination
salt sprays, wind-borne of soil
soil,particles,
water, andforest air [31]. These
fires, and water
rock
contaminations
weathering, can are most dangerous
contribute and harmful
to the presence to human
of heavy metals in and natural
soil. environments
Biogenic sources, such[28].
Various sources of heavy metals and their environmental pathways
as the decay of organic matter, can also release heavy metals into soil [36]. are shown in Figure 2.

Figure
Figure2.
2. Various
Various sources
sources of
of heavy
heavy metals
metals and
and their
their environmental
environmental pathways.
pathways.

Heavy metal contamination of soil can arise from both natural and anthropogenic
sources. Heavy metals in contaminated areas can typically be obtained from parent soil,
also referred to as a lithogenic source. Numerous heavy metals do not exist separately;
instead, they exist as synthetic structures that can be readily and directly absorbed by living
cells and tissues [35]. Zn, Hg, Cd, Pb, Cu, Ni, As, and Cr are among the most commonly
found heavy metals in soil. Other heavy metals, such as aluminum (Al), barium (Ba), cobalt
(Co), manganese (Mn), selenium (Se), and silver (Ag), can also be present in soil at elevated
levels and can pose environmental and health risks. Natural events, such as volcanic
emissions, ocean salt sprays, wind-borne soil particles, forest fires, and rock weathering,
can contribute to the presence of heavy metals in soil. Biogenic sources, such as the decay
of organic matter, can also release heavy metals into soil [36].
Anthropogenic activities, such as industrial processes, mining, and agriculture, can
significantly increase the presence of heavy metals in soil beyond natural levels, leading
 to potential environmental and health hazards. Hazardous materials, such as As, Cd, Cr,
Cu, Hg, Pb, and others, can be found in various sources, including sewage, paints, alloys,
electronic products, and wastewater from mines. These materials can easily leach into soil
and accumulate over time, contaminating soil [37]. Heavy metal contamination can5 ofsome-
Toxics 2023, 11, 422 24
times result from accidental spills or leaks from industrial sites or transportation. The or-
igins of heavy metal pollution in soils vary and can be attributed to natural and human
activities [38]. Fortoinstance,
potential environmental
the E-wasteand health hazards.
incinerator siteHazardous materials, such
in East Jerusalem wasas As, Cd, Cr, on
studied
Cu, Hg, Pb, and others, can be found in various sources, including sewage, paints, alloys,
soil samples takenelectronic
from 29 different locations specified varying mobility of heavy metals
products, and wastewater from mines. These materials can easily leach into
[39]. These activities canaccumulate
soil and release heavy metals
over time, into thesoil
contaminating air,[37].
water,
Heavy and soil,
metal leading tocan
contamination con-
sometimes result from accidental spills or leaks from industrial
tamination and potential health hazards for humans and wildlife. Therefore, effective sites or transportation. The
origins of heavy metal pollution in soils vary and can be attributed to natural and human
management andactivities
control[38].
of anthropogenic sources are necessary to reduce environmental
For instance, the E-waste incinerator site in East Jerusalem was studied
heavy metal pollution.
on soil samples taken from 29 different locations specified varying mobility of heavy
metals [39]. These activities can release heavy metals into the air, water, and soil, leading to
contamination and potential health hazards for humans and wildlife. Therefore, effective
3. Recent Developments in Heavy Metal Remediation Strategies
management and control of anthropogenic sources are necessary to reduce environmental
Soil contamination by pollution.
heavy metal heavy metals has become a growing concern due to rapid ur-
banization and industrialization.
3. Recent Developments Heavy metals,
in Heavy Metalsuch as lead,Strategies
Remediation arsenic, cadmium, and mer-
cury, are persistent andSoiltoxic in the environment,
contamination by heavy metalsand has they
becomecan accumulate
a growing concernindue
thetosoil over
rapid
time. This contamination
urbanizationcanand
seriously affect the
industrialization. environment
Heavy and
metals, such as human
lead, arsenic,health
cadmium,[40].
andSoil
mercury, are persistent and toxic in the environment, and they
remediation (Figure 3) is thus a critical process to help protect the environment and can accumulate in the soilhu-
over time. This contamination can seriously affect the environment and human health [40].
man health. Soil can become contaminated
Soil remediation (Figure 3) is thuswith harmful
a critical substances,
process to such
help protect the as heavyand
environment met-
als, pesticides, and petroleum
human health. Soilproducts,
can becomethrough
contaminated industrial andsubstances,
with harmful agricultural
such aspractices,
heavy
metals,
waste disposal, and pesticides,spills
accidental and petroleum
[41]. products, through industrial and agricultural practices,
waste disposal, and accidental spills [41].

Figure 3. Remediation techniques for heavy metal removal.

Figure 3. Remediation techniques for heavy metal removal.
A soil remediation technique known as soil substitution reduces the concentration
of pollutants in to a permissible natural limit. Soil spading and soil substitution are two
A soil remediation
methodstechnique known as to
used in soil remediation soil substitution
mitigate the effectsreduces the concentration
of soil contamination by heavy of
pollutants in to ametals
permissible naturalSoil
or other pollutants. limit.
spading,Soilalso
spading
known asand soil substitution
soil turning are two
or soil tilling, involves
digging and mixing the polluted soil with pure soil to reduce
methods used in soil remediation to mitigate the effects of soil contamination by heavy contaminant concentrations.
This method is often used for large areas of contaminated soil, where removing and
metals or other pollutants.
replacing theSoil spading,
entire also soil
contaminated knownlayer as soil turning
is impractical. Soilor soil tilling,
spading helps toinvolves
aerate
digging and mixingthe the polluted
soil and promotessoil with pure
microbial soil
activity, to reduce
which contaminant
can accelerate the naturalconcentrations.
breakdown of
contaminants
This method is often used for in the ground.
large areasSoilof
substitution,
contaminated also known
soil,aswhere
excavation and disposal,
removing andis re-
placing the entire contaminated soil layer is impractical. Soil spading helps to aerate the
soil and promotes microbial activity, which can accelerate the natural breakdown of con-
taminants in the ground. Soil substitution, also known as excavation and disposal, is a
Toxics 2023, 11, 422 6 of 24

