AJAE 2(4):114-119 (2011) ISSN:1836-9448

Bioaccumulation and translocation factors of cadmium and lead in Aeluropus littoralis

Mohammad Rezvani1*, Faezeh Zaefarian2

1
Department of Agronomy, Qaemshahr Branch, Islamic Azad University, Qaemshahr, Iran
2
Department of Agronomy and Plant Breeding, Faculty of Crop Sciences, Sari Agricultural Sciences and Natural
Resources University, Sari, Mazandaran, Iran

Abstract

Phytoremediation is an eco-friendly and low cost potential strategy for cleaning up of heavy metals from contaminated soils. Selection of
promising plant is an important approach for successful phytoremediation. In two separate pot culture experiments, five levels of soil
cadmium (Cd) concentrations as 15, 30, 60, 120 and 240 mg Cd kg-1 soil and five levels of lead (Pb) including 500, 1000, 2000, 4000,
8000 mg Pb kg-1 soil were tested. Plant growth, bioaccumulation and translocation factors of Cd and Pb in A. littoralis were investigated.
Cd and Pb reduced the A. littoralis dry matter production significantly. Bioaccumulation factor of Pb was <1, which shows A. littoralis
could be an excluder of Pb. Our results also showed translocation factor of Cd was more than one and hence, A. littoralis could be
considered as accumulator of Cd. The incremental translocation of Cd to the shoots of A. littoralis, when exposed to the higher Cd in
soil, indicates a great performance of this plant for Cd phytoextraction and might be introduced as Cd- hyperaccumulator plant.

Keywords: Bioaccumulation factor; cadmium; lead; phytoextraction; translocation factor.

Abbreviations: R2_ correlation coefficient; Cshoot_ metals concentration in plant shoot (mgkg1); C root_ metals concentration in plant root
(mgkg-1); Csoil_ metals concentration in soil (mgkg-1); Cplant_ metal concentration in harvested component of plant (mgkg-1 ); Mplant_ mass
of the aboveground biomass (g); Mrooted zone_ mass of the soil volume (m3).

Introduction

Phytoremediation, is called cleaning up of terrestrial polluted
area as well as aquatic sites from heavy metal and organic
contaminants by green plants. An appropriate plant for
phytoremediation should ideally have high and fast biomass
production, and ability of translocation of contaminants into the
plant shoot (Cunningham and Ow, 1996). Cd causes a wide
various toxic effects when taken up by plants. It inhibits several
plant physiological processes such as oxidative reactions and
nitrogen metabolism, is well known to be harmful to plants
(Attila et al., 2001; Laspina et al., 2005). The Cd-contaminated
soils in agricultural lands, especially paddy fields, are created
by irrigation waters containing Cd, normally originated from
mines. Therefore, its toxicity has become a serious problem for
human health. Until now, soil dressing and soil washing have
improved Cd-polluted soil; however, these civil engineering
techniques need large quantities of uncontaminated
replacement soil, which is costly and impracticable for the
remediation of large areas. Therefore, phytoremediation, as a
new technique for rehabilitating contaminated soil, has recently
received considerable attention (Elizabeth, 2005). Pb is a major
anthropogenic contaminant, which has been released to the
environment since the industrial revolution. Therefore, Pb has
accumulated in different terrestrial and aquatic ecosystems
(Verma and Dubey, 2003). In addition, Pb is an extremely toxic
metal whose effects on human health (Juberg et al., 1997). The
movement of Pb from absorbing root hairs, is apparently
impeded by a number of biochemical and/or physical processes
involving Pb binding, inactivation and/or precipitation (Tandler
and Solari, 1969). Pb has been shown to accumulate in plants
from several sources including soil but the reports on
accumulation of the Pb within plants are variable (Al Salman
and Abdul Aziz, 2002). Pb is often found in the cytoplasm of
cells associated with electron-dense precipitates localized in
membranous inclusions, vesicles or organelles (Sinha et al.,
2006). Aeluropus littoralis, from the Poaceae family, is one of
the most abundant perennial halophytes found in Iranian saline
habitats and is highly tolerant to soluble salts. A. littoralis has a
rapid growth rate, high biomass production and widespread
root system distribution in saline and none saline soils
(Meyboudy et al., 2004). The present study was therefore
designed to investigate the plant growth, bioaccumulation and
translocation characteristics of cadmium and lead in A.
littoralis.
Results and discussion
Experiment I
Shoot weight was drastically reduced with increase in lead (Pb)
supply (Fig. 1) (p<0.05). Moreover, the addition of a range of
increasing rates of Pb decreased the shoot weight of plants (Fig.
2) (p<0.05). The reduction in plant growth by increasing Pb
doses was observed by Tomar et al. (2000), Munzuroglu and
Geckil (2002) and Muranyi and Kodobocz (2008). Results of
Zaefarian et al. (2010) showed decreasing in Alfalfa (Medicago
sativa L.) dry matter, when grown in Pb contaminated soil.
Ardakani et al. (2009) also found a reduction in barley
(Hordeum volgare L.) growth, when grown in Pb contaminated
soil. Sinha et al. (2006) have proposed that Pb was interfering
with a factor directly involved in cell elongation suggesting the
specific involvement of enzymes in the wall and ATPase
associated with the plasmalemma. The translocation factor
(TF) of Pb has expressed a linear decreased with increasing Pb
contents in the soil (R 2 = 0.71). The TF for Pb was changed
generally from 1.12 to 5.33 (Fig. 3) (p<0.05).

