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Bioremediation of soil contaminated with cadmium using hemp shives. A case study of modification of physiological parameters in T riticum aestivum

Volume 5 . - 2012
Scientic Bulletin of ESCORENA
Vol.5, July 2012
1. Preface
Prof. Dr. Lizica Mihut, Rector of Aurel Vlaicu” University of Arad.
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2. Introductory remarks
Prof. Dr. Ryszard Michal Kozlowski, FAO/ESCORENA Focal Point Coordinator.
_____________________________________________________________ 03
3. Current status of ESCORENA Network development and the new strategy and
emerging activities: Prof. Dr. Ryszard KOZŁOWSKI, Ass. Prof. Dr. Cecilia Sirghie, M.Sc. Maria
_____________________________________________________________ 05
4. Emerging role of ESCORENA Network: Michal Demes, Maria Mackiewicz-Talarczyk.
_____________________________________________________________ 15
5. Medicinal and Aromatic Plants Network (MAP) New Network of ESCORENA: Dr. Kirill
G. Tkachenko
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6. Some data about plants of the Russian Far East Flora and their using in Folk Medicine:
Dr. Kirill G. Tkachenko.
_____________________________________________________________ 19
7. Possibilities of re retardants application in the protection of wooden buildings in
the open-air museums: Ryszard KOZLOWSKI, Lizica MIHUT, Maria Silvia PERNEVAN, Malgorzata
_____________________________________________________________ 23
8. Bioremediation of soil contaminated with cadmium using hemp shives. A case study
of modication of physiological parameters in triticum aestivum: Lucian Copolovici, Dana
Copolovici, Ülo Niinemets and Cecilia Sirghie.
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8. BASTEURES - Project co-funded by EUROPEAN UNION trough the European Regional
Development Fund / Sectoral Operational Programme “Increase of Economic Competitiveness
/ “Investing for your future
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Volume 5 . - 2012
Lucian Copolovici1, Dana Copolovici1, Ülo Niinemets2 and Cecilia Sirghie1
1 ”Institute of Research , Development and Innovation in Technical and Natural Sciences ”
”Aurel Vlaicu” University , Arad, Romania
2 Estonian University of Life Sciences, Institute of Agricultural and Environmental Sciences
In the present study we show the possibility to use the hemp shives as biomass
remedying of soil contaminated with cadmium. The Triticum aestivum were employed as test
plant and assimilation rates and stomatal conductance to water vapor were measured. The
hemp shives determine a remediation of the physiological parameter for plants treated with 1
mg/L of cadmium.
Cadmium is one of the toxic heavy metal for human (Jomova and Valko 2011; Luparello
et al. 2011; Nzengue et al. 2011), animals (Thevenod 2010, 2009) and plants (Jahangir et al. 2009;
Verbruggen et al. 2009). It was shown that an expose to cadmium determine lung cancer (Park
et al. 2012), kidney disfunction (Liang et al. 2012), brast cancer (Julin et al. 2012) and testicular
injury (Wong and Cheng 2012; Siu et al. 2009). The source of cadmium contamination include
the rubber tires, industrial water cooling, plastics, pigments, plated ware, alloys, insecticides
(reviewed in (Reeves and Chaney 2008; Bertin and Averbeck 2006). The soil contamination
with cadmium can occur by direct inltration of contaminants from solid wastes, sewage, or
sewage sludge.
The removal of cadmium (and other heavy metals) from contaminated soil can been
done by transfer of contaminated soil to landlls. This procedure is expensive and determines
a risk sources for the whole ecosystem (Oberg and Bergback 2005). Due to this reason, the
bioremediation become low-cost and eco-friendly alternatives for cadmium removal from soil.
Bioremediation, as was shown in Mohanty and Patra (2011), typically use living organisms, to
remove toxic elements from the environment. There are many studies of dierent bacteria,
microbes and plants used for cadmium removal. For example metabolic active cells of
Saccharomyces cerevisiae have a potential application in cadmium removal (Wang et al.
2012). The recent study have been showing that Spinacia oleracea plants are not accumulate
cadmium so it can be used for phytoremediation of contaminated soils (Salaskar et al. 2011).
Other monitored natural attenuation (MNA) of contaminated soils (as is described in (Declercq
et al. 2012)) include in situ techniques which use the microbial biomass and bioaccumulators
(see (Mohanty and Patra 2011) for removal of pollutants.
It was shown that hemp plants (Cannabis sativa L.) accumulated heavy metals using
cellular mechanisms which allowing it to cope with high metal concentrations (Linger et al.
2005; Citterio et al. 2003; Gasiorek and Kozlowski 2003). Even more, the previous studies reveal
that short hemp bers have a good sorption potential (at a level of mmols) for Cd2+ ions
(Pejic et al. 2009). Based on this feature of Cannabis sativa plants, we used the hemp shives
as biomass remediation of soil contaminated with cadmium. We used Triticum aestivum as
monitoring plants to test the bioremediation capacity of hemp shives.
