Introduction
Exorbitant amount of industrial waste discharge is increasing heavy
metal toxicity in less developed areas of world. This problem would be a threat
to sustainability of agriculture (Sabir et
al. 2011). Above a certain concentration, heavy metals cause the reduction
of yield by deteriorating plant growth (Jalloh et al. 2009). Human and natural activities deposit heavy metal in
environment, and these metals are major cause of pollution (Gaur and Adholeya
2004). According to Appenroth (2010) the use
of pesticides, smelting, mining, industries, rock erosion and many other
anthropogenic activities are major sources of metal contamination. The issue of
soil quality must be taken seriously as it is main growing medium for plants.
Due to its solubility and toxicity, Cadmium (Cd) is
considered as major soil pollutant (Jain et
al. 2007). Cd is easily assimilated by plants and in soil it can reach at
high levels (Milone et al. 2003).
Industrial waste, mining, pesticides and phosphate fertilizers are important
sources of Cd (Jain et al. 2007).
Other sources like combustion of fossil fuels and use of contaminated water
change the productivity and quality of soil, which lead to reduce the yield of
crop (Dourado et al. 2013).
Biosynthesis of chlorophyll and membrane functions are affected due to Cd
toxicity (Jain et al. 2007). As Cd is non-essential element, so it is
very toxic even at lower concentrations (Vitoria et al. 2001; Milone et al.
2003). As the Cd salts is water soluble, Cd can be easily absorbed by plant
roots and transferred to aerial parts (Daud et
al. 2009). The consumption of these parts is a great risk for human and
animals health (Kubo et al. 2016),
since it is very toxic even at low doses (Li et al. 2014).
The management
of these issues has become very important to minimize the effect arising due to
Cd pollution on plant, soil and environment. However, it is very challenging
because the techniques for cleaning soil are very costly and complex (Barcelo
and Poschenrieder 2003). In this regard, many methods are used for cleaning
soil to reduce the pollutants. These methods are electrokinetic, excavation,
soil washing and incineration but all these techniques are very costly and
damage the soil quality and fertility (Wuana et al. 2010). Phytoremediation is a method in which plants extract
contaminants from soil by virtue of their natural abilities (Greipsson 2011).
This technique not only removes metals from soil but also cleans environment
from other pollutant e.g., PAHs, PCBs and pesticides. Phytoremediation is cost
effective and ecofriendly technique (Kalve et
al. 2011; Sarma 2011).
Members of
Chenopodiaceae family have the ability to minimize metal contents in soil by
accumulating them in leaf and other body parts (Zulfiqar et al. 2012; Haseeb et al.
2018). Bhargava et al. (2008)
reported that quinoa (Chenopodium quinoa
Willd.) is highly efficient among these species for Cd, nickel and chromium
hyperaccumulation. The grains of quinoa have high nutritional value (Jacobsen et al. 2003). It can tolerate 4080%
humidity, can bear diverse climatic conditions (Valencia-Chamorro 2003).
However, little is known about the Cd- phytoextractability
of quinoa. The objective of the study was to find phytoextraction ability,
morphological and physiological mechanism of C. quinoa under Cd toxicity.
Materials and Methods
Experimental location and source of seed
Experiment was carried out during NovApr,
of the years 20172018 in Old Botanical Garden, University of Agriculture,
Faisalabad (32.41° N, 73.07° E), to explore the remediation ability of quinoa
in different Cd contaminated soils. Four lines of quinoa (A1, A2, UAF-Q7, and
A9) were used in this study. Seeds of quinoa were obtained from Department of
Agronomy, UAF, Pakistan. Seed of four lines (A1, A2, UAF-Q7 and A9) were grown
in pots in Completely Randomized Design with three replicates. Plants were
treated at multiple leaves stage with six levels of cadmium chloride (0, 100,
200, 300 and 500 mM). Data were collected for growth and biochemical attributes
after 15 days of cadmium treatment and yield variables data were documented at
crop maturity.
