Bioremediation & Biodegradation
Research
Article
Research
Article
Hegazy et al., J Bioremed Biodeg 2013, 4:3
http://dx.doi.org/10.4172/2155-6199.1000185
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OpenAccess
Access
Variations of Plant Macronutrients and Secondary Metabolites Content in
Response to Radionuclides Accumulation
Hegazy AK1,3*, Al-Rowaily SL2, Kabiel HF3, Faisal M1 and Emam MH3
1
2
3
Department of Botany and Microbiology, College of Science, King Saud University, Riyadh, Saudi Arabia
Department of Plant Production, college of Food and Agricultural Sciences, King Saud University, Riyadh, Saudi Arabia
Botany Department, Faculty of Science, Cairo University, Giza, Egypt
Abstract
Current knowledge on the basic radionuclide tolerance indicates that plants may develop mechanisms preventing
the damaging effects of radionuclide stress. The radionuclides content was determined in the Mediterranean coastal
black sand soil and in the edible portions of the four food crop plant species, viz., Eruca sativa, Lycopersicon
esculentum, Pasidium guajava and Mangifera indica. Biochemical and nutritional constituents were assessed to
elucidate the possible effect of radionuclides on the edible portions of the plants. The ability of the four study plant
species to accumulate Uranium and Thorium in their edible portions from the coastal black sand soil is higher than
that absorbed from the inland agricultural soils. The nutritional constituents were affected by the high concentrations
of Uranium and Thorium in the plant tissues. The total protein, moisture content, total phenolic compounds, total
chlorophyll, total carotenoids, β-Carotene and Lycopene were positively correlated with Uranium and Thorium
concentrations in the plant tissues, while the mineral content, vitamin C and total flavonoids were suppressed by
high concentrations of Uranium and Thorium in the plant tissues. The fluctuations in the biochemical or nutritional
constituents of the plant edible portions are considered an important defense mechanism to control the redox state
of the cells accumulating radionuclides with high levels.
Keywords: Nutritive value; Antioxidants; Phenolic compounds;
Flavonoids; Uranium; Thorium
Introduction
Soil has always been important to humans and their health, providing
a resource that can be used for shelter and food production [1]. Some
elements are essential mineral nutrients for plants, with a requirement
throughout life and its absence produces specific deficiency symptoms.
In contrast all trace elements are toxic if their intake through ingestion
or inhalation is excessive. In particular Ag, As, Be, Cd, Hg, Pb and some
of the daughter products of Uranium are good examples of potentially
harmful elements that have no proven essential functions in humans,
and are known to have adverse physiological effects at relatively low
concentrations. Despite this, known causal relationships between
health problems and the elements in human foods derived from the
immediate soil environment are limited [1].
In some parts of the world, population growth and movement,
industrial development and food security have resulted in pressure to
use agricultural lands containing relatively high levels of radioactivity,
for instance in the monazite areas of India and Brazil, and in parts of
Iran with 226Ra anomalies where exposures up to tens of mSv, and in
extreme cases 100 mSv, occur annually [2] and in many localities of
black sand along the Mediterranean coast of Egypt [3-5].
In Egypt, the occurrences of black sand deposits are known at the
Nile mouth near Damietta and Rosetta and have been worked for their
heavy mineral content such as magnetite, ilmenite, zircon and monazite
[6,7]. Uptake of radionuclides from contaminated soil represents a
significant pathway of human radiation exposure, either due to the
direct consumption of cereals, fruits and vegetables or, indirectly,
following consumption of milk and meat from animals fed on
contaminated vegetable matter [8]. The understanding the radioactive
mineral uptake by crop plants and the knowledge of its distribution in
different organs is important in the agricultural management, to avoid
its possible negative health effects.
The geochemistry of Uranium and Thorium is of particular interest
J Bioremed Biodeg
ISSN: 2155-6199 JBRBD, an open access journal
for radiological studies. Fundamental knowledge of biogeochemical
behavior of these metal and processes involved in their environmental
migration are also of particular importance for power generation, water
supply, agriculture and environmental protection and remediation
[9]. Environmental contamination caused by radionuclides, in
particular Uranium (U) and its decay products, is a serious problem
worldwide [10]. Uranium is the heaviest naturally occurring element,
found in small amounts in soil, rock, surface water and groundwater.
Uranium can enter the human body through inhalation, ingestion, or
penetration through the skin [11]. Ingestion from food or water is the
main source of internally deposited Uranium in humans. It is both
an alpha-emitter with a radiotoxic potential and a heavy metal with a
chemotoxic potential. Chemical toxicity of U is predominantly caused
by the aqueous hexavalent uranyl ion [UO2]2+ due to its high reactivity
with oxygen binding centers. Hence, it resembles Ca2+ and Mg2+, but
with U complexes of higher stability are formed. [UO2]2+ has a strong
affinity for phosphate moieties and sugar alcohol groups of nucleotides
and polynucleotides and as such, causes DNA damage [10]. Yet, a wide
range of organisms in both terrestrial and aquatic environments take
up U including plants, bacteria, algae, and fungi [12].
The major health effect of depleted or natural Uranium exposure
has been reported to be chemical kidney toxicity rather than a radiation
*Corresponding author: Hegazy AK, Department of Botany and Microbiology,
College of Science, King Saud University, Riyadh, Saudi Arabia, Tel:
+966541792717; Fax: +96614675833; E-mail: [email protected]
Received December 21, 2012; Accepted April 15, 2013; Published April0 17,
2013
Citation: Hegazy AK, Al-Rowaily SL, Kabiel HF, Faisal M, Emam MH (2013)
Variations of Plant Macronutrients and Secondary Metabolites Content in Response
to Radionuclides Accumulation. J Bioremed Biodeg 4: 185. doi:10.4172/21556199.1000185
Copyright: © 2013 Hegazy AK, et al. This is an open-a ccess article distributed
under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the
original author and source are credited.
