AGRICULTURE AND BIOLOGY JOURNAL OF NORTH AMERICA

ISSN Print: 2151-7517, ISSN Online: 2151-7525, doi:10.5251/abjna.2017.8.4.159.167

© 2017, ScienceHuβ, http://www.scihub.org/ABJNA

A comparison between tree species grown in the Kingdom of Saudi Arabia

on their ability and tolerance to remove some heavy metals from the
polluted soil 2-Effect on plant growth and chlorophyll
Abdullah O. Al Thobaity1; Abdullah M. Al-Ansari1 and Ansary E. Moftah2
1
Dept. of Botany and Microbiology; College of Science; KSU
2
Dept. of Plant Production and Protection, College of Agric., Qassim Univ
a.o.u.t@hotmail.com
ABSTRACT

Pot culture experiments were conducted to investigate the remediation potentials of two native
tree species namely Tamarix nilotica and Conocarpus erectus to remove Pb or Zn (0, 100, 200,
400 and 800 mg.kg-1 soil) and Cd (10, 20, 40 and 80 mg.kg-1 soil) from the contaminated soils in
order to find out the most effective species that can be used to clean up the environment from
heavy metal pollution. Results of this study showed vegetative growth assigned by plant height,
number of leaves/plant, leaf area/plant and biomass decreased significantly at high
concentrations of Pb, Zn and Cd. Relative growth rate (RGR) and net assimilation rate (NAR)
values reduced with heavy metal pollutions in the presence of Pb and Cd; while with Zn both
parameters showed a significant increase as compared with those recorded at high HM
concentrations. The results indicated that T. nilotica and C. erectus are considered good
accumulator candidates of Pb, Zn and Cd metals.

Keywords: heavy metals, pollution, phytoremediation, growth, RGR, NAR.

INTRODUCTION the contaminated ground, and accumulate them in

roots, stems and branches. Logically, repeating
Many sources of pollution are becoming scary in
cycles of planting and harvesting of trees
Kingdom of Saudi Arabia, because of the oil
accumulated with heavy metals will eventually reduce
resources, industrial development, excessive use of
the concentration of toxic metals in soils to an
chemical fertilizers, huge amounts of vehicles and
acceptable level for other uses. A green house study
other activities. All these sources are introducing
shown that Acacia mangium and Acaccia
heavy metals in the environment either in the
auriculiformis accumulated considerable amount of
atmosphere or in the soil and water resources (Al-
Pb, Cd, As and Hg from sludge treated sand tailings
Homaidan et al., 2011). Recent studies showed that
(Aba-Alkhil and Moftah, 2013). Moreover,
potentially toxic elements of heavy metals, lead (Pb)
phytoremediation is one of the cost-effective
zinc (Zn) and cadmium (Cd), are common in many
approaches. Using trees to remove heavy metals
sites of the region (Adham et al., 2011). These
from the contaminated sites brings other benefits
elements were found in vegetables and fruit crops
such as improving its site quality. In this regard, a
produced from these sites or grown near the tailings
tree stand was found to have ameliorated the harsh
where their concentrations were relatively high
microclimate of polluted site and also have improved
(Franco-Hernández et al., 2010). Ingestion of toxic
its soil properties (Ayangbenro and Babalola, 2017).
metals contaminated food may cause severe health
Using timber species for phytoremediation approach
problems (Hezbullah et al., 2016). This has drawn
has additional benefit as it also yields timber at the
interest to develop a scientifically cost-effective
end of its rotation. Earlier studies showed that tree
remedial measure to remove heavy metals from the
species have a great potential to remove heavy
contaminated soils. One of the established
metals for the contaminated sites (Aba-Alkhil and
approaches was through phytoremediation ( Malik et
Moftah, 2015). In this regard, Moftah and Al-Ghanim
al., 2017).
(2009) found that Eucalyptus rostrata seedlings were
Phytoremediation is a way for cleaning the polluted able to accumulate high amounts of Pb when grown
sites by using trees to extract the heavy metals from in polluted soil of Qassim region. However, this ideal

