, Volume 43, Issue 2, pp 177–185 | Cite as

Growth, photosynthetic electron transport, and antioxidant responses of young soybean seedlings to simultaneous exposure of nickel and UV-B stress

  • S. M. Prasad
  • R. Dwivedi
  • M. Zeeshan


The effects of enhanced ultraviolet-B (UV-B, 0.4 W m−2) irradiance and nickel (Ni, 0.01, 0.10 and 1.00 mM; Ni0.01, Ni0.10, Ni1.00, respectively) treatment, singly and in combination, on growth, photosynthetic electron transport activity, the contents of reactive oxygen species (ROS), antioxidants, lipid peroxidation, and membrane leakage in soybean seedlings were evaluated. Ni0.10 and Ni1.00 and UV-B declined the growth and chlorophyll content, which were further reduced following combined exposure. Contrary to this, Ni0.01 stimulated growth, however, the effect together with UV-B was inhibitory. Carotenoids showed varied response to both the stresses. Simultaneous exposure of UV-B and Ni as well as UV-B alone reduced the activities of photosystems 1 and 2 (PS1 and PS2) and whole chain activity significantly, while Ni individually, besides strongly inhibiting PS2 and whole chain activity, stimulated the PS1 activity. Both the stresses, alone and together, enhanced the contents of superoxide radical (O 2 ⋅− ), hydrogen peroxide (H2O2), malondialdehyde (MDA), electrolyte leakage, and proline content, while ascorbate content declined over control. Individual treatments increased the activities of catalase (CAT), peroxidase, and superoxide dismutase (SOD), but Ni1.00 declined SOD activity significantly. Combined exposure exhibited similar response, however, CAT activity declined even more than in control. Compared to individual effects of UV-B and Ni, the simultaneous exposure resulted in strong inhibition of photosynthetic electron transport and excessive accumulation of ROS, thereby causing severe damage to soybean seedlings.

Additional key words

Glycine lipid peroxidation oxidative stress photosynthetic electron transport activity photosynthetic pigments reactive oxygen species 









3-(3,4 dichlorophenyl)-1,1-dimethyl urea


2,6-dichlorophenol indophenol




methyl viologen


p-nitroblue tetrazolium chloride




photon flux density






superoxide dismutase


ultraviolet-B radiation (280–320 nm).


