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In-Situ Monitoring of Chromium Uptake in Different Parts of the Wheat Seedling (Triticum aestivum) using Laser-Induced Breakdown Spectroscopy a

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Rohit Kumar , Durgesh Kumar Tripathi , Alamelu Devanathan , Devendra Kumar Chauhan b

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Laser Spectroscopy Research Laboratory, Department of Physics , University of Allahabad , Allahabad , India b

Department of Botany , University of Allahabad , Allahabad , India

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Mass Spectroscopy Section, Fuel Chemistry Division , Bhabha Atomic Research Centre , Mumbai , India Accepted author version posted online: 06 Aug 2013.Published online: 08 Apr 2014.

To cite this article: Rohit Kumar , Durgesh Kumar Tripathi , Alamelu Devanathan , Devendra Kumar Chauhan & Awadhesh Kumar Rai (2014) In-Situ Monitoring of Chromium Uptake in Different Parts of the Wheat Seedling (Triticum aestivum) using Laser-Induced Breakdown Spectroscopy, Spectroscopy Letters: An International Journal for Rapid Communication, 47:7, 554-563, DOI: 10.1080/00387010.2013.824901 To link to this article: http://dx.doi.org/10.1080/00387010.2013.824901

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In-Situ Monitoring of Chromium Uptake in Different Parts of the Wheat Seedling (Triticum aestivum) using Laser-Induced Breakdown Spectroscopy Rohit Kumar1, Durgesh Kumar Tripathi2, Alamelu Devanathan3, Devendra Kumar Chauhan2, and Awadhesh Kumar Rai1 1

Laser Spectroscopy Research Laboratory, Department of Physics, University of Allahabad, Allahabad, India 2 Department of Botany, University of Allahabad, Allahabad, India 3 Mass Spectroscopy Section, Fuel Chemistry Division, Bhabha Atomic Research Centre, Mumbai, India

ABSTRACT The present work is a methodological study to investigate the effect of chromium (VI) stress on wheat seedlings. Point detection capability of laser-induced breakdown spectroscopy (LIBS) was utilized for the monitoring of in-situ chromium uptake in wheat (Triticum aestivum) seedlings. Chromium accumulation and its effects on other elements in wheat seedling were investigated by comparing the intensities of spectral lines of chromium and other minerals present in the LIBS spectra. In-situ LIBS spectra of the different parts of the wheat seedlings were recorded by directly focusing the laser beam on the surface of root, stem, and leaf of the seedlings grown with and without chromium-containing solutions. The spectra obtained from the different parts (root, stem, and leaf) of the wheat plant were analyzed to determine the distribution pattern=accumulation of chromium. Effect of the chromium uptake on the distribution pattern of other elements like calcium (Ca), magnesium (Mg), sodium (Na), and potassium (K) was also investigated. It was observed that chromium concentrations in plant organs decreased in the following order: roots > leaves > stems. KEYWORDS Cr (VI), LIBS, PCA, wheat

INTRODUCTION Received 14 March 2013; accepted 10 July 2013. Address correspondence to Awadhesh Kumar Rai, Laser Spectroscopy Research Laboratory, Department of Physics, University of Allahabad, Allahabad, India-211002. E-mail: [email protected] Color versions of one or more of the figures in the article can be found online at www.tandfonline.com/lstl.

Chromium (Cr) is one of the most toxic heavy metals and occupies the seventh position in terms of abundance on the earth.[1] It is found in several oxidation states from þII to þVI in which Cr(III) and Cr(VI) are the most stable oxidation states. Each form of Cr shows extremely diverse biological and toxicological properties. Cr(III) differs from Cr(VI) in terms of mobility bioavailability and toxicity. In the human body, Cr(III) is regarded as one of the essential trace elements that is engaged in lipid and glucose metabolism, while Cr(VI) is toxic even in low concentrations. The toxicity and parasympathetic effect of Cr(VI) on living and nonliving organisms is because of its negatively charged ion, which has the capability to cross cellular 554


