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Open Journal of Applied Sciences, 2021, 11, 846-859
https://www.scirp.org/journal/ojapps
ISSN Online: 2165-3925
ISSN Print: 2165-3917
DOI:
10.4236/ojapps.2021.117062 Jul. 30, 2021 846 Open Journal of Applied S
ciences
Phytoextraction Capacity of
Chrysopogon nigritanus Grown
on Arsenic Contaminated Soil
Beda Amichalé Jean Cyrille1, Messou Aman1*, Ouattara Pétémanagnan Jean-Marie1,
Coulibaly Lacina1,2
1Laboratory of Environment and Aquatic Biology, Department of Sciences and Environment Management, Nangui Abrogoua
University, Abidjan, Côte d’Ivoire
2University of Man, Man, Côte d’Ivoire
Abstract
This study aims to investigate the capacity of
Chrysopogon
nigritanus
to ac-
cumulate As from contaminated soils
.
The ex
periment was conducted in a
greenhouse.
C.
nigritanus
was subjected to uncontaminated soil and As con-
taminated soil (50 mg/kg, 100 mg/kg and 150 mg/kg of As), for
180 days.
Plant growth and biomass produced, the
concentration of As in soil and
plant, bioaccumulation and transfer factors,
as the location of As in tissues
and cells of the plant have been determined. Plant growth decreased signifi-
cantly with increasing soil As concentration.
C.
nigritanus
accumulated more
As in roots biomass. The highest bioac
cumulation factor values were found in
contaminated soil at 50 mg As/kg (As 50), then
contaminated soil at 100 mg
As/kg (As 100) and contaminated soil at 150 mg As/kg (As 150). As was es-
sentially fixed to the intracellular compartment of the roots, stems a
nd leaves.
In roots tissues,
As was mainly retained in the rhizodermis and the pericycle.
While in stems tissues,
As was preferentially accumulated in the conductive
bundles. In the leaves, the final destination of As was epidermis tissues.
Keywords
Phytoextraction, C
hrysopogon
nigritanus
, Arsenic, Bioaccumulation Factor,
Transfer Factor
1. Introduction
Over the past few decades, arsenic (As) has been a focus of environmental con-
cerns due to its high toxicity [1]. Indeed, arsenic is classified as Group-1 carci-
How to cite this paper:
Cyrille, B.A.J
.,
Aman, M
., Jean-Marie, O.P. and Lacina, C.
(20
21) Phytoextraction Capacity of
Chr
y-
sopogon
nigritanus
Grown on Arsenic Con-
taminated Soil.
Open Journal of Applied Sci
-
ences
,
11
, 846-859.
https://doi.org/10.4236/ojapps.2021.117062
Received:
May 22, 2021
Accepted:
July 27, 2021
Published:
July 30, 2021
Copyright © 20
21 by author(s) and
Scientific
Research Publishing Inc.
This work is
licensed under the Creative
Commons Attribution International
License (CC BY
4.0).
http://creativecommons.org/licenses/by/4.0/
Open Access
B. A. J. Cyrille et al.
DOI:
10.4236/ojapps.2021.117062 847
Open Journal of Applied Sciences
nogen to humans based on strong epidemiological evidence. Its ingestion can
lead to abdominal pain, hyperpigmentation of the skin, vomiting, diarrhea, cho-
lera, an increased incidence of spontaneous abortions, late fetal deaths, prema-
turity and low birth weight [2]. Although arsenic occurs naturally in trace amounts
in soils, anthropogenic activities including mining, coal burning and agriculture
(herbicides and pesticides) lead to its high accumulation in the environment [3].
These pollutions can generate arsenic concentrations often above the toxicity
threshold (12 mg/kg) in soils [4] [5].
In Côte d’Ivoire, Sako
et
al.
