Environ Sci Pollut Res (2015) 22:18318–18332
DOI 10.1007/s11356-015-5463-x
REVIEW ARTICLE
Lead toxicity in rice: effects, mechanisms, and mitigation
strategies—a mini review
Umair Ashraf 1,2 & Adam Sheka Kanu 1,2 & Zhaowen Mo 1,2 & Saddam Hussain 3 &
Shakeel Ahmad Anjum 4 & Imran Khan 4 & Rana Nadeem Abbas 4 & Xiangru Tang 1,2
Received: 6 February 2015 / Accepted: 21 September 2015 / Published online: 3 October 2015
# Springer-Verlag Berlin Heidelberg 2015
Abstract Lead (Pb) is a major environmental pollutant that
affects plant morpho-physiological and biochemical attri-
butes. Its higher levels in the environment are not only toxic
to human beings but also harmful for plants and soil microbes.
We have reviewed the uptake, translocation, and accumulation
mechanisms of Pb and its toxic effects on germination,
growth, yield, nutrient relation, photosynthesis, respiration,
oxidative damage, and antioxidant defense system of rice.
Lead toxicity hampers rice germination, root/shoot length,
growth, and final yield. It reduces nutrient uptake through
roots, disrupts chloroplastic ultrastructure and cell membrane
permeability, induces alterations in leaves respiratory activi-
ties, produces reactive oxygen species (ROS), and triggers
some enzyme and non-enzymatic antioxidants (as defense to
oxidative damage). In the end, biochar amendments and
phytoremediation technologies have been proposed as soil
remediation approaches for Pb tainted soils.
Responsible editor: Elena Maestri
* Xiangru Tang
tangxr@scau.edu.cn
1
Department of Crop science and Technology, College of Agriculture,
South China Agricultural University, Guangzhou 510642, People’s
Republic of China
2
Scientific Observing and Experimental Station of Crop cultivation in
South China, Ministry of Agriculture, Guangzhou 510642,
Guangdong, People’s Republic of China
3
College of Resources and Environment, Huazhong Agricultural
University, Wuhan 430070, Hubei, People’s Republic of China
4
Department of Agronomy, University of Agriculture,
Faisalabad 38040, Punjab, Pakistan
Keywords Biochar . Lead . Photosynthesis .
Phytoremediation . Respiration . Rice
Introduction
After industrial revolution and ever increasing urbanization,
there has been a consistent addition of heavy metals (HMs) in
the environment, which is now becoming a challenge to pro-
duce from the contaminated soil (Govil et al. 2008; Granero
and Domingo 2002). Industrial processing, mining, automo-
biles, use of synthetic fertilizers, and other agro-chemicals are
building pools of various heavy metals of which lead (Pb),
cadmium (Cd), arsenic (As), and mercury (Hg), are of major
concerns (Huang et al. 2007; Li et al. 2008). HMs cause del-
eterious impacts on human health, soil life, plant metabolism,
and other aquatic and terrestrial ecosystems (Grimm et al.
2008). HMs in agricultural lands may transfer to consumer’s
body through soil-plant-food interaction and may cause some
serious defects and abnormalities (Chaney et al. 2004). Dif-
ferent types of pollutants vary in their speciations, specifica-
tions, concentrations, and toxicity levels posing a serious
threat to agricultural productivity, thus targeting a wide range
of crop plants (Arshad et al. 2008). Among various HMs that
affect plants, lead is one of the most hazardous metal and
ranked second after arsenic due to its potential of toxicity to
plants and human beings as well as occurrence and distribu-
tion over the globe (ATSDR 2003; Grover et al. 2010; Shahid
et al. 2011).
Lead is being added and accumulating profoundly in the
soil through anthropogenic activities (Alloway 2013; Mulli-
gan et al. 2001). Its eminency results from its current and
previous sources and its persistency in the soil (Andra et al.
2009; Punamiya et al. 2010). Agency for Toxic Substances
and Disease Registry (ATSDR 2003) ranked lead as the
Environ Sci Pollut Res (2015) 22:18318–18332
second most harmful element due to its occurrence, toxicity,
and exposure potential, after arsenic. Being a toxic substance,
and having high transfer rates (from soil to plant), it is there-
fore studied broadly especially in context to food safety, qual-
ity, and biotesting purposes (Uzu et al. 2009). It adversely
affects plant’s morpho-physiological and biochemical pro-
cesses such as seed germination and seedling growth, plant
phenology, and root/shoot ratio; disrupts cell membrane per-
meability, photosynthesis, plant respiratory processes, chloro-
phyll contents, chloroplastic lamellar organization and cell
division; and cause growth and developmental abnormalities
as well as ultrastructure changes (Dogan et al. 2009; Ling and
Hong 2009; Gupta et al. 2009, 2010; Maestri et al. 2010). It
further results in ROS production such as superoxide radicals
(O−2), hydroxyl radicals (•OH), and hydrogen peroxide
(H2O2) that react with micro and macro cellular organelles
to cause cell damage (Reddy et al. 2005). However, its effec-
tiveness depends on stress intensity and duration, plant stage
of stress exposure, lead concentration, and its bioavailability
in plant organs. Plants have their own metal uptake, accumu-
lation, translocation, detoxification, excretion, and compart-
mentalization mechanisms to respond to lead toxicity (Jiang
and Liu 2010). There is a wide range of genotypic variation
existing among rice plants regarding uptake, translocation,
and accumulation of Pb (Cheng et al. 2006). A study conduct-
ed by Liu et al. (2013) in China confirmed the genotypic-
specific behavior of rice regarding Pb translocation from roots
to shoot with higher translocation factors (TF) in hybrid indica
followed by indica and japonica.
Rice, a major food crop in many Asian regions, is now
prone to heavy metal toxicity due to recurrent usage of
metal-enriched agro-chemicals, frequent use of waste water,
and sewage sludge (as organic amendments), which devel-
oped pools of heavy metals within the soil (Fangmin et al.
2006). Pb accumulation in rice pronouncedly reduced leaf
chlorophyll, protein and nitrogen contents, carotenes, and hill
reaction while enhanced various enzymatic activities like cat-
alase, ribonuclease, and acid phosphatase (Chatterjee et al.
