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Current IssueEditorial BoardOnline First ArticlesArchive

volume 38 issue 4 (august 2015) : 469-476,   Doi: 10.5958/0976-0571.2015.00130.7

Physiological and proteolytic activities of Medicago truncatula under different cadmic treatments

E
Elmsehli Sarra
A
Aloui Achref
S
Smiti-Achi Samira
1Laboratoire de Physiologie Végétale, Faculté des Sciences de Tunis, Campus Universitaire El Manar II, 1060 Tunis, Tunisia.
Cite article:- Sarra Elmsehli, Achref Aloui, Samira Smiti-Achi (2025). Physiological and proteolytic activities of Medicago truncatula under different cadmic treatments . Legume Research. 38(4): 469-476. doi: 10.5958/0976-0571.2015.00130.7.

ABSTRACT

Medicago truncatula (A17) were cultivated under strictly controlled growth conditions, in a nutrient solution in the absence or presence of Cd (10, 20 and 50 µM CdSO4). After 20 days, decrease on the plant growth was detected and chlorosis appeared on the foliar limbs. Root growth, relative root growth (Cd -treated /untreated seedlings) and tolerance index (difference of root growth between Cd-treated and untreated seedlings) were considered as the indices of tolerance to this toxic metal. The results showed that the internal quantity of cadmium increases essentially in roots level with the elevation of the cadmium concentration in the growth medium. Different cadmium treatments significantly and considerably decreased shoot growth and root growth at Cd concentration 20µM. In addition, cadmium induced the proteolytic activity endopeptidase in roots. The increase of calcium, magnesium and potassium content in plant tissues in response to different Cd treatments reflected a kind of adaptive mineral strategy that apparently failed to give resistance to M. truncatula plant against Cd treatments.