Growth parameters
To collect data of morphological and growth variables
two plants of each line (from each pot) were uprooted and shoots were separated
from roots. Shoot and root length and their fresh weight were recorded. Plants
were oven dried at 65oC up to their constant weight and then dry
weights were taken.
Physiological attributes
Arnon (1949) method was used for the estimation of
chlorophyll contents. The contents of chlorophyll were extracted from 0.1 g
fresh leaf at 4.0°C from each pot using 80% acetone. Then the extracted
contents were placed overnight at 4oC in darkness. The samples
collected the next day and were then centrifuged at 10,000 rpm for 5 min.
Supernatant absorbance was measured with a spectrophotometer (IRMECO U2020) at
645 nm, 663 nm.
Julkenen-Tiitto
(1985) method was used for the determination of total phenolic content from
leaf tissue. A 0.5 g leaf sample was extracted in 80% acetone (10 mL) and the
material was then centrifuged at 10,000 rpm for 10 min. A 100 ΅L of supernatant
was taken in a test tube and added 1 mL DW, 0.5 mL Folin Ciocaltue reagent and
2.5 mL of 20% NaCO3 solution were mixed, vortexed briefly and kept
at room temperature for 20 min. The absorbance of the colored complex was taken
at 750 nm on a UV-Visible spectrophotometer. Acetone (80%) was used as blank.
Cadmium
determination
Dry material (0.1 g each of leaf, root and seed) was
taken into digestion flasks. Two mL sulfuric acid was mixed and incubated at
room-temperature in each flask overnight. The samples were digested at 150°C
for 40 min, then 2 mL of 35% H2O2 was poured in flasks,
and reheated at 250°C; repeated the above steps, until the material become
clear. This colorless solution was then diluted in volumetric flasks with
distilled water up to 50 mL and then used for metal analysis. Atomic absorption
spectrophotometer was used to assess contents of Cd.
Yield attributes
The length of the main panicles at crop maturity was
measured as mentioned by Jacobsen and Stolen (1993). The seeds and panicles
were dried on filter paper at 2530°C. After 10
days, seeds were manually threshed, and weights were recorded using digital
balance.
Statistical
analysis
Each treatment was replicated three times under
completely randomized design and two-way ANOVA of the data for each attribute
was computed using the COSTAT Computer Program. Cadmium levels and quinoa lines
were taken as factors and their interaction was determined. The treatment means
showing significant differences were labeled with different alphabets.
Results
Growth parameters
Table 1: Mean squares of analysis of variance of data for shoot and root fresh
weights and lengths of four quinoa lines A1, A2, UAF-Q7 and A9 when treated
with various levels of Cd
|
SOV |
df |
Shoot length |
Root length |
Shoot fresh weight |
Root fresh weight |
|
Treatment |
5 |
345.59** |
45.958** |
5156.3** |
0.5230** |
|
Varieties |
3 |
645.94** |
37.118** |
3563.3** |
0.1940* |
|
Treatment Χ Varieties |
15 |
30.585ns |
1.5636ns |
123.260* |
0.0450ns |
|
Error |
48 |
37.204 |
1.0273 |
63.294 |
0.0621 |
Significant at ** P<0.01; * P<0.05 and ns P>0.05
%20603-609_files/image002.png)
Fig. 1: Shoot and root fresh weights and root length of quinoa lines when grown
under various levels of Cd stress
Treatment of plants with increased Cd levels significant
changed the shoot fresh biomass of quinoa. Interaction of Cadmium levels and
all lines had significant (P≤0.05) effect.