Volume 4 • Issue 3 • 1000185
Citation: Hegazy AK, Al-Rowaily SL, Kabiel HF, Faisal M, Emam MH (2013) Variations of Plant Macronutrients and Secondary Metabolites Content
in Response to Radionuclides Accumulation. J Bioremed Biodeg 4: 185. doi:10.4172/2155-6199.1000185
Page 2 of 10
hazard [11]. However, little is known about the effects of long-term
Uranium exposure in humans. In animals, studies described effects
of chronic exposure to Depleted Uranium (DU) through drinking
water on the central nervous system, on reproduction or on xenobiotic
detoxification [11]. It was reported that vitamin D3 metabolism,
involved in mineral homeostasis and bone mineralization, was
affected after a long-term exposure with environmental doses of DU
or another radionuclide 137Cesium [11]. In plants, effects of U on
biomass, root growth, root cell viability and interactions with mineral
nutrients are reported [13]. Variable responses in plants are induced
upon U exposure, which are linked with the differences in Uranium
bioavailability [4,5]. Recent studies show an increase in the production
of Reactive Oxygen Species (ROS) and consequent stimulation of
antioxidant defenses in response to U exposure similar to that observed
upon exposure of plants to redox-active metals like Cu [10]. However,
the effect of U on the plant’s oxidative defense system is yet to be
thoroughly investigated.
Current knowledge on the ubiquitous basic metal tolerance
indicates that plants share several common mechanisms preventing the
damaging effects of the metallic stress instead of developing proteins
that could resist the heavy metal effects. These mechanisms involve
reduced metal uptake, oxidative defense, metal chelation, repair of
stress-damaged proteins and vacuolar compartmentalization [14].
Many nutritional factors are widely considered to be critical for human
health. Among them, free radicals have been of concern as one of the
factors contributing to chronic degenerative disease [15]. Usually
the human body has mechanisms for eliminating the free radicals by
some nutrients in the diet that have antioxidant activities. The dietary
antioxidant has been defined as a substance in commonly consumed
foods that significantly decreases the adverse effects of chemically
reactive species on normal physiological functions in humans [15]. In
recent years, an interest has been focused on antioxidant vitamins C
and E, phenolics and carotenoids due to their ability to scavenge active
oxygen species and free radicals [16]. Vegetables and fruits containing
vitamin E, beta-carotene, and lycopene constitute natural sources of
antioxidants. Antioxidants function to decrease DNA damage, reduce
lipid peroxidation, and inhibit malignant transformation or cell
proliferation [17].
Crop plant species or fruit trees raised in radionuclide contaminated
soil may take up radionuclides and accumulate them in their edible
portions. These absorbed radioactive elements may affect negatively or
positively the biochemical and phytochemical constituents of the plants
that can be used as a defense mechanism to control the undesirable
effects of toxic elements. The present study was conducted to assess the
radionuclides uptake by four commonly cultivated crop species in the
Mediterranean coastal black sand and inland soils. The physiological
and biochemical response that may be associated with radionuclides
uptake in the edible portions of the study plant species was assessed.
Materials and Methods
Study site
The present study was conducted in the Mediterranean coastal
black sand deposits Nile delta, Egypt. The site is located around Lake
El-Burullus between longitudes 31° 5′ E and latitudes 31° 35′ N. Black
sand deposits are rich in heavy minerals e.g. zircon (ZrSiO4), rutile
(TiO2) and ilmenite (FeTiO3). They are economically important and
are characterized by high concentrations of Thorium (232Th) and
Uranium (238U) in their crystalline structure [3,18]. Inland sites
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ISSN: 2155-6199 JBRBD, an open access journal
were selected in the main agricultural land of Nile delta as control for
comparison with the coastal black sand.
Study species
Two crop plant species namely Rocket (Eruca sativa Mill.) and
Tomato (Lycopersicon esculentum L.) and the two common fruit trees
Guava (Psidium guajava L.) and Mango (Mangifera indica L.) were
used in this study.
Determination of radionuclides content
The soil and the edible portions of the study plant species were
collected from the coastal black sand and from inland cultivated site.
The concentrations of Uranium and Thorium in the edible portions
of the study plant species were measured by spectrophotometric
technique [19], using high resolution Inductively Coupled Plasma
Mass Spectrometer (ICP-MS technique) model Jeol-JMS-PLASMAX2,
at the Central Laboratory for Elemental and Isotopic Analysis, Nuclear
Research Center, Atomic Energy Authority, Egypt. Plant samples were
oven dried at 105°C for 24 hours. Upon removal from the oven, the
samples were stored in desiccators and thoroughly ground into fine
powders. Exact 500 mg for each sample were dissolved in a mixture
of mineral acids using a microwave digestion system and then heated
to dryness. The residue was dissolved in 20 mL of 2% HNO3 (40 times
dilution). The measured Uranium and Thorium concentrations in soil
and plant samples were obtained in ppm and converted to unite of
Bq Kg-1 dry weight by multiplying the value of Uranium by 12.34 and
multiplying the value of Thorium by 4.04.
Phytochemical analysis
The edible portions of the plant materials were collected in plastic
bags and transferred in ice box to the laboratory within three hours
after collection. The material was handily cleaned and washed with
distilled water before further processing and analysis.
Macronutrients content
Moisture was determined according to Association of Official
Analytical Chemist [20], 5 g of air dried plant sample were accurately
weighed in porcelain crucible, and then dried in an oven at 105ºC until
constant weight was obtained. The loss in weight was calculated and
reported as percent moisture.
For ash determination, exact 2 g of air dried plant sample were
heated in a crucible at 100ºC until water was expelled. The crucible was
then left in a muffle furnace at 550ºC to a constant weight. The weight of
the residue was calculated and expressed as percent ash [20].