[6] found arsenic concentrations between 11.3
and 3809 mg/kg in soils in mining areas. Under some physicochemical condi-
tions, arsenic compounds are particularly soluble and consequently become
very bioavailable and can affect agricultural production and food quality due to
bioaccumulation [7]. In view that soils are limited resources and considered
non-renewable on a human scale, several techniques for decontaminating con-
taminated soils have been developed [8]. However, most of them, in particular
the physico-chemical methods (washing of soil, incineration and excavation/
burying, etc.), require significant investments and considerably disrupt the bio-
logical mechanisms of the soil [9]. On the other hand, biological methods, par-
ticularly those which use higher plants (phytoremediation), could be suitable
for soil remediation. Indeed, phytoremediation is a less expensive technique
that does not destroy soil biodiversity and can be applied to organic or inor-
ganic pollutants [10]. Plants can accumulate the metallic elements necessary for
their development as well as those not necessary, due to physiological adapta-
tions [11]. Moreover, hyperaccumulators are naturally capable of accumulating
high levels of metals. To date, around 400 plant species have been identified as
hyperaccumulating a given metal or metalloid [12]. However, few plant species
are known to be hyperaccumulators of As [13]. The majority of the identified
species are ferns of the Pteridaceae family [14] [15]. Due to their weak rooting
and slow growth, these plants would be less efficient for large-scale use [16].
Consequently, studies are increasingly focusing on plant species that have mod-
erate accumulations of arsenic but have rapid development with high biomass
[11]. In addition, the use of endogenous plants is recommended for the remed-
iation of contaminated local soils [17]. Among these plants,
Chrysopogon
ni-
gritanus
is of interest for conservation, stabilization and removal of some trace
metals (Al, As, Cd, Cu, Cr, Pb, Zn) soils [18]. It has a high biomass production
and dense root development which offers a large specific surface and delimits
an important rhizosphere zone. Finally, this plant grows in all regions of Côte
d’Ivoire [19]. It could therefore be suitable for remediation of arsenic-contaminated
soil. This study proposed to determine the capacity of
C.
nigritanus
to accumu-
late arsenic in contaminated soil. Specifically, this study involves in evaluating
the effect of arsenic concentration on plant growth, determining the potential
for extracting arsenic by
C.
nigritanus
and characterizes arsenic accumulation
mechanisms.
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2. Material and Methods
2.1. Material
2.1.1. Soil
The topsoil used for this study was air dried and then sieved to 2 mm, then ho-
mogenized and placed in each pot. The soil was artificially contaminated with
arsenic trioxide (As2O3) in order to obtain 50 mg/kg, 100 mg/kg and 150 mg/kg.
For each concentration, the soils were saturated with an amount of arsenic salt
determined according to Equation (1) [20] [21].
soil arsenic trioxide
arsenic trioxide As
Cm M
mM
××
=
(1)
m
arsenic trioxide = Mass of arsenic trioxide (mg);
M
arsenic trioxide = Molar mass of arsenic trioxide (g/mol);
M
As = Molar mass of arsenic (g/mol);
m
soil = Mass of soil in the pot (kg);
C
= Theoretical concentration of arsenic (mg/kg).
2.1.2. Plant Selection
Chrysopogon
nigritanus
chosen for this study is a plant that grows in all regions
of Côte d’Ivoire [19]. It has a high production of biomass and a dense root de-
velopment which offers a large specific surface and delimits a significant rhizos-
phere [18].
C.
nigritanus
has a high tolerance for arsenic [18].
2.2. Methods
2.2.1. Experimental Design
The experimental was conducted in a greenhouse (Length = 13 m and width =
11 m) at the experimental site of the Biotechnology and Environmental Engi-
neering Research Unit of Nangui Abrogoua University (Abidjan, Côte d’Ivoire).
It was performed with plants grown in 48 pots (capacity = 0.024 m3). These in-
clude twelve (12) pots per dose of soil contamination by arsenic (50 mg/kg, 100
mg/kg and 150 mg/kg),
i.e.
36 pots, and twelve (12) pots containing uncontami-
nated soil.
C.
nigritanus
plants used were taken from nurseries (4 weeks old) es-
tablished at the experimental site. Plants with the same morphological develop-
ment were selected and cultured in the pots. The experiment lasted 180 days.
2.2.2. Data Collection
Growth monitoring was carried out by weekly measurement of the height of the
studied plant stems using a tape measure in millimeters. As for the plant bio-
mass produced, two (2) replicates of plants per arsenic dose were harvested
monthly (30 days) and the plant biomasses (shoot and root) produced were de-
termined by weighing on a 10−3 precision Sartorius EB150FEG-I scale.
Arsenic concentrations in the soils were determined monthly (30 days). Four
(4) composite samples were taken by coring at the [0 - 10], [10 - 20], [20 - 30]
and [30 - 40] horizons of experimental pots. The samples were kept in hermeti-
cally sealed jars until analysis.