2004). Moreover, Pb accumulation in rice grains also employ
quality issues and adverse health complications (Shraim
2014). Fangmin et al. (2006) collected rice grain samples from
different regions of China and found the eminent Pb concen-
trations (> 0.2 mg kg−1) in rice grains. In a recent study,
Shraim (2014) reported high levels of Pb in rice grains col-
lected from USA (0.014–0.098 mg kg−1), Egypt (0.015–
0.031 mg kg−1), Pakistan (0.018–0.022 mg kg−1), India
(0.003–0.218 mg kg−1), and Thailand (0.012–0.02 mg kg−1).
So, increased lead contents in rice raised rice quality and food
security issues. Soil contamination with Pb and its subsequent
translocation and accumulation in rice plants (especially in
grains) and its subsequent effects on human health has previ-
ously been reported by various researchers (Davis et al. 1993;
Feng et al. 2011; Liu et al. 2013); however, further research is
18319
being employed nowadays on affects and speciation of Pb in
rice and its consequences on cell to whole plant level to de-
velop Pb-tolerant strains of rice which can store more Pb con-
tents within the roots and transfer its minimum to the edible
part to ensure food quality. In this review, we discussed Pb
uptake, accumulation, and translocation mechanism; its effect
on rice morphology and physiology; and some possible man-
agement strategies to alleviate Pb contamination in soil.
Uptake, translocation, and accumulation
mechanisms of lead
Plant characteristics like root surface area, root exudates, tran-
spiration pull, mycorrhizal associations in the rhizosphere, and
diversities of root varieties may affect lead solubility in the soil
and its availability and uptake mechanism by plants (Davies
1995). There have been a significant difference of lead uptake
and translocation was observed in different rice cultivars and
found a decreasing trend of lead content from roots to rice
grains and reported a significant but negative as well as pos-
itive correlation among connected and disconnected organs of
rice for their accumulated lead contents, respectively (Liu
et al. 2003).
The sensitivity and tolerance index of rice against Pb stress
mainly depends on uptake of Pb from the soil and internal
sequestration of the plants (Rout et al. 2001). Roots are the
first organ exposed to Pb and thus can be a major storage
organ for Pb (mostly in tolerant cultivars) or can play an in-
termediary role for exporting the Pb ions from soil to the
aboveground plant parts (in case of sensitive cultivars)
(Fangmin et al. 2006). Unlike some other higher plants, i.e.,
maize (Anjum et al. 2015) and Brassica (Ali et al. 2014), rice
is neither a better metal accumulator (plants that are able to
biodegrade or biotransform the pollutants/contaminants from
active to inactive form in their tissues and may survive even at
high levels of contaminates in their tissues) nor a good metal
excluders (that restrain the uptake of contaminants in to their
organs and avoid to make a part of their biomass; however,
can be regarded as a good indicator (translocate and accumu-
late metals to different organs depending on the environmental
toxicity and genotype) (Liu et al. 2003). However, different
rice genotypes show differential uptake and translocation
properties. Some rice genotypes (Pb-tolerant) prefer roots as
a major storage organ for Pb and transport a little toward
shoots while others accrue more in shoots (Pb-sensitive) than
roots (Zeng et al. 2008). They further observed a large varietal
difference in grain Pb contents under no and marginally Pb-
contaminated soils.
Interestingly, uptake, translocation, and storage mecha-
nisms of toxic metals (whose chemical properties pretend to
those of essential nutrients) in plants is similar as for micro-
nutrient acquisition by plants from the soil. Generally, rice
18320
acquire essential micro-nutrients from the soil through roots
(even at low concentrations) supported by soil pH, soil organ-
ic matter content, redox reactions, and chelating agents of
plant origin that solubilize the micronutrients within rhizo-
sphere, the same mechanism is used for Pb uptake (Zhang
et al. 1997; Yang et al. 2004; Hseu et al. 2010); however, there
are several factors that affect the lead uptake from the soil
presented in Fig. 1.
Pb2+ ions present in the soil solution when adsorbed to the
root surface not only disturb uptake of mineral nutrition by
roots but also enters passively into the roots of rice plants by
following translocating water streams (Cheng et al. 2006).
However, it is not adsorbed uniformly along roots, yet highest
adsorption of lead has been observed in young cells having
thin cell wall at root apices (except root cap cells) which assist
Pb uptake (Wang and Wu 1997). Additionally, the lowest
rhizodermic pH at root apices enhances lead solubility in the
soil solution. Lead may enter into the plants through a range of
pathways which include proton pumps, co- and anti-trans-
porters, and ionic channels.
In roots, H+ ATPase and H+ pumps are directly involved in
the plant response to Pb2+ toxicity and help to maintain a
negative membrane potential of root rhizodermal cells (Wang
et al. 2007). The involvement of H+/ATPase pumps was lately
confirmed by Zhang et al. (2011) under nutrient deficit condi-
tions in rice roots with 30 % increase in plasma membrane
(PM) H+ ATPase and 70 % increase in proton pumping activities.
However, such reports in rice under lead stress have not been
explored yet. On the other hand, Pb2+ may use calcium
permeable channels on rice root cells to enter in the plant system
but its movement is related with its competition with Ca2+
present in the soil solution. Further, Ca2+ helps rice to pervert
Pb translocation and its ultimate toxic effects on rice roots
(Kim et al. 2002).
Fig. 1 Factors affecting Pb uptake mechanism in rice (modified from
Tangahu et al. 2011)
Environ Sci Pollut Res (2015) 22:18318–18332
After uptake, lead moves to aerial parts of the plants. The
amount of lead that is taken up by the plants can be measured
in term of Bthe transfer factor (TF) [ratio between plant lead
contents to root lead]^ or Bthe bioconcentration factor [ratio
between plant lead contents to soil lead]^ which differs with
plant species and soil types (Bi et al. 2010; Liu et al. 2010).
This translocation of metallic ions is an important clue to
represent the metal uptake from soil and its speciation within
rice plant. Generally, crop plants needs trace amounts (10 to
15 ppm) of metals for metabolic activities, but with exceptions
of hyper-accumulators that accumulate metallic ions up to
thousands of ppm) and thrive to attain high biomass even in
toxic environments (U. S. Department of Energy 1994). Plants
can be divided into two categories based on transfer factors of
metallic ions a) non-accumulators (TF < 1) and hyper-
accumulators (TF > 1). Rice itself is a non-accumulator of
Pb with TF values are less than 1. Nonetheless, the varietal
differences regarding Pb translocation might be associated to
the differences in Pb forms within the rice plant, Pb loading
capacity, and possible transformations in the xylem tissues
(Liu et al. 2003, 2013).
