See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/340927345

Effect of Heavy Metals on Plant Growth: An Overview

Chapter · April 2020

DOI: 10.1007/978-3-030-41552-5_4

CITATIONS READS

71 2,249

8 authors, including:

Deepika Goyal Arti Yadav

15 PUBLICATIONS 205 CITATIONS

Dayalbagh Educational Institute
10 PUBLICATIONS 192 CITATIONS
SEE PROFILE
SEE PROFILE

Mrinalini Prasad Teg Bahadur Singh

Dayalbagh Educational Institute Dayalbagh Educational Institute
26 PUBLICATIONS 211 CITATIONS 9 PUBLICATIONS 193 CITATIONS

SEE PROFILE SEE PROFILE

All content following this page was uploaded by Sushma Mishra on 28 April 2022.

The user has requested enhancement of the downloaded file.

Effect of Heavy Metals on Plant Growth:
An Overview

Deepika Goyal, Arti Yadav, Mrinalini Prasad, Teg Bahadur Singh,

Preksha Shrivastav, Akbar Ali, Prem Kumar Dantu, and Sushma Mishra

Contents
1 Introduction 79
2 Source of Heavy Metals 80
2.1 Natural Sources of Heavy Metal Contamination 80
2.2 Anthropogenic Sources 81
3 Impacts of Heavy Metal Toxicity on Plants 82
3.1 Heavy Metals That Function As Micronutrients 82
3.2 Heavy Metals That Are Not Vital for Plant Growth 85
4 Plant Defense Mechanisms Adopted by Plants Against Heavy Metal Stress 87
4.1 Trichomes 88
4.2 Cell Wall and Root Exudates 89
4.3 Plasma Membrane 89
4.4 Vacuolar Compartmentalization 89
4.5 Mycorrhizae 90
4.6 Phytochelatins 90
4.7 Metallothioneins 90
5 Remediation of Heavy Metals 91
5.1 Cyanoremediation 91
5.2 Bioremediation 91
5.3 Mycoremediation 93
5.4 Phytoremediation 93
6 Future Perspective and Conclusions 94
References 95

1 Introduction

The term “heavy metal” refers to a metal or metalloid with atomic density at least
five times greater than that of water (Hawkes 1997; Tchounwou et al. 2012). The
common heavy metals found in environment include cadmium (Cd), lead (Pb),
nickel (Ni), silver (Ag), zinc (Zn), cobalt (Co), chromium (Cr), iron (Fe), arsenic
(As), and mercury (Hg). The presence of high concentration of heavy metals in
water, air, and soil poses a threat to all forms of life (Oliveira and Pampulha 2006).

D. Goyal · A. Yadav · M. Prasad · T. B. Singh · P. Shrivastav · A. Ali

P. K. Dantu · S. Mishra (*)
Department of Botany, Dayalbagh Educational Institute (Deemed University), Agra, India

© Springer Nature Switzerland AG 2020 79

M. Naeem et al. (eds.), Contaminants in Agriculture,
https://doi.org/10.1007/978-3-030-41552-5_4
80 D. Goyal et al.

This chapter, however, focuses on the effects of heavy metals on metabolism of

plants and their overall growth. An outline of the source of heavy metals, their tech-
niques of remediation, and various defense mechanisms present in heavy metal-­
tolerant plants, has also been discussed.

2 Source of Heavy Metals

Gathering of heavy metals in biosphere may take place by both natural and human
activities (Fig. 1). While, weathering of rocks is the chief natural source of heavy
metal contamination in environment, the anthropogenic sources include mining,
smelting operations, and agricultural activities (Herawati et al. 2000).

2.1 Natural Sources of Heavy Metal Contamination

2.1.1 Weathering of Rocks

Heavy metals derived from rock materials represent the “lithogenic” component.
The type of parent rock is the factor which determines the concentration and com-
position of heavy metals formed in soil. The principal heavy metal pollutants con-
tributed by parent rock include Co, Cr, Fe, Mn, Ni, and Zn. Weathering of igneous
rocks, such as Augite, Olivine, and Hornblende, gives rise to considerable amounts
of heavy elements, while sedimentary rocks contribute only a small fraction
(Nagajyoti et al. 2010).

Agricultural sources Industrial sources Domestic effluents

Inorganic & organic fertilizers Mining (Pb, Cr and Cu) Household pipes used for
(Cr, Cu, Zn and Pb) Transport of ores (Cr, Cu and Zn) supply of water (Zn, Cu and Cr)
Liming (Pb, Cu and Zn) Smelting of metals (Cr, Cu and Pb) sewage sludge (Zn, Pb and Cr)
Animal manure (Zn,Cu, Ni and Pb) Recycling of metals (Pb, Cr and Zn) Waste generated by household
Pesticides, Herbicides, Fungicides activities (Hg, Co and Cu)
(Cd, Pb and As)

Fig. 1 Natural and anthropogenic sources of heavy metals and their composition
Effect of Heavy Metals on Plant Growth: An Overview 81

2.1.2 Other Natural Sources

Apart from rocks, volcanoes, wind-blown dusts and storms, natural fires, sea sprays,
and aerosols (in coastal areas) are other natural sources of heavy metals (Seaward
and Richardson 1990). Geothermal sources, likewise volcanic eruptions, have raised
noteworthy atmospheric toxic wastes and contaminants (Eshleman et al. 1971).

2.2 Anthropogenic Sources

2.2.1 Agricultural Sources

The inorganic and organic fertilizers, manure, limes, pesticides, etc., used in agri-
culture contain variable amounts of Cr, Cd, Ni, Zn, Pb, and other heavy metals
(Nriagu 1989; Yanqun et al. 2005). Similarly, most of the commonly used chemical
pesticides like Bordeaux mixture and lead arsenate contain Cu, Hg, Mn, Pb, or Zn.
Apart from these, use of municipal and industrial wastewater for irrigation is also a
predominant source of heavy metals in soil.

2.2.2 Industrial Sources

Industrial processes like mining, smelting, and metal processing mainly generate Cr
and Ni, while Vanadium (V), Titanium (Ti), and Mn are mainly derived from oil and
coal-related activities (Guan et al. 2018). Coal mining also liberates significant lev-
els of As, Cd, and Fe, while gold mining increases the level of Hg in the environ-
ment (Lacerda 1997). The heavy metals are generally generated in particulate and
vapor forms, which, on combining with water present in the atmosphere, form aero-
sols. Aerosols may be either spread by wind (dry deposition) or precipitated in rain-
fall (wet deposition), and cause contamination of soil and water bodies (Nagajyoti
et al. 2010). Also, coal and petroleum combustion and nuclear power stations give
rise to heavy metals such as Se, Cd, B, Cu, Cs, Zn, and Ni to the atmosphere (Verkleji
1993). Processing of plastics, microelectronics, wood preservation, textiles and
paper processing also cause heavy metal toxicity to the environment (Tchounwou
et al. 2012).

2.2.3 Domestic Effluents

Domestic effluents constitute the major source of heavy metal contamination in

water bodies. Domestic effluents may include untreated wastewater substances and
passed through the filters in biological treatment plants and waste substances are
passed through sewage outfalls. Most of the widely used enzymatic detergents
82 D. Goyal et al.

contain trace amounts of elements like Fe, Cr, Mn, Zn, Co, Sr, and B, thereby
contributing toward heavy metal pollution (Angino et al. 1970).

3 Impacts of Heavy Metal Toxicity on Plants

While, in aquatic systems, complete plant body is accessible to heavy metals and
ions, terrestrial plants uptake heavy metals from the soil mainly through their roots.
The uptake process is facilitated by some transport proteins, chelating agents pro-
duced in the rhizosphere, and plant-induced pH changes (Tangahu et al. 2011).
Other means of entry of heavy metals are stomata, lenticels, wounds, etc. (Shahid
et al. 2017). Heavy metals are also absorbed directly through the leaves because of
particles accumulated on the foliar surfaces of leaves.
Heavy metals basically cause formation of reactive oxygen species (ROS) and
free radicals that lead to uncontrolled oxidation and radical chain reactions, ulti-
mately damaging the cellular biomolecules like nucleic acids, lipids, and proteins
(Phaniendra et al. 2015). Plants, being primary producers, form the base of ecologi-
cal pyramid; thus, the heavy metals entering the plant body make their way through
successive trophic levels of the food chain. This problem gets exacerbated for the
heavy metals that are bioaccumulative, that is, they are neither degraded in the envi-
ronment nor easily metabolized by plants. In fact, some of the heavy metal-tolerant
plant species like B. napus, B. Juncea have intrinsic ability to accumulate heavy
metals in their body, thereby, threatening the contamination of food webs (Gall et al.
2015; Mourato et al. 2015).