cost-effective approach has many limitations, one of
them is heavy metal contaminated sites are normally
adverse to establishment and growth of plants.
Greening polluted sites with tree species is well
undocumented, but no documentation is available on
the phytoremediation potential of these tree species.
Hence, this study was embarked to determine the
bioaccumulation of Pb, Zn and Cd by two selected
tree species namely Tamarix nilotica and
Conocarpus erectus that are successfully grown on
sand soil and harsh conditions of the Kingdom.
MATERIALS AND METHODS
The present study was carried out at Qassim
University, KSA during 2016/2017 to determine the
ability of two tree species grow in the Kingdom of
Saudi Arabia to extract Pb, Zn and Cd from polluted
soil. Six month old seedlings of Tamarix nilotica and
Conocarpus erectus were transplanted in plastic pots
(30 cm×50 cm, diameter and depth) filled with sand
and peat moss (2:1 proportion), pH 7.2; one plant in
each pot. Before planting, soils were mixed with fine
metal powders of PbCl2, ZnCl2 or CdCl2 to bring Pb or
Zn levels of 00, 100, 200, 400 and 800 mg.kg-1 soil,
and Cd to 10, 20, 40 and 80 mg.kg-1 soil).
To evaluate the efficiency of phytoremediation, it was
necessary to homogenize the soil because the
concentration of distributed contaminants in the soil
plays a fundamental role in such studies. A
completely randomized design with 10 replicates for
each treatment was used in this experiment.
Seedlings were left to grow in a greenhouse under
natural light and temperature conditions. Plants of
uniform height within species were selected and
located in lines with a spacing of 2 m between lines
and 1 m between pots to avoid mutual shading.
Three weeks after transplanting, all seedlings were
fertilized 3 times, at 30 day intervals, with the
complete water-soluble fertilizer “Sangral” compound
fertilizer (20N-20P-20K, plus micronutrients) at the
rate of 2g/kg soil. All pots were irrigated every 3 days
to field capacity. Pots were weighed and supplied
with amounts of water equal to evapo-transpiration
losses. Plants were harvested 6 months after
transplanting. The following parameters were
determined:
Vegetative growth: Three samples were taken to
study the growth parameters during the experimental
period: 60, 120 and 180 days after treatments. The
following parameters were measured:
160
Agric. Biol. J. N. Am., 2017, 8(4): 159-167
- Plant heights (in cm) were measured from
soil surface to the top of each seedling.
- Number of leaves/plant was counted
manually.
- Leaf area in cm2/plant was determined using
leaf area meter (Planimeter).
- Fresh weight of shoots and roots (g).
- Relative growth rate (RGR) was determined
according to Cachorro et al. (1994) following
the equation:
RGR (mg g-1d-1) = (lnW2 – lnW1)/(t2 - t1)
Where: W1 and W2 are the dry weights at t1
and t2, respectively
- Net assimilation rate (NAR) was determined
as described by McCollum (1978) according
to the equation:
NAR (mg g-1cm-2d-1) = (ln A2 – ln A1)(W2 –
W1)/ (t2 – t1)(A2 –A1)
Where: ln is the natural logarithm; W1 and
W2 are the dry weights at t1 and t2,
respectively; A1 and A2 are the leaf area at t1
and t2, respectively.
Total chlorophyll: Total chlorophyll was determined
at the end of the experiment following the method of
Metzner et al. (1965). Briefly, fresh leaves (0.4 g)
were selected randomly from the middle part of each
plant, washed with deionized water, and
homogenized in a porcelain mortar with 80% acetone
solution. The homogenate was centrifuged at
16,000×g for 1 min twice and the measurement of
chlorophyll content was done by direct determination
of the absorbance at wavelengths 663 and 646 nm at
the clear supernatant fraction using
spectrophotometer (Shimadzu 1240 UV–Vis).
Statistical analysis: The experiment was arranged
in a completely randomized design and was analyzed
by analysis of variance. All data were statistically
analyzed and ANOVA was tested according to
Snedecor and Cochran (1980) with the aid of SPSS
(1990) computer program for statistics. Differences
among treatments were tested with LSD at 5% level
of significance.
 Agric. Biol. J. N. Am., 2017, 8(4): 159-167