Materials and methods
Wheat (Triticum aestivum L.) seeds (cv. Lovrin, source: Fundulea, Romania) were used
for the experiment. 40 seeds of T. aestivum were sown in plastic pots (5×5×5 cm) lled with
commercial garden soil including slow release NPK fertilizer with microelements (Biolan,
Finland). The sowing depth was 1 cm. The plants were grown in a growth chamber (Percival,
IA, USA) under a light intensity of 1000 µmol m-2 s-1 provided for a 12 h light period and day/
night temperatures of 25°C/18°C.
The soil was articial contaminated with cadmium at a level of 1 mg/L. For
bioremediation in the soil was added between 1 and 5 % of hemp shives. The hemp shives
were obtained from dew-retted bers. The measurements were done at three Zadoks growth
stage: 1.0 (6 days), 1.1 (9 days) and 1.2 (12 days).
The photosynthetic parameters of the plants were monitored using the GFS 3000
Portable Gas Exchange System (Walz, Eeltrich, Germany) as was described in previous studies
(Niinemets et al. 2010; Niinemets et al. 2011). The measurements were performed at a chamber
CO2 concentration of 385 μmol mol-1, photosynthetic quantum ux density was kept at 1000
μmol m-2 s-1, leaf temperature at 25ºC and chamber relative humidity at 70%. The air ow rate
was 750 μmol s-1.
The rates of net assimilation (A) and stomatal conductance to water vapor (gs) were
calculated from these measurements according to von Caemmerer and Farquhar (1981).
Results and discussions
In previous studies were shown that T. aestivum exposed to high concentration of
cadmium leads to depresses growth rate, reduction of photosynthesis, decreased chlorophyll
content, changing in phenols and enzymes activities (Lakhdar et al. 2012; Wang et al. 2011; Ci
et al. 2010; Duan et al. 2010; Khan et al. 2008; Samiullah et al. 2007; Ouzounidou et al. 1997). In
our case, the assimilation rate decreased with more than 10 % for plants growth in soil treated
Volume 5 . - 2012
with cadmium. The inhibition of photosynthesis is the result of damage to the PSII reaction
center in the leaf (see (Duan et al. 2010)). The plants growth in the soil treated with hemp
shives have the same level of photosynthesis as the control plants.
Figure 1. Changes in net assimilation rate (A) with the remediation agent (hemp shives) concentration
Even more, for the mature plants (12 days) the assimilation rates are higher than for the control
plants in case of hemp shives in soil of 1.5% (Figure 1). This trend can be explicate by the
possibility that the hemp shives to act as chelator of the cadmium ions as was shown for C.
sativa chestnuts shell extract (Stingu et al. 2012).
The values of stomata conductance to water vapor (gs) are as well inuence by the cadmium
Figure 2. Changes in stomatal conductance to water vapor (gs) with the remediation agent (hemp shives)
From gure 2 can be seen that in plants treated with cadmium the gs decrease in
average with 20 %. Even that the mechanism of stomata closure is not totally understand
(Sha et al. 2011), we can speculate that the negative eect of Cd2+ to gs are relating with the
inhibition of primary carbon metabolism (Vassilev et al. 1997). Using even a small concentration
of remediation agent (hemp shives – 1%) the gs values are comparative with control plants
(Figure 2). Interesting, the values of gs increased with the increasing of the hemp shives
concentration until more than 30% comparative with control plant at remediation agent
concentration of 2%. After that, the values of gs decreased slowly.
In the present study we have shown that hemp shives act as a soil remediation
agent against cadmium soil pollution. The treatment of the soil contaminate with cadmium
even with a small concentration of hemp shives determine the recover of the physiological
parameters in the Triticum aestivum L. plants. More work is necessary in order to understand of
the mechanism of the eect of the cadmium and hemp shives on the plant-soil interactions.
This work was supported by project co-funded by European Union through European
Regional Development Fund Structural Operational Program “Increasing of Economic
Competitiveness” Priority axis 2, operation 2.1.2. ID project 679, cod SMIS CNSR 12638.
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Greenhouse pot culture studies were conducted to evaluate the bioremediation potential of spinach for removal of cadmium. The results indicated that spinach was able to take up cadmium in substantial quantity in the shoot. There were no visual cadmium toxicity effects on spinach and no significant reduction in the dry matter yield up to 20 μg g-1 cadmium. Significant growth retardation of fenugreek crop grown after spinach was observed at all the levels of cadmium, with no cadmium uptake in the shoot. This study revealed that spinach is a cadmium-tolerant crop and can be used for phytoremediation purpose.