Often, plant roots absorbed lead (as they are first that come
into contact) and its movement toward aerial parts Verma and
Dubey (2003) implicated that a major part of the absorbed
lead is localized within rice root cells while a small fraction
is transported toward shoots where it is distributed in organ
specific manner to different parts. However, even within root
cells of rice, Pb is unevenly distributed where root cells hinder
the apoplastic and symplastic transport of Pb to restricts its
translocation toward shoots. They further explored the partial-
ly halophytic nature of rice which accrues Pb against concen-
tration gradient. Endoderm (as a physical barrier), blocked
lead transport through it by Casperian strips and force to fol-
low symplastic pathway. Indeed, transpiration pull drives lead
ions from root to shoot via xylem (Liao et al. 2006) while from
shoot to leaves via vascular flow (Krzesłowska et al. 2010);
nonetheless, amount of transported Pb is genotype specific
(Liu et al. 2003). However, these reasons are not enough to
explain the complete phenomenon of low translocation rate
from root to aboveground plant parts. The exact lead uptake
mechanism at molecular level is still unidentified. So, in-depth
studies are still needed in future to explore the complete up-
take, accumulation, translocation, and exclusion mechanisms
of lead at molecular and gene level by transcriptomic,
metabolomic and genomic studies.
Effect of Pb on rice
Pb impairs rice growth and yield by altering its physiological
and biochemical attributes. Effects are evident at all growth
stages from germination to maturity. Some of the effects of Pb
Environ Sci Pollut Res (2015) 22:18318–18332
toxicity on rice and its extent of damage is elaborated in the
following section.
Germination, growth, and yield
Lead adversely affects seed germination, root/shoot ratio, and
their fresh and dry weight in rice (Mishra and Choudhari
1998). The effects were more adverse at higher concentrations
of Pb2+ (Zeng et al. 2006). A significant inhibition in morpho-
logical response and photosynthetic pigments with higher bio-
accumulation of Pb in roots and ultrastructural aberrations in
pollens were observed in two contrastive rice cultivars Pokkali
and IRRI-112 against Pb stress (Arce and Yllano 2008).
Pb2+ at 0.5 to 1 mM significantly inhibited rice root length
(about 40 %) in 20-day-old rice seedlings demolished viability
of rice root cells and promoted cell death by triggering ROS
production (Verma and Dubey 2003). Yang et al. (2000) found
a rapid development of adventitious roots and 10-fold higher
root biomass with low Pb and higher oxalate contents in tol-
erant rice cultivars than sensitive ones which suggest that ox-
alate compounds are involved in reduced uptake of Pb. They
further accentuated that exogenous feeding of oxalate to the
growing medium ameliorate the Pb-induced root inhibition in
rice. Pb inhibits rice seedling growth and viability and
upregulates ROS production; however, enhanced Ca2+ accu-
mulation, myelin basic protein (MBP) kinase (a signaling
pathway for systematic responses under stress conditions) ac-
tivities, calcium-dependent protein kinase (CDPK) (involved
in rapid biochemical activation under abiotic stresses) inhibits
Pb-induced cell death and mitogen-activated protein (MAP)
kinase activation (one of the main pathways by which extra-
cellular stimuli are transduced into intracellular responses)
(Huang and Huang 2008).
Rice growth and yield reduced when exposed to lead. Pb2+
in the soil (1000 ppm) not only reduced rice biomass but also
paddy yield about 12 % (Gu et al. 1989). In a study conducted
by Xie and Huang (1994), they found that lead, even at
2500 ppm, did not affect the growth of a hybrid rice genotype
named BShan you 63.^ Moreover, increased rice biomass and
yield in rice at 100 ppm has also been reported by (Wang and
Wu 1997). Conversely, Li et al. (2007) found significant re-
ductions in rice growth and yield at 1200 mg of lead kg−1 of
soil than control and found lower Pb2+ contents in rice grains
than root, shoot, and leaves. About 1216, 179, and 62 times
higher lead contents were recorded in roots, stems, and leaves,
respectively, than grains at maturity (Liu et al. 2003). So, a
great variation exists among lead concentration within plant
parts. Normally, lead concentration is recorded from max-
imum to minimum in the following order: root > shoot >
ear (up to heading stage) > grain (at ripening stage). Dif-
ferential response of rice to varying lead concentrations is
represented in Table 1.
18321
The degree of variation among these parts significantly
depends on soil lead concentration and plant growth stages.
Furthermore, grain lead concentration significantly correlates
with shoot and ear lead contents at heading stage (Liu et al.
2013). A positive correlation between grain yield vs straw
yield and grain yield vs spikelets per panicle exhibited that if
paddy yield reduced due to lead toxicity, then rice biomass
will also reduce under Pb toxic conditions whereas relative
changes of grain yield have a significant correlation with
changes in spikelet numbers produced (Fig. 2).
Plant-nutrient relationship
Lead toxicity in soil impaired plant nutrition, affects plant-
nutrient relationship (Gopal and Rizvi 2008), and changes
internal nutrient ratios among the plant tissues (Kabata-
Pendias and Pendias 1992). Research done so far regarding
lead toxicity and its relation with plant mineral nutrition is not
enough to make a definite conclusion about lead mechanism
of nutrition imbalance; but it can be stated from the previous
work that lead influences mineral uptake by plants. It restricts
the entry of divalent cations such as Ca2+, Mg2+, Fe2+, Zn2+,
and Mn2+ and anions like NO3− in various plants including
rice (Chatterjee et al. 2004). Two mechanisms might be in-
volved in reduced uptake of mineral nutrients. First mecha-
nism known as physical depends on size of metal ions and
second is the chemical one that might be due to metal-induced
changes in the cell metabolism by disrupting cell membrane
and alteration in enzymatic activities. Efflux of K+ ions from
roots showed sensitivity of K+-ATPase and -SH groups of
plasma membrane to Pb is an example of the second type of
mechanism (Sharma and Dubey 2005). However, it is hard to
conclude that reduction in ion uptake is due to blockage of
nutrients through roots, reduction in translocation from roots
to shoots, or alteration in distribution pattern of metal ions in
the plants.