An increase in fresh shoot weight of quinoa lines was found up to 300 mM of cadmium while further increase in cadmium
concentrations decreased shoot fresh biomass. Maximum weight was noted in
UAF-Q7 at 300 mM and A9 showed
minimum fresh weight at 500 mM Cd. All levels of Cd caused significant
(P<0.001) variations in fresh biomass of root and combine effect of
treatments and quinoa lines was non-significant. Root fresh biomass of all
lines improved up to 200 mM and decreased
at further increase in Cd concentrations. UAF-Q7 produced higher root fresh
biomass up to 300 mM while at 400
and 500 mM A1 performed better (Table 1; Fig. 1). Shoot and root lengths were
significantly affected by all levels of Cd in all lines quinoa but their
interaction had non-significant value. UAF-Q7 and A2 had more shoot length than A1 and A9 at
all levels of Cd. 300 mM showed
positive effect on this variable and further increase in Cd influenced
negatively except A1 that showed more shoot length than A2 at 400 mM UAF-Q7 had maximum root length at all levels of Cd. It
has been observed that root length steadily increased at 0 to 200 mM Cd then tended to decrease at further increased levels
of Cd (Table 1; Fig. 1).
Physiological
attributes
Chlorophyll a,
b, a/b and total chlorophyll showed
significant (P≤0.001)
variations by Cd levels and quinoa lines while their interaction was
non-significant for b, a/b and total
chlorophyll and significant (P≤0.001) for
chlorophyll a. UAF-Q7 and A2 had high
amount of chlorophyll a and b than others. Maximum values in all
lines of quinoa were found at 100 mM while at 500 mM all lines showed minimum values as compared to control.
In current study all factors showed no variations on chlorophyll a/b ratio. Almost all lines showed same
content of chlorophyll a/b ratio at
all levels of Cd (Table 2; Fig. 2).
Cd and all
lines of quinoa significantly affected phenolics and carotenoids. High levels
of Cd decreased carotenoids and increased total phenolics in all lines of
quinoa. The combined effect of quinoa lines and Cd concentrations was also
significant for total phenolics. A2 and UAF-Q7 presented high amount of total
phenolics as compared to A1 and A9 (Table 2; Fig. 2).
Cd
accumulation
The
Cd contents of roots and leaves showed significant Cd variations in all four
lines and Cd treatment. Interaction of Cd and lines was also significant. Seed
Cd content significantly influenced by Cd treatments. Cd contents in roots,
leaves and seed directly linked with applied Cd levels. As conc. of Cd treatment increased, accumulation of Cd
in different parts of plant increased. UAF-Q7 accumulated high content as
compared to others. Leaves of quinoa accumulated highest amount of Cd while
seeds accumulated lowest amount. In seed Cd content, A1 and A7 had more Cd than
A2 and UAF-Q7 (Table 3; Fig. 3).
Yield attributes
Cd treatment significantly reduced the panicle length
and grain weight while their cumulative effect was non-significant. Panicle
length and seed weight increased up to 300 mM. Further
level decreased the both parameters as compared to control (Table 3; Fig. 3).
Discussion
Table 2: Mean squares of analysis of variance of data for Chlorophyll a, b,
a/b, total chlorophyll, carotenoids
and phenolics of four quinoa lines A1, A2, UAF-Q7 and A9 when treated with
various levels of Cd
|
SOV |
df |
Chl. a |
Chl. b |
Total Chl. |
Chl. a/b ratio |
Carotenoids |
Phenolics |
|
Treatment |
5 |
0.6494** |
0.0018** |
2.2834** |
2.9413** |
0.1852** |
0.0374** |
|
Varieties |
3 |
1.1841** |
0.0022** |
4.9208** |
12.455** |
0.3551** |
0.0488** |
|
Treatment Χ Varieties |
15 |
0.0665** |
0.0001ns |
0.1646ns |
0.2674ns |
0.0099ns |
4.3510** |
|
Error |
48 |
0.0286 |
9.5236 |
0.0414 |
0.2613 |
0.0058 |
1.324 |
Significant at ** P<0.01 and ns P>0.05
%20603-609_files/image004.png)
Fig. 2: Chlorophyll
a, b, chlorophyll a/b ratio, total chlorophylls, carotenoids and phenolics contents
of quinoa lines when grown under various levels of Cd stress
From this study it was observed that shoot fresh biomass
is not affected by low Cd levels but slightly increased as opposed to power, so
we can assume it is the optimum level for quinoa growth in the local environment. The weight of the shrubs
under 100 mM increased
(Tapia et al. 2011) and the low dose of Cd increased while the higher
level of tomato biomass decreased (Rehman et al. 2011). Improvement
in the growth of tomato seedling was noted under low concentration level of Cd.