Total protein content was calculated by multiplying the total organic
nitrogen by 6.25. Total nitrogen was determined by kjeldahl method
[21]. The dried sample (1 g) was digested with concentrated sulfuric
acid in the presence of digestion catalyst (a mixture of copper sulfate
and anhydrous sodium sulfate, 1:10). The digestion was carried out
using Kjeldatherm; Gerhardt, laboratory instrument. After digestion,
the solution was treated with excess NaOH (50 ml, 50%). The ammonia
was received into (50 ml, 20%) boric acid and titrated with 0.1 N
sulfuric acid. Titration was carried out using Vapodest 50s; Gerhardt,
laboratory instrument. Crude fats were extracted and determined using
Soxtherm; Gerhardt, laboratory instrument according to Association
of Official Analytical Chemist [20]. Ten grams dried plant sample was
extracted using chloroform methanol (2:1 v/v). The extract was dried
over anhydrous sodium sulfate, and then the solvent was removed by
Volume 4 • Issue 3 • 1000185
Citation: Hegazy AK, Al-Rowaily SL, Kabiel HF, Faisal M, Emam MH (2013) Variations of Plant Macronutrients and Secondary Metabolites Content
in Response to Radionuclides Accumulation. J Bioremed Biodeg 4: 185. doi:10.4172/2155-6199.1000185
Page 3 of 10
heating at 80ºC under vacuum. The residue was cooled, weighed and
expressed as percent lipid.
For fiber determination, a known weight of the ground sample (2 g)
was boiled in 1.25% H2SO4 for 30 minutes and filtered then thoroughly
washed with hot distilled water. The residue was boiled with 1.25%
NaOH solution for 30 minutes, and then filtered. The residue was
washed with distilled water followed by ethyl alcohol and acetone, then
dried at 100ºC to constant weight. The ash content was determined
and subtracted from the dry weight of treated material to give the fiber
content [20].
Regarding total carbohydrate determination, a known weight (0.5
g) of the dried sample was placed in a test tube, and then sulfuric acid (10
ml-1 N) was added. The tube was placed overnight in an oven at 100ºC.
The solution was then filtered into measuring flask and completed to
the mark with distilled water. The total hydrolysable carbohydrates
were determined calorimetrically with the phenol-sulfuric acid method
according to Dubois M [22].
The energy content was estimated by multiplying the percentages
of crude protein, crude fat and digestible carbohydrates by their
respective Atwater factors 4, 9 and 4, respectively [23,24]. The obtained
value represents the nutritive value.
Macroelements
Analysis was made according to Wu et al. [25], by using a known
weight (0.5g) of the dried sample and wet digestion was conducted using
a microwave oven (Advanced Microwave Digestion System. ETHOS1).
Total content of macroelements were determined in the digested
solution using inductively coupled plasma emission spectrometry (ICP
6000 Series; Thermo Scientific) according to Allen et al. [26].
Vitamin A content
According to Neeld and Pearson [27], 2 g fresh plant material was
mixed with 2 ml 95% ethanol followed by 3 ml petroleum ether and
shaked for two minutes for extraction of vitamin A. After centrifugation
supernatant was placed in a cuvatte, then the absorbance was
determined at 450 nm against petroleum ether blank. Petroleum ether
was evaporated to dryness in a water bath then the residue was taken up
in 0.1 ml chloroform and 0.1 ml acetic anhydride was added. Vitamin
A was read at 620 nm against a blank consisting 0.1 ml chloroform and
1ml trifluoroacetic acid reagent. Vitamin A in the sample was calculated
as following: µg vitamin A/100 g fresh weight plant sample=OD620(OD450×0.3)×337, Whereas OD=Optical Density.
2 ml of 75 g/l sodium carbonate was then added. After incubation at
room temperature for 2 h, the absorbance of the reaction mixture was
measured at 760 nm against methanol blank. Gallic acid was used as
standard to produce the calibration curve.
Total flavonoids
Total flavonoids in 1 g sample were extracted with 10 ml 80%
ethanol for 20 min with continuous shaking [30]. After centrifugation
for 10 min, the supernatant was collected. Exact 0.5 ml of extract was
mixed with 1.5 ml of 95% ethanol, followed by 0.1 ml of 10% aluminum
chloride, 0.1 ml of 1 M potassium acetate and 2.8 ml distilled water.
After incubation at room temperature for 30 min, the absorbance of the
reaction mixture was measured at 415 nm. The flavonoid content was
calculated using a standard calibration of rutin solution.
Antioxidant activity
The antioxidant activity was determined by the free radical
scavenging effect of the plant extract assessed by the decolouration
of the methanolic solution DPPH (1,1 diphenyl-2-picryl hydrazyl)
radical according to Lee et al. [31]. Dried plant sample was dissolved in
methanol then 5 ml of DPPH solution added. Different concentrations
of the plant extract were prepared. Methanolic DPPH was used as
control. After 30 min, the absorbance was measured at 517 nm.
Rutin was used as reference free radical scavenger at the same dose.
The antioxidant activity was expressed as: DPPH decolouration
%=100×(A1-A2 /A2), whereas A1 is the absorbance of the control and
A2 the absorbance in the presence of the tested extracts.
Total chlorophyll
The determination was carried out according to the method
reported by Holden [32]. The fresh sample (0.5 g) was grounded in
a mortar with acetone in the presence of little amount of calcium
carbonate then filtered. The residue was washed with acetone several
times until the washing liquid was colourless. The absorbance was
measured at 663 and 645 nm against 80% aqueous acetone as blank.
The concentration was calculated from the following equation.
Chlorophyll a (mg/g)=((12.3×A663-0.86×A645)/ a×100×w) v
Chlorophyll b (mg/g)=((19.3×A645-3.6×A663)/ a×100×w) v
Whereas A663 and A645 are the absorbance at 663 and 645 nm; a
is the length of light path in cell; w is the fresh weight in gram and v is
the volume in ml.
Vitamin C content
Total carotenoids
Vitamin C was determined according to Iqbal [28]. To accurately
weighted 1 g of each sample, 10 ml of 0.05 M oxalic acid solution
was added then the solution was placed under shade for 24 h to
extract vitamin C. After filtration, the filtrate was transferred to 25 ml
volumetric flask then 2.5 ml of 0.05 M oxalic acid solution was added.
