, Volume 46, Issue 1, pp 49–55 | Cite as

Cadmium and zinc induced chlorosis in Indian mustard [Brassica juncea (L.) Czern] involves preferential loss of chlorophyll b

Original Papers


Plants of Indian mustard (Brassica juncea) were treated with either 50 µM Cd, 250 µM Zn, or 25 µM Cd+125 µM Zn and the progression of chlorosis in the mature leaves monitored. As relative chlorophyll (Chl) contents in the mature leaves decreased to 75, 50, and 25 % relative to controls, both mature and young leaves were harvested and the Chl pools extracted. The metal treatments caused a greater loss of Chl b than Chl a. As mature leaves underwent progressive chlorosis, the young leaves displayed a characteristic over-greening, due largely to increased content of Chl b. However, as the young leaves began to experience chlorosis, a greater loss of Chl b was also observed. Thus during metal induced chlorosis, there is a preferential turnover of the Chl b pool in mature and young leaves.

Additional key words

heavy metals 



chlorophyll a oxidase






N,N′-ethylenediamine-di(O-hydroxyphenyl)acetic acid


2-[morpholino] ethanesulfonic acid


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  1. Angadi, S.-B., Mathad, P.: Effect of copper, cadmium and mercury on the morphological, physiological and biochemical characteristics of Scenedesmus quadricauda (Turp.) de Breb.-J. environ. Biol. 19: 119–124, 1998.Google Scholar
  2. Aravind, P., Prasad, M.-N.-V.: Zinc protects chloroplasts and associated photochemical functions in cadmium exposed Ceratophyllum demersum L., a freshwater macrophyte.-Plant Sci. 166: 1321–1327, 2004.CrossRefGoogle Scholar
  3. Balsberg Påhlsson, A.-M.: Toxicity of heavy metals (Zn, Cu, Cd, Pb) to vascular plants.-Water Air Soil Pollut. 47: 287–319, 1989.CrossRefGoogle Scholar
  4. Begonia, G.B., Davis, C.D., Begonia, M.F.T., Gray, C.N.: Growth responses of Indian mustard (Brassica juncea (L.) Czern.) and its phytoextraction of lead from a contaminated soil.-Bull. Environ. Contam. Toxicol. 61: 38–43, 1998.PubMedCrossRefGoogle Scholar
  5. Bhattacharjee, S., Mukherjee, A.-K.: Heavy metals alter photosynthetic pigment profiles as well as activities of chlorophyllase and 5-aminolevulinic acid dehydratase (ALAD) in Amaranthus lividus seedlings.-J. environ. Biol. 24: 395–399, 2003.PubMedGoogle Scholar
  6. Bhattacharyya, M., Choudhuri, M.-A.: Effect of lead and cadmium on the bio-chemical changes in the leaves of terrestrial (Vigna) and aquatic (Hydrilla) plants under solution culture.-Indian J. Plant Physiol. 37: 99–103, 1994.Google Scholar
  7. Bindhu, S.-J., Bera, A.-K.: Impact of cadmium toxicity on leaf area, stomatal frequency, stomatal index and pigment content in mungbean seedlings.-J. environ. Biol. 22: 307–309, 2001.PubMedGoogle Scholar
  8. Blaylock, M.J., Salt, D.E., Dushenkov, S., Zakharova, O., Gussman, C., Kapulnik, Y., Ensley, B.D., Raskin, I.: Enhanced accumulation of Pb in Indian mustard by soil-applied chelating agents.-Environ. Sci. Technol. 31: 860–865, 1997.CrossRefGoogle Scholar
  9. Chatterjee, C., Sinha, P., Dube, B.K.: Zinc stress in mustard as altered by sulfur deficiency.-J. Plant Nutr. 28: 683–690, 2005.CrossRefGoogle Scholar
  10. Dangl, J.L., Dietrich, R.A., Thomas, H.: Senescence and programmed cell death.-In: Buchanan, B.B., Gruissem, W., Jones, R.L. (ed.): Biochemistry and Molecular Biology of Plants. Pp. 1044–1100. American Society of Plant Physiologists, Rockville 2000.Google Scholar
  11. Ebbs, S.D., Kochian, L.V.: Toxicity of zinc and copper to Brassica species: Implications for phytoremediation.-J. environ. Qual. 26: 776–781, 1997.CrossRefGoogle Scholar
  12. Ebbs, S.D., Kochian, L.V.: Phytoextraction of zinc by oat (Avena sativa), barley (Hordeum vulgare), and Indian mustard (Brassica juncea).-Environ. Sci. Technol. 32: 802–806, 1998.CrossRefGoogle Scholar
