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Plants and their Interaction to Environmental Pollution 139 Copyright © 2023 Elsevier Inc. All rights reserved.
https://doi.org/10.1016/B978-0-323-99978-6.00006-6
CHAPTER
8
Effect of heavy metals on growth,
physiological and biochemical
responses of plants
Arslan Hafeez, Rizwan Rasheed, Muhammad Arslan Ashraf,
Freeha Fatima Qureshi, Iqbal Hussain, and Muhammad Iqbal
Department of Botany, Government College University Faisalabad, Faisalabad, Pakistan
Abbreviations
OH• hydroxyl radicals
Al aluminum
As arsenic
Cd cadmium
Cr Chromium
Cu copper
H2O2 hydrogen peroxide
Hg mercury
Mn manganese
NOXs NADPH oxidases
O2•− superoxide
Pb lead
ROS reactive oxygen species
Sb antimony
Zn zinc
1. Introduction
The elements with specific gravity five times greater than water are referred to as heavy
metals (Abdullateef etal., 2014; Yadav etal., 2021). Plants are subjected to variety of biotic and
abiotic environmental stresses due to their sessile nature (Husen, 1997, 2021a,b,c, 2022). In
spite of all other environmental stresses, heavy metal (HM) stress is one of the most important
140 8. Effect of heavy metal pollution on plants
stresses having negative impact on plant growth, development and yield. Also, heavy metal
toxicity modulates physiological and biochemical responses in plants. Metallic elements
which are relatively high in their density and are toxic even at very low concentration are
known as heavy metals. Heavy metals is a collective term refers to group of metalloids and
metals having atomic density three or more times greater than that of water or higher than
4 g/cm3 (Onakpa etal., 2018). Therefore, when compared with density of heavy metals chem-
ical properties are most prompting factor (Gill, 2014).
Heavy metals are cadmium (Cd), Chromium (Cr), lead (Pd), Nickel (Ni), arsenic (As),
Cobalt (Co), iron (Fe), Silver (Ag), Zinc (Zn) and Platinum (Pt) group elements (Ghori etal.,
2019). Heavy metals contamination in soil occurs in environment through both natural and
anthropogenic activities. The parent material is the main source of pollution from which they
are originated in soil(Choudhary etal., 2022; Kumar etal., 2022). Ninety five percent of to-
tal earth’s crust is composed of ingenious rocks while almost 5% is made up of sedimen-
tary rocks (Sarwar etal., 2017). Overall, basaltic ingenious rocks contain a large amount of
heavy metals such as Cd, Co, Ni and Cu, however, shales are rich in Cd, Cu, Pb, Mn and Zn.
Heavy metals from these rocks enters into the soil environment through natural processes
such as terrestrial, meteoric, biogenic, and volcanic processes,leaching,surface winds, and
erosion (Muradoglu etal., 2015). Urbanization and industrialization are the main anthropo-
genic sources that contributes to the entry of heavy metals into the biosphere (Bi etal., 2020).
Other anthropogenic activities such as application of fertilizers (Atafar etal., 2010), pesticides
(Zhang and Wang, 2020), fossil fuel combustion (Muradoglu etal., 2015), sewage irrigation
(Sun etal., 2013), smelting and mining (Chen etal., 2015a,b) and municipal wastes disposal
(Khan etal., 2016) significantly contributes to increased heavy metal concentration in agricul-
tural soils.
As an illustration, irrigation with wastewater of industries results in significant heavy
metal contamination of agricultural lands. In general, there may be different types of heavy
metals pollution in the soils at the industrial areas, depending on the kind of industries, raw
material used and their products (He etal., 2015). Plants uptake heavy metals via roots, so
their accumulation in fruit trees, vegetables and other crops may occur, leading to the entry
of heavy metals into the food chain. The entry of toxic heavy metals into the food chain
through plants is the major pathway through which humans and animals are exposed to
them. Exposure to heavy metals may cause several types of cancer, growth retardation, en-
docrine disruption, kidney damage, neurological and immunological effects in humans. In
plants, growth and yield of many crops may be affected by high concentrations of heavy met-
als (Edelstein and Ben-Hur, 2018). Usually in urban areas soils are contaminated with Cu, Pb,
Cd and Zn from paints, traffic, industrial wastes and many other sources (Iqbal etal., 2020).
2. Effect of heavy metal pollution on plants
As heavy metals are nonbiodegradable and some of them like Hg, Mn, Fe, Cu, Co, Zn,
As, and Ni are accumulated in soil for long time through sewage disposal and industrial
waste (Ashraf etal. 2017; Yadav etal., 2021)(Ashraf etal., 2017; Yadav etal., 2021). Even
though some of the heavy metals are necessary for normal growth and functioning of
plants and are considered as essential micronutrients, however, many can have deleterious
2. Effect of heavy metal pollution on plants 141
effects and may directly affect the metabolism, senescence, physiology and growth of
plants (Ghori etal., 2019). Soil physiochemical properties plays a principal role in the the
uptake and accumulation of heavy metals in plants. Mainly, heavy metals are accumulated
in the root cells of plants because cell walls may trap them or casparian strips may block
them. Excessive accumulation of heavy metals in plant tissues may directly or indirectly
impairs several morphological, biochemical and physiological functions and successively
interferes with the productivity of crop (Mehta etal., 2020). Production of crop is reduced
by heavy metals through induction of harmful effects to different physiological functions
in plants such as photosynthesis, germination of seed, seed reserves remobilization and ac-
cumulation during germination and plant growth (Shahid etal., 2014). Generation of reac-
tive oxygen species (ROS) including radicals such as hydroxyl radicals (OH•), superoxide
radicals (O2•−) and nonradicals likes singlet oxygen and hydrogen peroxide (H2O2), is one
of the most rapid effects of toxic heavy metals in plants (Smeets etal., 2005; Singh etal.,
2022; Tamás etal., 2017). Reactive oxygen species may generate either indirectly, through
NADPH oxidases (NOXs) or through the inhibition of enzymes via essential cations dis-
placement or directly, by the ROS-active metals via Haber-Weiss/Fenton reactions (Shahid
etal., 2014). In plants, major sites for the production of ROS are mitochondria, chloroplasts
and peroxisomes as well as in the endoplasmic reticulum, cell wall and plasma membrane
(Das and Roychoudhury, 2014; Kärkönen and Kuchitsu, 2015). A mechanistic diagram il-
lustrating the effects of heavy metals on plants is given in Fig.1.