membranes easily by means of sulfate ionic channels and react with the intracellular components.[2] These complexes decrease metabolic reactions and generate various reactive oxygen species (ROS) and consequently cause oxidative stress.[3,4] Chromium adversely affects the internal and external integrity of plants, such as their growth, water balance, yields, antioxidant metabolism, pigments, cellular arrangements, and so forth.[4–7] Further, in plants, Cr(VI) has also been found to delay seed germination, photosynthesis, and growth and alter the water balance and nutrient accumulation.[4–7] Cr compounds are extensively used in industries, and this can contaminate soil and water due to its improper disposal; therefore, bioavailability of Cr also increases.[3] In India, numerous agricultural and other sites are found to be much polluted with Cr, owing to intense industrial activities, and this causes substantial loss in crop yield.[5,8,9] Impacts of chromium on physiological, biochemical, cellular, and molecular levels of plant have been well investigated.[4,5] However, in situ monitoring or point-to-point detection of Cr in various parts of the plants after exogenous application of Cr is still lacking. Therefore, in the present study, wheat (Triticum aestivum), which is widely cultivated for food consumption, was selected as the model organism for this purpose. To investigate=estimate the metal concentration in biological materials, various analytical techniques were widely used, including atomic absorption spectroscopy (AAS), ion mobility spectroscopy (IMS), inductively coupled plasma-atomic emission spectroscopy (ICP-AES), inductively coupled plasmamass spectroscopy (ICP-MS), graphite furnace atomic absorption spectroscopy (GFAAS), and electrothermal atomic absorption spectroscopy (ETAAS).[10–13] However, these techniques are time consuming and require lengthy sample preparation steps. Further, due to use of chemicals for sample preparation, it may result in unwanted contamination in the sample as well as the environment. Moreover, these techniques are laboratory based and cannot be used for in situ or in vivo analysis of elements present in different parts of the plant. Due to these limitations, these conventional techniques are not suitable for studying the spatial distribution of elements in different parts of the plants. In order to overcome these limitations, we Monitoring of Chromium Uptake in Wheat Seedling

employed LIBS for the investigation of accumulation of Cr in the root, stem, and leaf of wheat plants. LIBS has several attractive features such as point detection capability, requires less sample preparation, and can provide rapid multielemental analysis of any type of sample. During the past few years, our group extensively employed LIBS to study various biological materials.[14–16] The present work aimed to investigate the toxic effects of Cr(VI) on the growth, physiological parameters, and pattern of element distribution of wheat seedlings as well as to assess the feasibility of using LIBS for monitoring the distribution of Cr in the root, stem, and leaves of the wheat plant. LIBS is an elemental analysis technique and hence it is not possible to obtain details of the species present in the sample. The present work deals with the total amount of chromium present in the different parts of the wheat seedlings.

EXPERIMENTAL Plant Materials and Growth Conditions Wheat (Triticum aestivum) seeds were purchased from the local market of Allahabad, India. Before use, uniform-sized seeds were surface sterilized with 10% (v=v) sodium hypochlorite solution for 10 min, washed with distilled water, and soaked in water for 4 hr. After sterilization and soaking, healthy, uniform-sized seeds were kept in Petri plates (150 mm, Riviera) lined with Whatman No. 1 filter papers moistened with half-strength Hoagland’s solution.[17] The seeds were kept at a temperature of 28 2 C in the dark and the seeds germinated in 4 days. Thereafter, seedlings were grown under a photon flux density (PFD) of 150 photons m2 s1 and at a relative humidity of 50–60% with a day= night cycle of 12=12 hr at 28 2 C for 8 days in a growth chamber. Uniform-sized seedlings were selected and were transferred in half-strength Hoagland’s solution to acclimatize them for 7 days. After acclimatization, Cr(VI) (K2CrO4) 20 mM, 40 mM, 60 mM, 80 mM, 100 mM, 120 mM, and 150 mM were given to the seedlings for screening and obtaining an effective dose of Cr(VI) on wheat seedlings, where a substantial effect on the growth of the plant can be observed. It was found that the seedlings died when we 555

FIGURE 1 Dose-response curve of Cr of three independent


experiments.

treated the plants with 120-mM and 150-mM Cr stresses. Hence, 100 mM Cr was selected for further studies, since it showed considerable reduction in fresh mass of the wheat seedlings (Fig. 1). Figure 1 shows the dose-response curve of Cr (means standard error) of three independent experiments. Different letters on bars indicate significantly different values at a particular treatment according to the Duncan’s multiple range test at p < 0.05 significance level. The 100-mM Cr solution with Hoagland’s solution was provided for 7 days to the seedlings. After 7 days of Cr treatment, root, leaf, and stem samples from the control and treated seedlings were analyzed.