a method of soil remediation that involves removing contaminated soil and replacing it
with pure soil. This approach is often used for small, localized areas of contamination, such
as around underground storage tanks or industrial sites. Soil substitution can effectively
reduce the risk of exposure to the contaminant and restore the soil to a healthy state. Both
ground spading and soil substitution can be effective methods for soil remediation, but
they each have advantages and disadvantages.
The choice of method will depend on the nature and extent of the contamination and
other factors, such as cost and accessibility. It is essential to carefully assess the situation
and consult with experts to determine the best approach for remediation [35]. This method
calls for treating the replaced soil to stop further contamination [42]. Another process
of making the contaminated soil less potent is adding new ground and covering the old.
This technique effectively reduces the climate-damaging effects of toxic emissions, but it
is costly, necessitates a sizable working area, and is only suitable for treating soil that is
locally severely contaminated. Furthermore, carrying out earthworks while utilizing the
strategy for replacing the soil may also disturb the local environment [43].
Thermal desorption is used in soil remediation to volatilize heavy metals and met-
alloids, such as mercury and arsenic, from contaminated soil. While thermal desorption
is a method of soil remediation that involves heating contaminated soil to release the
contaminants, it does not necessarily involve the use of microwaves, steam, or infrared
radiation. Once the heavy metals have been volatilized, a negative vacuum tension is
applied, or a transporter gas is used to collect and remove the volatile heavy metals from
the contaminated soil. Two types of thermal desorption methods exist: high-temperature
desorption and low-temperature desorption. High-temperature desorption is typically
performed at temperatures between 320 and 560 ◦ C and is used for heavily contaminated
soils. On the other hand, low-temperature desorption is performed at temperatures be-
tween 90 and 320 ◦ C and is used for less contaminated soils [35,42]. This innovation has
the advantage of being a simple technique for soil remediation. However, the equipment
needed to complete thermal desorption is expensive and the process takes a long time [43].
Soil washing typically involves mechanical agitation of the soil using water or aque-
ous solutions containing chelating agents and/or surfactants. The chelating agents and
surfactants help to solubilize and mobilize contaminants, such as heavy metals, pesticides,
and petroleum hydrocarbons. The washing process generates a wastewater stream or
leachate that contains the dissolved contaminants. The wastewater is then treated using a
range of technologies, such as chemical precipitation or biological treatment, to remove or
immobilize the contaminants before discharge into the environment [11]. Soil washing typ-
ically involves several stages of physical and chemical processes to remove contaminants
from soil. The soil is first physically washed to remove large debris and impurities; then, it
undergoes several chemical extraction stages to remove the remaining contaminants. The
extracted contaminants are treated and disposed of separately, and the cleaned soil can be
returned to its original location [44].
Electrokinetic remediation is another method used for soil remediation to clean up
contaminated soil. It involves using an electric field gradient to remove heavy metals
and other contaminants from the soil. This method involves placing electrodes in the
soil and passing a direct current through the soil between the electrodes. This creates an
electric field gradient that drives the movement of heavy metals and other contaminants
from the soil toward the electrodes [45]. The contaminants are then removed from the
soil by a process known as electroosmosis, where a liquid solution is drawn through the
soil by the electric field, carrying the contaminants with it. Electrokinetic remediation
has some advantages over other soil remediation methods. It is particularly effective for
heavy metals and other ionizable contaminants and can be used for various soil types [44].
Additionally, it does not require the removal of contaminated soil, which can be beneficial
for preserving the site’s integrity [35,42]. In this method, two cathodes are embedded in
the degraded soil to produce a weak electric field [35]. The primary way of transporting
foreign materials from soil to anodes is done through electromigration, electrophoresis,
Toxics2023,
Toxics 2023,11,
11,422
x FOR PEER REVIEW 77 of
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or electroosmotic
electroosmotic streaming.
streaming. When
When thethe contaminant
contaminant adsorbs
adsorbs or advances
or advances at anode,
at the the anode, it
it can
can be removed.
be removed. ThisThis method
method is practical
is practical for treating
for treating low-vulnerability
low-vulnerability soil,soil, requires
requires little
little ef-
effort, andisissimple
fort, and simpletotouse
use[46].
[46].Since
Sinceititdoes
doesnot notdisrupt
disruptthe
thetypical
typical biological
biological system in the
soil, this treatment method is considered safe for the ecosystem. However, the treatment
effectiveness of this approach is low, and and itit has
has no
no effect
effect on
on the
the pH
pH value
value of of the
the soil.
soil. A
longer-term investment in remediation is required if interlaced or covered metal objects objects
are present in
are present in the
thesoil,
soil,because
becausethey theywill
will cause
cause thethe current
current stream
stream to divert.
to divert. The high
The high con-
concentration of obscure
centration of obscure toxins
toxins willwill
alsoalso affect
affect the the viability
viability of electrokinetic
of electrokinetic remediation.
remediation.
Phytoremediation
Phytoremediation is is aa promising
promising soilsoil remediation
remediation technique
technique that
that has gained attention
has gained attention
from
from various experts due to its efficiency, cost-effectiveness, and eco-friendly nature. It
various experts due to its efficiency, cost-effectiveness, and eco-friendly nature. It
involves
involves using
usingplants
plantsto to
remove
remove or degrade
or degradecontaminants from the
contaminants fromsoilthe
[44]. The
soil advantages
[44]. The ad-
of phytoremediation
vantages techniquestechniques
of phytoremediation are shownare in shown
Figure 4.in Figure 4.

Figure 4.
Figure 4. Advantages
Advantages of
of phytoremediation
phytoremediation techniques.
techniques.

4.
4. Heavy
Heavy Metal
Metal Removal
Removal from from Contaminated
Contaminated Soil Soil by
by Phytoremediation
Phytoremediation
Phytoremediation uses metal-aggregating
Phytoremediation uses metal-aggregating plants to plants to reestablish
reestablish debased
debased natural
natural re-
re-
sources, namely, soil and water [47]. The uptake of heavy metals from contaminated
sources, namely, soil and water [47]. The uptake of heavy metals from contaminated soil soil
can
can occur
occur over
over the
the course
course of of several
several distinct
distinct cycles
cycles during
during phytoremediation.
phytoremediation. The specific
The specific
system depends on the type of toxin, the plant species used, and other ecological
system depends on the type of toxin, the plant species used, and other ecological factors. factors. In
aInprocess known
a process knownas phytostabilization,
as phytostabilization, plants are used
plants to immobilize
are used pollutants
to immobilize in soil
pollutants in and
soil
prevent their spread to new areas. Plant roots release proteins and organic acids
and prevent their spread to new areas. Plant roots release proteins and organic acids into into the
soil during the rhizodegradation cycle, which separates soil impurities. Phytoextraction
the soil during the rhizodegradation cycle, which separates soil impurities. Phytoextrac-
involves the uptake
tion involves of contaminants
the uptake by plant
of contaminants by roots
plant and
rootstheir
andaccumulation in the above-
their accumulation in the
ground plant tissues [36]. Phytodegradation is the process by which
above-ground plant tissues [36]. Phytodegradation is the process by which plants plants break down
break
contaminants in their tissues through metabolic processes [44]. Phytoaccumulation is when
down contaminants in their tissues through metabolic processes [44]. Phytoaccumulation
plants take up contaminants and store them in their tissues without breaking them down.
is when plants take up contaminants and store them in their tissues without breaking
Phytovolatilization is when plants release contaminants into the air through transpiration
them down. Phytovolatilization is when plants release contaminants into the air through
or other mechanisms [36]. Each of these processes has advantages and limitations, and
transpiration or other mechanisms [36]. Each of these processes has advantages and limi-
the best approach depends on the specific situation. For example, phytoextraction may
tations, and the best approach depends on the specific situation. For example, phytoex-
be effective for removing high concentrations of contaminants from the soil, while phy-
traction may be effective for removing high concentrations of contaminants from the soil,
tostabilization may be more appropriate for lower concentrations of contaminants or for
while phytostabilization may be more appropriate for lower concentrations of contami-
preventing their spread to other areas [48].
nants or for preventing their spread to other areas [48].
The removal of heavy metals from soil and water and the selection of suitable plant
The removal of heavy metals from soil and water and the selection of suitable plant
species can both be accomplished through phytoremediation [49]. Plants are viable options
species can both be accomplished through phytoremediation [49]. Plants are viable op-
for phytoremediation due to their physiological capacity to withstand and accumulate
tions for phytoremediation due to their physiological capacity to withstand and
Toxics 2023, 11, x FOR PEER REVIEW 8 of 24