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Open Journal of Applied Sciences
To assess the arsenic accumulation by
Chrysopogon
nigritanus
, two (2) plant
replicas (shoot and root) per dose of arsenic were taken from the culture pots
every month (30 days). In each pot, the harvested plants were separated into
shoot and root parts. Each plant sample was washed with distilled water and
high purity water to remove dust and soil. After air-drying, each plant sample
was dried at 65 EC to a constant weight. The dried samples were crushed using a
plant tissue grinder (RESPSCH S100).
2.2.3. Samples Analysis
Arsenic concentrations in soils were carried out according to the standard NF
ISO 11466: 1995. The soil sample (0.5 g) was digested with 10 mL of aqua regia
(7.5 mL of HCl and 2.5 mL of HNO3). The content was filtered at 0.45 µm and
diluted up to 50 mL with distilled water. Arsenic concentrations were deter-
mined by Plasma-Coupled Induction Atomic Emission Spectrometry (ICP-AES).
The mineralization of plant samples was made according to the standard NFX
31-151: 1993. Subsample (20 g) of crushed plant material was oven-dried at 500
EC for 2 hrs and 0.5 g of that burned sample was digested with 10 mL of aqua
regia. Then, the sample was put in an oven at 180 EC for 30 min for ending di-
gested process. The filtrate obtained after cooling was used for arsenic analysis
by Plasma Coupled Induction Atomic Emission Spectrometry (ICP-AES).
Table 1 summarizes the different methods and standards used to analyze soil
and plants samples.
2.2.4. Phytoextraction Efficiency
Two factors were calculated to evaluate plant phytoextraction efficiency. The
Bioaccumulation Factor (BF) was calculated to estimate arsenic uptake in the
plant. It presents an index of the ability of a plant to accumulate arsenic relative
to the concentration in the medium [22]:
Arsenic concentration in roots Arsenic concentration in shoots
BF Arsenic concentration in soil
+
=
(2)
The Transfer Factor (TF) defined as the ratio between arsenic concentration
in plant shoots and its concentration in roots [23]. It determined the relative
movement of metal from roots to shoots
:
Arsenic concentration in shoots
TF Arsenic concentration in roots
=
(3)
Table 1. Methods and standard for sample analysis.
Samples type
Parameter
Methods of analysis
Standards
Soil
Arsenic
Dige
stion with aqua regia and reading with a
Plasma
-Coupled Induction Atomic Emission
Spectrometry
(ICP-AES)
NF ISO 11466:
1995
[42].
Plant
Arsenic
Calcination, digestion with aqua regia and reading
with a
Plasma-Coupled Induction Atomic Emission
Spectrometry
(ICP-AES)
NFX 31
-151:
1993
[43].
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ciences
TF
> 1: accumulation of As in the shoot biomass of plants;
TF
< 1: accumulation of As in the root biomass of plants.
2.2.5. Localization of Arsenic in C. nigritanus Tissues and Cells
This study determined the distribution of arsenic in plant roots, stem and leaves,
precisely at the tissue and the cell level. For the analyses, samples of leaves, stems
and roots of
C.
nigritanus
were taken from the culture pot with the best yield of
arsenic phytoremediation every month. Those samples were fixed for 24 h in
2.5% glutaraldehyde (pH 7.2). Then, they were rinsed two or more times with
distilled water. A 2 mm cross-section of the samples (leaf, stem or root) was fol-
lowed by dehydration in successive baths of 30 min of ethanol (from 70% -
100%). The samples were subsequently dried in the open air and fixed on pads
placed on a plate carried in the metallizer to spray them with gold. The plate was
finally mounted on the stage of Scanning Electron Microscopy with Energy dis-
persive X-ray spectroscopy (SEM-EDX) to perform arsenic weight (%) in the
tissue and the cell.
2.2.6. Statistical Analysis
Statistical analysis of the data was performed with R software. The normality of
the data distribution was verified with the Shapiro test. Parametric tests such as t
test and ANOVA test were used to evaluate the differences between growth and
biomass produced by the plant in the culture pots, concentrations of As in soils,
transfer factor and bioaccumulation factors. Statistical significance was defined
at the level of p < 0.05.