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Barley plants (Hordeum vulgare L. cv. Obzor) were grown as a water culture in a climatic room. One part of them was subjected to a long-term Cd2+ stress - 12 d with 5.4×10−5 M Cd. The Cd2+ stress inhibited formation of the photosynthetic apparatus and its capacity for 14C photoassimilation, decreased the content of soluble proteins, increased the dark respiration rate and the free amino acids content, disturbed plant water relations, as well as the distribution of 14C within primary photoproducts of the treated barley plants.
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The effect of composted municipal solid waste (MSW) and sewage sludge (SS) on photosynthetic activity of wheat (Triticum durum L.) was investigated. Chloro-phyll fluorescence and gas exchange parameters were assessed following application of up to 300 t ha -1 of MSW compost or SS. 100 t ha -1 MSW compost was optimal for the plant growth, which showed 78% stimulation as com-pared to the control. This was associated with higher maximum quantum efficiency (F v /F m) of photosystem II (PSII) and the actual quantum efficiency of PSII open centers at light adapted state (DF/F 0 m). Maximal values of net photosynthetic rate and stomatal conductance were recorded at 100 t ha -1 MSW compost (?40 and ?116%, respectively). Ribulose bisphosphate carboxylase/oxygen-ase (RubisCO) activity was also significantly stimulated at 100 t ha -1 , while less significant impact was found in SS treatment. A marked accumulation of Ni, Pb, Cu, and Zn in concomitance with membrane lipid peroxidation were observed at 200–300 t ha -1 MSW compost and SS, resulting in lower photosynthetic activity and altered PSII functional integrity. Altogether, these results suggest that the MSW compost at 100 t ha -1 would be suitable for wheat cultivation, within the critical limits of heavy metal accumulation. However, long-term field experiments seem necessary to more accurately evaluate the safety of MSW application.
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Two cultivars of wheat (Triticum aestivum L.), namely PBW343 (high yielding type) and WH542 (low yielding type), were treated with Cd(NO 3) 2 0 and 100 mg kg-1 soil to test the physiological basis for reduced photosynthesis and growth. Activity of carbonic anhydrase and stomatal conductance were reduced by cadmium treatment suggesting mesophyll and stomatal effects on cadmium-induced reduction in photosynthesis. This decrease was more pronounced in WH542 compared to PBW343 leading to greater reductions in growth characteristics in WH542 at 30, 60 and 90 days after sowing. The effect of cadmium on both the cultivars was more conspicuous at 30 days after sowing.
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Interaction between Cd2+ of different concentrations (1, 2, and 3 mg/L) and metabolic active cells of Saccharomyces cerevisiae was studied in YPD batch cultures for a time period of 168 hours. Temporal variations of cell biomass, protein yields, and aqueous and intracellular Cd2+ concentrations were measured. S. cerevisiae cells were inhibited to grow by the presence of Cd2+ at low concentration, and appears to show distinctive responses to different levels of Cd2+ stress. Total intracellular Cd accumulation is found to progressively increase over the whole experimental course, and is positively related to the initial Cd concentration to some extent. The intracellular Cd2+ amount per biomass was, however, observed to increase in the early growth stage, but decrease progressively in late growth stage and finally reach to a stable level in the 3 mg/L Cd-amended system. An inverse pattern in the temporal variation of the intracellular Cd2+ amount per biomass is present in 1 mg/L system with the transitional pattern being found in 2 mg/L system. Both intracellular and surface biosorptive Cd might contribute to the total removal of Cd from the solution, with 20% contribution from the intracellular Cd of metabolic cells of S. cerevisiae. Our data shed light on the potential application of metabolic cells in bioremediation of Cd contamination.
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The effects of different cadmium concentrations [17 mg(Cd) kg−1(soil) and 72 mg(Cd) kg− 1(soil)] on Cannabis sativa L. growth and photosynthesis were examined. Hemp roots showed a high tolerance to Cd, i.e. more than 800 mg(Cd) kg−1(d.m.) in roots had no major effect on hemp growth, whereas in leaves and stems concentrations of 50 – 100 mg(Cd) kg−1(d.m.) had a strong effect on plant viability and vitality. For control of heavy metal uptake and xylem loading in hemp roots, the soil pH plays a central role. Photosynthetic performance and regulation of light energy consumption were analysed using chlorophyll fluorescence analysis. Seasonal changes in photosynthetic performance were visible in control plants and plants growing on soil with 17 mg(Cd) kg−1(soil). Energy distribution in photosystem 2 is regulated in low and high energy phases that allow optimal use of light and protect photosystem 2 from overexcitation, respectively. Photosynthesis and energy dissipation were negatively influenced by 72 mg(Cd) kg−1(soil). Cd had detrimental effects on chlorophyll synthesis, water splitting apparatus, reaction centre, antenna and energy distribution of PS 2. Under moderate cadmium concentrations, i.e. 17 mg(Cd) kg−1(soil), hemp could preserve growth as well as the photosynthesis apparatus, and long-term acclimation to chronically Cd stress occurred.