REFERENCES

  1. Ahmad, .P, Sharma, S. and Srivastava, P.S. (2007). In vitro selection of NaHCO3 tolerant cultivars of Morus alba (Local and Sujanpuri) in response to morphological and biochemical parameters. Hort. Sci. 34: 114-122.
  2. Aloui, A., Recorbet, G., Gollotte, A., Robert, F., Valot, B., Gianinazzi-Pearson, V., Aschi-Smiti, S. and Dumas-Gaudot, E. (2009). On the mechanisms of cadmium stress alleviation in Medicago truncatula by Arbuscular mycorrhizal symbiosis: A root proteomic study. Proteomics. 9: 420-433.
  3. Baldet, P., Defraud, C., Chevalier, C., Brouquise, R., Juste, O. and Raymound, P. (2002). Contrasted response to carbohydrate limitation in tomato fruit at two stages of development. Plant Cell and environment. 25: 1639-1649.
  4. Brouquisse, R., Fisher, C. and Raymond, P. (1997) La protéolyse chez les plantes supérieures: Nature, fonction, et régulation, In: J-F Morot-Gaudy édit. Assimilation de l’azote chez les plantes, Aspects physiologique, biochimique et moléculaire, pp. 327-350.
  5. Brouquisse, R., Gaudillère, J.P. and Raymond, P. (1998). Induction of a carbon-starvation-related proteolysis in whole maize plants submitted to light/dark cycles and to extended darkness. Plant Physiol. 117: 1281-1291.
  6. Chen, Y.X., He, Y.F., Luo, Y.M., Yu, Y.L., Lin, Q. and Wong, M.H. (2003). Physiological mechanism of plant roots exposed to cadmium. Chemosphere. 50: 789-793.
  7. Chugh, L.K. and Swahney, S.K. (1999). Photosynthetic activities of Pisum sativum seedlings grown in presence of cadmium. Plant Physiol. Biochem. 37: 297-303.
  8. Cosio, C., Enrico, M. and Keller, C. (2004). Hyperaccumulation of cadmium and zinc in Thlaspi caerulescens and Arabidopsis halleri at the leaf cellular level. Plant Physiology. 134:716-725.
  9. Dalcorso, G., Farinati, S. and Furini, A. (2010). Regulatory networks of cadmium stress in plants. Plant Signal Behav. 5: 663-667.
  10. Das, P., Samantaray, S. and Rout, G.R. (1997). Studies on cadmium toxicity in plants. Environ. Pollut. 98: 29-36.
  11. Dong, J., Wu, F. and Zhang, G. (2006). Influence of cadmium on antioxidant capacity and four microelement concentrations in tomato seedlings (Lycopersicon esculentum). Chemosphere. 64: 1659-1666.
  12. Dražic, G., Mihailovic, N. and Lojic, M. (2006). Cadmium accumulation in Medicago sativa seedlings treated with salicylic acid. Biol. Plantarum. 50: 239-244.
  13. Elloumi, N., Ben Abdallah, F., Rhouma, A., Ben Rwina, B., Mezghani, I. and Boukhris, M. (2007). Cadmium-induced growth inhibition and alteration of biochemical parameters in almond seedlings grown in solution culture. Acta Physiologiae Plantarum. 29: 57-62.
  14. Finger-Teixeira, A., de Lourdes, M.L.F., Ricardo Soares, A., da Silva, D. and Ferrarese-Filho, O. (2010). Cadmium-induced lignification restricts soybean root growth. Ecotoxicology and Environmental Safety. 73: 1959–1964.
  15. Gill,S.S., Hasanuzzaman, M., Nahar, K., Macovei, A. and Tuteja, N. (2013). Importance of nitric oxide in cadmium stress tolerance in crop plants. Plant Physiol Biochem. 63: 254-261.
  16. Groppa, M.D., Rosales, E.P., Iannone, M.F. and Benavides, M.P. (2008). Nitric oxide, polyamines and Cd-induced phytotoxicity in wheat roots. Phytochemistry. 69: 2609-2615.
  17. Haag-Kernel, A., Schäfer, H.J., Heist, S. and Rausch, C. 1999). Cadmium exposure in Brassica juncea causes a decline in transpiration rate and leaf expansion without effect on photosynthesis. J. of Experimental Botany. 50: 1827-1835.
  18. Hall, J.L. (2000). Cellular mechanisms for heavy metal detoxification and tolerance. J. Exp. Bot. 53: 1-11.
  19. Hirschi, K.D. (2004). The calcium conundrum, both versatile nutrient and specific signal. Plant Physiol. 136: 2438-2442.
  20. Horchani, F., Gallusci, P., Baldet, P., Cabasson, C., Maucourt, M., Rolin, D., Smiti, S. and Raymond, P. (2008). Prolonged root hypoxia induces ammonium accumulation and decreases the nutritional quality of tomato fruits. J. Plant Physiology. 165: 1352-1359.
  21. Hsu, Y.T. and Kao, C.H. (2003a). Changes in protein and amino acid contents in two cultivars of rice seedlings with different apparent tolerance to cadmium. Plant Growth Regal. 40: 147-155.
  22. Hsu, Y.T. and Kao, C.H. (2003b). Role of abscisic acid in cadmium tolerance of rice (Oryza sativa L.) seedling. Plant, cell and Environment. 26: 867-874.
  23. Hsu, Y.T. and Kao, C.H. (2004). Accumulation of ammonium ion in cadmium tolerant and sensitive cultivars of Oryza sativa. Australian society of agronomy, new directions for a diverse planet.
  24. Khan, M.N., Siddiqui, M.H., Mohammad, F., Naeem, M. and Khan, M.M.A. (2010). Calcium chloride and gibberellic acid protect linseed (Linum usitatissimum L.) from NaCl stress by inducing antioxidative defence system and osmoprotectant accumulation. Acta Physiol. Plant. 32: 121-132.