114
 14
6
12 y = 9.938e-1E-04x 5 y = -0.0004x + 4.5451
Shoot weight (g)

10 R² = 0.918 R² = 0.7138
4
8

Pb TF
6 3

4 2
2 1
0 0
0 2000 4000 6000 8000 10000 0 2000 4000 6000 8000 10000
Soil Pb (mgkg-1) Soil Pb (mgkg-1)

Fig 1. Relationship between soil Pb concentration and shoot Fig 3. Relationship between Pb translocation factor and soil
weight Pb concentration .

14
1.6
12 y = -0.0082x + 9.6485 1.4
Shoot weight (g)

10 R² = 0.313 1.2
1

Pb BAF
8
0.8
6
0.6
4 0.4 y = -7E-08x2 + 0.0006x + 0.0568
2 0.2 R² = 0.8571
0 0

0 100 200 300 400 500 600 0 2000 4000 6000 8000 10000
Soil pb (mgkg-1)
Pb sh oo t (mgkg-1)

Fig 2. Relationship between shoot Pb cocentration and shoot Fig 4. Relationship between soil Pb concentration and Pb
weight bioaccumulation factor.

Our result showed a TF>1 suggesting that Pb could be

effectively translocated from the roots to the shoots. The
current literatures show variable TF ranges of Pb in different
plants. Tang et al. (2009) indicated that in Arabis paniculata
Franch, in range of Pb concentration (9- 267 µM) the TF was
below one. In addition, a U shape pattern of TF was observed
in their work. However, in our experiment a linearly reduction
of TF was observed. This observation was in accordance to Sun
et al. (2009) and Sun et al. (2008) results. They also found TF
more than one in Solanum nigrum. A key trait of metal hyper-
accumulators is the efficient metal transport from roots to
shoots, characterized by the TF being greater than one (Zhao et
al., 2006). A. littoralis could be labeled as accumulator of Pb
based on TF>1. Bioaccumulation factor of Pb ranged from 0.13
to 1.35, suggesting considerable bioaccumulation of Pb from
soil even in soils with relatively low Pb concentrations (Fig. 4)
(p<0.05). In our experiment, BAF of Pb was <1 (except in
4000 mg Pb kg-1 soil), that shows A. littoralis could be an
excluder of Pb (Ma et al., 2001). Bioaccumulation factors
decreases with increasing soil heavy metal concentrations
(Efroymson et al., 2001; Zhao et al., 2003) that was in contrary
to our result. MER of Pb at the different treatments of Pb was
decreased significantly with increasing Pb concentration of soil
(Fig. 5) (p<0.05). Mertens et al. (2005) suggested reduction in
MER by increasing concentration of metals in soil. These
results was also reported by Sun et al. (2008) who worked
on Solanum nigrum. In addition to trace metal concentrations
in soils and plants, the extraction capacity should be taken into
consideration with depth of the rooting zone, the density of the
soil and the biomass production and mortality of the
aboveground components of harvested biomass. Expression
of extraction capacity as a ratio, which takes the produced
biomass and the soil volume into account would be more
informative (Mertens et al., 2005). The amounts of Pb taken up
by plants were calculated by multiplying plant biomass with Pb
concentration in plant. As shown in Fig. 6, they ranged from
465.64 to 3455.62 mg Pb, in control and 1000 mg Pb kg-1 soil,
respectively (p<0.05)(Fig. 6). The reduction in Pb uptake might
be due to disturbed photosynthesis and nitrogen metabolism in
excess Pb conditions that reduced biomass production. The
detrimental effect of excess Pb in radish was evident in the
form of retarded growth and reduced biomass (Gopal and
Rizvi, 2008). Jiang and Liu (1999) and Uveges et al. (2002)
have suggested that lower concentrations of Pb have a
stimulatory effect on root growth and inhibitory effect at higher
concentrations. Moreover, Pb at high concentration reduced the
dry matter of cabbage and sunflower (Kastori et al., 1998).
Experiment II
We observed that increasing doses of Cd in the soil affected
shoot weight in a negative exponentially decreasing regression
(R 2= 0.89)(p<0.05)(Fig. 7). Inhibition of growth and biomass
production of plants exposed to Cd stress is a widely observed
effect in several studies. In Populus cultivars Cd excess
decreased plant dry matter production (Gu et al., 2007). Our
findings were also agreed with Pilipovic et al. (2005) and
Shukla et al. (2003). The reduction in dry matter of Vigna
radiata (L.) Wilczek at higher concentration of heavy metals
was also observed by Jaleel et al. (2009).

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 8
7 14
12

Shoot weight (g)

6 y = 11.232e-0.004x
10 R² = 0.893
5
8
y = 5.5184e-0.0004x
MER (%)

4 6
3 R2 = 0.8559 4
2 2
1 0
0 0 50 100 150 200 250
0 2000 4000 6000 8000 10000 Soil Cd (mgkg-1)
Soil Pb (mgkg-1)

Fig 5. Relationship between soil Pb concentration and MER

Fig 7. Relationship between soil Cd concentration and shoot
weight.