Mostly, lead effects on mineral accumulation in aerial
plant parts are similar and follow a common trend while in
roots, it varies among plant species to species and amount of
lead in the soil/rhizosphere (López et al. 2007; Gopal and
Rizvi 2008). Reduced mineral uptake caused by Pb might be
due to competition between metal ions of similar size to lead
like K+ ions with Pb (almost similar atomic radii) or fluctu-
ations in plant physiological functions (Sharma and Dubey
2005). Further, phosphorous is negatively correlated with
soil Pb contents (Paivoke 2002). Pb lowers the nitrate uptake
from the soil but did not cause nitrogen efflux out of the
plant cells. The reduction in nitrogen contents in plants ex-
posed to Pb stress might be induced by the reduced nitrate
reductase activity (the rate-limiting enzyme in nitrate assim-
ilation) (Xiong et al. 2006; Sengar et al. 2009). A significant
reduction in nitrate in paddy soils and nitrate reductase ac-
tivity in rice seedlings under lead-polluted medium were
18322 Environ Sci Pollut Res (2015) 22:18318–18332

Table 1 Differential response of rice under Pb stress

Sr. # Factor studied Experiment type Experimental Findings Reference

Location

1 Single and combined Green house study (pot Beijing (China) Rice biomass production did not reduced (Yizong et al. 2009)
(Cu, Cd, and Pb stress) experiment) significantly either in single or combined
in rice stress of Cu, Cd, and Pb but increased
concentrations of the respective element in
root and shoot were noted. In combined
stress, Pb enhanced Cu and Cd uptake in
roots and shoot, Cu contamination
stimulated Pb and Cd concentration in
roots, while Pb contents were not affected
in rice plants exposed to Cd stress
2 Pb, Cd, Cr, Zn, and Cu Field investigation Nanjing (China) A substantial difference in metal ions (Pb, (Feng et al. 2011)
contaminants uptake in (exposed) and green Cd, and Zn in leaves, only Zn in stem and
exposed and un- house (unexposed) rice; Pb and Cd in grains) were recorded
exposed rice plants a comparative study) between stressed and non-stressed rice
plants. A significant accumulation of Pb
and Cd (46 and 41 %, respectively) while
non-significant accumulation of Cr, Zn,
and Cu were recorded in rice grain though
foliar uptake from the atmosphere. Apart
from Zn, all other HMs (under study)
ascribed to the uptake through roots, while
leaves accumulated a significant
concentrations of Pb and Cd from external
atmosphere
3 Cd and Pb stress with Field experiment Jiangsu (China) Cd and Pb uptake significantly affected (Bian et al. 2014)
biochar amendments by biochar amendments in the
in rice contaminated soil. Cd contents in
different tissues and Pb concentration
only in root tissues of rice reduced
appreciably, depending upon rate of
biochar application. It further reduced
extractable Cd and Pb contents of the
soil
4 Moisture/water content Laboratory work (Geel) Belgium Moisture/water content corrections have a (Vassileva and
corrections in crucial role (60 % for Cu, 25 % for Cd, Que’tel 2008)
(saturated and non- and 7 % for Pb) in non-saturated rice
saturated rice samples) samples while less than 1 % degree of
and cadmium, copper, uncertainty on dry mass correction was
and lead fractions observed for the saturated rice samples.
However, principles of sample saturation
with water before processing may lead to
some technical hitches and sample
contamination risks
5 Lead (0, 50, 100, and Lab experiment Shenyang (China) Rice shoot length, rice biomass, chlorophyll (Li et al. 2012)
200 M) under and carotenoid contents, net
endophyte-infected photosynthesis, transpiration rate, Fv/Fm
and non-infected rice ratio, antioxidant activity (SOD, CAT,
seedlings POD) was higher while MDA levels found
lower in case of endophyte-infected rice
seedlings than non-infected under Pb stress
6 Lead (500 and Pot experiment Jiangsu (China) Grain Pb concentration significantly (Liu et al. 2013)
1000 mg kg−1) Rice correlated with rice shoot and ear lead
cultivars: concentration while not with root lead
Liangyoupeijiu, contents. Among rice cultivars,
Shanyou 63 (Hybrid translocation factor (TF) of Pb was
Indica); CV6, Yangdao higher from shoot to grains than from
6 (Indica); Wuyunjing root to shoot. TF from shoot to rice
7, Yu 44 (Japonica) grains was in the following order:
japonica < indica < hybrid indica.
However, TF of lead from root to shoot
was non-significant
Environ Sci Pollut Res (2015) 22:18318–18332 18323

Table 1 (continued)

Sr. # Factor studied Experiment type Experimental Findings Reference

Location

7 Pb toxicity levels: 0, 100, Pot experiment Hangzhou (China) Soil microbial activity and leaves chlorophyll (Zeng et al. 2006)
300, 500, 700, and contents increased initially than further
900 mg kg−1 of soil increase in Pb toxicity (> 500 mg kg−1 of
soil) inhibited soil microbial activity (that
might also be related to soil clay particles
and organic matter contents) and caused
oxidative damage to rice plants
8 Control, 200, 400, 800, Pot experiment Hangzhou (China) Lead concentration in different plant parts (Li et al. 2007)
1200 mg of Pb kg−1 increased linearly with Pb toxicity. Roots
soil (Ultisol and accumulated more Pb followed by stalk,
Inceptisol) leaves, and grains. Moreover, effects was
more obvious in Ultisol than Inceptisol
9 Pb (Control, 500 and Pot experiment Jiangsu (China) Higher levels of lead toxicity reduced rice (Liu et al. 2011)
1000 mg kg−1 soil) biomass, root/shoot length while enhanced
Rice cultivars: root lead concentration in all three rice
Shanyou 63 (Hybrod cultivars. The root Pb accumulation were
Indica),Yangdao 6 recorded as: Wuyunjing 7 < Yangdao 6 <
(indica) and Shanyou 63. Futher, it was found that rice
Wuyunjing 7 cultivars with japonica consanguinity were
(japonica) proved more tolerant than indica
consanguinity
10 Pb levels: 0 (CK), 100, Pot experiment Hangzhou (China) Lead toxicity at higher levels impaired plant (Zeng et al. 2007)
300, 500, 700, and physiological parameters and soil
900 mg/kg soil microbial activity as well. However,
initially, rice biomass and chlorophyll
contents consistently increased, reached its
peak at a specific lead concentration, then
decreased gradually. Pb also induced
proline accumulation
11 Lead (Control, Pot experiment Jiangsu (China) Paddy yield fluctuations correlated with (Liu et al. 2003)
800 mg kg−1); Rice spikelets per panicle which otherwise
cultivars: CV5, CV6, positively related with dry straw biomass
NPT3, IR36 of rice that significantly affected by Pb
(Philippines), Yang toxicity. Different rice cultivars showed
dao No. 6, Nan jing different Pb uptake and translocation rates.