  25. Liu, J., Li, K., Xu, J., Liang, J., Lu, X., Yang, J. and Zhu, Q. (2003). Interaction of Cd and five mineral nutrients for uptake and accumulation in different rice cultivars and genotypes. Field Crops Res. 83: 271-281.
  26. Mengel, K. (2007). Potassium, In Handbook of Plant Nutrition; Barker, A.V., Pilbeam, D.J., Eds.; CRC Press: Boca Raton, FL, USA, pp. 91-120.
  27. Metwally, A., Safronova, V., Belimov, A.A. and Dietz, K.J. (2005). Genotypic variation of the response to cadmium toxicity in Pisum sativum L. J. Exp. Botany. 56: 167-178.
  28. Pacifici, R.E. and Davies, K.J.A. (1990). Protein degradation as an index of oxidative stress. Methods Enzymology. 186: 485-502.
  29. Perfus-Barbeoch, L., Leinhardt, N., Vavasseur, A. and Forestier, C. (2002). Heavy metal Toxicity, Cd permeates through calcium channels and disturbs the plant water status. Plant J. 32: 539-548.
  30. Rodríguez-Serrano, M., Romero-Puertas, M.C., Pazmiño, D.M., Testillano, P.S., Risueño, M.C., del Río, L.A. and Sandalio, L.M. (2009). Cellular response of pea plants to cadmium toxicity: Cross talk between reactive oxygen species, nitric oxide, and calcium. Plant Physiol. 150: 229-243.
  31. Romero-Puertas, M.C., Palma, J.M., Gómez, M., Del Rio, L.A. and Sandalio, L.M. (2002). Cadmium causes the oxidative modification of proteins in pea plants. Plant cell Environ. 25: 677-686.
  32. Rosielle, A.A. and Hamblin, J. (1981). Theoretical aspects of selection for yield in stress and non-stress environments. Crop Sci. 21: 943-946.
  33. Saglio, P.H. and Pradet, A. (1980). Soluble sugars, respiration and energy charge during ageing of excised maize root tips. Plant Physiol. 66: 516-519.
  34. Sandalio L.M., Dalurzo H.C., Gómez M., Romero-Puertas M.C. and del Río L.A. (2001). Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J. Exp. Bot. 52: 2115-2126.
  35. Schützendübel, A., Schwanz, P., Teichmann, T., Gross, K., Langenfeld-Heyser, R., Godbold, D.L. and Polle, A. (2001).
  36. Cadmium–Induced Changes in antioxidative systems, hydrogen peroxide content, and differentiation in scots pine roots. Plant physiology. 127: 887-898.
  37. Siddiqui, M.H., Al-Whaibi, M.H. and Basalah, M.O. (2011). Interactive effect of calcium and gibberellin on nickel tolerance in relation to antioxidant systems in Triticum aestivum L. Protoplasma. 248: 503-511.
  38. Sledge, M.K., Pechter, P. and Payton, M.E. (2005). Aluminum tolerance in Medicago truncatula germplasm. Crop Sci. 45: 2001-2004.
  39. Somashekaraiah, B.V., Padmaja, K. and Prasad, A.R.K. (2006). Phytotoxicity of cadmium ions on germinating seedlings of mung bean (Phaseolus vulgaris): Involvement of lipid peroxides in chlorphyll degradation. Physiologia Plantarum. 85: 85-89.
  40. Tanaka, A. and Tsuji, H. (1998). Effects of calcium on chlorophyll synthesis and stability in the early phase of greening in cucumber cotyledons. Plant Physiol. 65: 1211-1215.
  41. Vangronsveld, J. and Clijsters, H. (1994). Toxic effects of metals, In Plants and the Chemical Elements. Biochemistry, Uptake, Tolerance and Toxicity. Ed. M.E. Farago. pp. 149-177.
  42. Wintermans, J.F.G.A. and de Mots, A. (1965). Spectrophotometric characteristics of chlorophylls a and b and their phenophytins in ethanol. Biochemistry and Biophysics ACTA. 109: 448-453.
  43. Wójcika, M., Vangronsveld, J. and Tukiendorf, A. (2005). Cadmium tolerance in Thlaspi caerulescens: Growth parameters, metal accumulation and phytochelatin synthesis in response to cadmium. Environmental and Experimental Botany. 53: 151-161.
  44. Woolhouse, H.W. (1983). Toxicity and tolerance in the response of plants to heavy metals. Encycl. Plant Physiol. 12: 246- 300.
  45. Wu, F., Dong, J., Jia, G.X., Zheng, S.J. and Zhang, G.P. (2006). Genotypic difference in the response of seedling growth and Cd toxicity in rice (Oryza sativa L.). Agric. Sci. China. 5: 68-76.
  46. Wu, F., Zhang, G., Dominy, P., Wu, H. and Bachir, D.M. (2007). Differences in yield components and kernel Cd accumulation in response to Cd toxicity in four barley genotypes. Chemosphere. 70: 83–92.
  47. Xu, J., Wang, W., Yin, H., Liu, X., Sun, H. and Mi, Q. (2010). Exogenous nitric oxide improves antioxidative capacity and reduces auxin degradation in roots of Medicago truncatula seedlings under cadmium stress. Plant Soil. 326: 321-330.
  48. Yuguan, Z., Min, Z., Luyang, L., Zhe, J., Chao, L., Sitao, Y., Yanmei, D. and Fashui, H. (2009). Effects of cerium on key enzymes of carbon assimilation of spinach under magnesium deficiency. Biological Trace Element Research. 131: 154-164.
  49. Zhang, G., Fukami, M. and Sekimoto, H. (2002). Influence of cadmium on mineral concentrations and yield components in wheat genotypes differing in Cd tolerance at seedling stage. Field Crops Res. 77: 93-98.
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    volume 38 issue 4 (august 2015) : 469-476,   Doi: 10.5958/0976-0571.2015.00130.7

