Physiological Responses and Tolerance of Halophyte Sesuvium portulacastrum L. to Cesium

Abstract

Cesium (Cs) is a soil contaminant and toxic to the ecosystem, especially the plant species. In this study, we have assessed the potential of a halophyte Sesuvium portulacastrum for its Cs tolerance and accumulation. Thirty days old S. portulacastrum plants were subjected to different concentrations of Cs (0, 5, 10, 25, 50, and 150 mg·L⁻¹ Cs) using cesium chloride. The biomass and photosynthetic pigments were not affected up to 25 mg·L⁻¹ Cs treatment while a significant decline in pigment levels was observed at higher concentrations. The Cs treatments increased protein content at low concentrations while higher concentrations were inhibitory. Under Cs exposure, significant induction of antioxidant enzymes such as ascorbate peroxidase (APX), catalase (CAT), glutathione reductase (GR), and superoxide dismutase (SOD) was observed. The antioxidant enzyme activities were upregulated up to 50 mg·L⁻¹ Cs but decreased significantly at 150 mg·L⁻¹. The accumulation of Cs was dose and tissue-dependent as evidenced by a higher accumulation of Cs in leaves (536.10 μg·g⁻¹) as compared to stem (413.74 μg·g⁻¹) and roots (284.69 μg·g⁻¹). The results suggest that S. portulacastrum is a hyper-accumulator of Cs and could be useful for the phytoremediation of Cs-contaminated soils.

Full text

Research Article
Physiological Responses and Tolerance of Halophyte Sesuvium
portulacastrum L. to Cesium
Ganesh C. Nikalje ,
1
,
2
Manoj Shrivastava ,
2
,
3
T. D. Nikam ,
4
and Penna Suprasanna
2
1
Department of Botany, R. K. Talreja College of Arts, Science and Commerce, Affiliated to University of Mumbai,
Ulhasnagar 421003, India
2
Nuclear Agriculture and Biotechnology Division, Bhabha Atomic Research Centre, Mumbai 400085, India
3
Indian Agricultural Research Institute, Centre for Environment Science and Climate Resilient Agriculture CESCRA, Pusa,
New Delhi 110012, India
4
Department of Botany, Savitribai Phule Pune University Pune, Pune 411007, India
Correspondence should be addressed to Ganesh C. Nikalje; ganeshnikalje7@gmail.com
Received 9 September 2022; Accepted 6 October 2022; Published 18 October 2022
Academic Editor: Euripedes Garcia Silveira Junior
Copyright ©2022 Ganesh C. Nikalje et al. is is an open access article distributed under the Creative Commons Attribution
License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is
properly cited.
Cesium (Cs) is a soil contaminant and toxic to the ecosystem, especially the plant species. In this study, we have assessed the
potential of a halophyte Sesuvium portulacastrum for its Cs tolerance and accumulation. irty days old S. portulacastrum plants
were subjected to different concentrations of Cs (0, 5, 10, 25, 50, and 150 mg·L
−1
Cs) using cesium chloride. e biomass and
photosynthetic pigments were not affected up to 25 mg·L
−1
Cs treatment while a significant decline in pigment levels was observed
at higher concentrations. e Cs treatments increased protein content at low concentrations while higher concentrations were
inhibitory. Under Cs exposure, significant induction of antioxidant enzymes such as ascorbate peroxidase (APX), catalase (CAT),
glutathione reductase (GR), and superoxide dismutase (SOD) was observed. e antioxidant enzyme activities were upregulated
up to 50 mg·L
−1
Cs but decreased significantly at 150 mg·L
−1
. e accumulation of Cs was dose and tissue-dependent as evidenced
by a higher accumulation of Cs in leaves (536.10 μg·g
−1
) as compared to stem (413.74 μg·g
−1
) and roots (284.69 μg·g
−1
). e results
suggest that S. portulacastrum is a hyper-accumulator of Cs and could be useful for the phytoremediation of Cs-
contaminated soils.