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  1. Almog, O., Lotan, O., Shoham, G., Nechushtai, R.: The composition and organization of photosystem I. — J. basic clin. Physiol. Pharmacol. 2: 123–140, 1991.PubMedGoogle Scholar
  2. Arnon, D.I.: Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. — Plant Physiol. 24: 1–15, 1949.Google Scholar
  3. Arora, A., Sairam, R.K., Srivastava, G.C.: Oxidative stress and antioxidant system in plants. — Curr. Sci. 82: 1227–1238, 2002.Google Scholar
  4. Bates, L.S., Waldren, R.P., Teare, I.D.: Rapid determination of free proline for water stress studies. — Plant Soil 39: 205–207, 1973.CrossRefGoogle Scholar
  5. Brown, P.H., Welch, R.M., Cary, E.E.: Nickel: A micronutrient essential for higher plants. — Plant Physiol. 85: 801–803, 1987.Google Scholar
  6. Caldwell, M.M., Bjorn, L.O., Bornman, J.F., Flint, S.D., Kulandaivelu, G., Teramura, A.H., Tevini, M.: Effects of increased solar ultraviolet radiation on terrestrial ecosystems. — J. Photochem. Photobiol. 46: 40–52, 1998.CrossRefGoogle Scholar
  7. Carlson, R.W., Bazzaz, F.A., Rolf, G.L.: The effect of heavy metals on plants II. Net photosynthesis and transpiration of whole corn and sunflower plants treated with Pb, Cd, Ni, and Ti. — Environ. Res. 10: 113–120, 1975.CrossRefPubMedGoogle Scholar
  8. Dai, Q., Yan, B., Huang, S., Liu, X., Peng, S., Miranda, M.L.L., Chavez, A.Q., Vergara, B.S., Olszyk, D.M.: Response of oxidative stress defense systems in rice (Oryza sativa) leaves with supplemental UV-B radiation. — Physiol. Plant. 101: 301–308, 1997.CrossRefGoogle Scholar
  9. Devine, M., Duke, S.O., Fedtke, C.: Physiology of Herbicide Action. — PTR Prentice-Hall, Englewood Cliffs 1993.Google Scholar
  10. Dube, S.L., Bornman, J.F.: Response of spruce seedlings to simultaneous exposure to ultraviolet-B radiation and cadmium. — Plant Physiol. Biochem. 30: 761–767, 1992.Google Scholar
  11. Egashira, T., Takahama, U., Nakamura, K.: A reduced activity of catalase as a basis for light dependent methionine sensitivity of a Chlamydomonas reinhardtii mutant. — Plant Cell Physiol. 30: 1171–1175, 1989.Google Scholar
  12. Elstner, E.F., Heupel, A.: Inhibition of nitrite formation from hydroxylammonium chloride: A simple assay for superoxide dismutase. — Anal. Biochem. 70: 616–620, 1976.CrossRefPubMedGoogle Scholar
  13. Gabrielli, R., Mattioni, C., Vergnano, O.: Accumulation mechanism and heavy metal tolerance of nickel hyperaccumulator. — J. Plant Nutr. 14: 1067–1080, 1991.Google Scholar
  14. Gahagen, H.E., Holm, R.E., Abeles, F.B.: Effect of ethylene on peroxidase activity. — Physiol. Plant. 21: 1270, 1968.Google Scholar
  15. Giannopolitis, C.N., Ries, S.K.: Superoxide dismutases. I. Occurrence in higher plants. — Plant Physiol. 59: 309–314, 1977.Google Scholar
  16. Gong, M., Li, Y.J., Chen, S.Z.: Abscisic acid induced thermotolerance in maize seedlings is mediated by calcium and associated with antioxidant systems. — J. Plant Physiol. 153: 488–496, 1998.Google Scholar
  17. Goodwin, T.W.: Carotenoids. — In: Paech, K., Tracey, M.W. (ed.): Handbook of Plant Analysis. Pp. 272–311. Springer-Verlag, Berlin 1954.Google Scholar
  18. Gopal, R., Mishra, K.B., Zeeshan, M., Prasad, S.M., Joshi, M.M.: Laser induced chlorophyll fluorescence spectra of mung plants growing under nickel stress. — Curr. Sci. 83: 880–884, 2002.Google Scholar
  19. Heath, R.L., Packer, L.: Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. — Arch. Biochem. Biophys. 125: 189–198, 1968.CrossRefPubMedGoogle Scholar
  20. Hideg, E., Vass, I.: UV-B induced free radical production in plant leaves and isolated thylakoid membranes. — Plant Sci. 115: 251–260, 1996.CrossRefGoogle Scholar
  21. Jansen, M.A.K., Gaba, V., Greenberg, B.M.: Higher plants and UV-B radiation: balancing, damage, repair and acclimation. — Trends Plant Sci. 3: 131–135, 1998.CrossRefGoogle Scholar
  22. Jordan, B.R., Chow, W.S., Strid, A., Anderson, J.M.: Reduction in cab and psbA RNA transcripts in response to supplemental ultraviolet-B radiation. — FEBS Lett. 284: 5–8, 1991.CrossRefPubMedGoogle Scholar
  23. Kondo, N., Kawashima, M.: Enhancement of the tolerance to oxidative stress in cucumber (Cucumis sativus L.) seedlings by UV-B irradiation: Possible involvement of phenolic compounds and antioxidative enzymes. — J. Plant Res. 113: 311–317, 2000.Google Scholar
  24. Krupa, Z., Skorzynska, E., Maksymiec, W., Baszynski, T.: Effect of cadmium treatment on the photosynthetic apparatus and its photochemical activities in greening radish seedlings. — Photosynthetica 21: 156–164, 1987.Google Scholar