    Physiological and proteolytic activities of Medicago truncatula under different cadmic treatments

    E
    Elmsehli Sarra
    A
    Aloui Achref
    S
    Smiti-Achi Samira
    1Laboratoire de Physiologie Végétale, Faculté des Sciences de Tunis, Campus Universitaire El Manar II, 1060 Tunis, Tunisia.
    Cite article:- Sarra Elmsehli, Achref Aloui, Samira Smiti-Achi (2025). Physiological and proteolytic activities of Medicago truncatula under different cadmic treatments . Legume Research. 38(4): 469-476. doi: 10.5958/0976-0571.2015.00130.7.

    ABSTRACT

    Medicago truncatula (A17) were cultivated under strictly controlled growth conditions, in a nutrient solution in the absence or presence of Cd (10, 20 and 50 µM CdSO4). After 20 days, decrease on the plant growth was detected and chlorosis appeared on the foliar limbs. Root growth, relative root growth (Cd -treated /untreated seedlings) and tolerance index (difference of root growth between Cd-treated and untreated seedlings) were considered as the indices of tolerance to this toxic metal. The results showed that the internal quantity of cadmium increases essentially in roots level with the elevation of the cadmium concentration in the growth medium. Different cadmium treatments significantly and considerably decreased shoot growth and root growth at Cd concentration 20µM. In addition, cadmium induced the proteolytic activity endopeptidase in roots. The increase of calcium, magnesium and potassium content in plant tissues in response to different Cd treatments reflected a kind of adaptive mineral strategy that apparently failed to give resistance to M. truncatula plant against Cd treatments.