  13. Ebbs, S.D., Lasat, M.M., Brady, D.J., Cornish, J., Gordon, R., Kochian, L.V.: Phytoextraction of cadmium and zinc from a contaminated soil.-J. environ. Qual. 26: 1424–1430, 1997.Google Scholar
  14. Elless, M.P., Blaylock, M.J., Huang, J.W., Gussman, C.D.: Plants as a natural source of concentrated mineral nutritional supplements.-Food Chem. 71: 181–188, 2000.CrossRefGoogle Scholar
  15. Epstein, A.L., Gussman, C.D., Blaylock, M.J., Yermiyahu, U., Huang, J.W., Kapulnik, Y., Orser, C.S.: EDTA and Pb-EDTA accumulation in Brassica juncea grown in Pb-amended soil.-Plant Soil 208: 87–94, 1999.CrossRefGoogle Scholar
  16. Espineda, C.-E., Linford, A.-S., Devine, D., Brusslan, J.-A.: The AtCAO gene, encoding chlorophyll a oxygenase, is required for chlorophyll b synthesis in Arabidopsis thaliana.-Proc. nat. Acad. Sci. USA 96: 10507–10511, 1999.PubMedCrossRefGoogle Scholar
  17. Fargaová, A.: Phytotoxic effects of Cd, Zn, Pb, Cu and Fe on Sinapis alba L. seedlings and their accumulation in roots and shoots.-Biol. Plant. 44: 471–473, 2001.CrossRefGoogle Scholar
  18. Huang, J.W., Cunningham, S.D.: Lead phytoextraction: Species variation in lead uptake and translocation.-New Phytol. 134: 75–84, 1996.CrossRefGoogle Scholar
  19. Ito, H., Ohtsuka, T., Tanaka, A.: Conversion of chlorophyll b to chlorophyll a via 7-hydroxymethyl chlorophyll.-J. biol. Chem. 271: 1475–1479, 1996.PubMedCrossRefGoogle Scholar
  20. Ito, H., Takaichi, S., Tsuji, H., Tanaka, A.: Properties of synthesis of chlorophyll a from chlorophyll b in cucumber etioplasts.-J. biol. Chem. 269: 22034–22038, 1994.PubMedGoogle Scholar
  21. Ito, H., Tanaka, A.: Determination of the activity of chlorophyll b to chlorophyll a conversion during greening of etiolated cucumber cotyledons by using pyrochlorophyllide b.-Plant Physiol. Biochem. 34: 35–40, 1996.Google Scholar
  22. Ito, H., Tanaka, Y., Tsuji, H., Tanaka, A.: Conversion of chlorophyll b to chlorophyll a by isolated cucumber etioplasts.-Arch. Biochem. Biophys. 306: 148–151, 1993.PubMedCrossRefGoogle Scholar
  23. Kayser, A., Schroder, T.J., Grunwald, A., Schulin, R.: Solubilization and plant uptake of zinc and cadmium from soils treated with elemental sulfur.-Int. J. Phytoremed. 3: 381–400, 2001.CrossRefGoogle Scholar
  24. Kim, H.-S., Lee, K.-J.: Physiological responses of one-year-old Zelkova serrata Makino seedlings to ozone in open-top chamber.-J. kor. Forest Soc. 84: 424–431, 1995.Google Scholar
  25. Lang, M., Zhang, Y., Chai, T.: Identification of genes upregulated in response to Cd exposure, in Brassica juncea L.-Gene 363: 151–158, 2005.CrossRefGoogle Scholar
  26. Lu, C., Lu, Q., Zhang, J., Kuang, T.: Characterization of photosynthetic pigment composition, photosystem II photochemistry and thermal energy dissipation during leaf senescence of wheat plants grown in the field.-J. exp. Bot. 52: 1805–1810, 2001.PubMedCrossRefGoogle Scholar
  27. Marschner, H.: Mineral Nutrition of Higher Plants.-Academic Press, London 1995.Google Scholar
  28. Marschner, H., Cakmak, I.: High light intensity enhances chlorosis and necrosis in leaves of zinc, potassium, and magnesium deficient bean (Phaseolus vulgaris) plants.-J. Plant Physiol. 134: 308–315, 1989.Google Scholar
  29. Masuda, T., Polle, J.-E.-W., Melis, A.: Biosynthesis and distribution of chlorophyll among the photosystems during recovery of the green alga Dunaliella salina from irradiance stress.-Plant Physiol. 128: 603–614, 2002.PubMedCrossRefGoogle Scholar
  30. Masuda, T., Tanaka, A., Melis, A.: Chlorophyll antenna size adjustments by irradiance in Dunaliella salina involve coordinate regulation of chlorophyll a oxygenase (CAO) and Lhcb gene expression.-Plant mol. Biol. 51: 757–771, 2003.PubMedCrossRefGoogle Scholar