RESULTS number of leaves in C. erectus was much higher than

that in T. nilotica. In this concern the reduction
Data recorded in Table (1) indicated that plant
percent in Tamarix at 180 days of treatments was
heights decreased as heavy metal (HM)
about 53.8%, 51.9% and 76,2% at 800 ppm of Pb,
concentration increased to reach minimum height at
800 ppm of Zn and 80 ppm of Cd, respectively. While
800 ppm of Pb or Zn and 80 ppm of Cd, at which
the corresponding decrease in number of leaves in
heights of T. nilotica plants were reduced by about
Conocarpus plants were about 59.8%, 55.7% and
27.2%, 17.0% and 33.9% , respectively at 180 days
79.2%, respectively as compared with control plants.
after treatments. The comparable decrease in C.
It seems that Cd showed more negative effects than
erectus plant heights were about 30.8%, 19.5% and
Pb or Zn, while Zn showed the minimum negative
40.3%, respectively, at 180 days after treatments.
effect on number of leaves/ plant. Data in the figure
Table (1): Effects of heavy metals on plant showed clearly that T. nilotica was more tolerant to
heights (cm) of T. nilotica and C. erectus. heavy metals than C. erectus plants.
Conocarpus
Tamarix nilotica
erectus
HM
180 120 60 180 120 60
Ppm
Day Day Day Day Day Day
63.6 59.6 55.5 68.8 65.7 59.4 00
60.3 56.4 53.3 66.1 62.7 58.8 100
58.8 53.0 50.8 64.0 61.1 55.7 200 Pb
53.6 49.6 45.7 61.7 58.0 52.5 400
44.6 44.2 40.2 50.1 52.6 46.3 800

9.8 10.3 10.2 6.8 7.9 7.2 LSD5%

63.6 59.6 55.5 68.8 65.7 59.4 00

64.0 60.9 56.6 69.1 65.9 60.1 100 Fig (1). Effects of heavy metals on number of
leaves in T. nilotica and C. erectus seedlings.
61.1 58.2 54.8 65.2 62.5 58.8 200 Zn
Leaf area/plant: Data recorded in Fig. (2) indicated
57.0 55.2 51.6 61.1 59.6 56.2 400 clearly that heavy metals, particularly Pb and Cd
51.2 50.6 48.3 57.1 56.2 53.2 800 affected badly the leaf area of Tamarix and
Conocarpus plants. Leaf area/plant of T. nilotica and
6.3 4.7 4.1 6.2 4.4 3.4 LSD5% C. erectus showed a linear decrease with increasing
63.6 59.6 55.5 68.8 65.7 59.4 00 HM concentrations in root media. The maximum
reduction in leaf area was recorded at the highest
59.1 56.6 53.3 63.3 60.8 58.2 10 concentrations of heavy metals; at which leaf area of
54.6 53.4 51.1 58.8 57.7 55.9 20 Cd T. nilotica was decreased by about 47.5%, 46.4%
and 62.7% at 800 ppm of Pb, 800 ppm of Zn and 80
49.4 48.0 46.0 53.5 52.8 51.4 40 ppm of Cd, respectively, at 180 days of treatments.
38.0 37.8 36.8 45.5 44.0 43.2 80 The matching values of C. erectus were about
52.9%, 53.1% and 69.5%, respectively, as compared
8.5 6.4 4.5 8.4 6.1 3.6 LSD5% with control treatments.
It was clear that Cd had a deleterious effects more
Number of leaves/plant: Data plotted in Fig. (1) than those recorded with Pb or Zn treatments. In
showed clearly that number of leaves/plant addition T. nilotica was more tolerant to high levels of
decreased as HM concentration increased to reach heavy metals that C. erects seedlings.
its minimum value at the highest levels of HMs. The
reduction ratio in number of leaves of T. nilotica and
C. erectus plants reached its maximum at 180 days
after treatments; however the reduction percentage in
161
 Agric. Biol. J. N. Am., 2017, 8(4): 159-167