3.1 Heavy Metals That Function As Micronutrients

Some heavy metals, like Cu, Fe, Mn, Mo, and Zn, function as micronutrients; that
is, these are required in small quantities (less than 1 pound per acre) for important
physiological functions of plants (Misra and Mani 1991). The optimum concentra-
tion of these heavy metals and their role(s) in plant development have been men-
tioned in Table 1. Just as lack of these nutrients results in deficiency symptoms, their
elevated levels in soil also lead to toxicity effects, which have been described below.

3.1.1 Iron

Iron is an important constituent of several plant proteins and enzymes like leghemo-
globin, cytochromes, ferrodoxin, catalase, peroxidase, aconitase, and superoxide
dismutase (Marschner 1995). However, elevated levels of iron cause production of
ROS, that is, free radicals, which alter membrane permeability and damage mem-
brane structure (De Dorlodot et al. 2005).
Effect of Heavy Metals on Plant Growth: An Overview 83

Table 1 Range and functional roles of a few environmentally important heavy metals in plants
Land plants
Elements (μg/g dry wt) Roles in plants
Fe 140 Component of hemoglobin, myoglobin, and cytochromes
Cu 4.15 Required for photosynthesis, acts as cofactor of superoxide
dismutase, ascorbate oxidase
Zn 8–100 Main player of replication and transcription, cofactor of carbonic
anhydrase, alcohol dehydrogenase
Mn 15–100 Required for photosynthesis during splitting of water, cofactor of
malic dehydrogenase, oxalosuccinic dehydrogenase
Co 0.05–0.5 Found in the form of vitamin B12
Ni 1 Fixes nitrogen in legumes, main component of urease enzyme

3.1.2 Copper

Copper (Cu) is a vital co-factor for plastocyanin and cytochrome oxidase, which are
involved in key physiological processes of plants like photosynthesis and respira-
tion. However, just like other micronutrients, excessive amount of Cu has been
reported to adversely affect plant growth in Brassica juncea (Singh and Tewari
2003), Solanum melongena (Neelima and Reddy 2002), Alyssum montanum
(Ouzounidou 1994), among others. A conspicuous impact of copper toxicity is
thickening of root apices in Pinus seedlings, inhibition of production of root hair in
Betula papyrifera, and seedlings of Lonicera tatarica (Arduini et al. 1995; Patterson
and Olson 1983). Excessive Cu causes production of some new roots and thickening
of taproot in Citrus paradisi (Zhu and Alva 1993). Excessive Cu causes chlorosis in
Banksia ericifolia (heath banksia), Casuarina distyla (she-oak) and Eucalyptus exi-
mia (yellow bloodwood) (Mitchell et al. 1988).

3.1.3 Zinc

Like other micronutrients, zinc (Zn) is an essential micronutrient for many meta-
bolic processes of plants. However, beyond its optimum range (15–60 ppm), it
adversely affects roots, shoots, seed germination, and flowering responses in French
marigold (Choi et al. 1996). Elevated levels of Zn in soil cause decline in the level
of chlorophyll pigments leading to chlorosis in younger leaves. Zn toxicity pro-
motes senescence and causes reduction in plant biomass (Mirshekali et al. 2012).
Moreover, it also acts as genotoxic pollutant by causing structural and numerical
aberrations in chromosome of plants, thus affecting cell division (Sharma and
Talukdar 1987).
84 D. Goyal et al.

3.1.4 Manganese

Manganese (Mn) is an important micronutrient and cofactor of enzymes required in

photosynthesis. However, excess amount of this heavy metal causes reduction in
plant growth and visible symptoms like leaf bronzing and shortening of internodes
(Crawford et al. 1989). While Mn concentration in the range of 500 μM caused
reduced shoot growth in rice, soybean showed chlorosis at a concentration of
200 μM (Lidon and Teixeira 2000; Lavres et al. 2009).

3.1.5 Cobalt

Cobalt (Co) occurs naturally in earth’s crust in the form of erythrite [Co3(AsO4)2],
cobaltite [CoAsS] and smaltite [CoAs2] (Nagajyoti et al. 2010). The effects of Co
toxicity have been studied in various crops like barley, tomato, and oilseed rape,
where it has been found to inhibit biomass and shoot growth (Li et al. 2009).
Excess Co causes leaf distortion, giving an appearance of a structure like hook with
rudimentary leaflets. Exogenous application of Co to tomato leaves leads to great-
est accumulation of this heavy metal in roots and older leaves, while, lowest in
stem. The plant showed altered enzymatic activity of peroxidase, catalase, ribo-
nuclease, and acid phosphatase (Gopal et al. 2003). Co toxicity also causes
decreased transpiration rate and water potential, an effect that is not found in Cu or
Cr toxicity.

3.1.6 Nickel

Nickel (Ni) acts as a cofactor of urease, the enzyme which metabolizes urea into
ammonia (usable form of nitrogen) within plants. Deficiency of Ni causes accumu-
lation of toxic urea within the tissue and formation of necrotic legions on the leaf
tips (Bhalerao et al. 2015).This enzyme helps in nitrogen fixation in many plant
species. Ni also helps in disease tolerance (Sengar et al. 2008), but the mechanis-
mis not very clear. Deficiency of this mineral nutrient causes reduction in size of
leaflets with small rounded tips; this condition is called mouse-ear. At higher con-
centration (>50 μg/g dry weight), Ni acts as a phytotoxic metal and adversely
affects growth inmany plant species (Crooke 1956). Ni is reported to inhibit gas
exchange and photosynthesis in plants such as maize and sunflower (Lo and Chen
1994; Mishra et al. 1973). Seregin and Kozhevnikova (2006) reported effect of Ni
toxicity on wheat and found 1 mM NiSO4 solution causes decrease in the meso-
phyll thickness, reduction in size of vascular bundles, change in vessels diam-
eter etc.
Effect of Heavy Metals on Plant Growth: An Overview 85

3.2 Heavy Metals That Are Not Vital for Plant Growth

Other heavy metals like lead, arsenic, manganese, and cadmium are highly deleteri-
ous to plants. Table 2 shows a comparative toxicity effect of different heavy metals
on plants, which varies with different species.

3.2.1 Lead

Lead (Pb) is a widespread toxic element in the soil, ranging from about 400–800 mg/
kg in most soils, to up to 1000 mg/kg in soil in industrialized areas (Sharma and
Dubey 2005). At present, there is no report on the role of Pb in plant growth and
development. The problem of Pb toxicity is aggravated by the fact that it is hard to
degrade and is extremely persistent in both water and soil. In fact, according to
Saxena et al. (1999), Pb has been found to be present in the environment for
150–5000 years. Pb exposure causes inhibition of plant root growth and cell divi-
sion in root tips of Lemna minor (Eun et al. 2002). Pb toxicity causes reduction in
the root length and root dry mass in Pisum sativum, Triticum aestivum, Zea mays,
and Sedum alfredii (Samardakiewicz and Wozny 2005). Lead causes inhibition of
stem and root elongation, and leaf expansion in Allium species (Gruenhage and
Jager 1985), Hordeum vulgare (Juwarkar and Shende 1986), and Raphanus sativus.
In Zea mays, Pb accumulation interferes with microtubule organization and disrup-
tion in microtubules, resulting in altered cell division (Eun et al. 2002). It is found
through numerous studies that Pb leads to increased production of ROS in plant
cells, resulting in lipid peroxidation, membrane damage, and oxidative stress
(Reddy et al. 2005; Liu et al. 2010). Pb toxicity hinders photosynthesis by obstruct-
ing electron transport, inhibition of Calvin cycle, and stomatal closure. It also causes
reduced uptake of magnesium and iron (the constituents of chlorophyll), resulting
in inhibition of chlorophyll synthesis (Burzynski 1987), and increase in chlorophyl-
lase enzyme activity (Drazkiewicz 1994) and alterations in lipid composition of

Table 2 The range of metal toxicity in several plant species

Plant species Range of metal toxicity References
Hordeum Hg > Pb > Cu > Cd > Cr > Ni > Zn
vulgare
Lolium Cu > Ni > Mn > Pb > Cd > Zn > Al > Hg > Cr > Fe
perenne
Triticum Cu > Cr > Ni > Zn > Pb ≈ Cd > Al > Fe
aestivum
Vicia faba Cd > Ni > Zn ≈ Co
Zea mays Cu ≈ Tl > Ag > Cd > Hg > Co > Zn > Pb or Tl3+ > Cu2+ > Ivanov et al. (2003)
Ag+ > Hg2+ ≈ Cd2+ > Ni2+ > Zn2+ ≈ Pb2+ ≈ Co2+ > Sr2+
Phaseolus Hg2 ≈ Cr Parmar et al.
sp. (2002)
86 D. Goyal et al.

thylakoid membrane (Stefanov et al. 1995). It has also been reported that Pb alters
nitrate assimilation, shoot nitrate content, free amino acids, and growth in Brassica
pekinensis (Xiong et al. 2006).