No. 11, Liang you pei Generally, Pb contents decreased from
jiu, Shan you 63, Wu roots (highest) to grains (lowest). At
yu jing No. 3, 9520, heading stage, lead in leaves significantly
Guang ling xiang jing, and positively correlated with grain lead
Y49, Zhen dao 88, contents at maturity. Moreover, Pb in
Nong ken 57, Xiao li te grains is not uniformly distributed and out
hao (China), Z35, Yu of total Pb accumulated by grains about
44 (Japan), H01, H04, 33 % was present in polished rice
H02 (Korea)
12 138 rice cultivars grown Field experiment Jiaxing (China) Substantial genotypic difference among all (Zeng et al. 2008)
in Cr, Cd, and Pb 138 cultivars were observed regarding
(slightly, moderately grain Cr, Cd, and Pb contents. HMs in rice
and highly) toxic soils grains are related to genotype and
environmental (soil type; in this case)
interaction. Among these three HMs, grain
Cr-contents are not correlated with Cd and
Pb while a significant interaction were
noted between Cd and Pb concentration in
rice grains grown in contaminated soil

also reported by Tariq and Rashid (2013) and Sharma and conclude regarding nutrient relation with Pb toxicity as
Dubey (2005). However, Burzynski and Grabowski (1984) much work is still needed to explore the uptake and trans-
concluded that decline in nitrate uptake might be due to location mechanisms of nutrients, and plant-nutrient relation
moisture stress caused by Pb in the soil. So, it is hard to grown in lead-contaminated soil.
18324
Fig. 2 Correlation between
relative changes (RC) of a grain
yields vs straw weights and b
grain yield vs spikelets per
panicle of rice exposed to Pb
stress over control. r** indicates
significance at P≤0.01 (Liu et al.
2003)
Photosynthetic activity and related attributes
Lead, being a heavy metal, interacts with photosynthetic ma-
chinery during plant development, i.e., hyper-accumulation in
leaves and then subsequent partitioning in to various leaf tis-
sues, e.g., stomata and leaf mesophyll, interacts with cytosolic
enzymes and their functions, chloroplast and acyl lipid mem-
branes, interfere with PS II and PS I, as well as interferes at
molecular level with normal physio-anatomical and biochem-
ical functions (Prasad and Strzałka 1999). Lead toxicity
inhibited photosynthesis adversely by distortion of chloroplast
structure, reduction in rate of chlorophyll, plastoquinone and
carotenoid synthesis, disruption of electron transport chain,
cause CO2 deficiency by stomatal closure, and reduction in
the enzymatic activity of Calvin cycle (Xiong et al. 2006;
Singh et al. 2010). It also causes changes in lipid composition
of thylakoid membranes in the chloroplasts (Stefanov et al.
1995). Pb diminished chlorophyll production by reduced up-
take of Mg and Fe (essential components of chlorophyll)
(Burzynski 1987).
The main reasons of reduced photosynthetic activity due to
Pb may be the affinity of lead for protein N and S ligands;
cause damage to chloroplastic ultrastructure (Islam et al.
2007); hindrance in the electron transport chain (ETC) reac-
tions (Qufei and Fashui 2009); breakdown of chlorophyll con-
tents by enhanced activity of chlorophyllase (Liu et al. 2008);
inhibition and substitution of Mg and Fe by Pb (divalent cat-
ions) in chlorophyll (Chatterjee et al. 2004; Cenkci et al.
2010); reduced activities of ferredoxin NADP+ reductase as
well as delta-aminolevulinic acid dehydratase at the source of
chlorophyll production (Gupta et al. 2009); reduced CO2
levels due to stomatal closure (Romanowska et al. 2006);
plastoquinone and carotenoid inhibition (Chen et al. 2007;
Cenkci et al. 2010); and inhibited enzymatic catalysis of Cal-
vin cycle (Liu et al. 2008).
The effect of Pb toxicity on photosynthetic machinery
varies with rice genotype. Normally, chlorophyll b is more
prone to distortion under Pb-stressed conditions than chloro-
phyll a (Xiong et al. 2006). Pb effects on PS I, cytochrome b/f
complex, as well as donor and acceptor sites of PS II. Further,
it was reported that electron transport of PS II is more
Environ Sci Pollut Res (2015) 22:18318–18332
susceptible to Pb than PS I (Sersen et al. 1998). Pb displaces
Cl−, Ca2+ and Mn2+ from oxygen evolving complex of PS II
and cause its dissociation (Rashid et al. 1991). In vitro con-
formational changes have been observed in the subunits of
light-harvesting chlorophyll (LHC) following Pb binding
(Ahmed and Tajmir-Riahi 1993). The possible effect of Pb
stress on photosynthesis has been shown in Fig. 3.
The process of chlorophyll cessation is catalyze by
chlorophyllase, pheophorbide oxygenase, red chlorophyll ca-
tabolite reductase, and Mg-dechelatase that dissociates it in to
magnesium, phytol, and product of porphyrin after primary
cleavage, that is also responsible for chlorophyll bleaching
(loss of green color) (Harpaz-Saad et al. 2007). However, in
a study conducted by Bazzaz et al. (1975), it was reported that
inhibition of photosynthesis due to Pb may be due to stomatal
closure and not because of direct effect of Pb on photosynthe-
sis (Fig. 4).