Fig (2). Effects of heavy metals on leaf area of T.

nilotica and C. erectus seedlings.
Plant biomass: Data recorded in Figs (3 and 4)
showed that heavy metal application, particularly at
high concentrations, affected the fresh and dry
weights of the plants of both tree species. It was clear
that Cd exhibited maximum inhibitory effect on plant
weights of both species, while the effect of Pb was
less than that of Cd. On the other side low levels of
Zn was likely to improve plant biomass as compared
with control treatment at the first sample (60 days
after treatment). In this regard 100 ppm of Zn
treatment caused an increase of about 2.5% and
2.0% in fresh weights (Fig. 3) and by about 7.6% and
10.1% in dry weights (Fig. 4) of T. nilotica and C.
erectus seedlings, respectively, as compared with
control plants. It was clear that heavy metal (HM)
treatments caused a gradual decrease in the fresh
and dry weights of shoots to reach their minimum at
800 ppm of Pb or Zn and 80 ppm of Cd.

Fig (3): Effect of Pb, Zn and Cd on the fresh weight of

T. nilotica and C. erectus trees.

162
 Agric. Biol. J. N. Am., 2017, 8(4): 159-167

In this regard, 800 ppm of Pb caused a decrease in

the dry weight of T. nilotica and C. erectus shoots by
about 42.1% and 17.8%, respectively as compared
with control. Similarly, 800 ppm of Zn caused a
decreased in the dry weight by about 42.1% and
21.1%, respectively. The corresponding decrease at
80 ppm of Cd was about 44.7% and 35.7%,
respectively.
Relative growth rate (RGR): Data registered in Fig.
(5) showed that RGR of both T. nilotica and C.
erectus was negatively affected with increasing
heavy metal concentrations. Most decrease in RGR
was reported at highest concentrations of HM
pollutants. Between 60 and 120 days of treatments
RGR of T. nilotica was reduced by about 81.0%,
77.5% and 96.5% at 800 ppm Pb, 800 ppm Zn and
80 ppm Cd, respectively. While the comparable
decrease in RGR of C. erectus was about 96.9%,
95.3% and 96.9%, respectively. These results
showed clearly that Cd was more effective in
reducing RGR that Pb or Zn, while Zn showed the
less effect on RGR of plants. In addition T. nilotica
was more tolerant to heavy metal pollution than C.
erectus.

Fig (5): Effect of Pb, Zn and Cd on RGR of T. nilotica

and C. erectus trees.
Net assimilation: The results found in Fig. (6)
indicated that net assimilation rate (NAR) decreased
with increasing HM pollutants in the growth media. As
Fig (4): Effect of Pb, Zn and Cd on the dry weight of T. metal concentration increased NAR tended to
nilotica and C. erectus. decrease to reach its minimum value at the highest
levels of heavy metals at which NAR values of T.
163
 Agric. Biol. J. N. Am., 2017, 8(4): 159-167

nilotica were decreased by about 35.0%, 50,4% and

72.4 at 800 ppm Pb, 800 ppm Zn and 80 ppm Cd,
respectively, between 60 and 120 days of treatments.
As for C. erectus, NAR values were decreased by
about 80.6%, 26.5% and 85.4%, respectively.
Data indicated clearly that Cd was more negative
effect than other heavy metals, Pb and Zn. In addition
NAR values of C. erectus were higher than those of
T. nilotica it might be

Fig (6): Effect of Pb, Zn and Cd on NAR of T. nilotica

and C. erectus trees.
Total Chlorophyll content: Data recorded in Fig. (7)
showed clearly that total chlorophyll contents of C.
erectus was higher than that of T. nilotica. Total Chl
of both tree species increased as time passed until
reached its maximum after 180 days. The pigment
was stimulated by low and medium HM
concentrations. Only the highest concentrations of Pb
and Zn resulted in a significant decrease in total Chl
at any sampling time as compared with control
plants, while the highest and medium concentrations
of Cd caused a significant inhibition in total Chl at any
sampling time.