3. Results
3.1. Plant Growth
During the treatment, stem lengths of
Chrysopogon
nigritanus
decreased in soil
as the dose of arsenic applied increase (Figure 1). However, no significant dif-
ferences were noted between contaminated soil at 50 mg As/kg (As 50) and the
control (t test: p > 0.05). However, comparing growth of plants in the control
and contaminated soil at 100 mg As/kg (As 100), they were significantly differ-
ent, the same between the control and contaminated soil at 150 mg As/kg (As
150) (t test: p < 0.05). Furthermore, significant differences are shown between
stem lengths of plants in As 50 and As 100 as well as between As 50 and As 150
(t test: p < 0.05). The order of
C.
nigritanus
stem lengths at the end of the expe-
riment is as follows: control (57.5 cm) > As 50 (48.5 cm) > As 100 (28 cm) > As
150 (25.25 cm).
3.2. Biomass Produced
Shoot and root biomasses harvested during the experiment are shown by Figure
2. It is noted that these biomasses have increased during the experimental and
the shoot part has remained higher than that root in all the pots. But, these bio-
masses decrease with increasing concentration of arsenic applied in the soil.
B. A. J. Cyrille et al.
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From day 30 to day 180, shoot biomasses increased from 12.28 to 379.41 g, from
8.47 to 328.86 g, from 11.07 to 203.4 g and from 4.4 to 137.95 g respectively on
uncontaminated (control) soil contaminated soil at 50 mg As/kg, 100 mg As/kg
and 150 mg As/kg. As for root biomass, the values ranged from 5.44 to 115.00 g
(control), from 2.46 to 97.00 g (As 50), from 2.24 to 51.25 g (As 100) and from
1.05 to 44.00 g (As 150). Shoot and root biomass of the control soil and conta-
minated soil at 50 mg As/kg were not significantly different (t test: p > 0.05).
Considering the contaminated soil, it noted that shoot and root biomass values
recorded in As 50 differ significantly from that As 100 and As 150 (t test: p <
0.05). On the other hand, no differences are observed between As 100 and As
150 (t test: p > 0.05). Figure 3 shows a view of the plant biomass at the end of
the experiment.
Figure 1. Stem length of
C.
nigritanus
during the experiment
;
As 50: con-
taminated pot at 50 mg As/kg; As 100: contaminated pot at 100 mg As/kg; As
150: contaminated pot at 150 mg As/kg; T: control pot
.
Figure 2. Fresh shoot (a) and root (b) biomasses produced by
Chrysopogon
nigritanus
during the expe-
riment; As 50: contaminated pot at 50 mg As/kg; As 100: contaminated pot at 100 mg As/kg; As 150:
contaminated pot at 150 mg As/kg; T: control pot.
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Figure 3. View of the plant biomass produced by
Chrysopogon
nigritanus
at the end of the experi-
ment; As 50: contaminated pot at 50 mg As/kg; As
100: contaminated pot at 100 mg As/kg; As 150:
contaminated pot at 150 mg As/kg; T: control pot.
3.3. Arsenic Accumulation Potential of Chrysopogon nigritanus
As concentrations recorded in root biomass of
C.
nigritanus
was higher than
concentrations in shoot (Table 2). From day 30 to day 180, As concentrations in
shoot biomass ranged from 0.91 - 11.64 mg/kg (As 50), 1.56 - 14.48 mg/kg (As
100) and 6.15 - 17.92 mg/kg (As 150). In the root, concentrations increased from
4.69 - 15.91 mg/kg (As 50), 5.42 - 30.28 mg/kg (As 100) and 10.85 - 41.32 mg/kg
(As 150).
Table 3 shows the Bioaccumulation Factor (BF) and Transfer Factor (TF) of
arsenic for
C.
nigritanus.
BF remained higher in As 50 (0.11 - 0.53) than As 100
(0.07 - 0.40) and As 150 (0.11 - 0.34). FT was less than 1 [0.19 - 0.58 (As 50), 0.28
- 0.41 (As 100) and 0.40 - 0.62 (As 150)]. BF and FT values obtained from con-
trol soil and contaminated soil were not different (ANOVA test: p > 0.05).