Respiratory activities and energy transformations
The exact mechanisms of respiratory activities and energy
transformations of rice under Pb stress are not known yet;
however, some previous studies about C3 plants can guide
us for understandings the rice anatomical features and energy
imbalances induced by Pb. Lead impairs respiratory activities
and adenosine triphosphate (ATP) contents and induces
alterations in leaves respiratory activities; however, effects
on root respiratory activities are still unidentified. For
example, van Assche and Clijsters (1990) argued that lead
toxicity in C3 plants inhibits ribulose-bisphosphate carboxyl-
ase; thus, reduced C-assimilation without damaging oxygen-
ase activity consequently reduces photosynthetic rates, which
may result an increase in photorespiration/photosynthesis ra-
tio as Pb do not affect photorespiration (a harmful indication
for plants exposed to lead toxicity); however, the exact mech-
anisms at cellular levels of Pb toxicity to disrupt
photosynthetic and respiratory activities in rice has not been
reported yet. Nonetheless, being C3, rice might also be
assumed to show similar responses as other C3 plants show,
but still, concomitant work is needed before deducting any
inference. Romanowska et al. (2005, 2006) also concluded
Environ Sci Pollut Res (2015) 22:18318–18332
Fig. 3 Possible mechanisms of Pb2+ stress on photosynthetic and transpiration activities in rice. (−) Decrease/inhibition; (+) Increase/activation (revised
from: Ashraf et al. 2010)
that Pb accelerates respiratory processes by increasing dark or
mitochondrial respiration without affecting photorespiration.
Additionally, increased rate of respiration in lead-prone plants
are correlated with ATP production in mitochondria, energy
that is used by plants to survive under lead stress. Increase in
ATPs and ATP/ADP ratio has also been reported in the leaves
of Pb-treated C3 plants. Up to 50 % increase in respiration and
fully oxidized substrates (glycine, succinate, and malate) in
mitochondria of isolated leaves of some C3 and C4 plants
was recorded by Romanowska et al. (2002) exposed to
5 mM Pb (NO3)2 for 1 day (24 h).
Although Pb affects photophosphorylation, their site of ac-
tion and its related mechanisms in rice are still unidentified.
Mostly divalent cations such as Pb, Cd, Ni, Zn, and Co may
bind to mitochondrial membranes and cause decoupling of
phosphorylation by disrupting electron transport chain reac-
tions. It triggers NAD+-malate dehydrogenase activity in
leaves’ protoplasts, hampered hill reaction, and severely af-
fects cyclic photophosphorylation than noncyclic photophos-
phorylation (Romanowska et al. 2002). Along with damaging
secondary structures of PSII, Pb+ also blocked energy transfer
pathways among amino acids and renders absorption of visi-
ble light (Qufei and Fashui 2009). Pb also caused swelling of
mitochondria, vacuolization of dictyosomes and endoplasmic
reticulum, and damage to cristae (Jiang and Liu 2010). Pb
toxicity significantly inhibits the leaf development, guard
cells, chlorophyll development, and cell wall elasticity and
thus resulted in reduced growth and abnormal plant
18325
functioning. Some studies explored the toxic effects of Pb
on chloroplastic and mitochondrial structures, but to know
about specific mechanisms of Pb on respiration, further re-
search is needed.
Oxidative damage and antioxidant defense
HMs toxicity including lead (Pb) quite often leads to the gen-
eration of reactive oxygen species (ROS) in rice that might be
generated during cell metabolic processes, may appear as a
byproduct of reduced form of molecular oxygen O2 or due to
excitation of highly energized molecules. The ROS may in-
clude superoxide anion radicals (O−2), hydroxyl radicals (OH),
hydrogen peroxide (H2O2), and alkoxy radicals (RO) (Munné-
Bosch and Penuelas 2003). The over production of these spe-
cies in plants is regarded as oxidative stress, a renowned fea-
ture of Pb stress (Liu et al. 2008; Yadav 2010). However, the
degree of damage due to ROS depends on metal stress level, its
type and form, plant nature, and time of exposure, etc. ROS
react with cell membranes, organelles, and biomolecules like
proteins, lipids, chloroplasts, nucleic acids (DNA or RNA),
and diminished cell normal functions, induced cell abnormal-
ities and death (Clemens 2006; Singh et al. 2010).
Lead impaired cell membrane structures by interfering with
lipid bilayer, changing its composition and causing leakage of
K+, as polyunsaturated fatty acids and their esters are highly
vulnerable to ROS (Liu et al. 2008; Gupta et al. 2009). ROS
forms reactive aldehydes by eliminating H2 from unsaturated
18326
Fig. 4 Pictorial depiction of Pb ions adsorption on biochar surface (Lu
et al. 2012)
fatty acids and thus imparts cell membrane by distorting lipid
bilayer (Mishra et al. 2006). Pb ions thus cause lipid peroxi-
dation and reduce saturated fatty acids while enhances unsat-
urated fatty acid contents of plasma membranes in many plant
species including rice (Singh et al. 2010). ROS reacts with bis-
allylic hydrogens present on polyunsaturated fatty acids in
three different steps: (a) initiation (lipid radical formation),
(b) progression (lipid peroxyl radical formation as a product
of lipid radical + oxygen reaction), and (c) termination (pro-
duction of non-radical product after molecular reactions with
lipid peroxyl radicals) (Bhattacharjee 2005). Resultantly, these
changes in lipid membranes cause cell abnormalities by
disrupting cellular membranes (Gupta et al. 2009), cell organ-
elles like mitochondria, peroxisomes (Małecka et al. 2008),
and chloroplastic ultra structures (Hu et al. 2007). Lipid per-
oxidase activity was increased more than 170 % when rice
seedlings were exposed to Pb (NO3)2 for 20 days (Verma
and Dubey 2003). Under Pb stress, rice produces two types
of antioxidants (enzymatic and non-enzymatic) to protect the
oxidative damage of biomolecules from ROS. Enzymatic an-
tioxidants include superoxide dismutase (SOD), catalases
(CAT), and peroxidases. Moreover, peroxiredoxins (enzymes
of guthathion-ascorbate cycle) are also involved in ROS de-
fense mechanism against Pb stress to rice. Higher levels of Pb
Environ Sci Pollut Res (2015) 22:18318–18332
reduced CAT activity while triggered SOD, POD, and GR
activity in rice seedlings (Verma and Dubey 2003). Catalase
splits hydrogen peroxide (H2O2) to water (H2O) and molecular
oxygen (O2) while SOD reduced superoxides to H2O2 and O2,
thus proved as an initial scavenger to ROS under Pb toxicity.