FIG.1 Schematic representation of phytotoxic effects of heavy metal(loid)s on plants and different defense re-
sponses in plants to tolerate metal toxicity.
142 8. Effect of heavy metal pollution on plants
3. Cadmium (Cd)
Cadmium (Cd) is a highly toxic metal that is nonessential for plants and have become a
significant pollutant in the environment largely due to anthropogenic activities such as in-
dustrial waste, mining, extensive fertilizer, pesticide application, wastewater irrigation, and
vehicular use. Plants can efficiently uptake Cd and translocate it to the aerial parts such as
stem, leaves, flowers, and fruits. Cd stress evokes alterations in various morphological, phys-
iological, biochemical, anatomical and molecular processes of plants. Major phytotoxic symp-
toms of Cd stress includes nutritional imbalance, reduced photosynthesis and chlorophyll
biosynthesis, leaf chlorosis, disruption of membrane integrity, oxidative stress, inhibited root
and shoot growth and biomass, reduced seed germination, browning of root tip, enzyme
inhibition, disrupted respiration and hampered nucleic acid synthesis (Li etal., 2021a,b,c,d;
Wang etal., 2019; Guo etal., 2017). Cd stress negatively influence plants from seed germina-
tion up to final yield stage. Consistently, Moori and Ahmadi-Lahijani (2020) reported that Cd
stress caused significant reduction in seed germination percentage, seed germination rate and
seed vigor index in thyme seeds. Sweet basil (Ocimum basilicum L.) seeds exposed to varying
cadmium levels also showed reduced seed germination percentage (Fattahi etal., 2019). Cd
concentration of 50 mg/kg in soil considerably reduced seed germination of Coriandrum sa-
tivum seeds (Sardar etal., 2021). Cd-induced alteration in physiological and biochemical pro-
cesses in seeds, such as inhibition of seed imbibition, a crucial step in hydration of enzymes
involved in significant metabolic activities, is one of the primary reasons for reduced seed
germination (Huybrechts etal., 2019; Zayneb etal., 2015). Exposure to low concentrations
of heavy metals including Cd resulted in prolonged seed dormancy at room temperature
(Kranner and Colville, 2011). Sassafras seedlings under aggravating Cd levels in soil man-
ifested reduced plant height and biomass of leaves, branches and roots (Zhao etal., 2021).
Mung bean seedlings exposed to two different doses of cadmium (50 and 100 μM) exhibited
remarkably reduced plant height, shoot and root dry weights, root length and number of
lateral roots. However, the Cd induced inhibitory effects was highly significant in treatment
with 100 μM (Leng etal., 2021). Similarly, wheat seedlings under 5 μM/L Cd stress manifested
lower fresh and dry biomass along with reduced root and shoot length (Zeshan etal., 2021).
Strawberry seedlings turned yellow and appeared macular with inhibited growth and de-
creased biomass when exposed to Cd stress (Wu etal., 2021). Rice seedlings grown for 7 days
on a nutrient solution contaminated with Cd resulted in significantly reduced shoot and root
length, fresh and dry weights. This was attributed to high concentration of Cd in aerial plant
parts, which also caused toxic symptoms on the plants. Further, authors also mentioned that
the presence of high concentration of Cd in the shoots might have disturbed the photosys-
tems (Riaz etal., 2021). Spinach (Spinacia oleracea) plants exposed to Cd stress manifested
reduced plant height, fresh and dry biomass, root length, leaf length and area (Waheed etal.,
2021). The presence of high Cd content in plants interrupt important metabolic processes that
leads to necrosis and ultimately hampers the growth (Xue etal., 2013). Moreover, Cd stress in
plants reduces hydraulic conductivity thus reducing cell wall extensibility and retardation in
growth (Zhang etal., 2013; Liu etal., 2021; Abd_Allah etal., 2017).
Two melon cultivars namely Xiulv (Cd-sensitive) and Hamilv (Cd-tolerant) under Cd
stress manifested differential growth inhibition response. Cd stress significantly reduced dry
mass of shoots and roots in both cultivars. However, the reduction was greater in Xiulv than
3. Cadmium (Cd) 143
Hamilv (Zhang etal., 2015). Similarly, different chickpea cultivars were subjected to two Cd
levels (25 and 50 μM). Cadmium toxicity considerably reduced fresh and dry biomass as well
as plant height of all cultivars examined. Maximum reduction in these attributes was evi-
dent at 50 μM Cd stress. Cultivars namely IC8 and NC2 outperformed under Cd treatments
with greater growth, biomass and plant water content and indicated as Cd tolerant cultivars.