    REFERENCES

    1. Ahmad, .P, Sharma, S. and Srivastava, P.S. (2007). In vitro selection of NaHCO3 tolerant cultivars of Morus alba (Local and Sujanpuri) in response to morphological and biochemical parameters. Hort. Sci. 34: 114-122.
    2. Aloui, A., Recorbet, G., Gollotte, A., Robert, F., Valot, B., Gianinazzi-Pearson, V., Aschi-Smiti, S. and Dumas-Gaudot, E. (2009). On the mechanisms of cadmium stress alleviation in Medicago truncatula by Arbuscular mycorrhizal symbiosis: A root proteomic study. Proteomics. 9: 420-433.
    3. Baldet, P., Defraud, C., Chevalier, C., Brouquise, R., Juste, O. and Raymound, P. (2002). Contrasted response to carbohydrate limitation in tomato fruit at two stages of development. Plant Cell and environment. 25: 1639-1649.
    4. Brouquisse, R., Fisher, C. and Raymond, P. (1997) La protéolyse chez les plantes supérieures: Nature, fonction, et régulation, In: J-F Morot-Gaudy édit. Assimilation de l’azote chez les plantes, Aspects physiologique, biochimique et moléculaire, pp. 327-350.
    5. Brouquisse, R., Gaudillère, J.P. and Raymond, P. (1998). Induction of a carbon-starvation-related proteolysis in whole maize plants submitted to light/dark cycles and to extended darkness. Plant Physiol. 117: 1281-1291.
    6. Chen, Y.X., He, Y.F., Luo, Y.M., Yu, Y.L., Lin, Q. and Wong, M.H. (2003). Physiological mechanism of plant roots exposed to cadmium. Chemosphere. 50: 789-793.
    7. Chugh, L.K. and Swahney, S.K. (1999). Photosynthetic activities of Pisum sativum seedlings grown in presence of cadmium. Plant Physiol. Biochem. 37: 297-303.
    8. Cosio, C., Enrico, M. and Keller, C. (2004). Hyperaccumulation of cadmium and zinc in Thlaspi caerulescens and Arabidopsis halleri at the leaf cellular level. Plant Physiology. 134:716-725.
    9. Dalcorso, G., Farinati, S. and Furini, A. (2010). Regulatory networks of cadmium stress in plants. Plant Signal Behav. 5: 663-667.
    10. Das, P., Samantaray, S. and Rout, G.R. (1997). Studies on cadmium toxicity in plants. Environ. Pollut. 98: 29-36.
    11. Dong, J., Wu, F. and Zhang, G. (2006). Influence of cadmium on antioxidant capacity and four microelement concentrations in tomato seedlings (Lycopersicon esculentum). Chemosphere. 64: 1659-1666.
    12. Dražic, G., Mihailovic, N. and Lojic, M. (2006). Cadmium accumulation in Medicago sativa seedlings treated with salicylic acid. Biol. Plantarum. 50: 239-244.
    13. Elloumi, N., Ben Abdallah, F., Rhouma, A., Ben Rwina, B., Mezghani, I. and Boukhris, M. (2007). Cadmium-induced growth inhibition and alteration of biochemical parameters in almond seedlings grown in solution culture. Acta Physiologiae Plantarum. 29: 57-62.
    14. Finger-Teixeira, A., de Lourdes, M.L.F., Ricardo Soares, A., da Silva, D. and Ferrarese-Filho, O. (2010). Cadmium-induced lignification restricts soybean root growth. Ecotoxicology and Environmental Safety. 73: 1959–1964.
    15. Gill,S.S., Hasanuzzaman, M., Nahar, K., Macovei, A. and Tuteja, N. (2013). Importance of nitric oxide in cadmium stress tolerance in crop plants. Plant Physiol Biochem. 63: 254-261.
    16. Groppa, M.D., Rosales, E.P., Iannone, M.F. and Benavides, M.P. (2008). Nitric oxide, polyamines and Cd-induced phytotoxicity in wheat roots. Phytochemistry. 69: 2609-2615.
    17. Haag-Kernel, A., Schäfer, H.J., Heist, S. and Rausch, C. 1999). Cadmium exposure in Brassica juncea causes a decline in transpiration rate and leaf expansion without effect on photosynthesis. J. of Experimental Botany. 50: 1827-1835.
    18. Hall, J.L. (2000). Cellular mechanisms for heavy metal detoxification and tolerance. J. Exp. Bot. 53: 1-11.
    19. Hirschi, K.D. (2004). The calcium conundrum, both versatile nutrient and specific signal. Plant Physiol. 136: 2438-2442.
    20. Horchani, F., Gallusci, P., Baldet, P., Cabasson, C., Maucourt, M., Rolin, D., Smiti, S. and Raymond, P. (2008). Prolonged root hypoxia induces ammonium accumulation and decreases the nutritional quality of tomato fruits. J. Plant Physiology. 165: 1352-1359.
    21. Hsu, Y.T. and Kao, C.H. (2003a). Changes in protein and amino acid contents in two cultivars of rice seedlings with different apparent tolerance to cadmium. Plant Growth Regal. 40: 147-155.
    22. Hsu, Y.T. and Kao, C.H. (2003b). Role of abscisic acid in cadmium tolerance of rice (Oryza sativa L.) seedling. Plant, cell and Environment. 26: 867-874.
    23. Hsu, Y.T. and Kao, C.H. (2004). Accumulation of ammonium ion in cadmium tolerant and sensitive cultivars of Oryza sativa. Australian society of agronomy, new directions for a diverse planet.
    24. Khan, M.N., Siddiqui, M.H., Mohammad, F., Naeem, M. and Khan, M.M.A. (2010). Calcium chloride and gibberellic acid protect linseed (Linum usitatissimum L.) from NaCl stress by inducing antioxidative defence system and osmoprotectant accumulation. Acta Physiol. Plant. 32: 121-132.