Toxics 2023, 11, 422 8 of 24

accumulate heavy metals as well as their adaptability to various environmental condi-

tions. Furthermore, the use of specific plant species for phytoremediation can be tailored
heavy metals
to the type of as well metal
heavy as their adaptability
pollution, to various
as different plantenvironmental
species haveconditions. Further-
varying abilities to
more, the use
accumulate of specific
specific heavyplant
metals species for phytoremediation
[50]. There are various techniques can bethat
tailored to thedevel-
have been type
of heavy
oped metal
for the pollution,
removal as different
of heavy plant species
metals through have varyingprocesses.
phytoremediation abilities to accumulate
specific
However, compared to physiological strategies, they are less viabledeveloped
heavy metals [50]. There are various techniques that have been and more expen-for the
removal of heavy metals through phytoremediation processes.
sive [51]. Standard techniques, such as physicochemical cycles, are typically used to re-
moveHowever,
contaminants compared to physiological
from soil. Due to theirstrategies,
more notable theyeffectiveness
are less viableandandlowermore ex-
costs,
pensive [51]. Standard
physiological strategiestechniques,
are generally such as physicochemical
recognized as additional cycles, are typically
promising options used to
for soil
remove contaminants from soil. Due to their more notable effectiveness
remediation [31]. Bioremediation can also involve using microorganisms to break down and lower costs,
physiological strategies areinto
or transform contaminants generally recognized
less toxic as additional promising
forms. Microorganisms can degrade options
organic for pol-
soil
remediation [31]. Bioremediation can also involve using microorganisms
lutants or transform heavy metals into less harmful substances. For example, some bacte- to break down
or
ria transform
can convert contaminants
poisonous forms into of
less toxic forms.
mercury Microorganisms
into less toxic elementalcan degrade
mercury, organic
which can
pollutants
then be released into the atmosphere. Other microorganisms can break down organicsome
or transform heavy metals into less harmful substances. For example, pol-
bacteria can convert
lutants, such poisonous
as petroleum forms of mercury
hydrocarbons, into less
into harmless toxic elemental
byproducts. mercury, which
Phytoremediation is
can then be released into the atmosphere. Other microorganisms can break down organic
a plant-based method that uses plants to absorb and remove contaminants from soil or
pollutants, such as petroleum hydrocarbons, into harmless byproducts. Phytoremediation
water [52]. Plants with high phytoremediation capabilities are often characterized by fast
is a plant-based method that uses plants to absorb and remove contaminants from soil or
growth, high biomass, deep roots, and efficient uptake and transport of heavy metals or
water [52]. Plants with high phytoremediation capabilities are often characterized by fast
other contaminants to their above-ground parts. The use of phytoremediation can be a
growth, high biomass, deep roots, and efficient uptake and transport of heavy metals or
cost-effective and environmentally friendly approach to remediate contaminated sites
other contaminants to their above-ground parts. The use of phytoremediation can be a
[53].
cost-effective and environmentally friendly approach to remediate contaminated sites [53].
Due to its unique ability to eliminate dangerous synthetic substances through plant
Due to its unique ability to eliminate dangerous synthetic substances through plant
underground root growth, bioaccumulation, impurity debasement, or movement [54], the
underground root growth, bioaccumulation, impurity debasement, or movement [54],
phytoremediation approach has many advantages in ecological clean-up. Various tech-
the phytoremediation approach has many advantages in ecological clean-up. Various
niques for phytoremediation are shown in Figure 5. Using phytoremediation for heavy
techniques for phytoremediation are shown in Figure 5. Using phytoremediation for heavy
metal removal
metal removalfrom frompolluted
pollutedsoils
soilscan
can
alsoalso allow
allow forfor
thethe cultivation
cultivation ofcrops
of oil oil crops for bio-
for biodiesel
diesel or bioenergy production. In a study on the use of sunflower
or bioenergy production. In a study on the use of sunflower and canola crops for the and canola crops for
the phytoremediation of heavy-metal-contaminated soils, it was
phytoremediation of heavy-metal-contaminated soils, it was found that not only did the found that not only did
the plants
plants reduce reduce
heavy heavy
metalmetal concentrations
concentrations in theinsoil,
thebutsoil,they
butalso
theyproduced
also produced high
high yields
yields
of of oil
oil for usefor
inuse in biofuel
biofuel production
production [55]. [55].
ThisThis suggests
suggests thatthat phytoremediation
phytoremediation couldcould
be
be valuable for environmental remediation and sustainable energy
valuable for environmental remediation and sustainable energy production [56]. Table production [56]. Table1
1 shows
shows the
the potential
potential plant
plant species
species which
which can
can bebe used
used forfor heavy
heavy metal
metal remediation.
remediation.

Figure 5.
Figure 5. Techniques for phytoremediation.
Techniques for phytoremediation.
Toxics 2023, 11, 422 9 of 24

Table 1. Potential plant species for heavy metal remediation.

S. No. Plant Species Contaminants Removed Ref.

1 Brassica juncea L. Cd, Cu, Zn [57–59]
2 Populus sp. Cd [60]
3 Helianthus annuus Zn [61]
4 Melica jacquemontii Poaceae Fe [62]
5 Medicago sativa, Brassica nigra Pb [63]
6 Eleocharis acicularis Cu [64]
7 Lemna minor Pb, Cd, Ni, Cr [65]
8 Brassica rapa L. U [66]
9 Alyssum murale, Berkheya coddii Ni [67]
10 Azolla filiculoides Hg (II), Pb (II) [68]
11 Jatropha curcas Al, Cd, Fe, Cr, Pb, Zn, Ni, Cu [69]
12 Viola bashanensis Zn [70]
13 Aeollanthus subacaulis Cu [71]
14 Oryza sativa Cd, Zn, Fe, Cu, Pb, Cr, Mn [72,73]
15 Schima superba Mn [74]

4.1. Phytoextraction
This process involves using the natural ability of plants to absorb and accumulate
pollutants through their roots and above-ground parts and transform or degrade them into
less harmful substances. The plants uptake these pollutants through their root systems and
then transport them to their above-ground biomass, accumulating them in various plant
parts, such as leaves, stems, and fruits. In some cases, the pollutants can be removed from
a site by harvesting the plants and disposing of them elsewhere. The plants can be used for
various purposes, such as biofuel production or livestock feed, provided the accumulated
toxins are safe. This process is referred to as phytoextraction [75]. Metal exchange to shoots
is a significant physiological interaction because projections are much easier to collect
than roots—the most effective phytoremediation method for removing heavy metals and
metalloids. The main idea behind phytoextraction is to grow appropriate plant species on
site, collect the metal-enriched biomass, and then treat it to reduce its mass and size [49].
The collected biomass can be processed in several ways, such as fertilizing the soil,
drying it out, and heating it until it disintegrates. This process is called “phytomining”,
and it is used to extract metals, such as nickel, cobalt, and zinc, from the enriched plant
material. However, phytoextraction is not always economically feasible, especially for
metals such as lead and cadmium, which have a lower market value [76]. Lemna valdiviana
is a species of duckweed that is native to North America and is known for its ability to
accumulate heavy metals and metalloids, such as arsenic, in its tissues. Lemna valdiviana
can actually remove up to 82% of arsenic from contaminated water, according to studies on
the plant [77]. This makes it a promising candidate for the phytoremediation of arsenic-
contaminated water sources. However, further research is needed to fully understand
the plant’s arsenic accumulation mechanisms and optimize its use in phytoremediation
applications [77]. Bixa orellana and Zea mays L. are exciting examples of plants with high
phytoremediation potential for heavy metals, particularly chromium and lead. It is also
noteworthy that adding chelating agents, such as ethylenediaminetetraacetic acid (EDTA),
can enhance the phytoextraction process by increasing the solubility and availability of
heavy metals in soil [78]. A study on lettuce species and their ability to accumulate copper
is also valuable in identifying plant species that can effectively remove specific heavy
metals from contaminated soils [79].