3.2.2 Arsenic

Arsenate (Ar) is an analog of phosphate and a toxic metalloid. It is widely distrib-

uted in the environment due to various natural and anthropogenic activities such as
mining and fossil fuel combustion (Bhattacharyya et al. 2003). High concentration
of As causes detrimental effects on plant growth by causing cell necrosis, chlorosis,
and electrolyte leakage from cell membranes (Singh et al. 2006). The toxicity of As
also leads to formation of ROS that can damage nucleic acids, proteins, and cause
peroxidation of lipids present in membrane (Moller et al. 2007). Chinese brake fern
(Pteris vitatta) was found to be the first hyperaccumulator of this heavy metal, and
today, this species is currently being used as a potent As tolerant and the potential
of tolerance is up to 1500 ppm in soil (Shen et al. 2014).

3.2.3 Mercury

Mercury (Hg) is found to occur in different forms like metallic mercury (HgS and
methyl-Hg), inorganic mercury, and organic mercury (Hg2+). Excessive level of
Hg2+ is toxic to plant cells and induces evident injuries and physiological disorders
in plants (Zhou et al. 2007). Hg2+ affects mitochondria, leaf stomata, binds to water
channel proteins, and acts as a barrier of water flow in plants (Zhang and Tyerman
1999; Messer et al. 2005). Photosynthesis, transpiration rate, and water uptake and
chlorophyll synthesis are also adversely affected by exposure to mercury. Hg is
found to cause loss of magnesium, manganese, potassium, and accumulation of iron
(Boening 2000). Hg affects the antioxidant defense system, by causing interference
with the nonenzymatic antioxidants like glutathione, thiols, and enzymatic antioxi-
dants like ascorbate peroxidase, superoxide dismutase, and glutathione reductase
(Israr et al. 2006). Other harmful effects of Hg include interference with the trans-
port of vital micronutrients, inactivation or denaturation of proteins, and disruption
of cell organelles and cell membranes.

3.2.4 Cadmium

Cadmium (Cd), like Hg, Co, Pb, and As, is a nonessential element for plants. The
impacts of Cd toxicity can be seen on the activity of enzymes involved in photosyn-
thesis and nitrogen metabolism (Alcántara et al. 1994; Mathys 1975). Cd also
adversely affects stomatal opening, mineral uptake, and water balance in plants. Cd
accumulation reduces ATPase activity of plasma membrane and alters membrane
Effect of Heavy Metals on Plant Growth: An Overview 87

permeability and metal ion homeostasis (Fodor et al. 1995). High Cd levels have
been reported to reduce the level of osmoprotectants, mainly proline, and alter the
genetic stability in Solanum nigrum (Al Khateeb and Al-Qwasemeh 2014).

4  lant Defense Mechanisms Adopted by Plants Against

P
Heavy Metal Stress

As mentioned earlier, heavy metals interact with biomolecules likewise nuclear pro-
teins and DNA and cause production of ROS. This causes morphological, meta-
bolic, and physiological abnormalities in plants (Manara 2012). Hence, plants have
evolved some defense mechanisms for heavy metal tolerance (Table 3). These
include two broad strategies: either to avoid, or tolerate heavy metal toxicity
(Fig. 2). Physical barriers like thick cuticle, trichomes, cell wall, plasma membrane,
and mycorrhiza constitute the first line of protection in plants to counteract heavy
metals (Hall 2002; Wong et al. 2004; Harada et al. 2010). If, however, the heavy
metals manage to cross these biophysical barriers, plants synthesize and secrete
certain chemicals to mitigate the harmful effects of heavy metals. These chemicals
include metallochaperones or chelators like nicotianamine, spermine, putrescine,
mugineic acids, organic acids, phytochelatins, glutathione, etc., and metallothio-
neins or cellular exudates such as phenolic compounds and flavonoids, protons, heat
shock proteins, some amino acids (proline and histidine), and hormones (jasmonic
acid, salicylic acid, and ethylene) (Viehweger 2014; Dalvi and Bhalerao 2013;
Sharma and Dietz 2006).

Table 3 Potential plant defense mechanisms involved in the detoxification of heavy metals
Mechanism of heavy metal tolerance Metal References
Trichomes Zn, Cu, Cd, Ni Emamverdian et al. (2015)
Mycorrhizas Zn, Cu, Cd Jentschke and Godbold (2000)
Cell wall, exudates Ni, Al Ma et al. (1997)
Plasma membrane
Reduced uptake Arsenate, Ni Meharg and Macnair (1992)
Active efflux Zn
Phytochelatins Cd Cobbett (2000)
Metallothioneins Cu Murphy and Taiz (1995)
Organic acids, amino acids Cd, Al, Cu, Ni, Al Rauser (1999)
Heat shock proteins Cd Neumann et al. (1994)
Vacuolar compartmentation Zn
88 D. Goyal et al.

5 4 2 1
3 Ectomycorrhiza
Trichomes

8
CAT ABC Transporters
ROS

SOD GSH CDF Transporters

6 PC 7
HMA Transporters
MC 9

MT NRAMP Transporters

HSP
CaCa Transporter

Cytosol Vacuole

Cell wall

Fig. 2 Detoxification strategies of heavy metals. (1) Restriction of metal translocation to roots by
ectomycorrhiza. (2) Deposition of heavy metals into trichomes. (3) Metal ion binding to cell wall
and root exudates. (4) Restriction of metal ions movement to cytosol. (5) Effluxing of metal ions
by the cell membrane to apoplast region. (6) Metal chelation in the cytosol by phytochelatins,
metallothioneins, and heat shock proteins. (7) Induction of oxidative stress and defense mecha-
nisms. (8) Transport of metal ions in cytosol by various transporters. (8) Sequestration of metal
ions into vacuole. heavy metals, MC metal chelating protein, MT metallothionein, HSP heat
shock protein, SOD superoxide dismutase, CAT catalase, ROS reactive oxygen species, GSH glu-
tathiones, PC plastocyanin

4.1 Trichomes

Trichomes, the hair-like structures on plant surface, which are commonly associated
with their role in protecting the plants against herbivorous insects, also function in
heavy metal tolerance. Trichomes either serve as a depository site for heavy metals
or secrete various secondary metabolites that lead to detoxification of toxic heavy
metals (Emamverdian et al. 2015). The first mechanism of heavy metal tolerance
has been reported for trichomes of Alyssum lesbiacum, which store significant
amount of Ni (Krämer et al. 1997); and trichomes of Arabidopsis halleri that store
higher concentrations of Zn (Sarret et al. 2002). The trichome number was found to
increase in tobacco seedlings treated with Cd (Choi et al. 2001).
Effect of Heavy Metals on Plant Growth: An Overview 89

4.2 Cell Wall and Root Exudates

The role of cell wall in defense response has not been very well documented.
Bringezu et al. reported that Silene vulgaris, a heavy metal-tolerant plant, accumu-
lated toxic heavy metals in epidermal cell walls, either bound to a protein or as sili-
cates (Bringezu et al. 1999). Root exudates act as metal chelators, which enhance
the uptake of certain metals from soil. For instance, Ni-chelating exudates from roots
were found to chelate histidine, while citrate accumulated in the roots of tolerant
plant Thalspi sp. helped to reduce Ni uptake, thus playing a role in Ni-detoxification
strategy (Hall 2002). Roots of Fagopyrum esculentum (Buckwheat) secrete oxalic
acid under conditions of Al stress, and accumulate nontoxic Al-oxalate in the leaves
and detoxify Al both externally and internally (Ma et al. 1997).

4.3 Plasma Membrane

As mentioned above in the previous sections, heavy metals alter plasma membrane
permeability, causing increased ion leakage from cells and hence disrupting ion
homeostasis. For example, high levels of Cu and Cd have been reported to cause
increased potassium efflux from roots by altering the H+ ATPase pump and chang-
ing the lipid composition (Wainwright and Woolhouse 1977; Ros et al. 1990; Fodor
et al. 1995; Demidchik et al. 1997). Therefore, to overcome this, some heavy metal-­
tolerant plants modify their plasma membrane to reduce heavy metal uptake and
facilitate more efflux of crucial ions like potassium. Holcus lanatus shows arsenic
tolerance by suppressing high-affinity arsenate transport system and synthesizing
phytochelatins and oligomers of gluthathiones (Meharg and Macnair 1992). In
tobacco, plasma membrane transporters bind calmodulin and extend Ni tolerance
and Pb2+ hypersensitivity (Arazi et al. 1999). In Arabidopsis thaliana, cadmium
metal ions are effluxed from the plasma membrane by ABC transporters (Kim
et al. 2007).

4.4 Vacuolar Compartmentalization

Apart from efflux of ions through plasma membrane (discussed above), sequestra-
tion into vacuole is another protective mechanism adopted by plants to reduce the
levels of toxic metals in cytosol (Ernst et al. 1992). Meristematic cells of Festuca
rubra and Hordeum vulgare store zinc in vacuole and help in the detoxification of
heavy metals (Davies et al. 1991; Brune et al. 1994). Vesicles from the roots of
Zn-tolerant and -sensitive plant of Silene vulgaris were isolated, and Zn transport
was found to be 2.5 times higher in vesicles of the tolerant lines in comparison to
the sensitive ones, suggesting the role of tonoplast in zinc tolerance.
90 D. Goyal et al.