Whereas, IC8-B exhibited greater reductions and indicated as Cd sensitive cultivar (Ullah
etal., 2020). Rasheed etal. (2018) reported that Cd stress significantly reduced the shoot and
root fresh and dry biomass in two okra cultivars namely Shabnum 786 and Arka Anamika
with greater reduction observed in cv. Arka Anamika. This reduction in growth of okra plants
was attributed to increased chlorophyll degradation, disturbed plant water relations, altered
nutrient uptake and their distribution pattern under Cd stress.
The loss of chlorophyll pigments is one of the most extensively reported manifestations
of Cd stress in plants (Ci etal., 2010; Daud etal., 2015; Per etal., 2016; Ma etal., 2018). It has
been reported that Cd stress can alter the process of chlorophyll biosynthesis via interacting
with the thiol groups of the enzymes 5-aminolevulinic acid synthesis and protochlorophyl-
lide reductase complex or elevated ROS generation (Choudhury etal., 2017; Wu etal., 2019).
Recently, Zhou etal. (2021) reported that Cd stress significantly impacted chlorophyll content
and photosynthetic parameters in two wheat varieties. Savory (Satureja hortensis) plants un-
der Cd stress exhibited reduced concentrations of chlorophyll pigments (a and b), total chlo-
rophyll and carotenoids content (Azizi etal., 2020).
Cadmium stress significantly reduced net photosynthetic rate (Pn), stomatal conductance
(Gs), transpiration rate (Tr), chlorophyll a, b and total chlorophyll content, whereas, increased
intercellular CO2 concentration (Ci) (El Rasafi etal. 2020). Similarly, Kaya etal. (2020) reported
considerable reduction in chlorophyll a, b content as well as maximum photochemical effi-
ciency of photosystem II (Fv/Fm) in wheat plants under 0.10 mM Cd stress. In maize hybrids
subjected to Cd stress, significant reduction in physiological attributes such as photosynthe-
sis rate, transpiration rate, chlorophyll content and stomatal conductance was recorded and
the highest reduction in these traits was attained at maximum level (15 μM) of Cd stress used
in the study. Moreover, maize hybrids showed variable response to Cd doses (Akhtar etal.,
2017). Another study on maize plants reported remarkable reduction in chlorophyll fluores-
cence parameters like maximum quantum yield of PSII (Fv/Fm), quantum yield of PSII elec-
tron transport (ΦPSII) and coefficient for photochemical quenching (qP), whereas, an increase
was evident in nonphotochemical quenching (NPQ) values (Qu etal., 2019).
Cadmium stress causes oxidative damage in plants through excessive production of ROS
such as singlet oxygen (1O2), superoxide radicals (O2•−), hydrogen peroxide (H2O2), and hy-
droxyl radicals (OH•) (Rasheed etal., 2018; Rahman etal., 2016). Plants cope with oxidative
stress by scavenging toxic ROS mainly through upregulating enzymatic and nonenzymatic an-
tioxidant systems (Nadarajah, 2020; Pandey etal., 2017; Ashraf etal., 2018). Cd stress increases
accumulation of malondialdehyde (MDA), a biomarker for peroxidation of lipids under oxi-
dative stress (Guo etal., 2014) which is strongly associated with increased production of ROS
under stress (Li etal., 2012). Cadmium induced oxidative stress has been reported in various
crops such as tomato (Wei etal., 2021a,b; Faizan etal., 2021; Kumar etal., 2021), Brassica rapa
(Li etal., 2021a,b,c,d) aromatic rice (Imran etal., 2021), canola (Sanjari etal., 2019); common
bean (Rady etal., 2019), saffron (Moradi etal., 2019). Maize plants subjected to Cd stress (100
and 200 μM) displayed increased H2O2, MDA levels and electrolyte leakage (EL) percentage.
144 8. Effect of heavy metal pollution on plants
Activities of superoxide dismutase (SOD) and catalase (CAT) antioxidant enzymes signifi-
cantly enhanced while decrease in glutathione S-transferase (GST) activity was observed
under Cd stress. Maximum enhancement in aforementioned attributes was at 200 μM than
100 μM (Alam etal., 2021). Okra plants exposed to Cd stress (1 mM) displayed higher cellu-
lar levels of H2O2 and MDA along with enhanced activities of enzymatic (SOD, POD, APX)
and nonenzymatic (phenolics, ascorbic acid, flavonoids, and anthocyanins) antioxidants.