4.2. Phytostabilization
Phytostabilization is a phytoremediation technique that uses metal-tolerant plant
species to immobilize heavy metals in soil and reduce their bioavailability. This is achieved
using plants with deep root systems that can penetrate and stabilize the soil, preventing
heavy metals from leaching into the environment [80]. This can occur through various
Toxics 2023, 11, 422 10 of 24

mechanisms, including precipitation or complexation of heavy metals in the rhizosphere,

uptake, and accumulation of heavy metals in root tissues, and adsorption onto root cell
walls. The immobilized heavy metals become less mobile and bioavailable, reducing the
potential for human and environmental exposure [81]. Phytostabilization is a technique
that helps preserve soil health at heavy-metal-contaminated sites. It involves using plants
to immobilize heavy metals in the soil and prevent their dispersion by wind or runoff.
This technique is advantageous because it does not require the removal of contaminated
biomass, unlike phytoextraction [43]. To achieve effective phytostabilization, appropri-
ate plant species tolerant to heavy metal conditions must be selected, have dense root
systems, and be able to produce a significant amount of biomass. Additionally, soil amend-
ments adjust metal speciation, reduce metal solubility and bioavailability, and improve the
physicochemical and biological properties of soil. These amendments can include organic
or inorganic materials that increase soil organic matter content and essential nutrients,
improving plant colonization and water-holding capacity [82].

4.3. Phytovolatilization
This technique eliminates poisons from soil without requiring the land to be taken
away or dealt with. Nonetheless, the viability of phytovolatilization relies upon the
toxins present, the plant species utilized, and natural conditions. For example, in the
phytovolatilization of Hg, the vaporized Hg can be recondensed and redeposited in the
environment, resulting in water and soil pollution. Therefore, phytovolatilization must
be utilized cautiously, and ecological conditions, for example, wind speed and direction,
must be assessed to limit potential ecological harm [55]. Phytovolatilization is viable in
controlling certain environmental pollutants, yet it is not broadly utilized as it has certain
limitations. The fundamental disadvantage is the likelihood of airborne toxins causing
pollution in surrounding areas. Hence, it is necessary to use this strategy cautiously and
only in areas with low population densities or air contamination restrictions exist [44].

4.4. Rhizofiltration
Rhizofiltration is a promising approach for removing contaminants from water and liq-
uid waste, and several plant species have been identified as effective in this process. Plants
with fibrous root systems and large surface areas are well-suited for rhizofiltration [28].
For example, Typha latifolia effectively removes methyl parathion from hydromorphic soils,
while bean species (Phaseolus vulgaris) have been found to extract uranium and cesium from
groundwater efficiently. Arundo donax is effective in rhizofiltrating copper from constructed
wetlands, and Eichhornia crassipes, Salvinia molesta, and Pistia stratiotes have been identified
as promising options for heavy metal removal from industrial sludge [83]. Rhizofiltration
has the advantage of being relatively low-cost and environmentally friendly compared to
other remediation methods. However, significantly reducing contaminant levels may take
longer than other methods, such as chemical treatments or excavation [36].

4.5. Rhizodegradation
Rhizodegradation is a natural and cost-effective method for the remediation of con-
taminated soils. It is a complex process involving interaction between plant roots, mi-
croorganisms, and contaminants [51]. Rhizodegradation is a type of phytoremediation
that consists in using plants and their associated root-zone microorganisms to degrade
pollutants in soil. The rhizosphere is the zone of soil surrounding the roots of plants, where
there is a high concentration of microorganisms that can interact with the plant and the
contaminants. The selection of plant species also plays a crucial role in rhizodegradation,
as different plants release different types and quantities of exudates, which can influence
the microbial community and their ability to degrade contaminants. Rhizodegradation has
several advantages over traditional remediation methods, including its low cost, reduced
environmental impact, and potential for long-term effectiveness [41]. However, the effi-
ciency of the process depends on several factors, such as the type of contaminants present
Toxics 2023, 11, 422 11 of 24

in the soil, the type of plants used, and the environmental conditions. The effectiveness of
rhizodegradation can depend on selecting appropriate plants and microorganisms for a
particular site. Different plant species and their associated root-zone microorganisms can
degrade different types of pollutants and survive and thrive in different environmental
conditions [84].

4.6. Phytodesalination
Phytoremediation has been widely studied and accepted to remove salt from impacted
soils using halophytic plants [85]. Halophytes are plants that are adapted to grow in
highly saline environments, and they are more effective in heavy metal conditions than
glycophytic plants, which grow in non-saline environments [86]. Studies have shown that
halophytic plants, such as Suaeda maritima and Sesuvium portulacastrum, can remove 504 kg
and 474 kg of salt from a 1-hectare salt-impacted field in just four months [87]. These plants
can accumulate sodium chloride from highly saline soils, which helps improve crop yield
and quality. Additionally, this method helps reduce soil salinity levels, allowing glyco-
phytic crops, such as Hordeum vulgare, to grow normally. Overall, phytoremediation using
halophytic plants is a promising strategy for remediating salt-impacted soils, improving
crop yield, and reducing the negative impacts of salinity on plant growth [6].