1. Introduction
e excess level of cesium (Cs) in soil imposes a negative
impact on plant growth and development [1]. Cs restricts
the uptake of potassium (K) due to its chemical resem-
blance with potassium and creates severe potassium
deficiency followed by subsequent chlorosis in plants
[2, 3]. Most of the Cs in the natural atmosphere are
nonradioactive Cs-133 and are present in the soil at about
25 μg·g
−1
soil [4]. e group I alkali metal Cs is mostly
nonradioactive Cs-133 but some occur as radioactive
isotopes (Cs-137, Cs-134) which enter into the ecosystem
[5]. It is not only incorporated into the food chain but
also emits βand cradiations which have long half-lives
[6]. Different physical and chemical methods are used for
the removal of radionuclides and toxic metals. However,
their widespread and large-scale applications have lim-
itations due to high costs and some side effects [7]. Some
alkaliphilic bacteria such as Microbacterium sp TS-1 can
grow in presence of 1.2 M cesium chloride [8]. e studies
on ecto- and endo-mycorrhizal fungi revealed that they
reduce Cs toxicity by limiting Cs availability to their host
plant through immobilization between 10 and 100% of
the total Cs activity [9]. Some plant species are endowed
with the ability to extract or absorb radionuclides and
other heavy metals from the soil. is ability can be
utilized for environmental clean-up. Under increasing Cs
treatment (0.4 mM, to 3 mM), Arabidopsis thaliana, Calla
Hindawi
Advances in Agriculture
Volume 2022, Article ID 9863002, 7 pages
https://doi.org/10.1155/2022/9863002

palustris, Pennisetum purpureum, and Ocimum basilicum
showed increased uptake of Cs [10–13], respectively.
Similarly, Sorghum bicolor accumulated 5270 mg·kg
−1
in
roots and 4513 mg·kg
−1
in hydroponically grown aerial
parts without significant change in plant height and dry
weight [14].
Being native flora of saline soils, halophytic plants are
better suited to tolerate high salt due to efficient ROS
scavenging, compartmentation, and excretion mechanisms
to maintain water balance [15, 16]. is mechanism of
tolerance in halophytes has also been shown towards metal
stress and different inorganic pollutants [17–19].
S. portulacastrum is a facultative halophyte that grows
luxuriantly on the tropical and subtropical shores of five
continents [20]. It is highly tolerant to different abiotic
stresses such as salt, drought, heavy metals, and textile dyes
[20]. In the last decade, apart from its salt tolerance
mechanism, this plant has been extensively studied for its
applicability in phytoremediation of heavy metals such as
cadmium, arsenic, lead, nickel, copper [21–23], textile dyes
[24], and desalination [25]. Sesuvium plants rapidly uptake
the toxic compounds and translocate them to aerial parts
such as leaves. In leaves, these compounds are sequestered
into vacuoles without any toxicity [26]. However, the effect
of stable Cs on S. portulacastrum has not been studied
warranting such studies will help to assess toxicity and/or
accumulation.
e evaluation of Sesuvium for cultivation on Cs-con-
taminated soil requires a study about Cs toxicity, tolerance,
and accumulation in different organs. erefore, the re-
sponses of Sesuvium to Cs were studied in hydroponics to
provide a homogenous substrate and avoid interference of
soil particles. e effect of increasing the concentration of Cs
was analyzed by monitoring plant growth in terms of root
length, shoot length and fresh weight, and physiological and
biochemical status in terms of percent tissue water content,
chlorophyll content, phosphate soluble proteins, and anti-
oxidant enzymes. e hypothesis of this study is that
Sesuvium is a hyper-accumulator of Cs and the objectives are
to study the Cs accumulation potential of Sesuvium and
analyze the effect of Cs on the growth and biochemical
responses of Sesuvium.