Moreover, levels of proline, total free amino acid, total soluble protein also increased with de-
creased CAT activity and reducing sugars under Cd stress. In this study, Cd stress exerted no
influence on total soluble sugars of okra plants (Rasheed etal., 2018). In chickpea plants, Cd
stress elevated H2O2 (215.66%), MDA (61.70%) and EL (76.25%) when compared with control
plants. Increased activities of SOD (89.76%), CAT (110.25%), APX (59.66%) glutathione reduc-
tase (GR; 46.78%), GST (100.19%), reduced glutathione (GSH; 63.47%), oxidized glutathione
(GSSG; 39.57%) and GSH/GSSG ratio (17.06%) was observed in Cd treated plants. In contrast,
activity of dehydroascorbate reductase (DHAR; 46.78%) and monodehydroascorbate reduc-
tase (MDHAR; 45.90%), ascorbic acid (ASA; 59.18%) was decreased under Cd stress. Methyl
glyoxal (MG) increased by 82.98% in Cd supplied plants whereas, glyoxalase system enzymes,
glyoxalase (Gly) I and GlyII activities declined by 38.82% and 28.57%, respectively, under Cd
stress (Ahmad etal., 2021a,b). A different response was noted in Cd stressed pea plants as they
demonstrated reduced GSSG content and enhanced GlyI activity. Authors suggested that de-
cline in GlyII activity of pea plants under Cd stress might be due to the proteolytic degradation
of enzymes (Jan etal., 2018). Rahul and Sharma (2021) found that Cd stress (500 μM) resulted in
greater accumulation of H2O2 and MDA content in Cd-sensitive genotypes S1 and S2 whereas,
a nonsignificant alteration was observed in Cd-tolerant genotypes T1 and T2 of castor (Ricinus
communis) when compared with their respective control plants.
Plants require essential nutrients to grow normally. Cd has a deleterious impact on plant
physiology, biochemistry, growth, yield, and productivity by interacting with other essen-
tial nutrients, causing nutritional imbalance. Cd interactions with other nutrients have been
shown to restrict their absorption and translocation in several crops such as wheat (Rahman
etal., 2021), rice (Mapodzeke etal., 2021), mulberry (Guo and Li, 2021), maize (Abbas etal.,
2020), soybean (El-Esawi etal., 2020), okra (Rasheed etal., 2018), tomato (Hédiji etal., 2015),
barley (González etal., 2015). It has been reported that Cd being a bivalent cation in na-
ture competes with Ca, Fe, Mg, Mn, and Zn during transport across membranes (Verbruggen
etal., 2009). Moreover, some metal transporters from NRAMP (natural resistance-associated
macrophage protein) and ZIP (zinc regulated transporter/iron regulated transporter related
protein) families has been reported to transport Mn, Fe as well as Cd (Ajeesh Krishna etal.,
2020; Chen etal., 2021). Recently, it has been observed that Cd stress in two menthol mint
(Mentha arvensis L.) cultivars namely kosi and kushal reduced the concentrations of three
mineral nutrients namely N, P, and K in both cultivars. Cultivar kosi exhibited 50% decrease
in N, 39.53% in P and 49.76% in K concentrations, whereas cultivar kushal displayed 57.57%
decrease in N, 14.58% in P, and 44.97% in K concentrations under Cd stress compared with
their respective control plants (Zaid etal., 2020). A submerged macrophyte Potamogeton crispus
L. under Cd polluted environment exhibited increased content of Ca, Na, Fe, and Mn while
a conspicuous decrease was observed in K and P content of leaves, which was attributed to
the reduced availability of energy (ATP) (Yang etal., 2011). Cadmium toxicity considerably
reduced N, Ca, Mg, and P contents in roots and shoots of alfalfa (Zhang etal., 2019). In shoots
4. Lead (Pb) 145
of Trifolium repens L. plants, Cd toxicity depreciated Cu, Mg, Fe, and K but considerably im-
proved the Ca content. However, Cd stress significantly reduced the Ca, Mg, and Fe content
but increased the content of K and Cu in roots when compared with control plants. Authors
suggested that Cd may entered the roots by employing Ca, Mg, and Fe transporters and is
further transported from roots to shoots via Cu and K transporters. Moreover, decrease in
root Ca content might be due to the competition among Cd and Ca at Ca + permeable chan-
nels site in the plasma membranes for entrance into the root cells (Liu etal., 2015). Wahid
etal. (2008) studied the effect of Cd stress on shoot nutrient content of mung bean at different
growth stages in sensitive and tolerant cultivars. There exists a remarkable difference among
both cultivars with a decline in content of K, Mg, Mn, and Fe at the seedling, vegetative and
reproductive stages under Cd toxicity. However, sensitive cultivar showed greater reduction
in nutrient content when compared with tolerant cultivar. Authors also suggested that better
nutrient accumulation pattern manifested by tolerant mungbean cultivar is imperative for its
Cd tolerance.
4. Lead (Pb)
Anthropogenic activities like industrial development causing soil contamination with dif-
ferent heavy metals, which is a growing ecological concern. Concentrations of heavy metals
in soil-plant system greatly impact agricultural production and yield. Lead (Pb) is a nones-
sential potentially hazardous metal for plants as well as for human and animal health upon
entering the food chain. Pb released into the environment mainly through mining and smelt-
ing activities, metal plating, Pb-based paints, cosmetics, automobiles, chimneys of factories,
pesticides and fertilizers (Tchounwou etal., 2012). The presence of Pb in agricultural soils
provokes detrimental effects on plant growth, reduced cell division, inhibition of enzymatic
activities, reduced photosynthesis, decreased seed germination, altered mineral nutrition pat-
tern, and water imbalance in plants (Kalaivanan and Ganeshamurthy, 2016). Pb stress induces
excessive accumulation of highly toxic reactive oxygen species (ROS) in plants, which causes
oxidative damage to nucleic acids, lipids, and proteins (Shahzad etal., 2018).
Lead toxicity adversely impact physiology and morphology of seeds obstructing germi-
nation process and early seedling growth (Seneviratne etal., 2019). During seed germination
process, Pb known to affect hydrolytic enzymes activity of α-amylase, β-amylase and protease,
which impose contrary impacts on radicle and hypocotyl growth. According to Sidhu etal.