5. Potential Biotechnological Approaches for Phytoremediation

Several aids or techniques can enhance phytoremediation, depending on the specific
contaminants and environmental conditions. Some of these aids include: Bioaugmentation:
This involves adding beneficial microorganisms to the soil, which can help to break down
contaminants and improve plant growth [56]. Phytoextraction: Utilizing plants that can
accumulate large concentrations of pollutants in their tissues allows for secure collection
and disposal. Rhizofiltration: This technique uses the roots of plants to filter contaminants
from water. The roots absorb the contaminants and then release them into the plant tissue,
where they can be broken down or stored [31]. Hyperaccumulation: This method makes
use of plants that can store exceptionally large concentrations of specific pollutants in their
tissues. These plants typically remove metals, such as nickel or lead. Soil amendments:
Adding certain substances to soil, such as activated carbon or organic matter, can help to
improve the soil structure and increase the availability of nutrients for the plants. Genetic
engineering: Researchers can modify plant characteristics to increase their ability to remove
specific pollutants, as heavy metals, in our case [45].
Plant biotechnology techniques undoubtedly contributed to the development of trans-
genic crops, and researchers have been working toward the development of efficient, ethical,
and cost-effective bioremediation techniques; however, there are still some challenges. Since
they differ from physical–synthetic remediation techniques, these biotechnologies have
emerged as alternative options aiming for natural rehabilitation. Other intrusive techniques
include high-temperature vitrification, corrosive washing, and the removal of soil from an
area, all of which have higher associated costs and have an impact on soil productivity and
biodiversity [88]. From a molecular viewpoint, a successful candidate for phytoremediation
should have an adequate root-uptake genetic system that allows it to take up pollutants
from soil efficiently. The plant should also have a high degree of root-to-shoot movement
so that the contaminants can be transferred from the roots to the above-ground portions of
the plant. The ability of a plant to withstand xenobiotic stress is influenced by several traits,
including those that encrypt detoxification catalysts and carriers that transport the toxin
out of the cell. Some important genes include phytochelatin synthase, which synthesizes
phytochelatins, which bind to heavy metals and other toxic compounds and transport
them out of the cell. Metallothioneins are also involved in binding heavy metals, and
glutathione S-transferases detoxify a wide range of xenobiotics. Transporters, such as ATP-
binding cassette transporters, multidrug and toxin efflux transporters, and oligopeptide
transporters, are also crucial in moving xenobiotics out of the cell. An inclusive transcrip-
tome analysis can provide valuable insights into the molecular mechanisms underlying
 Toxics 2023, 11, 422 12 of 24

hyperaccumulation and phytoremediation. Transcriptome analysis involves the sequencing

and analysis of all the messenger RNA molecules produced by a cell or tissue, which can
provide information on gene expression and regulatory mechanisms. This information can
help researchers understand how plants respond to xenobiotic stress and identify potential
targets for genetic engineering to improve phytoremediation performance [89].
Overall, the use of these aids and techniques can help to enhance the effectiveness
of phytoremediation and make it a more viable option for the clean-up of contaminated
sites. Like any other remediation technique, phytoremediation must be evaluated case-
by-case to determine its effectiveness and safety for a particular area. Factors such as soil
characteristics, contaminant type and concentration, climate, and plant species should all
be considered before implementing a phytoremediation strategy [53].

6. Factors Affecting Phytoremediation Potential

The accessible part of metals is the fraction plants can take up and is influenced by
Toxics 2023, 11, x FOR PEER REVIEW 14 of 24
soil pH, redox potential, and the presence of chelating agents or competing ions, as shown
in Figure 6. The inaccessible part of metals is firmly bound to soil minerals and cannot
be extracted by plant roots. Hence, it is essential to select appropriate plant species and
• optimize soil conditions
Management to enhance
practices: Properthe bioavailabilitypractices,
management of metals such
for effective
as soilphytoremedi-
amendments and
ation [44,54]. In addition, chelating agents, such as EDTA or citric acid, can enhance the
fertilization, can improve plant growth and the effectiveness of phytoremediation. In
uptake of metals by plant roots, but they may also increase the risk of metal leaching and
addition, the local microbial area in the rhizosphere can improve phytoremediation
contamination of groundwater [44]. The use of chelating agents to alter the bioavailability
by influencing
of strong metals maythe accessibility
be harmful andand
to plants versatility of heavy
influence their metals
behavior. in these
Along soils lines,
[99]. itHence,
studying microbial ecology and its interactions with plants and soils is
is essential to consider the advantages and disadvantages of chelating agents to guarantee necessary to
thatuse phytoremediation
they effectively.
are safe for the environment andTherefore, it is2essential
climate. Table to carefullyofassess
shows a compilation work phy-
toremediation’s
which has been carriedpotential risks and
out previously benefits
by many before its
researchers onimplementation
factors which affectin contami-
the
performance of phytoremediation.
nated sites [100].

Figure 6.6.Factors
Figure Factorsaffecting phytoremediation
affecting phytoremediation potential.
potential.

7. Phytoremediation: Challenges and Difficulties

7.1. Application of Phytoremediation Techniques Needs to Be Accelerated
Phytoremediation can be influenced by several factors, as mentioned in the previous
section. The biomass production of plants and the accumulation rate of toxins in the plants
can affect the time required for phytoremediation. The amount of biomass produced by
plants determines the amount of pollutant that can be removed from or stabilized in the
soil, and the rate of accumulation of toxins in plants affects the speed at which they can
be removed from the site. The slow growth of many hyperaccumulating plants can limit
Toxics 2023, 11, 422 13 of 24

Table 2. Factors affecting the performance of phytoremediation in earlier studies.

Plants Target Medium Inducing Factor Observation Ref.

Helianthus tuberosus showed adequate growth
in the presence of minor metal fixations and a
Based on metal and its
Helianthus tuberosus Soil pH range of 5 to 6. With the addition of [90]
concentration and pH
metals in the soil at pH 5, the grouping of
metals in shoots grew.
Lemna valdiviana collect more significant
pH (3.94–9.02) amounts of As (1190 mg kg−1 ) when the pH
Lemna valdiviana Water P (0–0.14 mmol·L−1 ) is between 6.30 and 9, the P concentration is [77]
N (0.09–13.71 mmol·L−1 ) 0.05 mmol L−1 , and the N concentration is
7.90 mmol L−1 .
Ulva ohnoi continued to develop favorably
between 18 and 25 ◦ C, S35. The focus factor
Ulva ohnoi Water Salinity and temperature [91]
with the highest value was 81.30% of Cd
added at 0.63 gL−1 to 18 C and S15.
According to all indications, the genotype
LXYC was the most suitable one for
Vicia faba L. Soil Genotype [92]
phytoremediation in soil that had been
moderately or slightly depleted in Pb and Cd.
Plants that communicate with ScZRC1, such
Arabidopsis thaliana
Soil/water Genetic modification as poplar and A. thaliana, could accumulate [93]
and Populus alba
more Zn.
At D20, the biomass and Cd accumulation
Festuca arundinacea Soil Planting density [94]
peaked (13.30 g Cd m−2 ).
Carbon nanotubes with At 5.23% to 27.97%, multi-walled carbon
Solanum nigrum L. Soil [95]
multiple walls nanotubes could increase plant biomass.
Under treatments containing 100 and
200 mg kg−1 biochar, respectively, the
Bidens pilosa L. Soil Activated carbon (biochar) [96]
accumulation of Cd increased by 16.44
and 39.37%.
The growth in digestate could increase
compact Cd fixation in the stems
Pennisetum hybridum Soil Digestate [97]
(7.94–42.39%), leaves (12.53–74.11%),
and roots (18.59–57.94%).
Under the treatment with Cd and urea, the
individual Cd convergences of the roots,
Willow Soil Urea [98]
xylem, bark, and leaves were 8.30, 8.15, 26.79,
and 33.04 mg kg−1 .