4.5 Mycorrhizae

Mycorrhizae, particularly ectomycorrhizae, are found to be effective in mitigating

the impacts of metal toxicity on host plant (Marschner 1995; Huttermann et al.
1999; Jentschke and Godbold 2000). Mycorrhizae have been reported to protect
plants against heavy metal stress by a number of mechanisms, such as depositing
heavy metals within cortical cells (Turnau 1998), chemical binding to cell wall or
mycelium, sequestration into vacuole or other storage organelles (Hall 2002), and
alteration in the pH of soil, resulting in immobilization of metals (Bano and Ashfaq
2013). Glomus mosseae, an arbuscular mycorrhiza of maize, binds some heavy met-
als like Zn, Cu, and Pb, and lowers its uptake by plants (Huang et al. 2005). In a
study, inoculation of Glomus etunicatum in Lactuca sativa has been reported to
increase the sequestration of zinc as compared to noninoculated plants (Farshian
et al. 2007).

4.6 Phytochelatins

Phytochelatins (PCs) are short-chain sulfur-rich repetitions of peptides synthesized

by the enzyme phytochelatin synthase (PCS). These metal binding proteins are syn-
thesized nontranslationally from reduced glutathione. PCs are reported to occur in
plants, microbes, animals, yeasts, and maintain metals homeostasis (Silva 2012;
Bian et al. 2013). PCs are used as biomarkers for the initial detection of heavy metal
toxicity in plants. PCs are found to be transported from roots to shoots, and this
translocation is mediated by phloem sap and xylem in Brassica napus (Yadav 2010).
A high concentration of Cu and As stimulated synthesis of PCs in Solanum nigrum
and Oryza sativa, which resulted in the immobilization of these metals by complex
formation (Fidalgo et al. 2013; Lemos Batista et al. 2014). It is reported that when
PCs genes are transferred in Arabidopsis thaliana, it shows an enhanced tolerance
to Cd and As (Guo et al. 2012).

4.7 Metallothioneins

Metallothioneins (MTs) are cysteine-rich, cytoplasmic metal-binding and low

molecular weight proteins found in both prokaryotes and eukaryotes. These pro-
teins are classified into four classes according to the arrangement of cysteine resi-
dues. In soybean, MT1, MT2, and MT3 detoxify Cd and MT4 detoxifies Zn (Pagani
et al. 2012). In plants, MT nullifies heavy metals toxicity through homeostasis of
intracellular metal ions, cellular sequestration, and metal transport adjustment
(Prasad 2004; Kohler et al. 2004).
Effect of Heavy Metals on Plant Growth: An Overview 91

5 Remediation of Heavy Metals

Heavy metal toxicity imposed on plants is the most challenging problem in most
countries. Removal of heavy metals from a contaminated site is known as remedia-
tion (Khan et al. 2000). Some of the conventional methods for remediation include
dredging (physical removal of the contaminated sediment layers), capping (cover-
ing the contaminated sediment surface with clean material, thus isolating the sedi-
ments), and incineration (waste treatment technology that involves the combustion
of organic substances contained in waste materials) (Azubuike et al. 2016).
Bioremediation, that is, the use of living organisms (mainly microbes) for the
removal of pollutants from contaminated site, has gained immense popularity in
recent years (Table 4). Some microbes are unique in producing enzymes that
degrade organic contaminants into nontoxic compounds. The remediation tech-
niques of heavy metals could be classified into four major types depending upon
the type of microorganism used: cyanoremediation, bioremediation, mycoremedi-
ation, and phytoremediation; these remediation strategies have been dis-
cussed below.

5.1 Cyanoremediation

Cyanoremediation is the use of algae for the removal of organic and inorganic pol-
lutants from the contaminated site. Some algae such as Chlorella, Spirulina,
Spirogyra, Oedogonium have been used for phycoremediation purposes. Deng et al.
(2007) reported the use of Cladophora fascicularis as an effective material, which
absorbs Pb (II). In another study, observed the biosorption capacity of Cladophora
and Spirogyra, for copper (Cu2+) and lead (Pb2+), respectively. In recent years, the
focus on algae for remediation has increased due to their wide occurrence, central
role in carbon dioxide fixation, and potential source of biofuel (Chekroun et al. 2013).

5.2 Bioremediation

In bioremediation, living organisms are used to degrade environmental contami-

nants into less toxic forms (Vidali 2001). In bioremediation, microbes enzymati-
cally attack the pollutants and convert them to harmless products. Some of the
widely used microorganisms in bioremediation are Pseudomonas putida,
Dechloromonas aromatica, Deinococcus radiodurans, Methylibium petroleiphilum,
and Alcanivorax borkumensis (Mani and Kumar 2014). Apart from being a cost-­
effective process, bioremediation involves minimal site disruption, and the possibil-
ity of simultaneous treatments. Although this approach is commonly used, it does
have some drawbacks. Bacteria are not capable of working on a broad category of
92 D. Goyal et al.

Table 4 Some of the widely used heavy metal remediation techniques using living organisms
Living
organism Species Metals References
Plants Pteris vittata Cu, Ni, Zn, As Ma et al. (2001)
Brassica juncea Se, Cd Banuelos et al. (2005)
Helianthus annuus Cd Mani and Kumar (2014)
Populus sp. Hg Lyyra et al. (2007)
Brassica napus Cd Selvam and Wong (2008)
Typha latifolia Pb Tiwari et al. (2008)
Nelumbo nucifera Zn, Cu, Pb, Ni Kumar et al. (2008)
Amaranthus viridis Cr Liu et al. (2008)
Helianthus annuus Cu, Zn, Pb, Hg, As, Mani et al. (2012)
Cd, Ni
Trifoliumpretense Cd Wu et al. (2009)
Spinacea oleracea Pb, Zn Mani et al. (2012)
Vetiveriazizanioides Cd, Pb Danh et al. (2009)
Nicotiana tabacum Cd Wojas et al. (2009)
Brassica juncea Pb Zarei et al. (2010)
Pistia stratiotes Cd, Pb, Zn Veselý et al. (2012)
Populustremula Zn, Cd, Cu Ruiz et al. (2011)
Gmelina arborea Al Dudhane et al. (2012)
Bacteria Pseudomonas veronii Cd, Zn, Cu Vullo et al. (2008)
Burkholderia species Cd, Pb Jiang et al. (2008)
Bacillus sp. Cd, Pb, Cu Guo et al. (2010)
Kocuria flava Cu Achal et al. (2011)
Serratia marcescens U Kumar et al. (2011)
Pseudomonas U Choudhary and Sar (2011)
aeruginosa
Bacillus cereus Cd, Zn Hrynkiewicz and Baum
(2012)
Halomonas sp. Sr Achal et al. (2012a)
Sporosarcinaginsengisoli As Achal et al. (2012b)
Fungi Penicillium canescens Cr Say et al. (2003)
Ganoderma lucidum Ar Loukidou et al. (2003)
Aspergillus fumigates Pb Ramasamy et al. (2011)
Lichen Cladoniarangiformis Pb Ekmekyapar et al. (2012)
Algae Chlorella pyrendoidosa U Singhal et al. (2004)
Chlorella fusca Pb, Zn, Cd, Cr, Cu, Ni Ahluwalia and Goyal
(2007)
Spirogyra sp. Pb, Cu Lee and Chang (2011)
Spirullinasp. Cr, Cu, Fe, Mn, Se, Zn Mane and Bhosle (2012)
Hydrodictylonsp. V, As Saunders et al. (2012)
Oedogoniumsp. V, As Saunders et al. (2012)
Effect of Heavy Metals on Plant Growth: An Overview 93

organic compounds; some are not capable of degrading contaminants such as

­chlorinated organic or high aromatic hydrocarbons.

5.3 Mycoremediation

Besides the use of bacteria, fungal species such as Aspergillus niger, Aureobasidium
pullulans, Ganoderma lucidum, and Cladosporium resinae are found to be capable
of mycoremediation (Mani and Kumar 2014). Fungi secrete more potent enzymes
even in nutrient-deficient conditions, which act on a broad category of natural
chemicals. Remediation through fungus may proceed faster than bacterial degrada-
tion because of their large filament surface area (Gadd 2010). Some fungal species
are reported to metabolize hydrocarbons and hence, used in mycoremediation of
oil-polluted regions. These are many fungi being used for mycoremediation purpose
such as Acremonium, Aspergillus, Aureobasidium, Candida, Cephalosporium,
Cladosporium, Cunninghamella, Fusarium, Geotrichum, Gliocladium, Graphium,
Hansenula, and Mortierella. Some fungi, such as Trichoderma, act as biocontrol
agents as well as remediate agricultural waste. Lentinus edodes, the gourmet mush-
room, has the potential of remediating more than 60% of pentachlorophenol from
soil (Pletsch et al. 1999). Such a potent fungus is being used as a boon in oil indus-
tries and refineries. Phanerochaete chrysosporium and other white rot fungi degrade
some xenobiotics like DDT and lindane (Kirk et al. 1992). Mycoremediation is a
very efficient method of remediation that produces fewer toxic chemicals as by-
products (Gadd 2009).