(2017) increasing levels of Pb in Coronopus didymus L. (Brassicaceae) caused a significant gradual
decline in the activities of all hydrolytic enzymes (α-, β-amylase and protease) in both roots
and shoots. Likewise, Pb stress reduced starch hydrolyzing enzymes activities resulting in
starch immobilization in Brassica campestris (Singh etal., 2011). Heavy metal induced reduction
in seed germination rate has also been attributed towards increasing levels of abscisic acid
(ABA) in seeds and also the generation of NADH-dependent extracellular H2O2 (Yang etal.,
2010; Fattahi etal., 2019). When maize seeds were allowed to germinate on Pb contaminated
soil with varying levels of Pb (0, 1, 2, 5, 10, and 20 mM), seeds exhibited inhibited germina-
tion percentage in a concentration dependent manner. Least germination percentage (15%)
was recorded at highest (20 mM) Pb concentration (Zhang etal., 2018). In another study on
maize, Pb adversely affected seed germination and seedling growth of two maize genotypes
146 8. Effect of heavy metal pollution on plants
namely EV-1098 and EV-77. A consistent decrease was evident in germination percentage
and index, plumule and radicle length, fresh and dry weight of seedlings with increasing Pb
levels. Maximal reduction in these parameters was recorded at the highest Pb concentration
(1.0 mg/L) provided in the growth medium. However, Pb toxicity exerted more inhibitory
effect on radicle length in genotype EV-1098 when compared with EV-77 (Ahmad etal., 2011).
Recently, Jatav etal. (2021) evaluated the crop specific response of pearl millet, finger millet
and oat under Pb stress and observed that all the three species did not vary in germination re-
sponse under control conditions. However, a gradual reduction in seed germination efficiency
of all three species under increasing levels of Pb toxicity was observed. At Pb levels ≥ 30 mg/L,
oat seeds exhibited significantly maximum reduction in seed germination efficiency than pearl
millet and finger millet. Lead induced reduction in seed germination has also been observed
in wheat (Yang etal., 2010), Brassica juncea L. (Soares etal., 2020), Ocimum basilicum L. (Fattahi
etal., 2019) upland rice (Wang etal., 2020) and alfalfa (Yahaghi etal., 2019).
Maize plants at seedling stage exposed to Pb toxicity showed considerably reduced fresh
and dry weight of shoots and roots. Roots being more vulnerable to metal stresses, Pb stress
induced alterations in anatomical features of maize seedling root tissues revealed increased
central cylinder diameter, cortex and endodermis thickness to 20%, 19%, and 53%, respec-
tively, while no change has been observed in metaxylem and protoxylem diameters under Pb
toxicity (Zanganeh etal., 2021). Fragrant rice cultivars grown in Pb polluted soil accumulated
varying concentrations of Pb, with highest concentration in roots and the lowest in grains
(Ashraf etal., 2020). Tartary buckwheat plants grown under varying levels of Pb stress (0, 100,
200, and 300 μM) for 15 and 30 days after sowing (DAS). Plants showed noteworthy reduction
in root and shoot length at both 15 and 30 DAS with increasing levels of Pb stress. However,
maximal reduction was observed at 30 DAS at 300 μM Pb stress level. Plant biomass accumu-
lation also displayed gradual decline with increasing Pb stress levels. The maximal reduction
was recorded in fresh and dry biomass accumulation to 61% and 94%, respectively, 15 days
after sowing. Authors reported that decline in growth related attributes might be the result of
Pb-induced inhibition of mitosis and restrained aquaporins, resulting in structural deformities
that hinder plant growth (Pirzadah etal., 2020). Wheat seedlings subjected to 2 mM Pb toxic-
ity exhibited reduced shoot and root length, fresh and dry weight. Also, a decline in Rubisco
and ATP sulfurylase (ATP-S) activities, total chlorophyll content, relative water content and
nutrient concentration was evident under Pb stress. The reduction in the growth parameters
might be linked with Pb stress disturbed physio-biochemical processes like ions concentration,
enzymes activity, respiration and photosynthesis (Alamri etal., 2018). Weryszko‐Chmielewska
and Chwil (2005) did a comprehensive microscopic analysis on soybean leaf exposed to var-
ied levels of Pb. They observed that Pb stress reduced the area of cotyledons and leaf blades
in soybean cv. Polan plants. Lead toxicity induced leaf epidermal alterations such as reduced
guard cell size, increased wax coating, number of stomata and trichomes per unit area. Lead
stress reduced leaf blade thickness, xylem and phloem area, and xylem vessel diameter. Also,
Pb stress caused chloroplast disintegration in leaf mesophyll cells. Bursted thylakoid stroma
and cracked chloroplast envelopes were also seen under Pb stress.