Treatment with Cd did not reduce shoot length (Rehman et al. 2011). The best criteria for a good hyperaccumulator plant,
is that under metal contamination, its biomass above ground did not decrease
significantly (Cui et al. 2013). No
decrease in dry shoot weight and plant weight of Solanum nigrum L. (Cd hyperaccumulator) at 25 mg kg-1 Cd
was observed (Sun et al. 2008).
Slight increase in Bidens pilosa L.
shoot biomass were reported at a concentration of 16 mg kg-1 of Cd
(Sun et al. 2009). In moso bamboo,
stem dry biomass did not reduce when grown at a Cd level of 5120 mg kg-1 (Li et al. 2016). Exposure to Cd stress changed the biomass of Holm oak
in controlled condition, but the high tolerance was observed in seedling with
high amounts of Cd accumulated in roots and shoots (Dominguez et al. 2011).
Table 3: Mean squares of analysis of variance of data for root, leaf and grain
cadmium contents, penicle length and 100-seed weight of four quinoa lines A1,
A2, UAF-Q7 and A9 when treated with various levels of Cd
|
SOV |
df |
Root Cd2+
contents |
Leaf Cd2+
contents |
Seed Cd2+
contents |
Panicle length |
100-seed weight |
|
Treatment |
5 |
426.97** |
872.189** |
0.5900** |
37.689** |
2.3917** |
|
Varities |
3 |
39.986** |
144.35** |
0.0158* |
9.3519** |
1.2292** |
|
Treatment Χ Varieties |
15 |
3.9743** |
10.485** |
0.0022ns |
0.2296ns |
0.0181ns |
|
Error |
48 |
0.5109 |
0.0059 |
0.0056 |
1.2778 |
0.0825 |
Significant at ** P<0.01; * P<0.01 and
ns P>0.05
%20603-609_files/image006.png)
Fig. 3: Leaf, root and seed Cd2+ contents and panicle length and 100
seed weight of quinoa lines when grown under various levels of Cd stress
In all quinoa
lines, the chlorophyll and carotenoids contents increased at 100 mM and decreased with further doses throughout Cd levels.
These data suggest that C. quinoa could reduce the damage to chlorophyll
even at 100 mM. High
quantity of carotenoids is reported to minimize oxidative damage from heavy
metals (Unyayar et al. 2005). Improvement of
the chlorophyll/carotenoids ratio may play a defensive role as they are known
as effective quencher for ROS, particularly for singlet oxygen (Caretto et al. 2002; Chaitanya et al. 2002; Tewari et al. 2002). However, carotenoids are also real ROS
dousers, which are produced under stress conditions and played an important
role as a light harvesting pigment. In tomatoes treated with Cd, the
chlorophyll content increased considerably (Rehman et al. 2011).
In plants,
total phenolics are of great importance because they are the major group of
secondary plant metabolites. Phenolics are (non-enzymatic) antioxidants and have
been involved in interaction with many abiotic and biotic factors (Reddy et al. 2004; Tomar and Agarwal 2013). In
the present study, the increase in phenolic compounds observed with increasing
the level of Cd. Phenolic contents synthesis increased with treatment of Cd in
sunflower (Abd-Allah et al. 2015),
tomato (Abd-Allah et al. 2016) and Cassia italiaca (Hashem et al. 2016). Cd application increased plant phenolic content in wheat (Tomar
and Agarwal 2013), pharbitis (Wada et al.
2014) and Vicia faba (Dawood et al. 2014). Phenolics and their
derivatives have an important role in promoting growth in plants under various
abiotic and biotic stress conditions. The phenolics synthesis increases the
antioxidants levels and contributes to cell wall formation and protects plants
in stress outbursts (Ahanger et al.