5.4 Phytoremediation

Phytoremediation is the application of plants and their associated microflora to

clean up environment in a cost-effective and noninvasive manner. This could be
brought about by a number of mechanisms like phytoextraction, phytostabilization,
phytoevaporation, and rhizodegradation.
Phytoextraction, also known as phytoabsorption, is a remediation process by
which heavy metals and other contaminated soil pollutants are absorbed by plant
roots and transported to shoots, forming the harvestable plant biomass. Till date,
more than 400 hyperaccumulator plants, mainly belonging to Poaceae, Brassicaceae,
Asteraceae, Caryophyllaceae, Lamiaceae, Fabaceae, Violaceae, and Euphorbiaceae,
have been reported. Our understanding of hyperaccumulation of heavy metals has
increased due to recent researches up to molecular level. Heavy metal storing plants
are characterized by greater abundance of roots in comparison to shoot biomass,
faster transpiration rate, and slow growth as compared to that of excluders.
Phytostabilization, also known as phytodeposition, phytosequestration, and phy-
toaccumulation, refers to the decrease in the availability and mobility of heavy
94 D. Goyal et al.

metals from soil. The mobility of contaminants is lowered by absorption and accu-
mulation into plant roots or immobilization within the rhizosphere, thereby reduc-
ing off-site contamination. The main aim is to prevent the migration of contaminants
by wind and water erosion and leaching. Phytostabilization can be enhanced by
using soil amendments like phosphates, organic matter and alkalizing agents etc.
that decrease solubility of metals in soil and minimize its leaching to groundwater.
Some plant species like Agrostis sp. and Festuca sp. are the most common species
used in the phytostabilization of Zn, Cu, and Pb. Willows (Salix sp.) facilitate both
phytostabilization and phytoextraction.
Phytoevaporation is another method of phytoremediation by which plants take
up heavy metals like Se and Hg from soil and convert them into volatile form,
thereby releasing it into the atmosphere. Species of the Brassicaceae family like
Brassica juncea can remediate up to 40 g Se/ha.
Rhizodegradation is the degradation of heavy metals by soil microflora, where
the enzymatic activity of soil microbes is enhanced by plant root exudates. Carex
pendula accumulates Pb in the roots under in situ conditions.

6 Future Perspective and Conclusions

Heavy metal-contamination of agricultural land is one of the abiotic stresses that

limit crop productivity. Genetic engineering and the recent genome editing
approaches have been used to confer heavy metal resistance in plants (Mishra 2019;
Sedeek et al. 2019). One of the strategies of tackling heavy metal toxicity in plants
is to target the initial step of uptake of heavy metals by plants. Research on mem-
brane proteins like ion channels and pumps should be promoted to understand the
molecular mechanism involved in the transport of heavy metals across cell mem-
branes and within the cells. Heavy metal accumulators, such as B. napus and B. jun-
cea, are widely used for phytoremediation due to their large biomass. A crucial, yet
often neglected, aspect of phytoremediation involves recovery or disposal of heavy
metals (accumulated in plants) in such a manner that the plant biomass can be prop-
erly handled and the associated environmental risks could be reduced. Further,
investigations should be focused on rhizosphere and soil microbial diversity, which
affect heavy metal solubility. Work could also be directed toward endophytes (non-
pathogenic microbes inside the plant organs) that provide resistance against heavy
metals. The role of government and environment protection agencies is imperative
in initiating awareness among people and formulating stringent laws in order to
check the anthropogenic production of these heavy metals. The knowledge about
harmful impacts of heavy metals on plant growth is very important not only for
improved plant growth and yield, but also to achieve pollution-free environment and
ecological harmony.

Acknowledgments The authors would like to thank Director, DEI, for his continuous support and
encouragement. SM is grateful to Dayalbagh Educational Institute, Deemed University, Agra, for
Effect of Heavy Metals on Plant Growth: An Overview 95

sanctioning the Research Project, DEI/Minor Project/2017-18 (iv), as a startup grant. DG is thank-
ful to DST-INSPIRE for providing fellowship.
The authors declare no conflict of interest.

References

Achal V, Pan X, Zhang D (2011) Remediation of copper-contaminated soil by Kocuriaflava CR1,

based on microbially induced calcite precipitation. Ecol Eng 37(10):1601–1605
Achal V, Pan X, Zhang D (2012a) Bioremediation of strontium (Sr) contaminated aquifer quartz
sand based on carbonate precipitation induced by Sr resistant Halomonas sp. Chemosphere
89(6):764–768
Achal V, Pan X, Fu Q, Zhang D (2012b) Biomineralization based remediation of As (III) contami-
nated soil by Sporosarcina ginsengisoli. J Hazard Mater 201:178–184
Ahluwalia SS, Goyal D (2007) Microbial and plant derived biomass for removal of heavy metals
from wastewater. Bioresour Technol 98(12):2243–2257
Al Khateeb W, Al-Qwasemeh H (2014) Cadmium, copper and zinc toxicity effects on growth,
proline content and genetic stability of Solanum nigrum L., a crop wild relative for tomato;
comparative study. Physiol Mol Biol Plants 20:31–39
Alcántara E, Romera FJ, Cañete M, De la Guardia MD (1994) Effects of heavy metals on both
induction and function of root Fe (lll) reductase in Fe-deficient cucumber (Cucumissativus L.)
plants. J Exp Bot 45(12):1893–1898
Angino EE, Magnuson LM, Waugh TC, Galle OK, Bredfeldt J (1970) Arsenic in detergents-­
possible danger and pollution hazard. Science 168:389–392
Arazi T, Sunkar R, Kaplan B, Fromm H (1999) A tobacco plasma membrane calmodulin-­binding
transporter confers Ni2+ tolerance and Pb2+ hypersensitivity in transgenic plants. Plant J
20:171–182
Arduini I, Godbold DL, Onnis A (1995) Influence of copper on root growth and morphology of
Pinus pinea L. and Pinus pinasterAit. seedlings. Tree Physiol 15:411–415
Azubuike CC, Chikere CB, Okpokwasili GC (2016) Bioremediation techniques–classifica-
tion based on site of application: principles, advantages, limitations and prospects. World J
Microbiol Biotechnol 32(11):180
Bano SA, Ashfaq D (2013) Role of mycorrhiza to reduce heavy metal stress. Nat Sci 5:16–20
Banuelos G, Terry N, LeDuc DL, Pilon SEA, Mackey B (2005) Field trial of transgenic Indian
mustard plants shows enhanced phytoremediation of selenium-contaminated sediment. Environ
Sci Technol 39(6):1771–1777
Bhalerao SA, Sharma AS, Poojari AC (2015) Toxicity of nickel in plants. Int J Pure and Appl
Biosci 3(2):345–355
Bhattacharyya R, Chatterjee D, Nath B, Jana J, Jacks G, Vahter M (2003) High arsenic ground-
water: mobilization, metabolism and mitigation − an overview in the Bengal Delta Plain. Mol
Cell Biochem 253:347–355
Bian M, Zho M, Sun D, Li C (2013) Molecular approaches unravel the mechanism of acid soil
tolerance in plants. Crop J 1(2):91–104
Boening DW (2000) Ecological effects, transport, and fate of mercury: a general review.
Chemosphere 40:1335–1351
Bringezu K, Lichtenberger O, Leopold I, Neumann D (1999) Heavy metal tolerance of Silene
vulgaris. J Plant Physiol 154:536–546
Brune A, Urbach W, Dietz KJ (1994) Compartmentation and transport of zinc in barley primary
leaves as basic mechanisms involved in zinc tolerance. Plant Cell Environ 17(2):153–162
Burzynski M (1987) The uptake and transpiration of water and the accumulation of lead by plants
growing on lead chloride solutions. Acta Soc Bot Pol 56:271–280
96 D. Goyal et al.