  31. Matile, P., Hörtensteiner, S., Thomas, H.: Chlorophyll degradation.-Annu. Rev. Plant Physiol. Plant mol. Biol. 50: 67–95, 1999.PubMedCrossRefGoogle Scholar
  32. Moran, R.: Formulae for determination of chlorophyllous pigments extracted with N,N-dimethylformamide.-Plant Physiol. 69: 1376–1381, 1982.PubMedCrossRefGoogle Scholar
  33. Moreno-Caselles, J., Moral, R., Perez-Espinosa, A., Perez-Murcia, M.-D.: Cadmium accumulation and distribution in cucumber plant.-J. Plant Nutr. 23: 243–250, 2000.Google Scholar
  34. Mukherjee, D., Ponmeni, G.: Effect of kinetin on the regulation of abscission and senescence in pigeonpea.-Physiol. mol. Biol. Plants 10: 223–231, 2004.Google Scholar
  35. Ohtsuka, T., Ito, H., Tanaka, A.: Conversion of chlorophyll b to chlorophyll a and the assembly of chlorophyll with apoproteins by isolated chloroplasts.-Plant Physiol. 113: 137–147, 1997.PubMedGoogle Scholar
  36. Porra, R.J., Schäfer, W., Cmiel, E., Katheder, I., Scheer, H.: Derivation of the formyl-group oxygen of chlorophyll b from molecular oxygen in greening leaves of a higher plant (Zea mays).-FEBS Lett. 323: 31–34, 1993.PubMedCrossRefGoogle Scholar
  37. Porra, R.-J., Schäfer, W., Cmiel, E., Katheder, I., Scheer, H.: The derivation of the formyl-group oxygen of chlorophyll b in higher plants from molecular oxygen. Achievement of high enrichment of the 7-formyl-group oxygen form 18O2 in greening maize leaves.-Eur. J. Biochem. 219: 671–679, 1994.PubMedCrossRefGoogle Scholar
  38. Prasad, K.V.S.K., Saradhi, P.P., Sharmila, P.: Concerted action of antioxidant enzymes and curtailed growth uner zinc toxicity in Brassica juncea.-Environ. exp. Bot. 42: 1–10, 1999.CrossRefGoogle Scholar
  39. Qadir, S., Qureshi, M.-I., Javed, S., Abdin, M.-Z.: Genotypic variation in phytoremediation potential of Brassica juncea cultivars exposed to Cd stress.-Plant Sci. 167: 1171–1181, 2004.CrossRefGoogle Scholar
  40. Salt, D.E., Pickering, I.J., Prince, R.C., Gleba, D., Dushenkov, S., Smith, R.D., Raskin, I.: Metal accumulation by aquacultured seedlings of Indian mustard.-Environ. Sci. Technol. 31: 1636–1644, 1997.CrossRefGoogle Scholar
  41. Salt, D.E., Prince, R.C., Pickering, I.J., Raskin, I.: Mechanisms of cadmium mobility and accumulation in Indian mustard.-Plant Physiol. 109: 1427–1433, 1995.PubMedGoogle Scholar
  42. Scheumann, V., Schoch, S., Ruediger, W.: Chlorophyll a formation in the chlorophyll b reductase reaction requires reduced ferredoxin.-J. biol. Chem. 273: 35102–35108, 1998.PubMedCrossRefGoogle Scholar
  43. Scheumann, V., Schoch, S., Ruediger, W.: Chlorophyll b reduction during senescence of barley seedlings.-Planta 209: 364–370, 1999.PubMedCrossRefGoogle Scholar
  44. Schneegurt, M.A., Beale, S.I.: Origin of the chlorophyll b formyl oxygen in Chlorella vulgaris.-Biochemistry 31: 11677–11683, 1992.PubMedCrossRefGoogle Scholar
  45. Shi, G.X., Xu, Q.S., Xie, K.B., Xu, N., Zhang, X.L., Zeng, X.M., Zhou, H.W., Zhu, L.: Physiology and ultrastructure of Azolla imbricata as affected by Hg2+ and Cd2+ toxicity.-Acta bot. sin. 45: 437–444, 2003.Google Scholar
  46. Singh, P.K., Tewari, R.K.: Cadmium toxicity induced changes in plant water relations and oxidative metabolism of Brassica juncea L. plants.-J. environ. Biol. 24: 107–112, 2003.PubMedGoogle Scholar
  47. Van Assche, F., Clijsters, H.: Effects of metals on enzyme activity in plants.-Plant Cell Environ. 13: 195–106, 1990.CrossRefGoogle Scholar
  48. Vassil, A.D., Kapulnik, Y., Raskin, I., Salt, D.E.: The role of EDTA in lead transport and accumulation by Indian mustard.-Plant Physiol. 117: 447–453, 1998.PubMedCrossRefGoogle Scholar

Copyright information

© Institute of Experimental Botany, ASCR 2008

Authors and Affiliations

  1. 1.Department of Plant BiologySouthern Illinois University CarbondaleCarbondaleUSA

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