2. Materials and Methods
2.1. Plant Material and Growth Conditions. In the present
study, a facultative halophyte S. portulacastrum L. was
assessed for accumulation and tolerance to stable Cs (
133
Cs).
e shoots (4–5 cm long) of naturally grown
S. portulacastrum were collected from the coastal areas of
Mumbai, India (19°03′51.6″N 72°58′44.2″E). e plants were
surface sterilized and hydroponically maintained as per
Nikalje et al. [19]. e experiments were carried out in a
plant growth chamber (Sanyo, Japan) with 14 h: 10 hr light/
dark cycle, 25/22°C day/night temperature, light intensity
150 μE·m
−2
·S
−1
, and relative humidity 65–75%. After four
weeks of growth, seedlings were subjected to different Cs
treatments.
2.2. Cesium Treatment. e rooted shoots were transferred
(twelve plants per treatment) into 500 ml half-strength
Hoagland’s nutrient solution added with Cs at various
concentrations: 0, 5, 10, 25, 50, and 150 mg·L
−1
using cesium
chloride. e plants were harvested after 28 days. e plant
parts viz. root, stem, and leaves were separated and used for
further analysis.
2.3. Growth and Biochemical Attributes. Plant growth was
measured in terms of root length, shoot length, and root and
shoot percent tissue water content (%TWC). e fresh
weight (FW) was immediately taken; leaves, stem, and roots
were oven dried separately at 60°C till constant dry weight
(DW).
Percent tissue water (%TWC) content was calculated
using the following formula [26]:
%TWC �(FW −DW)
FW
􏼢 􏼣×100.(1)
For the estimation of Chl a, Chl b, and total chlorophyll,
the leaves (300 mg) were crushed in 5 ml chilled 80% acetone
in precooled mortar and pestle in the dark. After centri-
fugation, the absorbance of the supernatant was taken at 645
and 663 nm [27].
e extraction and estimation of soluble protein content
were performed as per Lowry’s method [28] where Bovin
serum albumin served as standard. e antioxidant enzymes
activities such as superoxide dismutase [29], catalase [30],
ascorbate peroxidase [31], and glutathione reductase [32]
were performed with some modifications given by Nikalje
et al. [19].
2.4. Cesium Quantification. After oven drying at 60°C, the
plant samples (roots, stem and leaves separately) were finely
ground, weighed (quantity in g), and digested using 10 ml of
the di-acid mixture (HNO
3
: HClO
4
) (5:1) on a hot plate. e
Cs content in the digested extract was determined by atomic
absorption spectrophotometer (GBC906AA, Australia) us-
ing Cs hollow cathode lamp at 852 nm wavelength.
2.5. Experimental Design and Statistical Analyses. All the
experiments were performed in completely randomized
design in triplicates. A total of 12 plants were subjected to
each treatment and three biological and technical replicates
were used for each studied parameter. e data were ana-
lyzed by one-way analysis of variance (ANOVA) using the
statistical software SPSS 20.0. e treatment means were
compared by using Duncan’s multiple range test (DMRT) at
p≤0.05 and data were expressed as mean ±SE.
3. Results
3.1. Plant Growth and dry Biomass. S. portulacastrum plants
were challenged with different levels of Cs viz, 0, 5, 10, 25, 50,
and 150 mg·L
−1
. e results showed that up to 25 mg·L
−1
Cs,
plants did not exhibit significant growth retardation but
slight growth enhancement was observed at 5 and 10 mg·L
−1
2Advances in Agriculture

Cs. When Cs was applied beyond 50 mg·L
−1
, chlorosis was
observed, and growth was significantly inhibited (Figure 1).
At 5 and 10 mg·L
−1
Cs, it was seen that the root length was
higher as compared to control and other treatments while
there were no significant changes in shoot length (Figure 2).
On application of 25, 50, and 150 mg·L
−1
Cs, the length of
both root and shoot was decreased gradually. At 150 mg·L
−1
Cs treatment the root and shoot length decreased signifi-
cantly by 1.83-fold and 1.8-fold, respectively, at p ≤0.05
(Figure 2).