Several factors can affect the potential of phytoremediation to remove contaminants

from soil, including:
• Plant species: Different plant species have varying abilities to accumulate and re-
move contaminants from soil. Hyperaccumulator plants are particularly effective in
absorbing heavy metals from soil.
• Contaminant type and concentration: The type and concentration of the contaminant
in the soil can affect the plant’s ability to absorb and remove it. Some contaminants,
such as heavy metals, can be more difficult to remove than others.
• Soil properties: Soil properties, such as pH, organic matter content, and nutrient
availability, can affect the ability of plants to grow and absorb contaminants.
• Climate and weather conditions: Climate and weather conditions, such as tempera-
ture, precipitation, and sunlight, can affect plant growth and the rate of contaminant
removal.
Toxics 2023, 11, 422 14 of 24

• Soil moisture: The moisture content of the soil can affect the growth and health of the
plants, as well as the availability of the contaminants for uptake.
• Plant growth stage: The growth stage of the plant can affect its ability to absorb
contaminants, as well as the biomass produced for removal.
• Duration of treatment: The duration of phytoremediation treatment can affect the
effectiveness of contaminant removal. More extended treatment periods may be
necessary for some contaminants and soil types.
• Management practices: Proper management practices, such as soil amendments and
fertilization, can improve plant growth and the effectiveness of phytoremediation. In
addition, the local microbial area in the rhizosphere can improve phytoremediation
by influencing the accessibility and versatility of heavy metals in soils [99]. Hence,
studying microbial ecology and its interactions with plants and soils is necessary to
use phytoremediation effectively. Therefore, it is essential to carefully assess phytore-
mediation’s potential risks and benefits before its implementation in contaminated
sites [100].

7. Phytoremediation: Challenges and Difficulties

7.1. Application of Phytoremediation Techniques Needs to Be Accelerated
Phytoremediation can be influenced by several factors, as mentioned in the previous
section. The biomass production of plants and the accumulation rate of toxins in the
plants can affect the time required for phytoremediation. The amount of biomass produced
by plants determines the amount of pollutant that can be removed from or stabilized
in the soil, and the rate of accumulation of toxins in plants affects the speed at which
they can be removed from the site. The slow growth of many hyperaccumulating plants
can limit their effectiveness in phytoremediation [101]. Moreover, the remediation of a
contaminated site using phytoremediation alone can be a slow process, taking years to
even centuries for some metals. The availability and adaptability of foreign substances
in the soil, as well as the ability of the plants to retain them, frequently limit the uptake
and accumulation of heavy metals in plants. Additionally, the extent and depth of root
growth of the plants used for remediation can also limit their performance, as the roots
may not cover the entire depth and extent of the contaminated area. Indeed, the time
required for phytoremediation to effectively reduce or remove heavy metal contamination
can be a significant challenge [54]. Additionally, the root growth of these plants may not
reach the full depth of the contaminated area, limiting their effectiveness. As a result,
phytoremediation may need to be combined with other remediation techniques, and the
overall cost and time involved in the process must be carefully considered [102].

7.2. Lack of Effective Methods to Remove Contaminated Biomass

Phytoremediation is an environmentally friendly and cost-effective approach that can
be used alone or with other remediation techniques. However, phytoextraction can result
in contaminated biomass, which requires proper disposal to prevent further environmental
pollution. It is essential to consider the potential environmental impacts of both the phy-
toremediation process itself and the removal of the resulting contaminated biomass [103].
The six standard methods for disposing of contaminated biomass (composting, landfilling,
pyrolysis, leaching, cremation, and direct disposal) each have advantages and disadvan-
tages. They must be carefully evaluated based on the specific circumstances of each site, as
shown in Figure 7. Soil treatment involves using microorganisms to break down the con-
taminants in biomass, while compaction compresses biomass into a dense, stable material.
Pyrolysis is a process of thermal degradation that converts biomass into solid, liquid, and
gas fractions [104]. Leaching relies on the ability of soluble heavy metals to migrate through
a medium, and cremation involves thermal degradation of biomass into treatable-metal-
containing ash. Direct disposal is not recommended due to its potential environmental risks.
Further research is needed to develop effective and environmentally friendly methods for
disposing of contaminated biomass generated from phytoremediation [105].
 stable material. Pyrolysis is a process of thermal degradation that converts biomass into
solid, liquid, and gas fractions [104]. Leaching relies on the ability of soluble heavy metals
to migrate through a medium, and cremation involves thermal degradation of biomass
into treatable-metal-containing ash. Direct disposal is not recommended due to its poten-
tial environmental risks. Further research is needed to develop effective and environmen-
Toxics 2023, 11, 422 15 of 24
tally friendly methods for disposing of contaminated biomass generated from phytore-
mediation [105].

Figure 7. Pros and cons of various disposal methods of polluted biomass after
after phytoremediation.
phytoremediation.