4000 20
18 y = 0.0655x + 2.4019
16 R² = 0.9685
3000 14
12

CdTF
Pb uptake

2000 10
8
6
1000 4
2
0 0

0 2000 4000 6000 8000 10000 0 50 100 150 200 250

Soil Pb (mgkg-1)
Fig 6. Relationship between soil Pb concentration and Pb
uptake
Stunting, chlorosis, necrosis and desiccation are visual toxic
symptoms of Cd stress in plants (Das et al., 1997). Gu et al.
(2007) observed decline in the net photosynthetic and
transpiration rate of the Populus cultivars that related to
stomata constraints, such as stomatal conductance. Higher Cd
concentrations enhanced mesophyll impairment and therefore
the net photosynthetic rates in all four populus decreased. The
reduction in transpiration rate and stomatal conductance in the
excess Cd treatments may be the result of the strong effect of
Cd on guard-cell function (Gu et al., 2007). In addition, Rascio
et al. (1993) and Ouzounidou et al. (1997) suggested the Cd
damages on the structure of chloroplasts. The higher Cd
concentrations in the leaf tissues affecting indirectly on the
chlorophyll content through metabolic perturbations and by
accelerating plant senescence (Vassilev et al., 1997). Böddi et
al. (1995) have suggested a direct action of Cd on enzymes of
the chlorophyll biosynthesis pathway. There were significant
positive linear relationship between TF of Cd and Cd
concentration in soil as shown in Fig. 8 (p<0.05). The
maximum rate of TF was 18.5 with treatment of 250 mg Cd kg-
1
soil, which represents translocation of Cd was effectively
made from root to shoot. The tolerant mechanisms of Cd
tolerant plants have been reported previously by Baker and
Brooks et al. (1989) and Sun et al. (2008), including two
strategies: exclusion and accumulation (Zhou and Song, 2004).
As for the accumulation strategy, plants accumulated high
amounts of Cd in their tissues, which only a small amount of
Cd is stored in the roots and the rest will be translocated to the
shoots (Sun et al., 2009). Our result showed TF>1 therefore, A.
littoralis could be labeled as Cd-hyperaccumulator (Baker and
Brooks et al., 1989; Zhou and Song, 2004; Zhou et al., 2004).
The ability enhancement of Cd translocation to A. littoralis
shoot in higher concentrations of soil Cd indicates a great
Soil Cd (mgkg-1)
Fig 8. Relationship between soil Cd concentration and
translocation factor of Cd.
performance of the plant for Cd phytoextraction. Relationship
between concentration of soil Cd and BAF shows a significant
positive relationship (p<0.05)(Fig. 9). The BAF represents the
contaminant concentration in plants comparing with the
environment concentration (in soil) (Scragg, 2005). For a plant
to be efficient tool in the contaminated soil phytoremediation,