Separately meta phosphoric acid with acetic acid, 5% sulphuric acid
and ammonium molybdate solution were added to the sample then
the volume was made up 25 ml with distilled water. The sample was
then analyzed for vitamin C at 760 nm compared with the standard
L-ascorbic acid.
Carotenoids were extracted from the plant samples and determined
spectrophotometrically following [33]. One gram of each sample
was saponified overnight with 0.5 N KOH at room temperature. The
saponified fraction was then transferred to separating funnel and
extracted several times with diethyl ether. The extract was washed
with distilled water and 0.5 N KOH then dried over anhydrous
sodium sulfate. A known volume of ether extract was evaporated at
room temperature then 5ml petroleum ether added. Carotenes were
measured at 440 nm against petroleum ether blank.
Total phenolics
Total phenolic content was determined by the Folin-Ciocalteu
method described by Meda A [29]. Two grams of fresh plant material
was mixed with 2.5 ml of 0.2 N Folin-Ciocalteu reagent for 5 min, then
J Bioremed Biodeg
ISSN: 2155-6199 JBRBD, an open access journal
β-Carotene and lycopene
The β -carotene and Lycopene were extracted using the method
described by Tee and Lim [34]. From the extract, 2.5 ml was mixed
with 40 ml methanol containing 1g potassium hydroxide. From the
concentrated extract, 2 ml were evaporated under running nitrogen,
Volume 4 • Issue 3 • 1000185
Citation: Hegazy AK, Al-Rowaily SL, Kabiel HF, Faisal M, Emam MH (2013) Variations of Plant Macronutrients and Secondary Metabolites Content
in Response to Radionuclides Accumulation. J Bioremed Biodeg 4: 185. doi:10.4172/2155-6199.1000185
Page 4 of 10
re-dissolved in 2 ml acetone, passed through a 0.45 µm millipore
membrane and 30 µl aliquots were injected into the HPLC system
(Hewlett Packard, HP 1090 liquid chromatography).
Results
Radionuclides content
Uranium and Thorium concentrations of the study soil are
summarized in table 1. The concentrations of Uranium and Thorium
were significantly higher in the coastal black sand soil than in the
inland soils. The Uranium concentration in the black sand soil where
E. sativa and L. esculentum cultivated were 76.919 ± 3.105 and 95.429
± 3.105 BqKg-1 dry weight respectively, which was significantly higher
than that in the inland soil where values attained 45.247 ± 1.885
and 46.892 ± 2.468 BqKg-1 dry weight respectively. The Uranium
concentrations in the coastal black sand soil supporting P. guajava was
86.791 ± 1.885 BqKg-1 dry weight, while in the inland soil, was 60.877
± 1.425 BqKg-1 dry weight. The same trend of results was observed
with the concentration of Thorium. Concentrations of Uranium and
Thorium determined in the edible portions of the study species are
shown in figure 1. Uranium and Thorium concentrations in the plants
cultivated in the coastal black sand soil generally attained values higher
than that in the plants cultivated in the inland soil. In the leaves of E.
sativa Uranium and Thorium concentrations were 4.196 ± 0.494 and
0.525 ± 0.008 BqKg-1 dry weight respectively in the plants cultivated
in the inland soil but these concentrations significantly increased to
12.957 ± 2.221 and 1.657 ± 0.364 BqKg-1 dry weight respectively in the
plants cultivated in the coastal black sand soil. Similarly, Uranium and
Thorium concentrations in fruits of L. esculentum, P. guajava and M.
indica from coastal black sand soil were significantly higher than their
concentrations in the plants cultivated in the inland sites.
Study species
Study soil
Uranium (Bq Kg-1)
Thorium (Bq Kg-1)
Eruca sativa
Black sand
76.919 ± 3.105***
32.458 ± 0.617***
Inland site
45.247 ± 1.885
16.027 ± 0.617
Lycopersicum esculentum
Black sand
95.429 ± 3.105***
31.246 ± 1.017***
Inland site
46.892 ± 2.468
11.448 ± 0.617
Psidium guajava
Black sand
86.791 ± 1.885***
20.067 ± 0.617***
Inland site
60.877 ± 1.425
7.946 ± 0.617
Mangifera indica
Black sand
81.855 ± 1.885***
24.242 ± 0.808***
Inland site
9.749 ± 0.445
1.912 ± 0.102
Different superscript stars for the same species indicate a significant difference, *** significant at P ≤ 0.001.
Table 1: Uranium and Thorium concentrations (BqKg-1 dry weight) in the soil of coastal black sand and in the inland (control) sites in which the study plant species were
cultivated. Data are expressed as mean ± S.D (n=5).
Uranium content (BqKg-1)
20
18
16
14
Black Sand
Control
20
***
18
16
**
12
10
10
8
8
6
6
4
4
2
2
0
0
Es
2.0
Thorium content (Bq Kg-1)
**
14
12
1.8
*
Le
1.6
***
**
Pg
1.4
1.6
Mi
***
1.2
1.4
1.2
1.0
1.0
0.8
0.8
***
0.6
0.6
0.4
0.4
0.2
0.2
0.0
0.0
Es
Le
Pg
Mi
Study species
Figure 1: Uranium and Thorium content (BqKg-1 dry weight) in the edible portions of the four study crop plants Eruca sativa (Es), Lycopersicum esculentum (Le),
Psidium guajava (Pg) and Mangifera indica (Mi) cultivated in the coastal black sand and in the inland sites. Vertical bar around the mean is the standard deviation.
Different superscript stars for the same species indicate significant differences, *** significant at P≤0.001; ** significant at P ≤ 0.01 and * significant at P ≤ 0.05.