3.2. Percent Tissue Water Content (%TWC). e percent
tissue water content of both the root and shoot showed a
similar trend (Figure 3). e %TWC increased gradually up
to 25 mg·L
−1
Cs while it decreased significantly at 150 mg·L
−1
Cs. At 50 mg·L
−1
, the %TWC was not significantly different
from that of the control.
3.3. Chlorophyll Pigments. e chlorophyll pigments were
highly susceptible to high Cs treatment (Figure 4). e total
chlorophyll, chlorophyll-a, and chlorophyll-b contents were
maintained up to 10 mg·L
−1
Cs concentration. However, Cs
treatment of 25 mg·L
−1
and above caused a gradual decrease
in the content of chlorophyll pigments. As compared to the
control, the total chlorophyll, chlorophyll-a, and Chloro-
phyll-b content was decreased at 150 mg·L
−1
Cs by 2.08, 2.76,
and 2.7-fold, respectively, at p ≤0.05 (Figure 3).
0510
25 50 150
Figure 1: Effect of cesium on the growth of S. portulacastrum.
Plants were subjected to different concentrations of Cs (0, 5, 10, 25,
50, and 150 mg·L
−1
) and harvested after 28 days of treatment for
growth analysis.
ab aa
c
d
de
a
a
a
bb
c
0
2
4
6
8
10
12
Control 5 10 25 50 150
cm
Cs (mg.L-1)
Root length
Shoot length
Figure 2: Effect of cesium on root and shoot length of
S. portulacastrum. All the values are mean of twelve readings ±S.E.
One-way ANOVA significant at p ≤0.05. Different letters indicate
significantly different values in root or shoot (DMRT p ≤0.05).
bb
aa
b
c
b
b
a
ab
c
86
87
88
89
90
91
92
93
94
95
96
0 5 10 25 50 150
% tissue water content
Cs (mg.L-1)
Root
Shoot
Figure 3: Effect of cesium on % tissue water content of
S. portulacastrum. All the values are mean of twelve readings ±S.E.
One-way ANOVA significant at p ≤0.05. Different letters indicate
significantly different values in root or shoot (DMRT p ≤0.05).
0
1
2
3
4
5
6
7
8
9
Control 5 10 25 50 150
Chlorophyll (mg.g-1 FW)
Cs (mg.L-1)
Tot al ch l
Chl. A
Chl. B
aaa
b
dcd
aaa
b
dcd
aaabcc
Figure 4: Effect of cesium on chlorophyll content of
S. portulacastrum. All the values are mean of twelve readings ±S.E.
One-way ANOVA significant at p ≤0.05. Different letters indicate
significantly different values in total chlorophyll, chlorophyll-a, or
chlorophyll-b (DMRT p ≤0.05).
Advances in Agriculture 3

3.4. Antioxidant Enzyme Activities. Both root and shoot
tissues showed similar antioxidant enzyme activities viz.
superoxide dismutase (SOD), catalase (CAT), ascorbate
peroxidase (APX), and glutathione reductase (GR) under Cs
exposure (Figures 5(a)–5(d)). e antioxidant enzyme ac-
tivities were significantly increased up to 50 mg·L
−1
Cs,
treatment while, higher concentration (150 mg·L
−1
) induced
a significant decrease in enzyme activities. e SOD activity
was increased by 2-fold in the root and 2.5-fold in the shoot
at 50 mg·L
−1
Cs while it was decreased by 1.4–1.5-fold in the
root and shoot at 150 mg L
−1
Cs (Figure 5(a)). e CAT
activity was increased by 2.1-fold in the root and 1.8-fold in
the shoot at 50 mg·L
−1
Cs while 150 mg·L
−1
Cs induced a
decrease in activity by 1.7-fold in the root and 1.2-fold in the
shoot (Figure 5(b)). A similar trend was observed in the case
of APX activity which recorded an increase of 1.5-fold in
root and 2.4-fold in the shoot at 50 mg·L
1
Cs and a decrease
of 1.9-fold in root and 1.5-fold in the shoot at 150 mg·L
−1
Cs
(Figure 5(c)). Compared to other enzymes, the GR activity
showed higher activity (3.4-fold in the root and 5-fold in the
shoot at 50 mg·L
−1
Cs) whereas 150 mg·L
−1
Cs induced a
decrease of 0.8-fold in the root. Although GR activity was
decreased at 150 mg·L
−1
Cs in the shoot, it was still 3-fold
higher than control plants (Figure 5(d)).