In-Situ Analysis of the Wheat Plant The in-situ LIBS spectra of different parts of the wheat plant were recorded using the experimental

setup shown in Fig. 2. The second harmonic (532 nm) of the Nd:YAG laser (Continuum, Surelite III-10, USA) was focused on the surface of different parts (root, stem, and leaf) of the wheat plant using a 15-cm converging lens (Fig. 2). Emission from the plasma was collected using a collecting lens and was finally fed to the spectrometer through a fiber bundle. The spectrometer (Ocean Optics, LIBS 2000þ, USA), equipped with a charged-coupled device (CCD), is a four-channel spectrometer in which three channels are having a high resolution (FWHM is 0.1 nm; from 200 nm to 500 nm) and the fourth channel is having a low resolution (FWHM is 0.75 nm; from 200 nm to 900 nm). LIBS spectra of each part of the plant were recorded under optimized experimental conditions: at 10 mJ laser energy, repetition rate 4 Hz, and pulse width 4 ns, and the collection lens was set to get the maximum emission signal from the plasma plume. Five seedlings of both solutions were taken for the study and an average of 10 spots on each part of a seedling were taken to produce the data.

RESULTS AND DISCUSSION Effect of the Cr on the Wheat Seedlings Hexavalent chromium decreases seed germination and the root and shoot fresh mass and length due to its rapid accumulation in plants.[5,18] Due to toxic effects of Cr, it is reported in the literature that the net photosynthesis measured as CO2 assimilation and water use efficiency in

FIGURE 2 Experimental setup for recording of LIBS spectra of different parts of the seedlings. 556

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FIGURE 3 Effect of Cr stress on growth of wheat seedlings; photographs were taken after experiments.

the plant significantly decreases.[19] In addition to the negative impacts of Cr(VI) on the photosynthetic carboxylation reactions, photosystem II (PS II) electron transport and oxygen-evolving complex were also adversely affected by Cr(VI) stress.[5,20,21] Roots are generally more sensitive because they are in direct contact with nutrient solution containing Cr(VI). Inhibition in the growth of roots leads to the reduction in water and mineral element uptake, and this results in the inhibition of the growth of the whole plant. Toxic metals such as Cr can influence plant growth by damaging root growth, so the color of the roots changed to black with Cr addition and its development was also interrupted. Figure 3 shows the physical appearance of the experimental plants during the 7 days of treating with Cr(VI) along with plants grown in control solution. We observed that the morphology of wheat seedlings was adversely affected by treatment with Cr(VI) (Fig. 3). It is clear from Fig. 3 that due to the toxic effect of Cr, the newly emerged leaves were chlorotic and died. Moreover, control seedlings appear better than Cr(VI)-treated seedlings. We also observed that Cr(VI) caused a considerable decrease in the growth of wheat seedlings, measured as fresh weight and length of roots and shoots (stem and leaf), in comparison with the control plants (Fig. 4). Regression curves (Fig. 5) of fresh weight and dry weight Monitoring of Chromium Uptake in Wheat Seedling

FIGURE 4 Effect of Cr stress on root and shoot length and weight of wheat seedlings.

of seedling treated with Cr(VI) showed that an increase in Cr concentrations remarkably affected the fresh weight (r2 ¼ 0.988) and dry weight (r2 ¼ 0.995) of roots and shoots of wheat seedlings. It is also notable here that the regression analysis of the shoot length (r2 ¼ 0.984) and the root length (r2 ¼ 0.968) of wheat plants treated with Cr(VI) and control also shows the considerable decrease as the Cr(VI) concentration was increased. Thus, experimental results of the present study clearly demonstrate that Cr(VI) damages the plants in respect to growth, mass, and physiological parameters. It is reported that chromium (VI) is a powerful oxidizing agent that decreases growth by disturbing different metabolic processes as well as by enhancing oxidative damage to lipids and proteins due to the increased production of reactive oxygen species (ROS).[2,9,18,22,23] 557


FIGURE 5 Regression curves for fresh weight and dry weight of the root and stem.