A series of experiments is presented investigating short term and long term changes of the nature of the response of rate of CO2 assimilation to intercellular p(CO2). The relationships between CO2 assimilation rate and biochemical components of leaf photosynthesis, such as ribulose-bisphosphate (RuP2) carboxylase-oxygenase activity and electron transport capacity are examined and related to current theory of CO2 assimilation in leaves of C3 species. It was found that the response of the rate of CO2 assimilation to irradiance, partial pressure of O2, p(O2), and temperature was different at low and high intercellular p(CO2), suggesting that CO2 assimilation rate is governed by different processes at low and high intercellular p(CO2). In longer term changes in CO2 assimilation rate, induced by different growth conditions, the initial slope of the response of CO2 assimilation rate to intercellular p(CO2) could be correlated to in vitro measurements of RuP2 carboxylase activity. Also, CO2 assimilation rate at high p(CO2) could be correlated to in vitro measurements of electron transport rate. These results are consistent with the hypothesis that CO2 assimilation rate is limited by the RuP2 saturated rate of the RuP2 carboxylase-oxygenase at low intercellular p(CO2) and by the rate allowed by RuP2 regeneration capacity at high intercellular p(CO2).
Different vegetal biomass resources such as Picea abies bark, Castanea sativa chestnuts shell and Asclepias syriaca plant were considered to provide a source of natural bioactive compounds, which can be properly used in several directions such as: plant growth regulators and amendments in bioremediation. Having in mind a complex processing biomass technology, these raw materials are used in a first step to separate bioactive compounds by an aqueous extraction. The obtained extracts containing polyphenols were tested in germination tests to evaluate their influence on cadmium bioaccumulation in oat plant (Avena sativa). It was observed that the mentioned extracts modulated cadmium bioaccumulation, photosynthesizing pigments biosynthesis, plant growth and its development depending on metal ion concentration (5, 12.5, 25 mg/L), and extracts composition determined by vegetal raw material and their total polyphenols content (130, 122, 114 mg/L related to gallic acid). FTIR spectra and histo-anatomical cross section of the roots certify that P. abies bark and A. syriaca plant extracts amendments stimulated cadmium bioaccumulation, promoting the translocation of heavy metals to the aerial part of the plant, meanwhile chestnuts shell extract reduced the mobility of cadmium determining in situ inactivation of heavy metal ions.
Leaf carbonic anhydrase (CA) activity, net photosynthetic rate (PN), stomatal conductance (gS) and plant dry mass (DM) exhibited a dose-dependent response to cadmium (Cd) in wheat (Triticum aestivum L.) grown under low and sufficient zinc (Zn) levels at 30 d after seedling emergence in sand culture. Cadmium at 10 mM concentration enhanced CA, PN and DM at low Zn level but these remain unaltered at sufficient Zn. Stomatal conductance decreased with increasing CdCl2 concentration at both the Zn levels. Cd higher than 10 mMinhibited the characteristics irrespective of Zn level. The activity of superoxide dismutase (SOD) was not saturated the with highest Cd concentration (50mM) at both the Zn levels. However, the activities of ascorbate peroxidase (APX) and glutathione reductase (GR) increased up to 25 mM Cd and decreased at 50 mM Cd at both the Zn levels. It is suggested that CA activity was induced at low Cd (10 mM) under low Zn level increasing the photosynthesis. The synergies among the activities of antioxidative enzymes helped to maintain CA and thus photosynthesis and plant DM at low Cd concentration under low Zn level.
The effects of salinity (0, 75, 150 mM) and cadmium (Cd) (0, 2, 4 μM) stresses on biomass (dry matter), photosynthesis, and fluorescence parameters were studied in hydroponically-grown wheat genotypes (‘Bakhtawar-92’, ‘Pir Sabak-85’ and ‘Khyber-87’). Cadmium and sodium chloride (NaCl) alone significantly reduced dry matter weight of both shoots and roots, and the combined stress of NaCl + Cd resulted in more reduction of dry matter weight in comparison with that caused by Cd or NaCl stress alone. The addition of Cd and NaCl in the growth medium caused the significant reduction in net photosynthetic rate (Pn), fluorescence efficiency (Fv/Fm) and stomata conductance (Gs), and the significant increase in intercellular carbon dioxide (CO2) concentration. The results also showed that the inhibition of photosynthetic and fluorescence efficiency under salinity or cadmium stress differed among the three wheat genotypes, with ‘Bakhtawar-92’ having greater capacity of acclimation to both stresses than the other two genotypes.