J Bioremed Biodeg
ISSN: 2155-6199 JBRBD, an open access journal
Volume 4 • Issue 3 • 1000185
Citation: Hegazy AK, Al-Rowaily SL, Kabiel HF, Faisal M, Emam MH (2013) Variations of Plant Macronutrients and Secondary Metabolites Content
in Response to Radionuclides Accumulation. J Bioremed Biodeg 4: 185. doi:10.4172/2155-6199.1000185
Page 5 of 10
Proximate composition
The macronutrients content of the study plant species are shown
in table 2. Crude fibers attained value 0.737 ± 0.025 gm /100 gm dry
weight in leaves of E. sativa cultivated in the inland site, while in the
coastal black sand site, the value increased to 0.844 ± 0.018 gm/100 gm
dry weight. This is associated with the uptake of high level of Uranium
and Thorium and their accumulation in edible portions of the plants.
This was also observed in the nutritive values which increased from
27.279 ± 0.902 KCal in plants in the inland site to 32.461 ± 0.68 KCal
in plants in the coastal black sand. In L. esculentum, the chemical
composition didn’t showed significant difference between the values
in plants from the inland soil and plants from coastal black sand,
except for crude protein which significantly decreased. The total
carbohydrates and nutritive value significantly increased with the
increase of Uranium and Thorium content in the edible portions of the
plants cultivated in the coastal black sand site. For P. guajava cultivated
Proximate composition
Moisture content (%)
Eruca sativa
Black sand
Inland site
92.159 ± 0.164** 92.926 ± 0.234
in the inland soil, the moisture content reached 88.469 ± 0.163% and
significantly decreased to 83.582 ± 1.236% with the increased Uranium
and Thorium content in the coastal black sand site. In contrary, the
remaining chemical composition showed significant increase with
increased Uranium and Thorium in the plants (Table 2). For M. indica,
the measured proximate composition increased with uptake of more
Uranium and Thorium in the coastal black sand soil. The moisture
content reached 86.074 ± 0.071% in plants cultivated in the inland soil,
while decreased to 82.334 ± 0.202% in the coastal black sand site.
Macroelements content
The edible portions content of Ca, K and Na of the study plant
species are shown in figure 2. As indicated from the results, K content in
edible portions of study crop plant species (E. sativa and L. esculentum)
decreased with Uranium and Thorium uptake while in the edible
portions of the study fruit trees, values increased with accumulation
Lycopersicum esculentum
Psidium guajava
Black sand
Inland site
Black sand
93.338 ± 0.180
94.210 ± 0.546 83.581 ± 1.236** 88.469 ± 0.163 82.334 ± 0.202*** 86.074 ± 0.071
0.834 ± 0.079
Ash (g/100g)
1.404 ± 0.029**
1.618 ± 0.054
0.760 ± 0.020
Crude protein (g/100g)
3.335 ± 0.070***
2.120 ± 0.070
0.813 ± 0.022** 1.207 ± 0.114
Mangifera indica
Inland site
Black sand
Inland site
0.437 ± 0.033*
0.361 ± 0.005
0.331 ± 0.004***
0.064 ± 0.001
1.328 ± 0.100
1.203 ± 0.017
0.946 ± 0.011***
1.284 ± 0.007
Crude fat (g/100g)
0.669 ± 0.014**
0.600 ± 0.020
0.136 ± 0.004*
0.112 ± 0.011
2.09 ± 0.158***
0.907 ± 0.013
1.194 ± 0.014***
0.840 ± 0.004
Crude fibers (g/100g)
0.844 ± 0.018**
0.737 ± 0.025
0.779 ± 0.021
0.680 ± 0.064
4.597 ± 0.346***
3.003 ± 0.043
1.881 ± 0.022***
1.629 ± 0.009
Total carbohydrates (g/100g) 3.276 ± 0.068
Nutritive value (K.Cal/ 100g)
3.351 ± 0.111
4.953 ± 0.133** 3.636 ± 0.343
32.461 ± 0.680*** 27.279 ± 0.902
12.558 ± 0.946** 9.059 ± 0.128
15.196 ± 0.174*** 11.739 ± 0.060
24.289 ± 0.656* 20.382 ± 1.922 74.411 ± 5.603** 49.214 ± 0.694 75.312 ± 0.861*** 59.645 ± 0.306
Different superscript stars for the same species indicate a significant difference, *** significant at P ≤ 0.001; ** significant at P ≤ 0.01 and * significant at P ≤ 0.05.
Table 2: Proximate compositions (g/100 g fresh weight edible portion) of the study plant species cultivated in the coastal black sand and in the inland (control) sites. Data
are expressed as mean ± S.D (n=5).
8
Eruca sativa
Values (g/ 100g dry weight)
7
Black Sand
Control Soil
***
4
Lycopersicum esculentum
3
6
5
3
***
***
2
*
0
0
Ca
Values (g/ 100g dry weight)
K
Ca
Na
1.2
Psidium guajava
K
Na
Mangifera indica
***
1.0
***
1.5
***
0.8
1.0
0.5
***
1
1
2.0
***
2
4
***
0.6
0.4
***
***
0.2
0.0
0.0
Ca
K
Na
Ca
K
Na
Minerals content
Figure 2: Macro elements content (gm/100 g dry weight edible portion) of the four study crop plant species cultivated in the coastal black sand and in the inland sites.
Vertical bar around the mean is the standard deviation. Stars indicate significant differences, *** significant at P ≤ 0.001; ** significant at P ≤ 0.01 and * significant at
P ≤ 0.05.
J Bioremed Biodeg
ISSN: 2155-6199 JBRBD, an open access journal
Volume 4 • Issue 3 • 1000185
Citation: Hegazy AK, Al-Rowaily SL, Kabiel HF, Faisal M, Emam MH (2013) Variations of Plant Macronutrients and Secondary Metabolites Content
in Response to Radionuclides Accumulation. J Bioremed Biodeg 4: 185. doi:10.4172/2155-6199.1000185
Page 6 of 10
The content of vitamin A and vitamin C in the edible portions of
the study plant species are shown in figure 3. Vitamin A content has
significantly increased with the increased amounts of Uranium and
Thorium in the tissues of L. esculentum and P. guajava cultivated in the
inland soils, with values reached 2113.38 ± 2.09 and 822.70 ± 1.00 IU
in both species respectively. For plants cultivated in coastal black sand
soil, vitamin A content reached 2468.24 ± 1.00 and 892.29 ± 1.00 IU in
both species respectively. In E. sativa and M. indica, vitamin A content
decreased in plants from black sand soil. Concentration of vitamin C
(Figure 4) increased in the plants cultivated in the coastal black sand
soil, which is associated with increased accumulation of Uranium and
Thorium in the plant tissues.