3.5. Cesium Accumulation in Different Plant Parts. e ac-
cumulation of Cs in different parts of the plant (root, stem,
and leaves) is depicted in Figure 6; e Cs accumulation was
higher in aerial parts (leaves and stem) as compared to
underground parts (root). In leaves, the Cs level was highest
(536.10 μg·g
−1
) followed by the stem (413.74 μg·g
−1
) and
roots (284.69 μg·g
−1
) suggesting the dose and tissue-specific
nature of Cs accumulation in Sesuvium.
4. Discussion
e presence of metal toxicants including radiocesium in
soil, water, and air can cause serious consequences to human
health and the environment [33]. A recent survey on heavy
0
10
20
30
40
50
60
70
80
SOD (Units. mg-1 protein)
Root
Shoot
Control 5 10 25 50 150
Cs (mg.L-1)
cc
bc b
a
d
ccc
b
a
d
(a)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
1.8
Catalase (Units. mg-1 protein)
Root
Shoot
Control 5 10 25 50 150
Cs (mg.L-1)
cc
cab
a
d
cc
c
b
a
d
(b)
0
5
10
15
20
25
APX (Units. mg-1 protein)
Root
Shoot
Control 5 10 25 50 150
Cs (mg.L-1)
bbb
aa
c
dd
c
ba
c
(c)
GR (Units. mg-1 protein)
0.02
0.04
0.06
0.08
0.1
0.12
0.14
0.16
0.18
0.2
Root
Shoot
0
Control 5 10 25 50 150
Cs (mg.L-1)
d
cc
b
a
cd
d
c
c
b
a
c
(d)
Figure 5: Effect of cesium on antioxidant enzymes activity of S. portulacastrum: (a) superoxide dismutase (SOD), (b) catalase (CAT), (c)
ascorbate peroxidase (APX), and (d) glutathione reductase (GR). All the values are mean of twelve readings ±S.E. One-way ANOVA
significant at p ≤0.05. Different letters indicate significantly different values of antioxidant enzymes (DMRT p ≤0.05).
4Advances in Agriculture

metal pollution of global rivers and water lakes revealed that
the concentration of heavy metals in these water bodies is
exceeding significantly the standard threshold limits as per
World Health Organization (WHO) and the United States
Environmental Protection Agency (USEPA) [34]. Phytor-
emediation is one of the plant-based approaches to manage
environmental toxicity [35]. e results of our study
demonstrated that the impact of Cs depends on the level of
accumulation and localization besides the tolerance of the
plant species. It was observed that the growth of root and
shoot along with their relative water content was not affected
at 25 mg·L
−1
of Cs in Sesuvium. In Calendula alata, Borghei
et al. [36] observed maintenance of plant growth, root
length, shoot length, and chlorophyll contents at lower
concentrations up to 10 mg·L
−1
Cs but beyond this con-
centration, growth was retarded. Higher Cs concentration
(3 M Cs) also showed a reduction in shoot growth in the Cs
hyper-accumulator Pennisetum purpureum [10]. Excessive
Cs has also been found to induce black roots and slow
growth in Brassica juncea seedlings [37]. Higher concen-
trations of Cs affected the number of germinated seeds and
roots and the shoot length of seedlings [38]. Our results
showed that increasing the concentration of Cs caused a
reduction in the total chlorophyll content including, chlo-
rophyll-a and chlorophyll-b. e Cs-induced inhibition of
chlorophyll content has also been observed in other plant
species, such as Spinacia oleracea [39] Nitella pseudo-
flabellata [40], Salix paraplesia [41], and Brassica juncea
[37].