3.4. Localization of Arsenic in the Tissues and Cells of
Chrysopogon nigritanus
For this study, plant from soil contaminated at 50 mg As/kg was selected, whose
removal efficiency and bioaccumulation factor remained the highest during the
experiment. Figure 4 shows the weight of As (%) recorded in the tissues and
cells of roots, stems and leaves of
C.
nigritanus
. In roots tissues, we noted higher
weight of As in the rhizodermis and the pericycle. Furthermore, these weight of
As decrease from the rhizodermis to the endodermis, as well as from the peri-
cycle to the central cylinder. In stems tissues, As weights were higher in the
conductive bundles than in the epidermis and cortex. In the leaves, arsenic was
more retained in the conductive bundles during the first thirty (30) days. How-
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ever, from day 60 until day 180, As was strongly accumulated in epidermis tis-
sues. At the cellular, As remains essentially fixed to the intracellular compart-
ment of the roots, stems and leaves.
Figure 4. Weigth of As (%) recorded in the tissues (a) and cells (b) of
C.
nigritanus
.
Table 2. As concentrations (mg/kg) in
Chrysopogon
nigritanus
; As 50: contaminated pot
at 50 mg As/kg; As 100: contaminated pot at 100 mg As/kg; As 150: contaminated pot at
150 mg As/kg; D30: 30 days; D60: 60 days; D90: 90 days; D120: 120 days; D150: 150 days;
D180: 180 days.
D30
D60
D90
D120
D150
D180
As 50
Shoot
0.91 2.94 4.25 5.51 9.55 11.64
Root
4.69 6.41 8.17 9.44 12.96 15.91
As 100
Shoot
1.56 4.91 6.89 7.34 10.48 14.48
Root
5.43 12.86 17.04 20.03 24.10 30.28
As 150
Shoot
6.15 10 11.52 12.83 14.67 17.92
Root
10.86 16.19 22.95 28.22 31.86 41.32
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Table 3. Bioaccumulation Factor (BF) and Transfer Factor (TF) of arsenic; As 50: conta-
minated pot at 50 mg As/kg; As 100: contaminated pot at 100 mg As/kg; As 150: conta-
minated pot at 150 mg As/kg; D30: 30 days; D60: 60 days; D90: 90 days; D120: 120 days;
D150: 150 days; D180: 180 days.
D30
D60
D90
D120
D150
D180
BF
As 50
0.12 0.20 0.27 0.32 0.45 0.53
As 100
0.08 0.19 0.25 0.29 0.34 0.40
As 150
0.12 0.18 0.24 0.28 0.32 0.34
TF
As 50
0.19 0.46 0.52 0.58 0.58 0.57
As 100
0.28 0.38 0.40 0.37 0.37 0.35
As 150
0.57 0.62 0.50 0.40 0.40 0.39
4. Discussion
The potential of
C.
nigritanus
to accumulate arsenic in polluted soil was investi-
gated. The analysis of plant growth parameters (stem length, plant biomass) in
pots showed a significant influence of the arsenic dose in the soil on the devel-
opment of
C.
nigritanus
. In fact, if the plant grew of the dose of As used, the re-
sults indicate a significant reduction in stem length and plant biomass in pol-
luted soils at 100 mg/kg and 150 mg/kg in As. Behind
et
al.
[24], Tu and Ma [25]
and Manirul
et
al.
[26] made such observations respectively with
Brassica
juncea
,
Pteris
vittata
L.
and
Oryza
sativa
cultivated on soil contaminated with increasing
doses of arsenic. This would be due to the phytotoxicity of arsenic at high con-
centrations in the soil. Various biological and biochemical phenomena resulting
from the contact of plants with As may contribute to the inhibition of their
growth. These include the disruption of nutrient uptake and disruption of essen-
tial physiological processes (photosynthesis, respiration) in plant development,
and the replacement of essential ions of adenosine triphosphate (ATP) in plants
[26]. However, up to 50 mg As/kg, the growth parameters of
C.
nigritanus
are of
the same order as those of the control pot. This result could be explained by the
fact that this concentration of 50 mg As/kg is well below the toxicity threshold
(100 to 250 mg/kg) indicated by Truong [28].
In the shoot of
C.
nigritanus
, the concentrations of As obtained in the conta-
minated soils were lower than those determined in the root. In all the contami-
nated soils, a strong accumulation of As in the roots of plants was observed with
transfer factors (FT) less than 1. These results corroborate those of Srisatit
et
al.
[29] and Chiu
et
al.