Analysis of Cr Accumulation Using LIBS The LIBS spectra of different parts (root, stem, and leaf) of wheat seedling grown in control solution and stress solution are shown in Figs. 6–8. LIBS spectra of

different parts of the plant seedlings grown in control solution contain the spectral signature of elements like Ca, Fe, and Mg, whereas LIBS spectra of different parts of the seedlings grown in Cr solution represent the spectral signature of Cr at 357.8 nm, 359.5 nm, and 360.4 nm in addition to the above elements

FIGURE 6 LIBS spectra of root of the wheat seedling grown in two different solutions. 558

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FIGURE 7 LIBS spectra of stem of the wheat seedling grown in two different solutions.

(Ca, Fe, Mg, etc.) (Figs. 6–8). The presence of persistent lines of Cr at 357.8 nm, 359.5 nm, and 360.4 nm (inset of Fig. 6) in the LIBS spectra of the root of the plant grown in Cr stress clearly shows the accumulation of Cr in roots. But these lines are absent in the roots of the plant grown in control solution. In similar fashion, the LIBS spectra shown in Figs. 7 and 8 demonstrate the presence of Cr in stem and leaf, respectively. The above experimental result clearly indicates the presence of Cr along with other elements in the wheat plant, grown in the Cr solution. However, the spectral signature of Cr is not observed in the wheat plants grown in control solution. To compare the extent of accumulation and distribution of Cr in the various parts of the plants, we have compared the LIBS spectra of the different parts of the wheat plant grown in Cr solution and the results are shown in Fig. 9. According to Boltzmann distribution law, the intensity of the spectral line is given by the following equation:

Ikki

the concentration of a species, U (T) is the partition function, Ek is the upper energy level, and F is an experimental parameter. In order to use the Boltzmann equation for the spectral analysis of the elements present in the LIBS spectra, the laser-induced plasma should be stoichiometric in nature, it should be optically thin,

Ek

e ðkB T Þ ¼ Cs F Aki gk U ðT Þ

ð1Þ

where Ikki is the intensity of a spectral line of wavelength k, kb is the Boltzmann constant, Cs is Monitoring of Chromium Uptake in Wheat Seedling

FIGURE 8 LIBS spectra of leaf of the seedling grown in two different solutions in the spectral range of 357–362 nm.

559


FIGURE 9 Comparison of spectral lines’ intensity of LIBS spectra of root, stem, and leaf of seedling grown in Cr solution.

and local thermal equilibrium (LTE) in the plasma must exist.[24–27] In the present experiment, the calculated power density at the focal spot on the surface of the sample corresponding to 10 mJ laser energy is equal to 1011 W cm2, which fulfills the condition of stoichiometric ablation of the sample.[28] The measured intensity ratio of two Cr lines at 357.8 nm and 359.3 nm is 0.58, which is equal to products of the ratio of their transition probabilities, the ratio of their upper-level degeneracies, and the inverse ratio of their wavelengths (0.57). This shows that the laser-induced plasma in our experiment is optically thin. For thermal equilibrium, we have experimentally determined the electron density by measuring the FWHM of the Stark broadened line of Ca 422.5 nm and the theoretical Stark width obtained from plasma spectroscopy;[29] the electron density was found to be 9.26 1017 cm3, and this is greater than the limit given by McWhirter criteria 1.32 1015 cm3. We have also calculated the temperature by using the spectral lines of the different species present in the laser-induced plasma using the Boltzmann plot, and the parallel plot (Fig. 10) shows that the temperatures calculated by spectral lines of each species are nearly same; thus, the LTE holds in our experiment. The calculated temperature from the Boltzmann plot is 1.08 104 450 for root; similarly, 560

LTE is verified for the other parts of the plant. Thus, all the assumptions were fulfilled in the laser-induced plasma, and one can use the intensities of the spectral lines for further analysis. It is clear from Fig. 9 that the intensity of spectral lines of Cr at 357.8 nm, 359.5 nm, and 360.4 nm is maximum in the LIBS spectra of root followed by leaf and stem, which clearly demonstrates that the maximum uptake=accumulation of Cr is in root

FIGURE 10 Boltzmann plot for the calculation of the plasma temperature.