Robinia pseudoacacia plants grown in contaminated soil with varying levels of Pb showed
gradual reduction in photosynthetic pigments such as chl a, chl b and total chlorophyll con-
tent as Pb concentration increased. A progressive decrease was observed in photosynthetic
characteristics such as net photosynthetic rate (Pn), stomatal conductance (gs), transpiration
5. Arsenic (As) 147
rate (Tr) and mesophyll intercellular CO2 concentration (Ci) under increasing levels of Pb
stress. Furthermore, Pb stress also caused decrease in chlorophyll fluorescence parameters
namely maximum photochemical efficiency of photosystem (PS) II (Fv/Fm), quantum yield
(ΦPSII) and photochemical quenching (qP). However, a gradual increase was observed in ini-
tial fluorescence (Fo) and nonphotochemical quenching (qN) (Zhou etal., 2017). Previous lit-
erature showed that Pb toxicity negatively affects photosynthesis, which could be attributed
to metal induced reduction in photosynthetic related pigments (Hussain etal., 2017), inhib-
ited electron transport system (Gajić etal., 2009), alteration in chloroplast structure and sto-
matal closure (Islam etal., 2008).
Lead toxicity induces oxidative stress in plants, which has been indicated through ex-
cessive generation of reactive oxygen species (ROS) that damages cellular membranes and
organelles measured generally through lipid peroxidation markers such as malondialde-
hyde (MDA) and hydrogen peroxide (H2O2) (Zanganeh etal. 2021). Plants neutralizes ROS
through well- established antioxidant system comprised of both enzymatic such as superox-
ide dismutase (SOD), peroxidase (POD) and catalase (CAT) and nonenzymatic antioxidants
namely carotenoids, glutathione, ascorbate, flavonoids, phenylpropanoids and phenolic acids
(Hasanuzzaman etal., 2020). In a recent study, coriander (Coriandrum sativum L.) plants grown
in Pb contaminated soil with different concentrations of 0, 500, 1000, and 1500 mg/kg of soil
showed significantly higher MDA content with maximal accumulation at 1000 mg/kg Pb with
decrease at higher concentration. Flavonoids were also higher under Pb stress at 1500 mg/kg
Pb. Enzymatic activities of SOD and POD were significantly enhanced at 1000 mg/kg Pb and
reduced at 1500 mg/kg Pb, while CAT activity showed increment at 500 mg/kg Pb and de-
creased at higher concentrations. A 15% decrease in vitamin C content was also observed under
1500 mg/kg Pb. A notable increase of 93% in anthocyanin was observed at 500 mg/kg Pb while
it decreased at higher Pb concentrations when compared with control (Fatemi etal., 2021).
Lead toxicity in wheat plants caused higher cell oxidation levels (MDA and Lipoxygenase;
LOX). The relative gene expression and activities of SOD, CAT, guaiacol peroxidase (GPX)
and ascorbate peroxidase (APX) were significantly enhanced in both leaves and root tis-
sues under Pb stress at late booting stage. However, the gene expression level and activities
of antioxidant enzymes were greater in roots than the leaf tissue (Navabpour etal., 2020).
Another study on wheat reported that Pb stress aggravated the MDA content, O2•− and H2O2
generation. Lead toxicity resulted in a considerable increase in activities of SOD, glutathi-
one S-transferase (GST), APX and greater accumulation of proline with decreased leaf relative
water content (LRWC). Whereas, glutathione peroxidase (GPX), monodehydroascorbate re-
ductase (MDHAR) and dehydroascorbate reductase (DHAR) activities and ascorbate content
reduced with increasing Pb levels. Both glyoxalase (Gly) system enzymes activities GlyI and
GlyII were diminished under Pb stress with a concomitant increase in methylglyoxal (MG)
content (Hasanuzzaman etal., 2018).
5. Arsenic (As)
Arsenic (As) is commonly present in soils and is a potentially toxic metalloid for plants
(Dhakate etal., 2019). It significantly hampers plant growth and development leading to
reduced plant biomass and yield, which is a matter of great concern. Some anthropogenic
148 8. Effect of heavy metal pollution on plants
activities such as applications of herbicides or pesticides, coal burning and timber preser-
vatives contribute to the As contamination in the environment. Arsenic also causes dif-
ferent medical abnormalities in humans such as disturbed functioning of circulatory and
nervous system, oxidative stress, skin cancer, pulmonary diseases, urinary bladder and
kidney diseases (Bhat etal., 2021). Plants uptake As through phosphate transporters and
nodulin 26-like intrinsic aquaporin (NIP) channels. Arsenic modulates several metabolic
processes in plants resulting in reduced germination, growth and yield. Arsenic has been
reported to interact with the starch metabolism enzymes decreasing the seed germination
(Zia etal., 2017). Recently, Wu etal. (2020) reported that As exposure significantly reduced
seed germination percentage in rice plants. Similarly, garden cress (Lepidium sativum) seeds
showed significant inhibition in germination exposed to As stress (Nouri and Haddioui,
2021). Two maize plants administered As stress exhibited notably decreased plant height,
leaf area and stem diameter. However, the reductions was more prominent in Run Nong
35 than Dong Dan 80 (Anjum etal., 2016). Farooq etal. (2015) reported that As stress con-
siderably reduced root and shoot length and biomass in Brassica napus L. plants. Arsenic
toxicity lowers mitotic activity in root meristem resulting in reduced cell division rate in the
apical meristem, leading to inhibited expansion and elongation of the newly formed cells
(Mumthas etal., 2010). Reduction in plant biomass under As stress is generally attributed
to the reduced photosynthesis, soluble protein content, peroxidase activity and other phys-
iological mechanisms (Ahsan etal., 2008). Tomato plants treated with As stress showed a
visible As toxicity symptoms mirrored as conspicuous wilting and leaf necrosis alongside
reduced germination percentage and seedling shoot elongation (Marmiroli etal., 2014).