Secondary compounds content
Total phenolic compounds and total flavonoid content are shown
in figure 4. Total phenolic compounds varied between 102.521 ± 0.507
mg/100 gm fresh weight in fruits of M. indica to 161.98 ± 0.186 mg/100
gm fresh weight of P. guajava fruits cultivated in the inland soil. In
the coastal black sand soil, the total phenolic compounds increased
Vitamin A (IU)
2,500
Black Sand
Control Soil
Eruca sativa
Black Sand
Control Soil
**
***
100
140
120
80
60
60
40
40
20
20
***
0
0
Total Phenols
200
**
100
80
250
Lycopersicum esculentum
Total Phenols
Total Flavonoids
Psidium guajava
140
Total Flavonoids
Mangifera indica
***
120
***
***
100
150
80
***
60
100
40
50
20
0
0
Total Phenols
Total Flavonoids
Total Phenols
Total Flavonoids
Phenols and flavonoids
Figure 4: Total phenolic compounds and total flavonoid content (mg/100 g fresh
weight edible portion) of the four study plant species cultivated in the coastal
black sand and in the inland sites. Vertical bar around the mean is the standard
deviation. Stars indicate significant differences, *** significant at P ≤ 0.001; **
significant at P ≤ 0.01 and * significant at P ≤ 0.05.
***
***
2,000
12
***
1,500
1,000
***
500
0
Es
Le
Pg
Mi
250
Vitamin C (mg/ 100g fresh weight)
120
Antioxidant activity (%)
3,000
Values (mg/ 100g fresh weight)
Vitamins composition
140
Values (mg/ 100g fresh weight)
of more Uranium and Thorium. In contrast to K content, Na content
increased in the crop plant species and decreased in the fruit trees
with uptake of more Uranium and Thorium in plant tissues. Calcium
content didn’t show constant trend with the increase of Uranium and
Thorium content of the plants.
10
8
Black Sand
Control Soil
***
**
***
***
6
4
2
0
200
Es
Le
Pg
Mi
Study species
150
Figure 5: Antioxidant activity (%) of the four study crop plants Eruca sativa (Es),
Lycopersicum esculentum (Le), Psidium guajava (Pg) and Mangifera indica (Mi)
cultivated in the coastal black sand and in the inland sites.. Vertical bar around
the mean is the standard deviation. Stars indicate significant differences, ***
significant at P ≤ 0.001; ** significant at P ≤ 0.01 and * significant at P ≤ 0.05.
***
100
***
***
50
**
0
Es
Le
Pg
Mi
Study species
Figure 3: Vitamins composition (mg/100 g fresh weight edible portion) of
the four study crop plants Eruca sativa (Es), Lycopersicum esculentum (Le),
Psidium guajava (Pg) and Mangifera indica (Mi) cultivated in the coastal black
sand and in the inland sites. Vertical bar around the mean is the standard
deviation. Stars indicate significant differences, *** significant at P ≤ 0.001; **
significant at P ≤ 0.01 and * significant at P ≤ 0.05.
J Bioremed Biodeg
ISSN: 2155-6199 JBRBD, an open access journal
to 129.123 ± 0.85 mg /100 gm fresh weight in M. indica and 197.996
± 0.22 mg/100 gm fresh weight in P. guajava. As for E. sativa and L.
esculentum, the total phenolic compounds showed no significant
difference between coastal and inland sites. Total flavonoids content
attained lower values in plants cultivated in the coastal black sand site
than plants in the inland sites.
Antioxidant activity
As shown in figure 5, the antioxidant activity measured as DPPH
Volume 4 • Issue 3 • 1000185
Citation: Hegazy AK, Al-Rowaily SL, Kabiel HF, Faisal M, Emam MH (2013) Variations of Plant Macronutrients and Secondary Metabolites Content
in Response to Radionuclides Accumulation. J Bioremed Biodeg 4: 185. doi:10.4172/2155-6199.1000185
Page 7 of 10
free radical scavenging activity, decreased with the increase of Uranium
and Thorium content of plant tissues. For P. guajava, the antioxidant
activity attained value 6.722 ± 0.003% in plants cultivated in the inland
site and value 7.062 ± 0.003% in plants of the coastal black sand site.
Total chlorophylls and carotenes content
Total chlorophylls in leaves of E. sativa (Table 3) increased from
727.00 ± 2.00 mg/100 gm fresh weight in plants from the inland site to
952.00 ± 2.00 mg/100 gm fresh weight in plants from coastal black sand
site. Total carotenoids content showed significant increase with the
increase of Uranium and Thorium content of the plant edible portions.
Only for M. indica, the total carotenoids decreased with Uranium
and Thorium uptake from 9.481 ± 0.003 to 7.234 ± 0.001 mg/100 gm
fresh weight in the plants of the coastal black sand site. β-carotene and
Study species
Eruca sativa
Lycopersicum esculentum
`
Psidium guajava
Mangifera indica
lycopene in L. esculentum exhibited values 3.135 ± 0.01 and 9.520 ±
0.03 mg/100 gm fresh weight respectively in plants cultivated in the
inland sites. For plants cultivated in the coastal black sand soil, the
values increased to 4.128 ± 0.01 and 10.773 ± 0.003 mg/100 gm fresh
weight, respectively.
Relationship between uranium content and biochemical
constituents
The relationship between Uranium content of the plant and its
biochemical constituents showed positive linear relationship with
total carbohydrates, nutritive value, vitamin C, phenolic compounds,
flavonoids, antioxidant activity and beta-carotene contents (Figure 6).