8. Advancements in
8. Advancements in Research
Research to to Address
Address thethe Problems
Problems and and Challenges
Challenges
8.1. Techniques Used to Increase the Effectiveness of Phytoremediation
8.1. Techniques Used to Increase the Effectiveness of Phytoremediation
Genetic engineering can enhance plants’ phytoremediation potential by introducing
Genetic engineering can enhance plants’ phytoremediation potential by introducing
or modifying genes that can improve their ability to absorb and detoxify pollutants. This
or modifying genes that can improve their ability to absorb and detoxify pollutants. This
involves introducing genes that can increase plant metal uptake, transport, and detoxifi-
involves introducing genes that can increase plant metal uptake, transport, and detoxifi-
cation [55]. However, this approach raises ethical concerns and regulatory issues about
cation [55]. However, this approach raises ethical concerns and regulatory issues about
releasing genetically modified organisms (GMOs) into the environment. Another method
releasing genetically modified organisms (GMOs) into the environment. Another method
is to use a combination of different plant species, known as phytococktails, to remediate
is to use acontaminants
multiple combination simultaneously
of different plant species,
[14]. known ascan
This approach phytococktails,
increase the to remediate
overall effec-
tiveness of phytoremediation, as other plant species have additional metal uptakeeffec-
multiple contaminants simultaneously [14]. This approach can increase the overall and
tiveness of phytoremediation,
accumulation as other
capabilities. Lastly, plant species
improving have additionalprocess
the phytoremediation metal uptake
can alsoand
be
accumulation
achieved capabilities.
by optimizing Lastly,
growth improving
conditions, for the phytoremediation
instance, process
by adjusting soil can alsolev-
pH, nutrient be
achieved
els, by optimizing
and water availabilitygrowth conditions,
[101]. This for instance,
can enhance by adjusting
plant growth and metal soil pH, nutrient
uptake, thereby
levels, and water availability [101]. This can enhance plant growth and
increasing phytoremediation efficiency. However, this approach may require additional metal uptake,
thereby increasing
resources phytoremediation
and maintenance efficiency.
efforts. Overall, using However,
differentthis approach
strategies andmay require can
techniques ad-
ditional resources
significantly andthe
improve maintenance efforts.
effectiveness Overall, using different
of phytoremediation strategies and
for contaminated soilstech-
and
niquesbodies.
water can significantly
However, improve the effectiveness
each approach of phytoremediation
has its advantages and limitationsforand
contaminated
should be
soils and water bodies. However, each approach has its advantages and limitations
carefully evaluated based on the specific context and goals of the remediation project [45]. and
Agronomic measures, such as compost application, water guidelines, and further
developed culturing procedures, can further enhance the proficiency of the phytoreme-
diation of heavy metal contamination [106]. In addition, phytoremediation time can be
decreased by various means, such as genetic engineering, soil amendments, and plant
growth regulators. A plant’s capacity to accumulate and withstand heavy metals can be
enhanced genetically, and soil enhancements, such as biochar and fertilizers, can enhance
soil quality and increase the availability of nutrients for plants. Plant growth regulators
can promote plant growth and boost biomass production, leading to higher metal uptake
by plants [107]. However, it is essential to note that using some of these methods, such
as chelating agents and genetic engineering, may negatively impact the environment and
human health if not used properly. It is, therefore, necessary to carefully evaluate and mon-
itor these methods’ effectiveness and potential risks before their widespread application in
phytoremediation [48].
This information will help identify transporters and ion channels involved in metal
uptake and homeostasis, which can be targeted for genetic engineering to enhance phy-
 chelating agents and genetic engineering, may negatively impact the environment and
human health if not used properly. It is, therefore, necessary to carefully evaluate and
monitor these methods’ effectiveness and potential risks before their widespread applica-
tion in phytoremediation [48].
Toxics 2023, 11, 422 This information will help identify transporters and ion channels involved in 16 metal
of 24
uptake and homeostasis, which can be targeted for genetic engineering to enhance phy-
toremediation efficiency. Genetic engineering can also introduce metal-resistant genes
from other organisms into plants or modify plant enzymes involved in metal uptake and
toremediation efficiency. Genetic engineering can also introduce metal-resistant genes
detoxification processes [54]. However, using genetically modified plants in phytoreme-
from other organisms into plants or modify plant enzymes involved in metal uptake and
diation still faces regulatory and ethical challenges, and more research is needed to ensure
detoxification processes [54]. However, using genetically modified plants in phytoremedi-
their
ationsafety andregulatory
still faces effectiveness.andHereditary designing
ethical challenges, anddepends on the in
more research is vitro
neededpresentation
to ensure
of unfamiliar qualities into beneficiary cells to change their unique genetic
their safety and effectiveness. Hereditary designing depends on the in vitro presentation attributes and
acquire new assortments of existing items or produce new ones. The responses
of unfamiliar qualities into beneficiary cells to change their unique genetic attributes and of different
heavy-metal-pressure
acquire new assortments in different
of existingplants
itemsare determined
or produce newthrough
ones. The sub-atomic
responsesand genetic
of different
tests using the attributes of absorption abilities and resilience of hyperaccumulators
heavy-metal-pressure in different plants are determined through sub-atomic and genetic [54].
Selecting suitable plant species depends on several factors, such as
tests using the attributes of absorption abilities and resilience of hyperaccumulators [54]. the type and con-
centration of contaminants, soil, climatic conditions, and phytoremediation
Selecting suitable plant species depends on several factors, such as the type and goals. For ex-
ample, some plants are better suited to the remediation of organic
concentration of contaminants, soil, climatic conditions, and phytoremediation goals. Forcontaminants, while
others
example,aresome
moreplants
effective
are in removing
better suited heavy metals. In addition
to the remediation of organicto exploring
contaminants, new while
plant
species,
others aredeveloping genetically
more effective modified
in removing plants
heavy can expand
metals. the range
In addition of phytoremedia-
to exploring new plant
tion options.
species, Genetic
developing engineering
genetically can enhance
modified plants’
plants can expand metal-accumulating capacity, in-
the range of phytoremediation
crease their tolerance to toxic contaminants, and change their
options. Genetic engineering can enhance plants’ metal-accumulating capacity, root systems so that they
increase
capture and store contaminants better [45,51]. Overall, continued research
their tolerance to toxic contaminants, and change their root systems so that they capture and develop-
ment of phytoremediation
and store contaminants better technology
[45,51]. will be necessary
Overall, continued to research
increase andits effectiveness,
developmentex- of
pand the range of technology
phytoremediation plant species willandbegenotypes
necessary available,
to increaseand address the unique
its effectiveness, expand chal-
the
lenges
range of different
plant speciescontaminants
and genotypesand environmental
available, and conditions
address the [108]. A schematic
unique challengesrepre-of
sentation of various techniques
different contaminants to enhance phytoremediation
and environmental conditions [108]. Aefficiency
schematicisrepresentation
shown in Figure of
8.
various techniques to enhance phytoremediation efficiency is shown in Figure 8.

Figure 8. Various techniques to enhance phytoremediation efficiency.

efficiency.

8.2. Disposal of Harmful Plant Waste after Phytoremediation

Pyrolysis is an effective method for changing the form of heavy metals in biomass
and making them more stable. The pyrolysis temperature is also critical, as higher temper-
atures result in more substantial stability. Pyrolysis can also recover heavy metals from
contaminated biomass, such as Pteris vittata [54]. Heavy metals exist in various forms and
quantities in plants, such as lead (Pb), predominantly in the form of soluble inorganic and
amino acid salts in striped seaweed. In contrast, cadmium (Cd) mainly exists as gelatin
and protein in tea plants, Panicularia paniculata, and impatiens resin [109]. It also exists as
heavy metal phosphate and oxalate, which are insoluble in water, grain roots, gelatin, and
protein binding in grain malt. Therefore, it is essential to investigate the different forms of
heavy metals in plants to determine the appropriate removal techniques [110]. Disposal
of plant waste after phytoremediation is a critical step in the process. The plant biomass
accumulating heavy metals must be carefully handled and disposed of to avoid causing
further contamination.
The harvested plant material can sometimes be incinerated to recover any accumulated
metals in the biomass. However, incineration is not always practical or cost-effective and
may release pollutants into the air. Alternatively, the plant material can be landfilled or
deposited in isolated hazardous waste sites. However, the disposal of biomass in landfill or
Toxics 2023, 11, 422 17 of 24

hazardous waste sites can lead to long-term environmental pollution. To mitigate this, the
harvested plant material can be used for other purposes, such as composting or bioenergy
production. In composting, the plant biomass can be mixed and ‘diluted’ with other organic
materials and allowed to decompose to produce a nutrient-rich soil amendment. The
resulting compost can be used for agriculture, horticulture, or landscaping. In bioenergy
production, plant biomass can yield energy through various methods, such as anaerobic
digestion, pyrolysis, or combustion. This approach can help reduce the reliance on fossil
fuels and provide a renewable energy source [32].

9. Challenges and Future Recommendations

Toxics 2023, 11, x FOR PEER REVIEW Even though phytoremediation is a successful effective strategy for removing18pollu- of 24

tants from the environment, it has a few limitations and disadvantages on which limited
knowledge exists since most of the exploration has been carried out in controlled environ-
ments. If theplants
appropriate level of toxins
and in the soil
optimizing is too high, this
environmental can affect
conditions. the plant’s
Botanists and growth and
plant physi-
ability
ologiststocanremediate
providethe site. Additionally,
information some translocation,
on the uptake, plant species may be more suitable
and detoxification for
of con-
certain
taminants typesby of contamination
plants, than others
and microbiologists canand selecting
give the wrong
insight into the roleplant species
of soil could
microorgan-
lead
ismstoinlower phytoremediation
facilitating efficiency.
phytoremediation Furthermore,
processes. Aquaticthere is a riskwould
biologists of plant uptake
help of
finding
contaminants, which could lead to potential health risks if animals or humans
suitable plants for removal of specific contaminants and their efficacy in hydric and under consume the
contaminated plant material.
water soils. Furthermore, Finally, the economic
interdisciplinary research feasibility
can helpofto phytoremediation can be
identify the limitations
aand
limiting factor, as the costs associated with plant growth, monitoring,
challenges associated with phytoremediation and develop solutions to overcome and maintenance
can
thesebe challenges.
high [54,111]. ForInterdisciplinary
instance, molecularresearch on phytoremediation
biology techniques can betoused enhance efficiency
to develop ge-
isnetically
shown engineered
in Figure 9.plants
Disadvantages include the biomass after remediation
to increase their ability to accumulate and detoxify contami- being toxic
and,
nants,if it is burned,
while the ash alsocan
nanotechnology being toxic,the
enhance as well
uptakeas the
andtoxicity
transportof the end products by
of contaminants of
remediation
plants [6]. plant composting.