2015; Hashem et al. 2016).
Cd deposition
increased as its levels increased in roots, leaves and seeds. Seed had the
lowest Cd content accumulated than the leaves and roots. Ali et al. (2015) reported the same findings
that Cd content increased also in geminated seeds. Heavy metals absorption is
associated with increasing metal concentration (Xiong and Wang 2005).
Increasing concentrations of Cd improved leaf and root content of Cd (Muradoglu
et al. 2015). Similar findings were
observed in almond (Nada et al. 2007)
and Lepidium sativum (Gill et al. 2012), where Cd content
accumulation increased with higher levels of Cd application.
Conclusion
All quinoa lines showed tolerance to cadmium levels.
They survived even the high levels of cadmium application but showed better
growth up to 200 mM. UAF-Q7 and
A2 showed better results as compared to A1 and A9. Hence, they are more
efficient phytoremediator. The possible mechanisms involved are better growth,
diverse morpho-anatomical features, cadmium sequestration with carotenoids and
phenolics, metabolic adjustments and keep maximum nutrients in plant parts.
Author Contributions
AR, MA and SMAB planned the experiment. MS and SMAB
interpreted the results. AR and MA made the write up and statistically analyzed
the data. AR made the illustrations.
References
Abd-Allah EF, A Hashem,
AA Alqarawi (2016). Mitigation of cadmium induced stress in tomato (Solanum lycopersicum L.) by selenium. Pak J Bot 48:953961
Abd-Allah EF, A Hashem,
AA Alqarawi, HA Alwathnani (2015). Alleviation of adverse impact of cadmium
stress in sunflower (Helianthus annuus
L.) by arbuscular mycorrhizal fungi. Pak
J Bot 47:785795
Ahanger MA, RM Agarwal,
NS Tomar, M Shrivastava (2015). Potassium induces positive changes in nitrogen metabolism and
antioxidant system of oat (Avena sativa L. cultivar Kent). J Plant Interact 10:211223
Ali B, X Deng, X Hu, RA
Gill, S Ali, S Wang, W Zhou (2015). Deteriorative effects of cadmium stress on
antioxidant system and cellular structure in germinating seeds of Brassica napus L. J Agric Sci Technol 17:6374
Appenroth K-J (2010). Definition of Heavy Metals
and their role in biological systems. In: Soil
Heavy Metals, pp:1929. Vol. 19. Springer, Dordrecht, The Netherlands
Arnon DI (1949). Copper
enzyme in isolated chloroplasts polyphenoloxidase in Beta vulgaris. Plant Physiol 24:115
Barcelo J, C Poschenrieder (2003). Phytoremediation:
Principles and perspectives. Contrib Sci
2:333344
Bhargava A, S Shukla, J Srivastava, N Singh, D Ohri
(2008). Chenopodium: a prospective plant for phytoextraction. Acta Physiol Plantarum 30:111120
Caretto
S, A Paradiso,
L DAmico, L
De Gara (2002).
Ascorbate and glutathione metabolism in two sunflower cell lines of
differing α-tocopherol biosynthetic capability. Plant Physiol Biochem 40:509513
Chaitanya KV, D Sundar, S Masilamani, R Reddy (2002).