R. Kumar et al.

Monitoring of Chromium Uptake in Wheat Seedling

91 10 1 14 2 10 1 13 2 14.5 0.3 12 2 17 1 30.1 0.1 16 2 22 2 31 6

Control solution Cr solution

3.7 0.5 3.9 0.6 5.2 0.2

Cr solution

Control solution

H

4.9 0.5 61 6.5 0.5 19 1 15 0.4 12.4 0.6 52 7 52 7 21 0.2 22 1 19.6 0.5 6.3 0.4 42 8 13 1 8.1 0.5 6.8 0.5 8.6 0.5 10.2 0.7 11 0.8 10 1 5.5 0.6 4.9 0.3 3.1 0.7 1.9 0.2 Root Stem Leaf

6.3 0.6 6.9 0.8 7.4 0.2

Control solution Cr solution Control solution Cr solution Control solution Cr solution Control solution

followed by leaf and stem. Our result is supported by the fact that the root is in direct contact with the treated solution; therefore, there is a maximum accumulation in root followed by leaf and stem.[5,21] It is also reported that during the stress condition, plants developed a strategy to reduce the accumulation of metals in the upper part of the plant (leaf and stem).[20,21] LIBS spectra shown in the inset of Fig. 9 clearly support this fact. We have calculated the signal-to-background ratio for different spectral lines (357.8 nm, 359.3 nm, and 360.5 nm) of the Cr to confirm the general trend of the chromium uptake, and the results show that the signal-tobackground ratio of Cr is highest in the root followed by leaf and stem (Table 1). We have also evaluated the effect of the Cr stress on the presence=accumulation of other minerals= elements such as Mg, Ca, Na, and K present in leaf, root, and stem by comparing the intensity of the spectral lines of these elements in LIBS spectra of plants grown in different solutions (Table 2). The results of Table 2 shows that the concentration of Mg, Ca, Na, K, and N in Cr-stressed plants is highly affected and shows the considerable reduction compared to control plants. The dataset of Table 2 also shows that distribution of the elements in root, stem, and leaf is different for different elements, such as Na, K, and Ca and shows a pattern in which the concentration of these elements is highest in root followed by the stem and leaf. Besides this, Mg, N, O, and H show different behaviors; these elements are highest in leaf followed by the stem and root. The evaluation of these minerals’ deposition in plants is important because they are closely associated in the physiological and metabolic functions and play a major role during the course of stresses.[30] Statistical methods have been used to interpret spectroscopic data in many applications. Principal component analysis (PCA) is a multivariate analysis that characterizes and maps interrelationships among

Part of Control Cr the plant solution solution

1.77 0.01 1.31 0.01 2.3 0.3

O

0.5 0.1 0.63 0.01 1.6 0.6

N

3.6 0.8 3.3 0.9 3.3 0.6

K

Leaf

Na

Stem

Mg


357.8 359.3 360.5

Root

Ca

Wavelength(nm)

TABLE 2 Effect of Cr Uptake on the Other Minerals/Elements Present in Different Parts of the Wheat Seedlings

Signal-to-background ratio

Intensity of the atomic lines of different minerals in the LIBS spectra of wheat, plant grown in Cr(VI) and control solutions

Cr solution

TABLE 1 Signal (Atomic Lines of Cr)-to-Background Ratio in the LIBS Spectra of Different Parts of the Wheat Seedling

561


FIGURE 11 PCA plot to discriminate the LIBS data of different parts of seedlings grown in two different solutions.

datasets. Multivariate analysis on LIBS data can be used for instant classification of a variety of samples.[31–34] We have applied PCA on the LIBS data of the wheat seedling grown in the two different solutions. The result obtained from the PCA is plotted and shown in Fig. 11. It clearly reveals from the PCA plot (Fig. 11) that one can easily classify the different parts of the plants as well as plants grown in different solutions.

CONCLUSION The results of the present study indicate that Cr(VI) is very toxic and adversely affects the growth and physiological parameters of wheat plants. Further, the present study clearly reveals the ability of the LIBS technique for in situ=in vivo analysis of the accumulation of the major and minor elements in different parts of the plants without any sample preparation. In addition to this, the observation of the LIBS technique clearly supports the already established fact that Cr(VI) concentration is higher in roots followed by the leaf and stem due to the strategy adapted by plants. The present work demonstrates the feasibility of LIBS for the study of spatial distribution of Cr along with other minerals in wheat plants. It would be of interest to detect the species of Cr in the different parts of the plant as they are dependent on environmental factors in 562

which the plants are actually grown in the field, but LIBS is not suitable to directly obtain the speciation details.