Chekroun KB, Baghour M (2013) The role of algae in phytoremediation of heavy metals: a review.
J Mater Environ Sci 4(6):873–880
Choi JM, Pak CH, Lee CW (1996) Micronutrient toxicity in French marigold. J Plant Nutr
19:901–916
Choi YE, Harada E, Wada M, Tsuboi H, Morita Y, Kusano T, Sano H (2001) Detoxification of
cadmium in tobacco plants: formation and active excretion of crystals containing cadmium and
calcium through trichomes. Planta 213(1):45–50
Choudhary S, Sar P (2011) Uranium biomineralization by a metal resistant Pseudomonas aerugi-
nosa strain isolated from contaminated mine waste. J Hazard Mater 186(1):336–343
Cobbett CS (2000) Phytochelatins and their roles in heavy metal detoxification. Plant Physiol
123(3):825–832
Crawford TW, Stroehlein JL, Kuehl RO (1989) Manganese and rates of growth and mineral accu-
mulation in cucumber. J Am Soc Hort Sci 114:300–306
Crooke WM (1956) Effect of soil reaction on uptake of nickel from a serpentine soil. Soil Sci
81(4):269–276
Dalvi A, Bhalerao SA (2013) Response of plants towards heavy metal toxicity: an overview of
avoidance, tolerance and uptake mechanism. Ann Plant Sci 2:362–368
Danh LT, Truong P, Mammucari R, Tran T, Foster N (2009) Vetiver grass, Vetiveria zizanioides: a
choice plant for phytoremediation of heavy metals and organic wastes. Int J Phytoremediation
11(8):664–691
Davies KL, Davies MS, Francis D (1991) Zinc-induced vacuolation in root meristematic cells of
Festuca rubra L. Plant Cell Environ 14:399–406
De Dorlodot S, Lutts S, Bertin P (2005) Effects of ferrous iron toxicity on the growth and mineral
composition of an inter specific rice. J Plant Nutr 28:1–20
Demidchik V, Sokolik A, Yurin V (1997) The effect of Cu2+on ion transport systems of the plant
cell plasmalemma. Plant Physiol 114:1313–1325
Deng L, Su Y, Su H, Wang X, Zhu X (2007) Sorption and desorption of lead (II) from wastewater
by green algae Cladophora fascicularis. J Hazard Mater 143(1–2):220–225
Drazkiewicz M (1994) Chlorophyll occurrence, functions, mechanism of action, effects of internal
and external factors. Photosynthetica 30:321–331
Dudhane M, Borde M, Jite PK (2012) Effect of aluminium toxicity on growth responses and anti-
oxidant activities in Gmelina arborea Roxb. inoculated with AM fungi. Int J Phytoremediation
14(7):643–655
Ekmekyapar F, Aslan A, Bayhan YK, Cakici A (2012) Biosorption of Pb (II) by nonliving lichen
biomass of Cladoniarangi formis Hoffm. Int J Environ Res 6(2):417–424
Emamverdian A, Ding Y, Mokhberdoran F, Xie Y (2015) Heavy metal stress and some mechanisms
of plant defense response. Sci World J 2015:756120. https://doi.org/10.1155/2015/756120
Ernst WHO, Verkleij JAC, Schat H (1992) Metal tolerance in plants. Acta Bot Neerl 41:229–248
Eshleman A, Siegel SM, Siegel BZ (1971) Is mercury from Hawaiian volcanoes a natural source
of pollution? Nature 223:471–475
Eun SO, Youn HS, Lee Y (2002) Lead disturbs microtubule organization in the root meristem of
Zea mays. Physiol Plant 110:357–365
Farshian S, Khara J, Malekzadeh P (2007) Influence of arbuscular mycorrhizal fungus (Glomus
etunicatum) with lettuce plants under zinc toxicity in nutrient solution. Pak J Biol Sci
10:2363–2367
Fidalgo F, Azenha M, Silva AF, de Sousa A, Santiago A, Ferraz P, Teixeira J (2013) Copper-­
induced stress in Solanum nigrum L. and antioxidant defense system responses. Food Energy
Secur 2(1):70–80
Fodor E, Szabo NA, Erdei L (1995) The effects of cadmium on the fluidity and H+-ATPase activity
of plasma membrane from sunflower and wheat roots. J Plant Physiol 147:87–92
Gadd G (2009) Heavy metal pollutants: environmental and biotechnological aspects. In:
Encyclopedia of microbiology Elsevier, pp 321–324
Gadd GM (2010) Metals, minerals and microbes: geomicrobiology and bioremediation.
Microbiology 156(3):609–643
Effect of Heavy Metals on Plant Growth: An Overview 97

Gall JE, Boyd RS, Rajakaruna N (2015) Transfer of heavy metals through terrestrial food webs: a
review. Environ Monit Assess 187(4):201
Gopal R, Dube BK, Sinha P, Chatterjee C (2003) Cobalt toxicity effects on growth and metabolism
of tomato. Commun Soil Sci Plant Anal 34:619–628
Gruenhage L, Jager IIJ (1985) Effect of heavy metals on growth and heavy metals content of
Allium Porrum and Pisum sativum. Angew Bot 59:11–28
Guan Q, Wang F, Xu C, Pan N, Lin J, Zhao R, Luo H (2018) Source apportionment of heavy
metals in agricultural soil based on PMF: a case study in Hexi Corridor, northwest China.
Chemosphere 193:189–197
Guo H, Luo S, Chen L, Xiao X, Xi Q, Wei W, He Y (2010) Bioremediation of heavy metals
by growing hyperaccumulaor endophytic bacterium Bacillus sp. L14. Bioresour Technol
101(22):8599–8605
Guo J, Xu W, Ma M (2012) The assembly of metals chelation by thiols and vacuolar compart-
mentalization conferred increased tolerance to and accumulation of cadmium and arsenic in
transgenic Arabidopsis thaliana. J Hazard Mater 199:309–313
Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp
Bot 53:1–11
Harada E, Kim JA, Meyer AJ, Hell R, Clemens S, Choi YE (2010) Expression profiling of tobacco
leaf trichomes identifies genes for biotic and abiotic stresses. Plant Cell Physiol 51:1627–1637
Hawkes JS (1997) Heavy metals. J Chem Educ 74:1369–1374
Herawati N, Suzuki S, Hayashi K, Rivai IF, Koyoma H (2000) Cadmium, copper and zinc levels
in rice and soil of Japan, Indonesia and China by soil type. Bull Environ Contam Toxicol
64:33–39
Hrynkiewicz K, Baum C (2012) The potential of rhizosphere microorganisms to promote the plant
growth in disturbed soils. In: Environmental protection strategies for sustainable development.
Springer, Dordrecht, pp 35–64
Huang Y, Tao S, Chen YJ (2005) The role of arbuscular mycorrhiza on change of heavy metal
speciation in rhizosphere of maize in wastewater irrigated agriculture soil. J Environ Sci
17:276–280
Huttermann A, Arduini I, Godbold DL (1999) Metal pollution and forest decline. In: Prasad NMV,
Hagemeyer J (eds) Heavy metal stress in plants: from molecules to ecosystems. Springer-­
Verlag, Berlin, pp 253–272
Israr M, Sahi S, Datta R, Sarkar D (2006) Bioaccumulation and physiological effects of mercury
in Sesbania drummonii. Chemosphere 65:591–598
Ivanov VB, Bystrova EI, Seregin IV (2003) Comparative impacts of heavy metals on root growth
as related to their specificity and selectivity. Russian J Plant Physiol 50(3):398–406
Jentschke G, Godbold DL (2000) Metal toxicity and ectomycorrhizas. Physiol Plant 109:107–116
Jiang CY, Sheng XF, Qian M, Wang QY (2008) Isolation and characterization of a heavy metal-­
resistant Burkholderia sp. from heavy metal-contaminated paddy field soil and its potential in
promoting plant growth and heavy metal accumulation in metal-polluted soil. Chemosphere
72(2):157–164
Juwarkar AS, Shende GB (1986) Interaction of Cd-Pb effect on growth yield and content of Cd, Pb
in barley. Ind J Environ Health 28:235–243
Khan AG, Kuek C, Chaudhry TM, Khoo CS, Hayes WJ (2000) Role of plants, mycorrhizae and
phytochelators in heavy metal contaminated land remediation. Chemosphere 41(1–2):197–207
Kim DY, Bovet L, Maeshima M, Martinoia E, Lee Y (2007) The ABC transporter AtPDR8 is a
cadmium extrusion pump conferring heavy metal resistance. Plant J 50:207–218
Kirk TK, Lamar RT, Glaser JA (1992) The potential of white-rot fungi in bioremediation. In
Biotechnology and Environmental Science. Springer, Boston MA, pp 131–138
Kohler A, Blaudez D, Chalot M, Martin F (2004) Cloning and expression of multiple metallothio-
neins from hybrid poplar. New Phytol 164:83–93
Krämer U, Grime GW, Smith JAC, Hawes CR, Baker AJM (1997) Micro-PIXE as a technique
for studying nickel localization in leaves of the hyperaccumulator plant Alyssum lesbiacum.
Nucl Instrum Methods Phys Res, Sect B 130(1–4):346–350
98 D. Goyal et al.