Fig (7): Effects of Pb, Zn and Cd on total chlorophyll of

T. nilotica and C. erectus leaves.

164

DISCUSSION
It is well known that growth inhibition is a common
response to HM stress and is also one of the most
important agricultural indices of HM tolerance. Lead
is not generally considered to be an essential
element for plant growth. The effect of Pb on seedling
growth seems to be different with regards to plant
species, cultivars, organs and metabolic processes
(Patil and Umadevi, 2014). Growth disorders causing
reductions in biomass yields are commonly observed
in plants subjected to high metal levels (Panich-Pat et
al., 2010). In the present study, C. erectus seemed to
be more tolerant to Pb, Zn and Cd than T. nilotica,
thus high HM concentrations had less effect on the
biomass of C. erectus than on that of T. nilotica.
Inhibition of plant shoot and root growth as affected
by HM treatments has been found by Ang et al.
(2010). This negative effect could be attributed to the
reduction in the meristem activity. The suppression of
cells elongation by HM was also reported by de
Souza et al. (2012).
Based on growth attributes, our results indicated that
C. erectus was better adapted to contaminated soils.
However, The seedling stage experiment
demonstrated that the toxicity of a metal, in
comparison to another may not be the same at all the
stages of plant development. The toxicity of some
metals may be so severe that plant growth is reduced
before large quantities of the element can be
translocate (Umadevi and Avudainayagam, 2013).
The present study supported the findings of Malar et
al. (2014) who stated that plant biomass is a good
indicator for characterizing the growth performance of
plants in the presence of heavy metals.
In plant physiology, RGR is a measure used to
quantify the speed of plant growth. It is measured as
the mass increase per aboveground biomass per
day, for example as g g−1 d−1. It is considered to be
the most widely used way of estimating plant growth,
but has been criticized as calculations typically
involve the destructive harvest of plants (Hoffmann
and Poorter, 2002).
NAR is the increase in dry biomass per unit leaf area
and is a complex physiological variable associated
with photosynthetic and respiration rates, which
reflects a plant’s investment in light capture (Li et al.,
2016). NAR is a measurement of plant growth
(weight increase per unit time) by assessing change
in a particular part of the plant (usually leaf area)
rather than in the overall plant (Hale et al., 2017).
165
Agric. Biol. J. N. Am., 2017, 8(4): 159-167
It was found that RGR nearly decreased over time
(Fig. 5) as the biomass of unstressed plant increases,
The RGR decreases for several reasons - non-
photosynthetic biomass (roots and stems) increases,
the top leaves of a plant begin to shade lower leaves
and soil nutrients can become limiting under heavy
metal pollution. In the presence of heavy metal
stress, it was found that respiration scales with total
biomass, but photosynthesis only scales with
photosynthetic biomass and as a result biomass
accumulates more slowly (Marthews et al.,
2012). The RGR of trees in particular slow with
increasing size due in part to the large allocation to
structural material of the trunk required to hold
photosynthetic material up in the canopy (Philipson et
al., 2012).
The adverse effect of heavy metals on plant growth
was accompanied by decrease in RGR and NAR.
The RGR values of plants significantly declined due
to the increase in the concentration of HMs (Fig. 5).
In this study it has been established that high
concentrations of HMs caused inhibition in RGR and
NAR of C. erectus that was higher than that of T.
nilotica. In an early study, Chaab et al. (2016)
reported that reduction of plant dry weight led to
decrement of RGR and NAR values if leaf area was
affected. It was indicated that increasing heavy
metals in soil, promoted their concentration in plant
followed by chlorophyll content syntheses disruption
and dwindling plant growth to reduces dry matter
production and, as a consequence, RGR and NAR
decreases (Zeliha, et al., 2011).
Because changes in pigment content are related to
visual symptoms of plant disorder (Zengin and
Munzuroglu, 2005), Chl content is often measured to
assess the effect of HM stress on plant growth and
physiology. Many studies reported reduced
chlorophyll in different species under HM pollution
(Liu et al., 2014, Iqbal et al., 2017). Decreased Chl
content connected with HM pollution might be a result
of inhibition of some enzymes involved in Chl
biosynthesis. Heavy metals were reported to affect
Chl formation and inhibited the synthesis of Chl
precursor, aminolevulinic acid (ALA) (Gill, 2014).
Previous studies found that HM stimulated
chlorophyll degradation, and reduction in Chl content
was observed in plants grown in HM polluted soils
(Sharma and Dubey, 2005). Even moderate amounts
of some HMs such as Cd affected the content of
photosynthetic pigments, which could lead to a
reduction in photosynthetic potential and a disruption
of plant growth processes (de Souza et al., 2012). In