    25. Liu, J., Li, K., Xu, J., Liang, J., Lu, X., Yang, J. and Zhu, Q. (2003). Interaction of Cd and five mineral nutrients for uptake and accumulation in different rice cultivars and genotypes. Field Crops Res. 83: 271-281.
    26. Mengel, K. (2007). Potassium, In Handbook of Plant Nutrition; Barker, A.V., Pilbeam, D.J., Eds.; CRC Press: Boca Raton, FL, USA, pp. 91-120.
    27. Metwally, A., Safronova, V., Belimov, A.A. and Dietz, K.J. (2005). Genotypic variation of the response to cadmium toxicity in Pisum sativum L. J. Exp. Botany. 56: 167-178.
    28. Pacifici, R.E. and Davies, K.J.A. (1990). Protein degradation as an index of oxidative stress. Methods Enzymology. 186: 485-502.
    29. Perfus-Barbeoch, L., Leinhardt, N., Vavasseur, A. and Forestier, C. (2002). Heavy metal Toxicity, Cd permeates through calcium channels and disturbs the plant water status. Plant J. 32: 539-548.
    30. Rodríguez-Serrano, M., Romero-Puertas, M.C., Pazmiño, D.M., Testillano, P.S., Risueño, M.C., del Río, L.A. and Sandalio, L.M. (2009). Cellular response of pea plants to cadmium toxicity: Cross talk between reactive oxygen species, nitric oxide, and calcium. Plant Physiol. 150: 229-243.
    31. Romero-Puertas, M.C., Palma, J.M., Gómez, M., Del Rio, L.A. and Sandalio, L.M. (2002). Cadmium causes the oxidative modification of proteins in pea plants. Plant cell Environ. 25: 677-686.
    32. Rosielle, A.A. and Hamblin, J. (1981). Theoretical aspects of selection for yield in stress and non-stress environments. Crop Sci. 21: 943-946.
    33. Saglio, P.H. and Pradet, A. (1980). Soluble sugars, respiration and energy charge during ageing of excised maize root tips. Plant Physiol. 66: 516-519.
    34. Sandalio L.M., Dalurzo H.C., Gómez M., Romero-Puertas M.C. and del Río L.A. (2001). Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J. Exp. Bot. 52: 2115-2126.
    35. Schützendübel, A., Schwanz, P., Teichmann, T., Gross, K., Langenfeld-Heyser, R., Godbold, D.L. and Polle, A. (2001).
    36. Cadmium–Induced Changes in antioxidative systems, hydrogen peroxide content, and differentiation in scots pine roots. Plant physiology. 127: 887-898.
    37. Siddiqui, M.H., Al-Whaibi, M.H. and Basalah, M.O. (2011). Interactive effect of calcium and gibberellin on nickel tolerance in relation to antioxidant systems in Triticum aestivum L. Protoplasma. 248: 503-511.
    38. Sledge, M.K., Pechter, P. and Payton, M.E. (2005). Aluminum tolerance in Medicago truncatula germplasm. Crop Sci. 45: 2001-2004.
    39. Somashekaraiah, B.V., Padmaja, K. and Prasad, A.R.K. (2006). Phytotoxicity of cadmium ions on germinating seedlings of mung bean (Phaseolus vulgaris): Involvement of lipid peroxides in chlorphyll degradation. Physiologia Plantarum. 85: 85-89.
    40. Tanaka, A. and Tsuji, H. (1998). Effects of calcium on chlorophyll synthesis and stability in the early phase of greening in cucumber cotyledons. Plant Physiol. 65: 1211-1215.
    41. Vangronsveld, J. and Clijsters, H. (1994). Toxic effects of metals, In Plants and the Chemical Elements. Biochemistry, Uptake, Tolerance and Toxicity. Ed. M.E. Farago. pp. 149-177.
    42. Wintermans, J.F.G.A. and de Mots, A. (1965). Spectrophotometric characteristics of chlorophylls a and b and their phenophytins in ethanol. Biochemistry and Biophysics ACTA. 109: 448-453.
    43. Wójcika, M., Vangronsveld, J. and Tukiendorf, A. (2005). Cadmium tolerance in Thlaspi caerulescens: Growth parameters, metal accumulation and phytochelatin synthesis in response to cadmium. Environmental and Experimental Botany. 53: 151-161.
    44. Woolhouse, H.W. (1983). Toxicity and tolerance in the response of plants to heavy metals. Encycl. Plant Physiol. 12: 246- 300.
    45. Wu, F., Dong, J., Jia, G.X., Zheng, S.J. and Zhang, G.P. (2006). Genotypic difference in the response of seedling growth and Cd toxicity in rice (Oryza sativa L.). Agric. Sci. China. 5: 68-76.
    46. Wu, F., Zhang, G., Dominy, P., Wu, H. and Bachir, D.M. (2007). Differences in yield components and kernel Cd accumulation in response to Cd toxicity in four barley genotypes. Chemosphere. 70: 83–92.
    47. Xu, J., Wang, W., Yin, H., Liu, X., Sun, H. and Mi, Q. (2010). Exogenous nitric oxide improves antioxidative capacity and reduces auxin degradation in roots of Medicago truncatula seedlings under cadmium stress. Plant Soil. 326: 321-330.
    48. Yuguan, Z., Min, Z., Luyang, L., Zhe, J., Chao, L., Sitao, Y., Yanmei, D. and Fashui, H. (2009). Effects of cerium on key enzymes of carbon assimilation of spinach under magnesium deficiency. Biological Trace Element Research. 131: 154-164.
    49. Zhang, G., Fukami, M. and Sekimoto, H. (2002). Influence of cadmium on mineral concentrations and yield components in wheat genotypes differing in Cd tolerance at seedling stage. Field Crops Res. 77: 93-98.
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