Figure9.9. Interdisciplinary
Figure Interdisciplinaryresearch
researchon
onphytoremediation.
phytoremediation.

Phytoremediation isisaamultidisciplinary
Phytoremediation promising method forinvolving
field the remediation
variousofscientific
heavy metals from
disciplines
polluted
that aims soil, but it still
to develop andhas some phytoremediation
improve limitations and challenges thatInterdisciplinary
technology. must be addressed:
research
is• essential
It is a for
slowenhancing phytoremediation
process which efficiency
may take several yearsand addressing
to achieve the complex
significant environ-
results, espe-
cially in highly contaminated soils. The time required for remediation depends on
several factors, such as the type and concentration of contaminants, the plant species
used, soil properties, and environmental conditions.
• It can sometimes be less effective due to some hyperaccumulator plants’ slow growth
Toxics 2023, 11, 422 18 of 24

mental problems associated with soil contamination. Some scientific disciplines involved
in phytoremediation research include botany, plant physiology, soil science, microbiology,
chemistry, aquatic science, and environmental engineering. Combining the knowledge and
expertise of scientists from these disciplines makes it possible to develop more effective
phytoremediation strategies. For example, soil scientists can provide valuable information
on the physical and chemical properties of the soil, which can affect plant growth and
the uptake of contaminants. Environmental engineers can provide insight into the design
and implementation of phytoremediation systems, including selecting appropriate plants
and optimizing environmental conditions. Botanists and plant physiologists can provide
information on the uptake, translocation, and detoxification of contaminants by plants, and
microbiologists can give insight into the role of soil microorganisms in facilitating phytore-
mediation processes. Aquatic biologists would help finding suitable plants for removal
of specific contaminants and their efficacy in hydric and under water soils. Furthermore,
interdisciplinary research can help to identify the limitations and challenges associated
with phytoremediation and develop solutions to overcome these challenges. For instance,
molecular biology techniques can be used to develop genetically engineered plants to
increase their ability to accumulate and detoxify contaminants, while nanotechnology can
enhance the uptake and transport of contaminants by plants [6].
Phytoremediation is a promising method for the remediation of heavy metals from
polluted soil, but it still has some limitations and challenges that must be addressed:
• It is a slow process which may take several years to achieve significant results, espe-
cially in highly contaminated soils. The time required for remediation depends on
several factors, such as the type and concentration of contaminants, the plant species
used, soil properties, and environmental conditions.
• It can sometimes be less effective due to some hyperaccumulator plants’ slow growth
rates and lower levels of biomass production. These factors can limit the amounts of
heavy metals removed from contaminated soil within a given period. Additionally,
some plants may only accumulate specific types of heavy metals, which may not be
the most predominant contaminants in the soil. There may also be contaminants with
lower activation abilities or plants with lower absorption potential because of a few
firmly bound metal particles. Thus, there is a risk of only partial removal of pollutants
from the contaminated site in the absence of appropriate consideration.
Therefore, it is crucial to conduct field studies to validate the effectiveness of phy-
toremediation techniques in real-world conditions. Field studies can help to identify the
most effective plant species, planting densities, soil amendments, and other factors that can
maximize the removal of heavy metals from contaminated soils. Moreover, field studies can
also provide valuable information about the long-term sustainability and cost-effectiveness
of phytoremediation as a remediation technology [11,45,112]. Integrating scientific knowl-
edge from different fields is essential to advance phytoremediation technology further.
Additionally, more research is needed to assess the potential environmental impacts of
the byproducts and toxins produced during the phytoremediation process and ways to
enhance the growth of hyperaccumulating species in highly contaminated areas. The
exploration of commercial opportunities through market niches of green roof construction,
phytomining, and plant-based bioengineering projects also presents a potential avenue
for further development and application of phytoremediation technology [112]. By incor-
porating different advancements from various disciplines, inter-disciplinary cooperation
should be strengthened to speed up restoration, lower reclamation costs, and improve
restoration outcomes. The cleaning effectiveness of heavy-metal-contaminated substrates
should be improved through the optimization of rebuilding techniques, reduction in main-
tenance process duration, cost reduction, and avoidance of auxiliary impurities in the plant
recovery cycle.
Toxics 2023, 11, 422 19 of 24

10. Conclusions
Phytoremediation has excellent potential as a plant-mediated remediation technology.
However, its development and application have been limited by low remediation efficiency
and ineffective disposal methods available for contaminated biomass. While some research
has been conducted to improve phytoremediation efficiency, more investment is needed
to make it a practical and effective solution for large-scale remediation projects. This will
enable the technology to move from the lab to practical applications on a large scale. While
there are constraints, for example, long improvement times and reliance on the specific
environment and plant development, a considerable number of these restrictions can be
overcome by legitimate planning and appropriate species determination. However, more
research is needed to demonstrate the effectiveness of phytoremediation technology and
increase its application. Combining different remediation processes, such as phytoremedia-
tion and soil amendment, can also support the effective treatment of heavy metal pollution.
Additionally, genomic, proteomic, and metabolic studies can provide valuable information
on the mechanisms of plants’ heavy metal uptake, transport, and detoxification. This infor-
mation can be used to develop more effective phytoremediation strategies and overcome
existing limitations.
Furthermore, use of the existing microbial population can help expand the absorptive
capacity of roots by corroding common impurities and improving metal uptake. Genetically
engineered plants have the potential to enhance phytoremediation by increasing plant
growth rates and over-expressing genes that control metal uptake and transport. Phytore-
mediation is also more cost-effective than other remediation methods, with studies showing
5–13 times lower costs. Additionally, researchers can explore the secondary benefits of
phytoremediation, such as linking it to biomass production that can be used for bioenergy,
feedstock for pyrolysis and biofortified products, and carbon sequestration, which can
contribute to phytomanagement. Studying phytoremediation at molecular-genetic and
nano levels is also possible and promising.

Author Contributions: Writing—review and editing, A.K.P.; review and editing, M.M., S.S.A. and
M.K.; supervision, M.M.; funding acquisition, M.K. All authors have read and agreed to the published
version of the manuscript.
Funding: This research received no external funding.
Institutional Review Board Statement: Not applicable.
Informed Consent Statement: Not applicable.
Data Availability Statement: Data will be given upon request.
Acknowledgments: The authors express their gratitude to the Tamilnadu State Council for Science
and Technology, Management of the KPR Institute of Engineering and Technology, Coimbatore, and
ICAR-IISWC, Dehradun.
Conflicts of 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.

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