Only negative relationship attained with the total protein content.
Carotenes content (mg/ 100g)
Study site
Total chlorophyll
(mg/ 100g)
Total carotenoids
β-Carotene
Lycopene
Black sand
952.000 ± 2.000***
1.315 ± 0.005***
___
___
Inland site
727.000 ± 2.000
0.935 ± 0.005
___
___
Black sand
___
9.862 ± 0.003***
4.128 ± 0.007***
10.773 ± 0.003***
Inland site
____
8.440 ± 0.003
3.135 ± 0.005
9.520 ± 0.030
Black sand
___
3.563 ± 0.001***
4.112 ± 0.003***
___
Inland site
___
3.288 ± 0.001
7.633 ± 0.031
___
Black sand
____
7.234 ± 0.001***
4.983 ± 0.003***
___
Inland site
___
9.481 ± 0.003
2.174 ± 0.004
___
Different superscript stars for the same species indicate a significant difference, *** significant at P ≤ 0.001; ** significant at P ≤ 0.01 and * significant at P ≤ 0.05.
14
90
4
80
3
12
3
10
2
8
2
6
1
4
2
0
5
10
15
200
70
60
150
50
40
100
30
20
1
10
0
0
20
50
0
0
Uranium in plant (Bq kg-1)
160
100
150
80
100
60
40
50
20
0
0
10
15
Uranium in plant (Bq kg-1)
20
Antioxidant activity %
120
Flavonoids (mg/100 gm)
Phenols (mg/100 gm)
200
5
10
15
20
Antioxidant Activity %
β-Carotene (mg/100g)
Linear (Antioxidant Activity %)
Linear (β -Carotene (mg/100g))
12
140
0
5
Uranium in plant (Bq kg-1)
Phenols (mg/100 gm)
Flavonoids (mg/100 gm)
Linear (Phenols (mg/100 gm))
Linear ( Flavonoids (mg/100 gm) )
250
250
9
8
10
7
6
8
5
6
4
4
3
β-Carotene (mg/100g)
0
Nutritive Values (K.Cal)
Vitamin C (mg/100 gm)
Linear (Nutritive Values (K.Cal))
Linear (Vitamin C (mg/100 gm))
Vitamin C (mg/100 gm)
16
4
Nutritive values (K.Cal)
Total Carbohydrates (gm/100 gm)
Total Protein (gm/100 gm)
Linear (Total Carbohydrates (gm/100 gm))
Linear (Total Protein (gm/100 gm))
18
Total protein (gm/100 gm)
Total carbohydrates (gm/100 gm)
Table 3: Total chlorophyll and carotenes content (mg/100 g fresh weight edible portion) of the study plant species cultivated in the coastal black sand and in the inland
(control) sites. Data are expressed as mean ± S.D (n=5).
2
2
1
0
0
0
5
10
15
20
Uranium in plant (Bq kg-1)
Figure 6: Relationships between Uranium concentration in the plant and its biochemical constituents.
J Bioremed Biodeg
ISSN: 2155-6199 JBRBD, an open access journal
Volume 4 • Issue 3 • 1000185
Citation: Hegazy AK, Al-Rowaily SL, Kabiel HF, Faisal M, Emam MH (2013) Variations of Plant Macronutrients and Secondary Metabolites Content
in Response to Radionuclides Accumulation. J Bioremed Biodeg 4: 185. doi:10.4172/2155-6199.1000185
Page 8 of 10
Discussion
The concentrations of Uranium and Thorium accumulated in the
edible portions of the study plant species cultivated in the coastal black
sand soil were significantly higher than that in the inland soil. Similarly
[3] detected higher level of Uranium and Thorium in the tissues of
wild plants raised in the black sand soil than those in the inland soil.
Physiological responses of higher plants to environment have been
studied extensively over the world. Abiotic environmental stresses are
linked with all the living process of higher plants and greatly influence
plant growth and productivity [4,35,36]. Although some metals are
necessary for biological processes, they are toxic at high concentrations.
This is due to their oxidative capacity to form free radicals and their
ability to replace essential metals in enzymes, interrupting their normal
activity. Other metals are not essential and accumulate in different
organisms and become toxic even at low concentrations [37].
The macronutrients in the study species revealed that high
Uranium and Thorium content in the plant tissues was associated with
significant increase in total carbohydrates, ash, crude fibers, crude
fats and nutritive values of the four study species. These results are in
agreement with results obtained by Gang et al. [35], who found increase
in the total soluble sugars with the increase of Uranium and Thorium
concentration in the leaves of Capparis spinosa. Total protein content
was found to decline due to uptake of more U and Th in plants from
coastal black sand soil. This finding is supported by Srivastava et al. [10]
who reported decline in the level of total soluble protein in Hydrilla
verticillata after exposure to Uranium in comparison to the control
treatment. This is in contrary to the results of Bajpai et al. [38] that
revealed a positive correlation between protein content and the heavy
metal content of the plant. Inhibition of protein accumulation induced
by higher concentrations of heavy metals may attribute to the toxicity
of these metals on the enzymatic reactions responsible for protein
biosynthesis [39,40]. Increase of Uranium and Thorium content in
the edible portions of the study species caused general decline in the
content of Ca, K and Na. This observation can be explained by the
presence of a competition for uptake between radionuclides and other
captions present in the soil such as Zn, Mg, K, Na and Ca [41].
Vitamin C content was negatively affected with high U and Th
content in the plant tissues. As expected from its antioxidant based
function in plant metabolism, the level of vitamin C is responsive to
a wide variety of environmental stress factors including radioactive
elements [42]. Similarly, the total flavonoids content was found to
decrease in the plants from coastal black sand soil with the absorption
of high amounts of Uranium and Thorium. Similarly, study of Morsy
and Afifi [43] on some wild plant species grown on natural radioactive
soils revealed that Uranium has a negative effect on the flavonoids
content. In contrast to minerals, vitamin C and flavonoid content, the
phenolic compounds significantly increased with increased amounts
of Uranium and Thorium in plants. That was observed from the
relationship between phenolic compounds content in the four study
plant species and concentrations of Uranium in the edible portions
of these plants. This finding is in accordance with that obtained
by Srivastava et al. [10], where total phenolic compounds showed
significant increase in response to Uranium exposure.