Variation in heat stress-induced antioxidant enzyme activities among three
mulberry cultivars. Plant Growth Regul
36:175180
Cui S, TA Zhang, SL Zhao, P Li, QX Zhou, QR Zhang, Q Han
(2013). Evaluation of three ornamental plants for phytoremediation of
Pb-contaminated soil. Intl J Phytoremed
15:299306
Daud MK, YQ Sun, M Dawood, Y Hayat, MT Variath, YX Wu, U
Mishkat, U Najeeb, SJ Zhu (2009). Cadmium-induced functional and
ultrastructural alterations in roots of two transgenic cotton cultivars. J Hazard Mater 161:463473
Dawood MG, HAA Taie, RMA Nassar, M Abdelhamid, U
Schmidhalter (2014). The changes induced in the physiological, biochemical and
anatomical characteristics of Vicia faba by
the exogenous application of proline under seawater stress. S Afr J Bot 93:5463
Dominguez MT, T Maranon, JM Murillo, S Redondo-Gomez
(2011). Response of Holm oak (Quercus ilex subsp. ballota) and
mastic shrub (Pistacia lentiscus L.) seedlings to high concentrations of
Cd and Tl in the rizhosphere. Chemosphere
83:11661174
Dourado MN, PF Martins, MC Quecine, FA Piotto, LA Souza,
MR Franco, T Tezotto, RA Azevedo (2013). Burkholderia
sp. SCMS54 reduces cadmium toxicity and promotes growth in tomato. Ann Appl Biol 163:494507
Gaur A, A Adholeya (2004). Prospects of arbuscular
mycorrhizal fungi in phytoremediation of heavy metal contaminated soils. Curr Sci 86:528534
Gill SS, NA Khan, N Tuteja (2012). Cadmium at high dose
perturbs growth, photosynthesis and nitrogen metabolism while at low dose
it up regulates sulfur assimilation and antioxidant machinery in garden
cress (Lepidium sativum L.). Plant
Sci 182:112120
Greipsson S (2011). Phytoremediation. Natl Edu Knowl 3; Article 7
Hashem A, EF Abd_Allah, AA Alqarawi, D Egamberdieva
(2016). Bioremediation of adverse impact of cadmium toxicity on Cassia
italica Mill by
arbuscular mycorrhizal fungi. Saudi J Biol Sci 23:3947
Haseeb M, SMA, Basra, I
Afzal, A Wahid (2018). Quinoa response to lead: Growth and lead partitioning. Intl J Agric Biol 20:338‒344
Jacobsen SE, A Mujica, CR
Jensen (2003). The Resistance of quinoa (Chenopodium
quinoa Willd.) to adverse abiotic factors. Food Rev Intl 19:99109
Jacobsen
SE, O Stolen
(1993). Quinoa-morphology and
phenology and
prospects for its production as a new crop
in Europe. Eur J Agron 2:1929
Jain M, M Pal, P Gupta, R Gadre (2007). Effect of
cadmium on chlorophyll biosynthesis and enzymes of nitrogen assimilation in
greening maize leaf segments: role of 2-oxoglutarate. Ind J Exp Biol 45:385389
Jalloh MA, J Chen, F Zhen, G Zhang (2009). Effect of
different N fertilizer forms on antioxidant capacity and grain yield of rice
growing under Cd stress. J Haz Mat
162:10811085
Julkenen-Tiitto R (1985). Phenolic constituents in the
leaves of northern willows: methods for the analysis of certain phenolics. Agric Food Chem 33:213217
Kalve S, BK Sarangi, RA Pandey, T Chakrabarti (2011).
Arsenic and chromium hyperaccumulation by an ecotype of Pteris vittata-prospective for phytoextraction from contaminated
water and soil. Curr Sci 100:888894
Kubo K, H Kobayashi, M Fujita, T Ota, Y Minamiyama, Y
Watanabe, T Nakajima, T Shinano (2016). Varietal differences in the absorption
and partitioning of cadmium in common wheat (Triticum aestivum L). Environ
Exp Bot 124:7988
Li S, J Chen, E Islam, Y Wang, J Wu, Z
Ye, W Yan, D Peng, D Liu (2016). Cadmium-induced oxidative stress, response of
antioxidants and detection of intracellular cadmium in organs of moso bamboo (Phyllostachys pubescens). Chemosphere 153:107114
Li TQ, Q Tao, MJI Shohag, XE Yang, DL Sparks, YC Liang
(2014). Root cell wall polysaccharides are involved in cadmium
hyperaccumulation in Sedum alfredii. Plant Soil 389:387399
Milone MT, C Sgherri, H Clijsters, F Navari-Izzo (2003):
Antioxidative responses of wheat treated with realistic concentration of
cadmium. Environ Exp Bot 50:265276
Muradoglu F, M Gundogdu, S Ercisli, T Encu, F Balta, HZE
Jaafar, M Zia-Ul-Haq (2015). Cadmium toxicity affects chlorophyll a and b
content, antioxidant enzyme activities and mineral nutrient accumulation in
strawberry. Biol Res 48; Article p11
Nada E, BA Ferjani, A Rhouma, BR Bechir, M Imed, B Makki
(2007). Cadmium-induced growth inhibition and alteration of biochemical
parameters in almond seedlings grown in solution culture. Acta Physiol Plantarum 29:5762
Reddy AR, KV Chaitanya, M Vivekanandan (2004).