Increased GR activity helps in lowering the oxidized glutathi-
one activity to its reduced form thus maintains reduced gluta-
thione pool in rice under Pb stress. Non-enzymatic compo-
nents involved ascorbate, tocopherols, carotenes, glutathione,
and cysteine (Verma and Dubey 2003). These components
also play a crucial role to relieve oxidative damage under Pb
stress but proved not as effective as enzymatic antioxidants.
So, activities of enzymatic and non-enzymatic antioxidants to
quench ROS in rice under Pb stress conditions are important.
Lead mitigation strategies
Lead, being toxic to human beings, plants, animals, and soil
microbes, creating an alarming situation specifically in indus-
trial regions over the globe (European Commission DG ENV
E3 2002). Being non-biodegradable, once entered, it remains
in the soil and has long-term effects (Pehlivan et al. 2009).
Leaded fuels, industrial wastes, and lead plumbing pipes are
among the most common sources of Pb that contaminate the
soil. Mostly, lead accumulated in the top 20-cm soil layer, so
its presence in the root zone may be too toxic for plants to
grow (Traunfeld and Clement 2001).
Environmentalists already developed several approaches to
combat these kind of HMs and some of them are already used
but not proved effective due to some financial and technical
constraints in their adoption. Chemical and thermal ap-
proaches to remediate HMs contamination are not only costly
and difficult to operate as these approaches produce a large
amount of sludge but also become a source of soil degradation
(Hinchman et al. 1998).
Soil washing and onsite management like excavation
followed by disposing off contaminated soil are also proved
not so effective and can transport HMs from one site to anoth-
er and thus renders land to be used as plant growth medium
(Gaur and Adholeya 2004). So, proper remedial actions are
necessary to undertake and remediate lead contents for safe
food production and to avoid ecosystem disruptions. Soil lead
contents can be remediated by following these approaches:
Biochar amendments
Biochar, a carbon-rich compound, is a product of biowaste
prepared under oxygen-limited conditions (pyrolysis) have a
great potential to amend the Pb-contaminated soils (Lehmann
2007). Immobilization of Pb in paddy soils and its hampered
accumulation in rice due to biochar application is recently
explored (Bian et al. 2013; Zhang et al. 2013). Due to its high
Environ Sci Pollut Res (2015) 22:18318–18332
pH, porosity, cation exchange capacity (CEC), and active
functional groups, biochar retain Pb to adsorb and allow it to
translocate to the plants (Zhang et al. 2013; Joseph et al.
2013). Immobilizing role of CEC in chemically mobile metals
under biochar-amended paddy fields are also reported by
Uchimiya et al. (2011). Some short-term studies on contami-
nated soils with biochar amendments showed a remarkable
reduction in rice lead contents; however, its long-term effects
on Pb immobilization and its reaction with biochar are not
analytically examined (Zhang et al. 2013). Biochar applica-
tion improved soil structure, productivity, and cycling of some
minerals (P, K, and Si) by improving soil pH and soil organic
carbon (SOC) contents (Biederman and Harpole 2012). Or-
ganic molecules, cations, and anions present in the soil can
form precipitates by reacting with metallic cations present at
the biochar’s surface. For example, PO4 ions may convert into
Pb5(PO4)3OH after reacting with surface-adsorbed Pb (Cao
et al. 2011). Moreover, metallic cations have high adherent
capacity than anions (Keiluweit et al. 2010; Lin et al. 2012).
Mostly, Pb adheres to clay particles through ionic, covalent,
and hydrogen bonding (Bradl 2004) (Fig. 5). A strong corre-
lation of non-electrostatic Pb adsorption to biochar is also
reported by (Jiang et al. 2012).
Based on crop productivity and soil remediation, biochar
application relates to plant growth and development, im-
proved soil structure, increased water holding capacity, and
enhanced soil microbial activity in Pb-contaminated soils
(Sohi et al. 2010). However, organic and inorganic amend-
ments, along with biochar application, are required in most
of the cases for soil structure improvement and land stabiliza-
tion (Steiner et al. 2008; Van Zwieten et al. 2010).
However, duality in biochar action (improvement and de-
cline) in relation to plant growth exists. Different biochars
have different retention capacities thus increase or decrease
in soil Pb and nutrient status depends on the nature of biochar
used; however, application of fertilizer along with biochar
improved plant growth (Novak et al. 2009). Some biochars
Fig. 5 Theoretical illustration
about uptake mechanism of heavy
metals (HMs) and remediation of
contaminated soil through
phytoremediation technology
(Source: Interstate Technology
and Regulatory Council 2009)
18327
can retain nutrients within the soil and thus may increase nu-
trient use efficiency and reduce leaching losses but may re-
duce the nutrients’ availability to plants in non-fertile soils as
well (Major et al. 2009). Biochar application can be beneficial
in excessive plant nutrition while detrimental in limited nutri-
ent conditions. However, application of biochar with some
organic amendments could be more beneficial for soil reme-
diation. It further maintains a balance between nutrient acqui-
sition and immobilization or exclusion of pollutants including
Pb, thus required growth and plant biomass is difficult to attain
from contaminated lands (Peltz et al. 2010).
Moreover, organic amendments like compost with biochars
having high CECs might be an attractive approach for reme-
diation of Pb-contaminated soils but their same mechanism to
retain nutrients should be kept in mind before application. In
sum, biochar is an eco-friendly approach to mitigate soil Pb
contents; thus, its circumspect use should be encouraged to
reduce the HM risks in agricultural lands.
Phytoremediation technologies
Phytoremediation consists of two words Phyto (from Greek
origin) means plants and remedium (from Latin origin)
means to correct or eliminate an evil (Erakhrumen and
Agbontalor 2007). Several researchers defined it according
to their own way but in the simplest way, BPhytoremediation
is the use of plants to improve degraded environments^
(Moreno et al. 2008). Plants used for phytoremediation pur-
poses can uptake both organic and inorganic contaminants
from the soil. For organic contaminants acquisition, it impli-
cates phytodegradation, phytostabilization, rhizofiltration,
phytovolatilization, and rhizodegradation. For inorganic con-
taminants, uptake mechanism may involve
phytoaccumulation, phytostabilization, phytovolatilization,
and rhizofiltration (Prasad and De Oliveira Freitas 2003).