another study, Iqbal et al. (2013) assumed that lead
inhibits chlorophyll biosynthesis by impairing the
uptake of essential photosynthetic pigment elements,
such as magnesium, potassium, calcium and iron.
While Malar et al. (2014) related the reduced
accumulation of photosynthetic pigment linked with
HM treatments to the peroxidation of chloroplast
membranes as levels of ROS generation increased
under such conditions.
CONCLUSION
The present work is considered one of the important
studies focusing on the use of native tree species in
phytoremediation of Pb, Zn and Cd contaminated
soils. The results indicated that Conocarpus erectus
and Tamarix nilotica trees are considered good
accumulator candidates to Pb, Zn and Cd metals.
Therefore, both tree species could involve in the
phytoremediation technology program in order to
reclaim the heavy metal polluted soils.
REFERENCES
Aba-Alkhil MS and Moftah AE (2013). Lead and Cadmium
pollution on some desert plants (Phytoremediation).
Journal of Agriculture and Veterinary Sciences, 6(1)
25-32.
Adham, K.G.; N.A. Al- Eisa and M.H. Farhood (2011). Risk
assessment of heavy metal contamination in soil and
wild Libyan jird Meriones libycus in Riyadh, Saudi
Arabia. J. Environ. Biol. 32: 813-819.
Al-Homaidan, A.A.; A. A. Al-Ghanayem and A. H. Alkhalifa
( 2011). Green Algae as Bioindicators of Heavy Metal
Pollution in Wadi Hanifah Stream, Riyadh, Saudi
Arabia. International Journal of Water Resources and
Arid Environments 1(1): 10-15.
Ang LH, Tang LK, Ho WM, Hui TF and Theseira GW
(2010). Phytoremediation of Cd and Pb by Four
Tropical Timber Species Grown on an Ex-tin Mine in
Peninsular Malaysia. World Academy of Science,
Engineering and Technology, 62 244-248.
Ayangbenro AS and Babalola OO (2017). A New Strategy
for Heavy Metal Polluted Environments: A Review of
Microbial Biosorbents. Int. J. Environ. Res. Public
Health 2017, 14, 94; doi:10.3390/ijerph14010094.
Chaab, C.A., Moezzi A., Sayyad G. and Chorom M. (2016).
Alleviation of Cadmium Toxicity to Maize by the
Application of Humic acid. Life Science Journal 13(12):
56-63.
de Souza R, Caroline S, de Andrade L, Adrian S and Anjos
L (2012). Lead tolerance and phytoremediation
potential of Brazilian leguminous tree species at
seedling stage. Journal of Environmental
Management, 110 299-307.
166
Agric. Biol. J. N. Am., 2017, 8(4): 159-167
Franco-Hernández M.O., M.S. Vásquez-Murrieta, A.
Patiño-Siciliano, L. Dendooven (2010), Heavy metals
concentration in plants growing on mine tailings in
Central Mexico. Bioresource Technology, 101(11):
3864–3869.
Gill M (2014). Heavy metal stress in plants: A review.
International Journal of Advanced Research, 2(6)
1043-1055.
Hale, W.G., Saunders, V.A. and Margham, J.P.
(2017). "net assimilation rate." Collins Dictionary of
Biology, 3rd ed. http://medical-
dictionary.thefreedictionary.com/net+assimilation+rate
Hezbullah, M., Sultana, S. Chakraborty, S R. and Patwary,
M. I. (2016). Heavy metal contamination of food in a
developing country like Bangladesh: An emerging
threat to food safety. J. Toxicol. Environ. Health Sci.
8(1): 1-5. Doi: 10.5897/JTEHS2016.0352.
Iqbal MM, Murtaza G, Naz T, Javed W, Hussain S, Ilyas M,
Anjum MA, Shahzad SM, Ashraf M and Iqbal Z (2017).
Uptake, Translocation of Pb and Chlorophyll Contents
of Oryza Sativa as Influenced by Soil-Applied
Amendments under Normal and Salt-Affected Pb-
Spiked Soil Conditions. Asian J Agri and Biol.
2017;5(1):15-25.
Iqbal N, Trivellini A, Masood A, Ferrante A and Khan NA
(2013). Current understanding on ethylene signaling in
plants: The influence of nutrient availability. Plant
Physiology and Biochemistry, 73 127–138.
Li, X., Schmid, B., Wang, F., & Paine, C. E. T. (2016). Net
Assimilation Rate Determines the Growth Rates of 14
Species of Subtropical Forest Trees. PLoS
ONE, 11(3), e0150644.
http://doi.org/10.1371/journal.pone.0150644
Liu L, Sun H, Chen J, Zhang Y, Li D and Li C (2014).
Effects of cadmium (Cd) on seedling growth traits and
photosynthesis parameters in cotton (Gossypium
hirsutumL.). Plant Omics Journal, 7(4) 284-290.
Malar S, Vikram SS, Favas PJC and Perumal V (2014).
Lead heavy metal toxicity induced changes on growth
and antioxidative enzymes level in water hyacinths
(Eichhornia crassipes (Mart.)). Botanical Studies, 55
54-68.
Malik, Z.H., K.C. Ravindran and G. Sathiyaraj. (2017).
Phytoremediation: a novel strategy and eco- friendly
green technology for removal of toxic metals. Int. J.
Agri and Env. Res., 3(1): 1 - 18.
Metzner H, Rau H and Senger H (1965). Untersuchungen
zur synchronisier-barketein zelner pigment mangel
mutanten von Chloella. Planta (Berl.) 65 186-194.
Moftah, A.E. and W.M. Al-Ghanim (2009). Effect of
mycorrhization on growth, nutrient uptake, and
phytoremediation of Eucalyptus rostrata co-cultured