Kumar JN, Soni H, Kumar RN, Bhatt I (2008) Macrophytes in phytoremediation of heavy metal
contaminated water and sediments in Pariyej Community Reserve, Gujarat, India. Turkish J of
Fisheries and Aquatic Sci 8(2):193–200
Kumar R, Acharya C, Joshi SR (2011) Isolation and analyses of uranium tolerant Serratiamarcescens
strains and their utilization for aerobic uranium U (VI) bioadsorption. J Microb 49(4):568
Lacerda LD (1997) Global mercury emissions from gold and silver mining. Water Air Soil Pollut
97:209–221
Lavres J, Malavolta E, Nogueira NL, Moraes MF, Rodrigues A, Lanzoni M, Pereira C (2009)
Changes in anatomy and root cell ultrastructure of soybean genotypes under manganese stress.
Rev Bras Cienc Solo 33:395–403
Lee YC, Chang SP (2011) The biosorption of heavy metals from aqueous solution by Spirogyra
and Cladophora filamentous macroalgae. Bioresour Technol 102(9):5297–5304
Lemos Batista B, Nigar M, Mestrot A, Alves Rocha B, Barbosa Júnior F, Price AH, Feldmann
J (2014) Identification and quantification of phytochelatins in roots of rice to long-term
exposure: evidence of individual role on arsenic accumulation and translocation. J Exp Bot
65(6):1467–1479
Li HF, Gray C, Mico C, Zhao FJ, McGrath SP (2009) Phytotoxicity and bioavailability of cobalt
to plants in a range of soils. Chemosphere 75:979–986
Lidon FC, Teixeira MG (2000) Rice tolerance to excess Mn implications in the chloroplast lamel-
lae and synthesis of a novel Mn protein. Plant Physiol Biochem 38:969–978
Liu D, Zou J, Wang M, Jiang W (2008) Hexavalent chromium uptake and its effects on mineral
uptake, antioxidant defence system and photosynthesis in Amaranthus viridis L. Bioresour
Technol 99(7):2628–2636
Liu N, Lin ZF, Lin GZ, Song LY, Chen SW, Mo H (2010) Lead and cadmium induced altera-
tions of cellular functions in leaves of Alocasia macrorrhiza L. Schott. Ecotoxicol Environ Saf
73:1238–1245
Lo TY, Chen SM (1994) The effect of chemical treatment on the carotene and ascorbic acid con-
tents of tomato. J Chin Chem Soc 11:95–98
Loukidou MX, Matis KA, Zouboulis AI, Liakopoulou-Kyriakidou M (2003) Removal of As(V)
from wastewaters by chemically modified fungal biomass. Water Res 37(18):4544–4552
Lyyra S, Meagher RB, Kim T, Heaton A, Montello P, Balish RS, Merkle SA (2007) Coupling two
mercury resistance genes in Eastern cottonwood enhances the processing of organomercury.
Plant Biotechnol J 5(2):254–262
Ma JF, Zheng SJ, Matsumoto H (1997) Detoxifying aluminium with buckwheat. Nature
390:569–570
Ma LQ, Komar KM, Tu C, Zhang W, Cai Y, Kennelley ED (2001) A fern that hyperaccumulates
arsenic. Nature 409(6820):579
Manara A (2012) Plant responses to heavy metal toxicity. In: Plants and heavy metals. Springer,
Dordrecht, pp 27–53
Mane PC, Bhosle AB (2012) Bioremoval of some metals by living algae Spirogyra sp. and
Spirullina sp. from aqueous solution. Int J Environ Res 6(2):571–576
Mani D, Kumar C (2014) Biotechnological advances in bioremediation of heavy metals contami-
nated ecosystems: an overview with special reference to phytoremediation. Int J Environ Sci
Technol 11(3):843–872
Mani D, Sharma B, Kumar C, Balak S (2012) Cadmium and lead bioaccumulation during growth
stages alters sugar and vitamin C content in dietary vegetables. Proc Natl Acad Sci India Sect
B Biol Sci 82(4):477–488
Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic Press, Toronto
Mathys W (1975) Enzymes of heavy-metal-resistant and non-resistant populations of
Silenecucubalus and their interaction with some heavy metals in vitro and in vivo. Physiol
Plant 33(2):161–165
Meharg AA, Macnair MR (1992) Genetic correlation between arsenate tolerance and the rate of
influx of arsenate and phosphate in Holcus lanatus. Heredity 69:336–341
Effect of Heavy Metals on Plant Growth: An Overview 99

Messer RL, Lockwood PE, Tseng WY, Edwards K, Shaw M, Caughman GB, Lewis JB, Wataha JC
(2005) Mercury (II) alters mitochondrial activity of monocytes at sublethal doses via oxidative
stress mechanisms. J Biomed Mater Res B 75:257–263
Mirshekali H, Hadi H, Amirnia R, Khodaverdiloo H (2012) Effect of zinc toxicity on plant produc-
tivity, chlorophyll and Zn contents of sorghum (Sorghum bicolor) and common lambsquarter
(Chenopodium album). Int J Agric Res Rev 2:247–254
Mishra D, Kar M, Pradhan PK (1973) Chemical regulation of acid inorganic pyrophosphates activ-
ity during senescence of detached leaves. Exp Gerantol 8:165–167
Mishra S (2019) Targeted genome editing tools in plants. In: Innovations in life science research.
NOVA Science Publisher, New York. ISBN: 978-1-53615-868-7
Misra SG, Mani D (1991) Soil pollution. Ashish Publishing House, New Delhi
Mitchell RL, Burchett MD, Pulkownik A, McCluskey L (1988) Effects of environmentally hazard-
ous chemicals on the emergence and early growth of selected Australian native plants. Plant
Soil 112:195–199
Moller IM, Jensen PE, Hansson A (2007) Oxidative modifications to cellular components in plants.
Annu Rev Plant Biol 58:459–481
Mourato MP, Moreira IN, Leitão I, Pinto FR, Sales JR, Martins LL (2015) Effect of heavy metals
in plants of the genus Brassica. Int J Mol Sci 16(8):17975–17998
Muhammad D, Chen F, Zhao J, Zhang G, Wu F (2009) Comparison of EDTA- and citric aciden-
hanced phytoextraction of heavy metals in artificially metal contaminated soil by Typha angus-
tifolia. Int J Phytoremediation 11:558–574
Murphy A, Taiz L (1995) Comparison of metallothionein gene expression and nonproteinthiols in
ten Arabidopsis ecotypes (correlation with copper tolerance). Plant Physiol 109(3):945–954
Nagajyoti PC, Lee KD, Sreekanth TVM (2010) Heavy metals, occurrence and toxicity for plants:
a review. Environ Chem Lett. 8:199–216
Neelima P, Reddy KJ (2002) Interaction of copper and cadmium with seedlings growth and bio-
chemical responses in Solanum melongena. Nat Environ Pollut Technol 1:285–290
Neumann D, Lichtenberger O, Günther D, Tschiersch K, Nover L (1994) Heat-shock proteins
induce heavy-metal tolerance in higher plants. Planta 194(3):360–367
Nriagu JO (1989) A global assessment of natural sources of atmospheric trace metals. Nature
338:47–49
Oliveira A, Pampulha ME (2006) Effects of long-term heavy metal contamination on soil micro-
bial characteristics. J Biosci Bioeng 102(3):157–161
Ouzounidou G (1994) Change in chlorophyll fluorescence as a result of copper treatment: dose
response relations in Silene and Thlaspi. Photosynthetica 29:455–462
Pagani MA, Tomas M, Carrillo J (2012) The response of the different soybean metallothionein
isoforms to cadmium intoxication. J Inorg Biochem 117:306–315
Parmar NG, Vithalani SD, Chanda SV (2002) Alteration in growth and peroxidase activity by
heavy metals in Phaseolus seedlings. Acta Physiol Plant 24(1):89–95
Patterson WA, Olson JJ (1983) Effects of heavy metals on radicle growth of selected woody species
germinated on filter paper, mineral and organic soil substrates. Can J For Res 13(2):233–238
Phaniendra A, Jestadi DB, Periyasamy L (2015) Free radicals: properties, sources, targets, and
their implication in various diseases. Indian J Clin Biochem 30(1):11–26
Pletsch M, de Araujo BS, Charlwood BV (1999) Novel biotechnological approaches in environ-
mental remediation research. Biotechnol Adv 17(8):679–687
Prasad MNV (2004) Phytoremediation of metals in the environment for sustainable development.
Proc Indian Natl Sci Acad 70:91–98
Ramasamy P, Vino AB, Saravanan R, Subhapradha N, Shanmugam V, Shanmugam A (2011)
Screening of antimicrobial potential of polysaccharide from cuttlebone and methanolic extract
from body tissue of Sepia prashadi Winkworth, 1936. Asian Pac J Trop Biomed 1(2):244–248
Rauser WE (1999) Structure and function of metal chelators produced by plants. Cell Biochem
Biophys 31(1):19–48
100 D. Goyal et al.