Arsenic negatively affected the plant water relations in soybean reflected as significantly
reduced root absorption rate, leaf and root relative water content, stomatal conductance,
shoot water and osmotic potentials under As stress (Vezza etal., 2018). Arsenic stress neg-
atively influenced photosynthetic pigments in plants (Bali and Sidhu, 2021). For example,
a significant reduction was recorded in Chl. a, Chl. b content and Chl. a/b ratio in wheat
plants. Moreover, As adversely affected gas exchange attributes such as photosynthetic and
transpiration rates, water use efficiency, stomatal conductance, and internal CO2 concentra-
tion in wheat plants (Ali and Perveen, 2020). Rubisco activity and maximum efficiency of
photosystem (PS) II was also reported to be declined under As stress in rice plants (Khan
etal., 2021). Similarly, tea plants (Camellia sinensis L.) under As stress also showed marked
decrease in maximum photochemical efficiency of PSII (Fv/Fm), showing negative impact
of As on PSII activities (Li etal., 2021a,b,c,d). Arsenic induces oxidative stress in plants by
generating reactive oxygen species (ROS) that reacts and damage different cellular compo-
nents such as nucleic acid, proteins, and membrane lipids (Farooq etal., 2018). For example,
Zargari etal. (2020) reported an increase in hydrogen peroxide (H2O2) and malondialde-
hyde (MDA) content in alfalfa plants exposed to different levels of As stress. Plant detoxify
ROS through modulation in enzymatic and nonenzymatic antioxidant system. For instance,
Vetiver grass (Vetiveria zizanioides L. Nash) under As stress showed significantly higher
antioxidant activities of superoxide dismutase (SOD), ascorbate peroxidase (APX), catalase
(CAT), guaiacol peroxidase (GPX) and glutathione S-transferase (GST), which enhanced
plant tolerance to As induced oxidative stress (Singh etal., 2017). Osmolytes such as pro-
line, glycine betaine, soluble sugars and total proteins has also been reported to be higher
under As toxicity in pea plants (Garg and Singla, 2012).
6. Mercury (Hg) 149
6. Mercury (Hg)
Mercury (Hg) is a nonessential phytotoxic metal pollutant naturally found in soil. Many
anthropogenic activities such as seed disinfectants, untreated industrial wastes, synthetic fer-
tilizers, herbicides, and pharmaceuticals are significant sources of Hg contamination in the
environment. Its presence in agricultural soils is of great concern globally because Hg toxicity
affects plant growth, development, and yield at all growth stages. Exposure to Hg causes ab-
normal germination, reduces biomass, inhibits photosynthesis, disturbs protein functioning,
water relations and nutrient imbalance in plants (Azevedo etal., 2018; Safari etal., 2019; Sun
etal., 2018). Previous report suggested that wheat germination rate and number of seedlings
was significantly decreased under Hg stress (Popa etal., 2007). Reduced seed germination
under Hg stress has also been reported in crops such as maize (Deng etal., 2016) and Brassica
spp. (Ling etal., 2010). Cucumber seedlings administered various levels of Hg stress showed
stunted growth mirrored as reduced biomass, root and shoot length (Cargnelutti etal., 2006).
Similarly, three soybean cultivars namely Pusa-24, Pusa-37, and Pusa-40 treated with Hg stress
also showed reduced shoot and root length. However, the maximum reduction in both attri-
butes was more prominent in cultivar Pusa-24. Authors also observed high concentration of
Hg in the roots than shoots of Hg stressed soybean plants (Ahmad etal., 2021a,b). In contrast,
Mohammadi etal. (2021) observed higher accumulation of Hg in shoots when compared with
roots in okra plants under HgCl2 stress and recommended it as a hyperaccumulator plant for
phytoremediation of Hg polluted soil and waters. Rice plants under Hg toxicity exhibited
sharp reduction in average root length when compared with their respective controls (Chen
etal., 2015a,b). Elevated levels of Hg stress impaired chlorophyll content and photosynthesis
rate in higher plant species (Teixeira etal., 2018). In Sesbania drummondii seedlings, Hg level
up to 50 mg/L did not exert any negative effects on photosynthetic integrity. However, Hg
concentrations above 50 mg/L exhibited slight reductions in Fv/Fm and Fv/Fo values (Israr
etal., 2006). Safari etal. (2019) demonstrated significant reduction in chlorophyll pigments
of lemon balm plants under Hg toxicity. Authors suggested that reduction in chlorophyll
pigments was due to the Hg induced oxidative stress, disturbed mineral content uptake and
replacement of metal ions by Hg in photosynthetic pigments. Okra plants subjected to Hg
toxicity exhibited marked augmentation in total phenol, total flavonoids and anthocyanins
content. Further, phenol profiling showed that Hg-treated okra plants exhibited increase in
chlorogenic acid, rosmaric acid, apigenin, quercetin and rutin content (Mohammadi etal.,
2021). Mercury stress exert negative effect on nutrient uptake in plants (Tran etal., 2021).
For example, wheat plants grown under various concentrations of Hg stress demonstrated
reduced level of K, Ca, and Mg alongside increased electrolyte leakage in leaf tissues, which
is one of the main reasons for the impaired nutrient acquisition (Sahu etal., 2012).