e toxic metals induce different morphological,
physiological, and biochemical dysfunctions by the gen-
eration of reactive oxygen species which impose damaging
effects on plants [42]. In Arabidopsis, exogenous appli-
cation of a small chemical compound namely CsToAcE
increased Cs accumulation and tolerance. e CsToAcE1
interacts with a plant protein BETA GLUCOSIDASE 23
(AtβGLU23) and suppresses it. is protein negatively
regulates plant response to Cs [43]. Plants cope with the
toxic effects of heavy metals by the induction of an effi-
cient antioxidant defense system. Our results indicated
that higher antioxidant enzymatic activity (GR activity,
3.4-fold higher in root and 5-fold in the shoot, at
50 mg·L
−1
of Cs) in S. portulacastrum suggesting the role
of efficient antioxidant enzyme system in case of Cs
tolerance. Enhanced induction of antioxidant defense
(SOD, POD, CAT, and APX) has also been shown under
Cs treatment in Brassica juncea [44]. Recently, Adams
et al. [1] have observed Cs-induced higher glutathione
accumulation without reduction in the Cs accumulation
pattern in Arabidopsis thaliana. e Cs being the com-
petitor of potassium ion (K
+
) competes with potassium for
uptake. e unavailability of potassium causes growth
retardation in plants [45, 46]. In Gladiolus grandiflora,
supplementation of potassium showed alleviation of Cd-
induced toxicity [47]. Mostofa et al. [48] stated that
improvement of plant potassium use efficiency can in-
crease plant performance in Cs-contaminated soil. On the
contrary, in the case of halophytes instead of potassium
and chloride, sodium is an important macronutrient for
their growth [49]. is could be the probable reason for
the high tolerance of Cs in S. portulacastrum. A signifi-
cantly higher amount of Cs was accumulated in the aerial
parts (536.10 μg·g
−1
in leaves and 413.74 μg·g
−1
in the
stem) as compared to the underground parts (284.69 μg
g
−1
in roots) suggesting that root-to-shoot translocation
of Cs is rapid in S. portulacastrum. Such efficient and rapid
translocation of toxic compounds from root to shoot is a
prerequisite for effective phytoremediation as previously
suggested by other researchers [37, 44]. Our results
suggest that the facultative nature of S. portulacastrum
helps it to grow in both saline and nonsaline habitats
offering an additional advantage over true halophytes
which require a certain amount of salt for growth. Such
halophytic species also can be useful as candidates for
deciphering the mechanism of salt and metal tolerance,
and also for isolating stress-responsive genes which can be
applied to enhance the tolerance of sensitive, glycophytic
plants [50].
5. Conclusions
is study concludes that S. portulacastrum is a hyper-ac-
cumulator of toxic Cs metal. e higher accumulation of Cs
in aerial plant parts and less alteration in growth revealed the
potential of Sesuvium as a suitable candidate for the phy-
toremediation of Cs-contaminated soil. e efficient anti-
oxidant enzyme system and maintenance of growth are the
key components of Cs tolerance in Sesuvium. It is recom-
mended that S. portulacastrum can be cultivated in Cs-
contaminated soils and near nuclear power plants for
phytoremediation. Further studies are required to under-
stand the precise molecular mechanism of Cs tolerance, the
involvement of Sesuvium-associated microbes, and valida-
tion through field experiments to confirm the phytor-
emediation ability of Sesuvium.
0
100
200
300
400
500
600
Control 5 10 25 50 150
Accumulated Cs (µg.g-1)
Cs (mg.L-1)
Root
Shoot
Leaf
ed
cb
a
ed
c
b
a
ed
c
b
a
Figure 6: Cesium accumulation in root, stem, and leaves of
S. portulacastrum. All the values are mean of twelve readings ±S.E.
One-way ANOVA significant at p ≤0.05. Different letters indicate
significantly different values in root, stem, or leaves (DMRT
p≤0.05).
Advances in Agriculture 5

Data Availability
All relevant data are included within the article.
Conflicts of Interest
e authors declare that there are no conflicts of interest.
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