Phenolic compounds, among the most widely occurring groups of
phytochemicals, are of considerable physiological and morphological
importance in plants as they play an important role in growth,
reproduction, and protection against pathogens and predators
[42,44]. Phenolic compounds exhibit a wide range of physiological
properties and have been associated with the health benefits [44]. The
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antioxidant activity of phenolic compounds is due to their ability to
scavenge free radicals, donate hydrogen atoms or electron, or chelate
metal cations. The role of antioxidants in preventing oxygen radicaland hydrogen peroxide-induced cytotoxicity and tissue damage is
becoming increasingly recognized. The importance of the antioxidant
constituents of plant materials in the maintenance of health and
protection against diseases [45].
The total chlorophyll and carotenoids content are positively
correlated with Uranium and Thorium content of the study plant
species. Also, β-carotene and Lycopene content were positively
influenced by elevated amounts of Uranium and Thorium in plant
tissues. Our results are in agreement with the results of Bajpai et al.
[38] who found that carotenoids have significant positive correlation
with metal accumulation. Alternatively, the results obtained by Huang
GY [46] proved remarkable decrease in chlorophyll a, chlorophyll b,
chlorophyll (a+b) and carotenoids content in the leaves of mangrove
plants exposed to multiple heavy metals. Carotenoids are essential
components for the photosynthetic apparatus in plants, which
participate in the adaptation of plastids to changing environmental
conditions and prevent photo-oxidative damage of the photosynthetic
apparatus [46]. Previous studies have reported an increase [47] or
decrease [48] in the carotenoids content of plants in response to metal
stress. They are present as micro-components in fruits and vegetables
and represent important dietary sources of vitamin A [49]. Carotenoids
accumulation is often regarded as one of the mechanisms to counteract
stresses [50].
Several stress factors including exposure to toxic metals can lead
to an oxidative stress state that inhibits a range of enzyme activities
in plants, in particular those of the Calvin cycle [51]. Pollutant
metals disturb the oxidative balance and thus an important palliative
measure is the induction of antioxidants [52]. The induction of
antioxidant compounds and enzymes is of great importance to increase
tolerance of plants against different kinds of stress [53]. Carotenoids
accumulation is often regarded as one of the mechanisms to counteract
stress in organisms [50]. The role of β-carotene as 1O2 quencher was
established in plants and algae [54]. A significant rise in carotenoids
content as noticed under toxic metal stress might offer protection to
the chlorophyll and photosynthetic membrane from photooxidative
damage [55].
The antioxidant activity of fruits and vegetables is an important
aspect of their nutritional value since antioxidant molecules have a
critical role in the detoxification of free radicals in both plants and
humans [56]. It’s well known that amount of each antioxidant in tomato
fruits is strongly influenced by varietal differences (genetic influence), in
addition to agronomical, geographical and environmental parameters
[57]. Lycopene, the red isoprenoid pigment of tomato, constitutes
about 80-90% of total carotenoids content [57]. Recent epidemiological
studies have shown that supplementation of diets rich in lycopene is
associated with reduced risk of many chronic diseases, such as cancer
and heart diseases [16]. The antioxidant activity of lycopene has been
extensively evaluated based on its ability to scavenge free radicals
in cell culture and in animal models. Increased DNA damage and
elevated levels of lipid peroxidation in γ-irradiated hepatocytes are
accompanied by a decrease in the free radical scavengers. Pretreatment
of lycopene resulted in increased levels of these antioxidants. These
may be attributed to lycopene's ability to act as an antioxidant and
singlet oxygen quencher [58].
Various interactions are known to occur when plants are exposed
to unfavorable concentrations of more than one element [59]. As
Volume 4 • Issue 3 • 1000185
Citation: Hegazy AK, Al-Rowaily SL, Kabiel HF, Faisal M, Emam MH (2013) Variations of Plant Macronutrients and Secondary Metabolites Content
in Response to Radionuclides Accumulation. J Bioremed Biodeg 4: 185. doi:10.4172/2155-6199.1000185
Page 9 of 10
indicated from the present study the tissue concentrations of highvalue metabolites, such as vitamin C, phenolic compounds, flavonoids,
Lycopene and β-carotene and other antioxidant compounds are
variable under environmental stresses that may elicit the biosynthesis/
catabolism of stress responsive molecules [56].
In conclusions, the study of radionuclides content in crop plants
cultivated in the coastal black sand soil revealed their ability to
accumulate high concentrations of Uranium and Thorium in the edible
portions. The biochemical responses indicated that some nutritional
contents of the plants including protein, moisture, mineral, vitamin
C and total flavonoids contents showed negative correlation with
Uranium and Thorium content. The carbohydrates, crude fats, crude
fibers, nutritive value, total phenolic compounds, total chlorophylls,
total carotenoids, β-carotene and lycopene were significantly enhanced
by high Uranium and Thorium concentration in the plant tissues. The
results indicated that each of biochemical constituents of the test plants
were affected by elevated level of radionuclides in plants. The variations
between enhancement and suppression of the phenolic compounds
content of the study plant species can be considered as antioxidant
defense mechanism of cells in order to control the redox state of the
cell containing high radionuclides concentrations.
Acknowledgment
We thank the support of King Saud University, Deanship of Scientific
Research, College of Science Research center.
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in Response to Radionuclides Accumulation. J Bioremed Biodeg 4: 185. doi:10.4172/2155-6199.1000185
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Citation: Hegazy AK, Al-Rowaily SL, Kabiel HF, Faisal M, Emam MH (2013)
Variations of Plant Macronutrients and Secondary Metabolites Content
in Response to Radionuclides Accumulation. J Bioremed Biodeg 4: 185.
doi:10.4172/2155-6199.1000185
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