[30] who observed that vetiver accumulates arsenic mainly
in the roots. Indeed, according to Raab
et
al.
[31], with the exception of hyper-
accumulative plants, 75% to 90% of the As absorbed by plants is concentrated in
the roots. This observation was made on a set of 46 plant species. Furthermore,
Zhao
et
al.
[32] explain that by the reduction in this organ of arsenate ions to ar-
senite (thanks to arsenate reductase and the reducing power of glutathione)
which are subsequently complexed with phytochelatins and sequestered in root
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vacuoles [33]. This would justify the low rate of translocation of As to the aerial
parts of plants observed in many plant species [34]. Concerning the bioaccumu-
lation factors of As by
C.
nigritanus
, these decreased with the increase in the
dose of arsenic applied. This result could be explained by the fact that
C.
nigri-
tanus
would limit the accumulation of As when this pollutant is at high doses in
the soil, due to its high toxicity.
In view of its superior soil arsenic removal efficiency and bioaccumulation
factor compared to other pots, plant in the pot contaminated with 50 mg As/kg
was studied for the location of arsenic in
C.
nigritanus
tissues and cells. It show
that in roots, As is mainly stored in the rhizodermis and the pericycle. This trend
was observed by Chao
et
al.
[35] and Shi
et
al.
[36] on
Arabidopsis
thaliana
and
Oryza
sativa
species. These authors attributed that to the presence of the HAC1
(High As content 1) gene in the rhizodermis and pericycle of the root which
would favour the sequestration of arsenic in these tissues. At the stem, high
presence of arsenic is observed in the conductive bundles. In fact, conductive
bundle tissues, consisting of xylem and phloem, favorite the translocation of
traces elements. Indeed, xylem sap is the main means of transport of mineral
ions from the roots to the aerial parts. The circulation of raw sap takes place by
root growth and by foliar call during transpiration [37]. Regarding the distribu-
tion of arsenic in leaves, strong accumulation in the conductive bundles has been
observed during the first thirty (30) days. Subsequently, the As moves into the
epidermal cells. According to Lombi
et
al.
[38], the sequestration of arsenic in
the epidermis of leaves is a mechanism of detoxification of this pollutant in
plants. On the whole, it can be seen that arsenic is concentrated mainly in the
intracellular compartments of the roots, stems and leaves of
Chrysopogon
nigri-
tanus
. As most of this area is occupied by the vacuole, this would suggest that As
is mainly contained in the vacuoles [38]. This attests to the role of the vacuole in
maintaining cell homeostasis in the presence of an excess of As [39]. Indeed,
thanks to protein transporters, arsenic is sequestered in vacuoles [40]. However,
while intracellular compartments are the preferred arsenic storage areas, signifi-
cant fractions of As have been recorded on the cell walls of different organs
(stem, leaf, root) of the plant. According to Koch
et
al.
[41], As would be bound
to cell wall components such as cellulose, pectin and lignin.
5. Conclusion
The study showed the potential accumulation of arsenic by
Chrysopogon
nigri-
tanus
. Plant growth, bioaccumulation and transfer factors, as the location of As
in tissues and cells of the plant have been determined. The growth of
C.
nigrita-
nus
decreases in soil with increasing arsenic concentrations applied.
C.
nigrita-
nus
accumulated more arsenic in the roots than in the shoots (FT < 1)
.
Bioac-
cumulation factors decrease with increasing arsenic dose in soil. At the end of
the experiment, values of the bioaccumulation factor were 0.53 (As 50), 0.40 (As
100) and 0.34 (As 150). As was essentially fixed to the intracellular compartment
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of the roots, stems and leaves. In roots tissues, As was accumulated preferentially
rhizodermis and the pericycle while in stems tissues arsenic highly in the con-
ductive bundles. In the leaves, arsenic was more retained in the conductive bun-
dles during the first thirty (30) days. However, from day 60 until day 180, As was
strongly accumulated in epidermis tissues.
Acknowledgements
We are thankful to the members of the research team in Biotechnology and En-
vironmental Engineering of Nangui Abrogoua University (Abidjan, Côte d’Ivoire)
for their critical examinations and their useful suggestions, all of which have greatly
improved this manuscript.
Conflicts of Interest
The authors declare no conflicts of interest regarding the publication of this pa-
per.
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