  25. Kulandaivelu, G., Maragatham, S., Nedunchezhian, N.: On the possible control of ultraviolet-B induced response in growth and photosynthetic activities in higher plants. — Physiol. Plant. 76: 398–404, 1989.Google Scholar
  26. Kupper, H., Kupper, F., Spiller, M.: Environmental relevance of heavy metal substituted chlorophylls using the example of water plants. — J. exp. Bot. 47: 259–266, 1996.Google Scholar
  27. Lingakumar, K., Kulandaivelu, G.: Changes induced by ultraviolet-B radiation in vegetative growth, foliar characteristics and photosynthetic activities in Vigna unguiculata. — Aust. J. Plant Physiol. 20: 299–308, 1993.Google Scholar
  28. Madronich, S., Mckenzie, L.O., Bjorn, L.O., Caldwell, M.M.: Changes in biologically active ultraviolet radiation reaching the Earth’s surface. — J Photochem. Photobiol. B 46: 5–1, 1998.CrossRefPubMedGoogle Scholar
  29. Mahalingam, R., Fedoroff, N.: Stress response, cell death and signaling: The many faces of reactive oxygen species. — Physiol. Plant. 119: 56–68, 2003.CrossRefGoogle Scholar
  30. Matysik, J., Alia, Bhalu, B., Mohanty, P.: Molecular mechanisms of quenching of reactive oxygen species by proline under stress in plants. — Curr. Sci. 82: 525–532, 2002.Google Scholar
  31. Mohanty, N., Vass, I., Demeter, S.: Impairment of photosystem 2 activity at the level of secondary quinone electron acceptor in chloroplasts treated with cobalt, nickel and zinc ions. — Physiol. Plant. 76: 386–390, 1989.Google Scholar
  32. Oser, B.L.: Hawks Physiological Chemistry. — Pp. 702–705. McGraw Hill, New York 1979.Google Scholar
  33. Ouzounidou, G.: Cu-ions mediated changes in growth, chlorophyll and other ion contents in a Cu-tolerant Koeleria splendens. — Biol. Plant. 37: 71–78, 1995.Google Scholar
  34. Pandolfini, T., Gabbrielli, R., Comparini, C.: Nickel toxicity and peroxidase activity in seedlings of Triticum aestivum L. — Plant Cell Environ. 15: 719–725, 1992.Google Scholar
  35. Pardha Saradhi, P., Alia, Arora, S., Prasad, K.V.S.K.: Proline accumulates in plants exposed to UV-radiation and protects them against UV-induced peroxidation. — Biochem. biophys. Res. Commun. 209: 1–5, 1995.CrossRefPubMedGoogle Scholar
  36. Porra, R.J.: The chequered history of the development and use of simultaneous equations for the accurate determination of chlorophylls a and b. — Photosynth. Res. 73: 149–156, 2002.CrossRefGoogle Scholar
  37. Rai, L.C., Tyagi, B., Mallick, N., Rai, P.K.: Interactive effects of UV-B and copper on photosynthetic activity of the cyanobacterium Anabaena doliolum. — Environ. exp. Bot. 35: 177–185, 1995.CrossRefGoogle Scholar
  38. Rai, L.C., Tyagi, B., Rai, P.K., Mallick, N.: Interactive effects of UV-B and heavy metals (Cu and Pb) on nitrogen and phosphorous metabolism of a N2-fixing cyanobacterium Anabaena doliolum. — Environ. exp. Bot. 39: 221–231, 1998.CrossRefGoogle Scholar
  39. Rao, M.V., Paliyath, G., Ormrod, D.P.: Ultraviolet-B-and ozone-induced biochemical changes in antioxidant enzymes of Arabidopsis thaliana. — Plant Physiol. 110: 125–136, 1996.CrossRefPubMedGoogle Scholar
  40. Renger, G., Volker, M., Eckert, H.J., Fromme, R., Hohm-Veit, S., Graber, P.: On the mechanism of photosystem II deterioration by UV-B irradiation. — Photochem. Photobiol. 49: 97–105, 1989.CrossRefGoogle Scholar
  41. Sagisaka, S.: The occurrence of peroxide in a perennial plant Populas gelrica. — Plant Physiol. 57: 308–309, 1976.Google Scholar
  42. Srivastava, A., Tel, O.E.: Antioxidative enzymatic response of Lemna to environmental pollutants. — J. environ. Sci. Health A 27: 261–272, 1992.Google Scholar
  43. Strid, A., Chow, W.S., Anderson, J.M.: Effects of supplementary ultraviolet-B radiation on photosynthesis in Pisum sativum. — Biochim. biophys. Acta 1020: 260–268, 1990.Google Scholar
  44. Strid, A., Porra, R.J.: Alterations in pigment content in leaves of Pisum sativum after exposure to supplementary UV-B. — Plant Cell Physiol. 33: 1015–1023, 1992.Google Scholar
  45. Sullivan, J.H., Teramura, A.H.: Field study of the interaction between solar ultraviolet-B radiation and drought on photosynthesis and growth in soybean. — Plant Physiol. 92: 141–146, 1990.Google Scholar
  46. Teramura, A.H., Sullivan, J.H.: Effects of UV-B radiation on photosynthesis and growth of terrestrial plants. — Photosynth. Res. 39: 463–473, 1994.CrossRefGoogle Scholar
  47. Tevini, M., Teramura, A.H.: UV-B effects on terrestrial plants. — Photochem. Photobiol. 50: 479–487, 1989.Google Scholar

Copyright information

© Institute of Experimental Botany, Academy of Sciences of the Czech Republic, Praha 2005

Authors and Affiliations

  1. 1.Ranjan Plant Physiology and Biochemistry Laboratory, Department of BotanyUniversity of AllahabadAllahabadIndia

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