Mercury toxicity provokes excessive production of reactive oxygen species (ROS) that dam-
ages different cellular components such as nucleic acids, proteins, membrane lipids, causing
perturbation of many physiological, biochemical and molecular processes in plants (Nagajyoti
etal., 2010; Zhang etal., 2017). Plants have evolved diverse defense mechanisms comprised
of enzymatic and nonenzymatic antioxidants to detoxify ROS and prevent oxidative damage
(Sewelam etal., 2016). Chicory plants treated with Hg stress showed conspicuous increase in
H2O2 and thiobarbituric acid reactive substances (TBARS) along with increased activities of
antioxidant enzymes such as superoxide dismutase (SOD), peroxidase (POD), catalase (CAT),
150 8. Effect of heavy metal pollution on plants
ascorbate peroxidase (APX), glutathione reductase (GR) and Glutathione S-transferase (GST)
(Malik etal., 2019). Mercury stress resulted in increased accumulation of proline and soluble
sugars in duckweed (Lemna minor), contributing to the improved cell turgor and membrane
stability due to its function as osmolyte (Zhang etal., 2017).
7. Metal stress tolerance mechanisms in plants
Heavy metals (HMs) toxicity impairs plant growth and development through modulating
different cellular metabolic processes. Plants have evolved various homeostatic mechanisms
such as ROS signalling, upregulated antioxidant system, biosynthesis of root exudates, HMs
binding to the cell wall, sequestration and compartmentation that regulate HMs uptake, trans-
port, accumulation and their detoxification processes (Berni etal., 2019; Rizvi and Khan, 2019;
Fu etal., 2018; Jia etal., 2019; Xu etal., 2020). Root exudates such as amino acids, organic acids,
phenolics, sugars and nonproteinaceous amino acids like phytosiderophores are the important
components that involve in the metal detoxification and nutrient acquisition in the rhizosphere
(Bali etal. 2020). These compounds bind and forms stable complexes with the HMs in rhizo-
sphere, rendering them nontoxic and restricting their uptake, thereby reducing their bioavail-
ability to the plants, hence, contributing to the metal stress tolerance in plants (Huang etal. 2021).
For example, increased concentration of citric acid and malic acid in root exudates of makoi
(Solanum nigrum) and parthenium weed (Parthenium hysterophorus) under Cr stress has likely to
assist plant adaptation to Cr stress (UdDin etal., 2015). According to Javed etal. (2018), there is a
positive correlation between root exudates (citric acid, malic acid, glutamic acid, oxalic acid, fu-
maric acid) and root Pb contents in Portulaca oleracea plants, which may also maintain optimum
nutrient content and allow Portulaca oleracea adaptation to Pb spiked soil. In tomato plants, root
oxalate exudation was a significant factor in preventing Cd from entering roots (Zhu etal. 2011).
Phytosiderophores are natural chelating agents and have been reported to chelate Zn, Cu, Mn,
and Cd (Thakur etal. 2022). Heavy metal toxicity causes excessive formation of reactive oxygen
species (ROS) such as H2O2, O2•−, and OH•. A high concentration of ROS in cellular environment
causes oxidative stress, which results in lipid peroxidation of biomembranes alongside damage
to nucleic acid and other biomolecules. Plants detoxify HM-induced ROS through activation
of antioxidant system consisting enzymatic such as superoxide dismutase (SOD), peroxidase
(POD), catalase (CAT) and nonenzymatic (glutathione, carotenoids, ascorbate) antioxidants.
Two okra cultivars exhibited markedly higher antioxidant activities of SOD, POD, and ascor-
bate peroxidase (APX) under Cd stress. Moreover, the levels of nonenzymatic antioxidants such
as ascorbic acid, phenolics, flavonoids and proline were also higher in plants under Cd toxic-
ity. However, the activities of these antioxidant enzymes were more prominent in resistant cv.
Shabnam-786 than sensitive cv. Arka anamika (Rasheed etal. 2018). Metallothioneins are low
molecular weight, cysteine-rich metal binding proteins, which has been reported to play a major
physiological role in metal homeostasis and protect plants from oxidative damage through ROS
scavenging and sequestration of the HMs (Chaudhary etal., 2018). In this context, rice seed-
lings exposed to Cr toxicity manifested higher concentration of Metallothioneins (Yu etal., 2019).
Plants alleviate metal toxicity through activation of chaperones that protects and repair proteins
and play a key role in maintaining cellular homeostasis. Moreover, chaperones like HSP70 also
assist metallothioneins in sequestration and detoxification of metal ions (Haap etal., 2016).
References 151
8. Conclusion
The presence of heavy metals (HMs) in agricultural soils and the food chain are detrimen-
tal to plants and human health, which is a significant concern. Albeit, HMs are present in soil
naturally; however, many anthropogenic activities release excessive amounts of HMs into
the environment, posing a serious threat to environmental quality and agricultural yield.
This chapter implies that HMs stress negatively affects various metabolic processes in plants,
resulting in reduced plant growth and productivity. Heavy metal stress causes a reduction
in germination, seedling growth, shoot and root length, fresh and dry biomass, and chlo-
rophyll content. Moreover, HM toxicity impedes various processes such as photosynthesis,
respiration, and mineral nutrition in plants. Heavy metal toxicity causes overproduction of
ROS, which interact and damage vital cellular components such as nucleic acid, proteins, and
lipids. Plants cope with HM toxicity through modulation in the antioxidant system and the
accumulation of different secondary metabolites and osmolytes. However, the responses of
plants to HM toxicity were specific to their genotype, species, and growth stages.
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