the BAF have to be higher than 1. In our experiment BAF of
Cd had a range between 1.82 and 5.41 (BAF >1) that
suggesting a highly performance of A. littoralis for
phytoremediation of Cd-contaminated soil. The extraction ratio
of Cd at the different treatments of Cd was decreased
significantly with increasing Cd concentration of soil (Fig. 10).
Our results was according to the results of Mertens et al. (2005)
who indicated the metal extraction ratio will decreases with
increasing soil metal concentrations. Cd uptake increased by
increasing Cd doses in soil up to 30 mg Cd kg-1 soil and then
was stabled in more concentrations (p<0.05)(Fig. 11). Liu et al.
(2006) showed Cd uptake and accumulation in roots and shoots
of four maize cultivars varied depending on the different Cd
concentrations used and the Cd content in roots and shoots
increased significantly. Gu et al. (2007) also concluded that
increasing of Cd concentrations in soil, decreased Cd uptake by
Populus cultivars.
Materials and methods
Experiments design and plant growth conditions
Two pot experiments were conducted under glasshouse
conditions. The soil was collected from the top 20 cm layer
from arable plots. The soil was air dried and sieved to pass the
<2 mm sieve before use and analyzed for the following
properties: EC (3.02 dSm-1), Cl (337.3 mg kg-1), Na (82.4 mg
kg-1), organic carbon (OC, 0.076 %), total N (0.084 %) ,
116
 6 transplants of two-week old A. littoralis plant were transplanted

Cd bioaccumulation factor
5 into each pot.
4
y = 1.209ln(x) - 1.114 Plant analysis
3 R² = 0.937
2
1
A. littoralis is a permanent plant regrowing from underground
parts. Plant samples from shoots were taken at three different
0
stages including 80, 160 and 240 days after planting and
0 50 100 150 200 250
analyzed for Cd and Pb. At the each stage, plant samples were
Soil Cd (mgkg-1) divided into stems and leaves, washed thoroughly with distilled
water and oven dried at 70 °C for 24 h for further analyses.
Plant samples were then ground and digested in 5 ml acid
mixture of HClO 4 (Merck) (60%) and HNO3 (Merck) (85%,
Fig 9. Relationship between soil Cd concentration and s.g. 1.42) (15:85 v/v) overnight. Digestion was completed by
bioaccumulation factor of Cd. gradual increase of temperature from 60 to 195 °C (60 °C, 3 h;
100 °C, 1 h; 120 °C, 1 h; 150 °C, 30 min; 175 °C, 30 min; 195
°C, 2.5 h). After cooling, HCl (20%, 2.5 ml) was added, whirl
60 mixed and warmed to 80 °C for 30 min. The final volume was
50 brought to 10 ml with double distilled water and re-warmed to
y = -11.3ln(x) + 62.78 80 °C for another 30 min. Samples were filtered through
MER (%)