Reddy AM, Kumar SG, Jyothsnakumari G, Thimmanaik S, Sudhakar C (2005) Lead induced
changes in antioxidant metabolism of horsegram (Macrotyloma uniflorum (Lam.) Verdc.) and
bengalgram (Cicer arietinum L.). Chemosphere 60:97–104
Ros ROC, Cooke DT, Burden RS, James CS (1990) Effects of the herbicide MCPA and the heavy
metals, cadmium and nickel on the lipid composition, Mg2+-ATPase activity and fluidity of
plasma membranes from rice, Oryza sativa (cv. Bahia) shoots. J Exp Bot 41:457–462
Ruiz ON, Alvarez D, Torres C, Roman L, Daniell H (2011) Metallothionein expression in chlo-
roplasts enhances mercury accumulation and phytoremediation capability. Plant Biotechnol J
9(5):609–617
Samardakiewicz S, Wozny A (2005) Cell division in Lemna minor roots treated with lead. Aquat
Bot 83:289–295
Sarret G, Saumitou-Laprade P, Bert V, Proux O, Hazemann JL, Traverse A, Manceau A (2002)
Forms of zinc accumulated in the hyperaccumulator Arabidopsis halleri. Plant Physiol
130(4):1815–1826
Saunders RJ, Paul NA, Hu Y, de Nys R (2012) Sustainable sources of biomass for bioremediation of
heavy metals in waste water derived from coal-fired power generation. PLoS One 7(5):e36470
Saxena PK, Krishna Raj S, Dan T, Perras MR, Vettakkorumakankav NN (1999) Phytoremediation
of heavy metal contaminated and polluted soils. In: Heavy metal stress in plants. Springer,
Berlin, pp 305–329
Say R, Yilmaz N, Denizli A (2003) Removal of chromium (VI) ions from synthetic solutions by the
fungus Penicillium canescens. Eur J Miner Process Environ Prot 3(1):36–41
Seaward MRD, Richardson DHS (1990) Atmospheric sources of metal pollution and effects on
vegetation. In: Shaw AJ (ed) Heavy metal tolerance in plants evolutionary aspects. CRC Press,
Boca Raton, pp 75–94
Sedeek KE, Mahas A, Mahfouz M (2019) Plant genome engineering for targeted improvement of
crop traits. Front Plant Sci 10:114. https://doi.org/10.3389/fpls
Selvam A, Wong JWC (2008) Phytochelatin systhesis and cadmium uptake of Brassica napus.
Environ Technol 29(7):765–773
Sengar RS, Gupta S, Gautam M, Sharma A, Sengar K (2008) Occurrence, uptake, accumulation
and physiological responses of nickel in plants and its effects on environment. Res J Phytochem
2(2):44–60
Seregin IV, Kozhevnikova AD (2006) Physiological role of nickel and its toxic effects on higher
plants. Russ J Plant Physiol 53:257–277
Shahid M, Dumat C, Khalid S, Schreck E, Xiong T, Niazi NK (2017) Foliar heavy metal uptake,
toxicity and detoxification in plants: a comparison of foliar and root metal uptake. J Hazard
Mater 325:36–58
Sharma SS, Dietz KJ (2006) The significance of amino acids and amino acid-derived molecules in
plant responses and adaptation to heavy metal stress. J Exp Bot 57:711–726
Sharma P, Dubey RS (2005) Lead toxicity in plants. Braz J Plant Physiol 17:35–52
Sharma A, Talukdar G (1987) Effects of metals on chromosomes of higher organisms. Environ
Mutagen 9:191–226
Shen H, He Z, Yan H, Xing Z, Chen Y, Xu W, Wenzhong X, Ma M (2014) The fronds tono-
plast quantitative proteomic analysis in arsenic hyperaccumulator Pteris vittata L. J Proteome
105:46–57
Silva S (2012) Aluminium toxicity targets in plants. J Bot 2012:219462
Singh PK, Tewari SK (2003) Cadmium toxicity induced changes in plant water relations and
oxidative metabolism of Brassica juncea L. plants. J Environ Biol 24:107–117
Singh N, Ma LQ, Srivastava M, Rathinasabapathi B (2006) Metabolic adaptations to arsenic
induced oxidative stress in Pteris vittata L. and Pteris ensiformis L. Plant Sci 170:274–282
Singhal R, Joshi S, Tirumalesh K, Gurg R (2004) Reduction of uranium concentration in well
water by Chlorella (Chlorella pyrendoidosa) a fresh water algae immobilized in calcium algi-
nate. J Radioanal Nucl Chem 261(1):73–78
 Effect of Heavy Metals on Plant Growth: An Overview 101

Stefanov K, Seizova K, Popova I, Petkov VL, Kimenov G, Popov S (1995) Effects of lead ions on
the phospholipid composition in leaves of Zea mays and Phaseolus vulgaris. J Plant Physiol
147:243–246
Tangahu BV, Abdullah S, Rozaimah S, Basri H, Idris M, Anuar N, Mukhlisin M (2011) A review
on heavy metals (As, Pb, and Hg) uptake by plants through phytoremediation. Int J Chem Eng
2011:939161: 1–31. https://doi.org/10.1155/2011/939161
Tchounwou PB, Yedjou CG, Patlolla AK, Sutton DJ (2012) Heavy metal toxicity and the environ-
ment. In: Molecular, clinical and environmental toxicology. Springer, Basel, pp 133–164
Tiwari S, Kumari B, Singh SN (2008) Evaluation of metal mobility/immobility in fly ash induced
by bacterial strains isolated from the rhizospheric zone of Typha latifolia growing on fly ash
dumps. Bioresour Technol 99(5):1305–1310
Turnau K (1998) Heavy metal content and localization in mycorrhizal Euphorbia cyparissias zinc
wastes in Southern Poland. Acta Soc Bot Pol 67:105–113
Vidali M (2001) Bioremediation: an overview. Pure Appl chem 73(7):1163–1172
Verkleji JAS (1993) The effects of heavy metals stress on higher plants and their use as bio moni-
tors. In: Markert B (ed) Plant as bioindicators: indicators of heavy metals in the terrestrial
environment. VCH, New York, pp 415–424
Veselý T, Tlustos P, Száková J (2012) Organic acid enhanced soil risk element (Cd, Pb and Zn)
leaching and secondary bioconcentration in water lettuce (Pistia stratiotes L.) in the rhizofiltra-
tion process. Int J Phytoremediation 14(4):335–349
Viehweger K (2014) How plants cope with heavy metals. Bot Stud 55:1–12
Vullo DL, Ceretti HM, Daniel MA, Ramírez SA, Zalts A (2008) Cadmium, zinc and copper bio-
sorption mediated by Pseudomonas veronii 2E. Bioresour Technol 99(13):5574–5581
Wainwright SJ, Woolhouse HW (1977) Some physiological aspects of copper and zinc tolerance in
Agrostis tenuis Sibth.: cell elongation and membrane damage. J Exp Bot 28:1029–1036
Wojas S, Hennig J, Plaza S, Geisler M, Siemianowski O, Skłodowska A, Antosiewicz DM (2009)
Ectopic expression of Arabidopsis ABC transporter MRP7 modifies cadmium root-to-shoot
transport and accumulation. Environ Pollut 157(10):2781–2789
Wong HL, Sakamoto T, Kawasaki T, Umemura K, Shimamoto K (2004) Down-regulation of
metallothionein, a reactive oxygen scavenger, by the small GTPase OsRac1 in rice. Plant
Physiol 135:1447–1456
Wu H, Tang S, Zhang X, Guo J, Song Z, Tian S, Smith DL (2009) Using elevated CO2 to increase the
biomass of a Sorghum vulgare× Sorghum vulgare var. sudanense hybrid and Trifoliumpratense
L. and to trigger hyperaccumulation of cesium. J Hazard Mater 170(2–3):861–870
Xiong ZT, Zhao F, Li MJ (2006) Lead toxicity in Brassica pekinensis Rupr.: effect on nitrate
assimilation and growth. Environl Toxicol: An Int J 21(2):147–153
Yadav SK (2010) Heavy metals toxicity in plants: an overview on the role of glutathione and
phytochelatins in heavy metal stress tolerance of plants. S Afr J Bot 76(2):167–179
Yanqun Z, Yuan L, Jianjun C, Haiyan C, Li Q, Schratz C (2005) Hyper accumulation of Pb, Zn and
Cd in herbaceous grown on lead-zinc mining area in Yunnan, China. Environ Int 31:755–762
Zarei GH, Shamsi HO, Dehghani SM (2010) The effect of drought stress on yield, yield compo-
nents and seed oil content of three autumnal rapeseed cultivars (Brassica napus L.). J Res Agric
Sci 6(1):29–37
Zhang WH, Tyerman SD (1999) Inhibition of water channels by HgCl2 in intact wheat root cells.
Plant Physiol 120:849–857
Zhou ZS, Huang SQ, Guo K, Mehta SK, Zhang PC, Yang ZM (2007) Metabolic adaptations to
mercury-induced oxidative stress in roots of Medicago sativa L. J Inorg Biochem 101:1–9
Zhu B, Alva AK (1993) Distribution of trace metals in some sandy soils under citrus production.
Soil Sci Soc Am J 57:350–355

View publication stats