Plants usually use following metal uptake mechanisms under
phytoremediation technologies:
18328
Phytodegradation
Phytodegradation or phytotransformation includes both inter-
nally (through metabolic processes) and externally (by secret-
ing some compounds in the soil through plant roots) break-
down of contaminants (Prasad and De Oliveira Freitas 2003).
Phytostabilization
It includes plants that demobilize and adsorbed the contami-
nants within soil matrix and curtails its migration within the
soil or their movement to other places by deflation or erosions.
Plants falling in this category absorb and accumulate contam-
inants within their tissues, adsorb them on the root surfaces,
precipitate them in the rhizosphere, limits organic and metallic
ions’ movement, and thus reduce their bioavailability to the
plants (Erdei et al. 2005; Erakhrumen and Agbontalor 2007).
Rhizofiltration
In this process, plants usually absorb and sequesterize the soil
contaminants and even excess nutrients (present in the soil
solution near root zone) into their roots (Erdei et al. 2005
and Ibeanusi 2004).
Phytovolatilization
Phytovolatilization is the uptake of soil contaminants by
plants and then excrete them through volatilization. Most-
ly, it includes trees that absorbs high water concentrations
along with soil contaminants through their roots and then
excrete them through leaves by transpiration. Usually, the
amount of contaminates lost by phytovolatization is com-
paratively low than that which is taken up by the plants
(Erdei et al. 2005).
Rhizodegradation
Rhizodegradation is the degradation of soil contaminants
through soil microbes present within the root zone of the
plants. Plants excrete some natural substances containing car-
bon, sugar, acids, and alcoholic contents, which microbes use
to accomplish their nutrition and energy requirements and
helps to establish a dense root system that absorbs water from
the soil in large quantities (Prasad and De Oliveira Freitas
2003).
Hence, in above-mentioned phytoremediation technolo-
gies, plant root zone in contaminated soils is very important
because all soil contaminants are acquired and metabolized by
the plants are absorbed and compartmentalized firstly through
roots (Fig. 5). Moreover, some of the contaminants are also
degraded by enzymes emanated through roots (Merkl et al.
2005). Micropores in the root cell wall may be the main path
Environ Sci Pollut Res (2015) 22:18318–18332
for soil contaminants to enter into the plant roots for further
degradation (Hinchman et al. 1998). In sum, phytoremediation
is the cheapest, socially acceptable, esthetically pleasant, low
cost, and eco-friendly approach in heavy metal-contaminated
soils and can easily be employed to remediate hazardous land.
Although phytoremediation technologies have their own
benefits regarding soil cleaning in an eco-friendly and cost-
effective way, there are some certain limitations that should
also be kept in mind before adopting them. Firstly, it is a time-
consuming technology that may require several years to clean
a specific site where the plants used for soil cleaning purposes
might suffer from severe phytotoxic conditions due to inter-
mediates of organic and inorganic contaminants in the soil
solution (Bozkurt et al. 1999). Secondly, the amount of am-
putated soil contaminants are dependent on harvestable yield
and biomass production of the plants that otherwise depend on
plant species used, climatic conditions, nature of containment
in the soil, and metal removal capacity of the plants (Liu et al.
2003). Thirdly, plant root depth and root-containment contact
is crucial to get access to the contaminants present in the soil.
Soils having contaminates in lower profiles should be cleaned
by plants with deep root system while presence with upper soil
layers can be remediated with plants with shallow root system
(Casentini et al. 2011). However, sites with shallow contami-
nation should avoid flooding or erosion (Bozkurt et al. 1999).
Fourthly, soil chemical properties, level of contamination, and
plant age also have a significant impact on soil cleaning by
phytoremediation. Healthy and young plants might remove
higher metal contents than older and weak plants (Liu et al.
2007). Finally, the harvested plant produce from the contam-
inated lands may be regarded as hazardous waste, so it should
be dispose off properly; however, consumption of contaminat-
ed plant produce by animals/insects/birds and entrance of
these contaminants again in to the food chains is a serious
cause of concern.
Conclusion
Lead is the major inorganic contaminant that is being used
since antiquity. Its presence in soil or atmosphere is harmful
for living beings. In soil, it forms complexes with soil ele-
ments, interferes with plant-soil-environment relationships. It
is unique in its behavior, mobility, form, and solubility within
the soil and bioavailability to the plants. Several soil factors
like CEC, soil mineralogy, soil pH, soil biological activity, and
redox conditions affects its fate in the soil. Pb once entered
through roots reduced growth and yield of rice. However, its
translocation from roots to shoots is low due to Casparian
strips (acting as barriers) and it compartmentalized in root cell.
A little concentration of Pb is also absorbed through leaves
from the atmosphere. However, grain Pb contents are lower
than shoot and root Pb contents. Excessive lead contents
Environ Sci Pollut Res (2015) 22:18318–18332
within the plants reduce rice biomass, hampers biosynthesis of
chlorophyll and photosynthesis, interferes with mineral up-
take, and affects respiratory activities of rice. However, the
severity of toxicity depends on intensity, duration of exposure,
and plant growth stage. Production of ROS under Pb stress
disrupts cell structures and its biomolecules that lead to cell
death. To protect biomolecules from damage, plant produces
certain antioxidants to combat with toxic effects of Pb. Iden-
tification of exact pathways of plant response to Pb stress at
molecular level and its interference with plant nutrition are
fundamental clues for future research. However, application
of proteomics, metabolomics, transcriptomics, and genomic
approaches should be used for better understanding of molec-
ular basis and exact mechanisms of Pb toxicity in rice. Further,
as remediation, environmentalists and soil engineers devised
various approaches to remediate Pb contaminated soil in
which soil amendments with biochar application and
phytoremediation technologies are the most suitable, practica-
ble, and publically acceptable but this method of soil cleaning
still have some constraints that need to be resolved. In order to
use this method efficiently and to abate these constraints, fur-
ther research is needed on sustained basis.
Conflict of interest The authors declare that they have no competing
interests.
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