Drought-induced responses of photosynthesis and antioxidant metabolism in
higher plants. J Plant Physiol
161:11891202
Rehman F, F Khan, D Varshney, F
Naushin, J Rastogi (2011). Effect of cadmium on the growth of tomato. Biol Med 3:187190
Sabir M, A Ghafoor, Saifullah, MZU Rehman, HR Ahmad, T
Aziz (2011). Growth and metal ionic composition of Zea mays as
affected by nickel supplementation in the nutrient solution. Intl J Agric Biol 13:186190
Sarma H (2011). Metal hyperaccumulation in plants: A
review focusing on phytoremediation technology. J Environ Sci Technol 4:118138
Sun Y, Q Zhou, C
Diao (2008). Effects of cadmium and arsenic on
growth and metal accumulation of Cd-hyperaccumulator Solanum nigrum L. Bioresour Technol
99:11031110
Sun YB, QX Zhou, L Wang, WT Liu (2009). Cadmium
tolerance and accumulation characteristics of Bidens pilosa L. as a potential Cd-hyperaccumulator. J Hazard Mater 161:808814
Tapia E, C Montes, P Rebufel, A
Paradela, H Prieto, G Arenas (2011). Expression of an
optimized Argopecten purpuratus antimicrobial
peptide in E. coli and evaluation of the
purified recombinant protein by in vitro challenges against important plant
fungi. Peptides 32:19091916
Tewari RK, P Kumar, PN Sharma, SS Bisht (2002).
Modulation of oxidative stress responsive enzymes by excess cobalt. Plant Sci 162:381388
Tomar NS, RM Agarwal (2013). Influence of treatment of Jatropha curcas L. leachates and
potassium on growth and phytochemical constituents of wheat (Triticum aestivum L.). Amer J Plant Sci 4:11341150
Unyayar S, Y Keleş, FO Ηekiη (2005). The
antioxidative response of two tomato species with different drought tolerances
as a result of drought and cadmium stress combinations. Plant Soil Environ 51:5764
Valencia-Chamorro SA
(2003). Quinoa. In: Encyclopedia of Food Science and Nutrition,
pp:48954902. Caballero B (ed.). Academic Press, Amsterdam, The Netherlands
Vitoria AP, PJ Lea, RA Azevedo (2001). Antioxidant
enzymes responses to cadmium in radish tissues. Phytochemistry 57:701710
Wada KC, K Mizuuchi, A Koshio, K Kaneko, T Mitsui, K
Takeno 2014. Stress enhances the gene expression and enzyme activity of
phenylalanine ammonia-lyase and the endogenous content of salicylic acid to
induce flowering in Pharbitis. J Plant Physiol 171:895902
Wuana RA, FE Okieimen, JA Imborvungu (2010). Removal of
heavy metals from contaminated soil using chelating organic acids. Intl J Environ Sci Technol 7:485496
Xiong ZT, H Wang (2005). Copper toxicity and
bioaccumulation in chinese cabbage (Brassica pekinensis Rupr.). Environ
Toxicol 20:188194
Zulfiqar S, A Wahid, M
Farooq, N Maqbool, M Arfan (2012). Phytoremediation of soil cadmium by using Chenopodium species. Pak J Agric Sci 49:435445