FUNDING Financial assistance from the BRNS, BARC, Mumbai (No. 2009=37=30=BRNS=2063), is gratefully acknowledged. Mr. Rohit Kumar is grateful to BRNS-BARC for giving financial support as S.R.F. Dr. Durgesh Kumar Tripathi is also grateful to UGC for providing the D. Phil fellowship.

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6. Gikas, P.; Romanos, P. J. Effects of Tri-Valent (Cr(III)) and Hexa-Valent (Cr(VI)) chromium on the growth of activated sludge. Hazard. Mater. 2006, 133, 212–217. 7. Schiavon, M.; Pilon-Smits, E. A. H.; Wirtz, M.; Hell, R.; Malagoli, M. Interactions between chromium and sulfur metabolism in Brassica juncea. J. Environ. Qual. 2008, 37, 1536–1545. 8. Vajpayee, P.; Tripathi, R. D.; Rai, U. N.; Ali, M. B.; Singh, S. N. Chromium (VI) accumulation reduces chlorophyll biosynthesis, nitrate reductase activity and protein content in Nymphaea alba L. Chemosphere 2000, 41, 1075–1082. 9. Pandey, V.; Dixit, V.; Shyam, R. Antioxidative responses in relation to growth of mustard (Brassica juncea Cv. Pusa jaikisan) plants exposed to hexavalent chromium. Chemosphere 2005, 61, 40–47. 10. Murphy, A. P.; Coudert, M.; Barker, J. Plants as biomarkers for monitoring heavy metalcontaminants on Landfill sites using sequential extraction and inductively coupled plasma atomic emission spectrophotometry (ICP-AES). J. Environ. Monit. 2000, 2, 621–627. 11. Borkowski-Burnecka, J. Microwave assisted extraction for trace element analysis of plant materials by ICP-AES. Fresenius J. Anal. Chem. 2000, 368, 633–637. 12. Wieteska, E.; Zioek, A.; Drzewinska, A. Extraction as a method for preparation of vegetable samples for the determination of trace metals by atomic absorption spectrometry. Anal. Chim. Acta. 1996, 330, 251–257. 13. Morales-Munoz, S.; Luque-Garcıa, J. L.; Luque de Castro, M. D. Acidified pressurized hot water for the continuous extraction of cadmium and lead from plant materials prior to ETAAS. Spectrochim. Acta Part B 2003, 58, 159–165. 14. Chauhan, D. K.; Tripathi, D. K.; Rai, N. K.; Rai, A. K. Detection of biogenic silica in leaf blade, leaf sheath, and stem of Bermuda grass (Cynodon dactylon) using LIBS and Phytolith analysis. Food Biophys. 2011, 6, 416–423. 15. Tripathi, D. K.; Kumar, R.; Chauhan, D. K.; Rai, A. K.; Bicanic, D. Laser-induced breakdown spectroscopy for the study of the pattern of silicon deposition in leaves of Saccharum species. Instrument. Sci. Technol. 2011, 39(6), 510–521. 16. Pathak, A. K.; Kumar, R.; Singh, V. K.; Agrawal, R.; Rai, S.; Rai, A. K. Assessment of LIBS for spectrochemical analysis: A review. Appl. Spectrosc. Rev. 2012, 47(1), 14–40. 17. Arditti, J.; Dunn, A. S. Experimental plant physiology; Holt, Rinehart and Winston: New York, 1969. 18. Shanker, A. K.; Carlos, C.; Loza-Tavera, H.; Avudainayagam, S. Chromium toxicity in plants. Environ. Int. 2005, 31, 739–753. 19. Clijsters, H.; Van Assche, F. Inhibition of photosynthesis by heavy metals. Photosynth. Res. 1985, 7, 31–40. 20. Bishnoi, N. R.; Dua, A.; Gupta, V. K.; Sawhney, S. K. Effect of chromium on seed germination, seedling growth and yield of peas. Agric. Ecosyst. Environ. 1993, 47, 47–57.

Monitoring of Chromium Uptake in Wheat Seedling

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