with Medicago sativa in lead-contaminated soils. Inter.
J. Plant Sci. 20: 12-15.
Panich-Pat T, Upatham S, Pokethitiyook P, Kruatrachue M
and Lanza G (2010). Phytoextraction of metal
contaminants by Typha angustifolia: Interaction of
Lead and Cadmium in soil-water microcosms. Journal
of Environmental Protection, 1 431-437.
Patil G and Umadevi M (2014). Cadmium and lead effect
on growth parameters of four Eucalyptus species.
International Journal of Biosciences, 5 72-79.
Sharma, P. and R.S. Dubey (2005). Lead toxicity in plants.
Braz. J. Plant Physiol. 17(1):35-52
Snedecor, G.W. and G. W. Cochran (1980). Statistical
Methods, 7th edition. The Iowa State University Press,
Ames, Iowa.
167
Agric. Biol. J. N. Am., 2017, 8(4): 159-167
Umadevi M and Avudainayagam, S. (2013). Effect of
cadmium and chromium on fast growing pulp wood
tree species. International Journal of Biosciences,
3(10) 92-104.
Zengin FK and Munzuroglu O (2005). Effects of some
heavy metals on content of chlorophyll, proline and
some antioxidant chemicals in bean (Phaseolus
vulgaris L.) seedlings. Acta Biologica Cracoviensia
Series Botanica, 47(2) 157–164.
Zeliha L, Ahmet A, Fatih D. 2011. Influence of salinity on
the growth and heavy metal accumulation capacity of
Spirodela polyrrhiza (Lemnaceae). Turk J Biol. 35:
215-220.