40 R² = 0.960 cellulose filter (0.2 µM) (Barazani et al., 2004). Standard

30 materials were included for assurance control. Standard
20 materials were Cd(NO3) 2, KNO 3, Mg(NO3 )2, Cu(NO3)2,
Fe(NO 3)2, Mn(NO3)2 and Zn(NO 3)2. Analysis of Cd and Pb in
10 the stems and leaves was performed by atomic absorption
0 spectrophotometery (M SERIES; Thermo, China).
0 50 100 150 200 250 300
Translocation factor
Soil Cd (mgkg-1)
Cd and Pb translocation from shoot to root was measured by
TF which is given below:
Fig 10. Relationship between soil Cd concentration and MER.
TF=Cshoot/Croot (1)

Where Cshoot and Croot are metals concentration in the shoot

450
(mgkg-1) and root of plant (mgkg-1), respectively. TF>1
400
represent that translocation of metals effectively was made to
350
the shoot from root (Baker and Brooks, 1989; Zhang et al.,
300
Cd uptake

2002; Fayiga and Ma, 2006).

250
200 Bioaccumulation factor
150
100 BAF of Cd and Pb was calculated by:
50
0 BAF=C shoot/Csoil (2)
0 50 100 150 200 250
Soil Cd (mgkg-1) Cshoot and Csoil are metals concentration in the plant shoot
(mgkg-1) and soil (mgkg-1), respectively. BAF was categorized
further as hyperaccumulators, accumulator and excluder to
Fig 11. Relationship between soil Cd concentration and Cd those samples which accumulated metals>1 mg kg-1, and < 1,
uptake respectively (Ma et al., 2001; Cluis, 2004).

available P (17 mg kg-1), K (213.75 mg kg-1 ), Fe (5.54 mg kg-
1
), Cu (47.8 mg kg-1 ), Zn (490 mg kg-1 ), Mg (1992.5 mg kg-1),
Mn (162.5 mg kg-1 ), as well as for Cd (0.25 mg kg-1 soil dry
weight). Ten Kg of soil was placed into pots. In the experiment
one, the soil was contaminated using five levels of Pb (as
Pb(NO3)2 ): 500, 1000, 2000, 4000, 8000 mg Pb kg-1 soil plus
an uncontaminated control. In the experiment two, the soil was
contaminated using five levels Cd (as CdCl2 ): 15, 30, 60, 120,
240 mg Cd kg-1 soil plus an uncontaminated control.
Experiments were complete randomized design with 5
replications.In the both experiments, healthy and equal-sized
shoots were chosen and grown in vessels for the initiation of
new roots. The transplants were grown in a glasshouse at
natural day/night duration and at average temperatures of 30 ±
3 C and 15 ± 3 C, day and night regime, respectively. Three
Metal extraction ratio (MER)
The metal extraction ratio has been applied to evaluate the
ability of remedying contaminated soil by a hyperaccumulator.
MER is defined as the ratio of metal accumulation in the shoots
to that in soil (Mertens et al., 2005), which is calculated as
follows:
MER= (Cplant×Mplant/C soil×Mrooted zone)×100 (3)
Where C plant is the metal concentration in the harvested
component of the plant biomass, Mplant is the mass of the
harvestable aboveground biomass produced in one harvest, Csoil
is the metal concentration in the soil volume, and Mrooted zone is
the mass of the soil volume rooted by the species under study.

117
Data analysis
For statistical analysis, the sum of Cd and Pb concentration of
shoot for the three stages of harvest (i.e. concentration stage 1+
concentration stage 2+ concentration stage 3) used as the
experimental data. In addition, the correlation analysis was
carried out by the statistical software SPSS 18.
Conclusions
The present investigation revealed that A. littoralis could be
great plant for phytoextraction of Cd from contaminated soil. In
fact, the highest efficiency of Cd phytoextraction was occurred
when the soil was contaminated by 250 mg Cd kg-1 soil. Both
BF and TF values more than one, indicated that A. littoralis is
potentially useful for remedying Cd-contaminated soil and
introduce as Cd-hyperaccumulator plant. Also, this research
suggests more investigations by applying more concentrations
of Cd. But, in the Pb contaminated soils A. littoralis use
exclusion strategy and could be an excluder of Pb.
Acknowledgments
The authors would like to thank the financial support of the
Islamic Azad University, Qaemshahr Branch, Iran.
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