Protoplasma

, Volume 248, Issue 3, pp 503–511 | Cite as

Interactive effect of calcium and gibberellin on nickel tolerance in relation to antioxidant systems in Triticum aestivum L.

  • Manzer H. Siddiqui
  • Mohamed H. Al-Whaibi
  • Mohammed O. Basalah
Original Article
First Online:
Received:
Accepted:

Abstract

Nickel toxicity affects many metabolic facets of plants and induces anatomical and morphological changes resulting in reduced growth and productivity. To overcome the damaging effects of nickel (Ni) stress, different strategies of the application of nutrients with plant hormones are being adopted. The present experiment was carried out to assess the growth and physiological response of wheat plant (Triticum aestivum L.) cv. Samma to pre-sowing seed treatment with GA3 alone as well as in combination with Ca2+ and/or Ni stress. The pre-sowing seed treatment of Ni decreased all the growth characteristics (plant height, root length, fresh, and dry weight) as well as chlorophyll (Chl) content and enzyme carbonic anhydrase (CA: E.C. 4.2.1.1) activity. However, an escalation was recorded in malondialdehyde content and electrolyte leakage in plants raised from seed soaked with Ni alone. Moreover, all the growth parameters and physiological attributes (Chl content, proline (Pro) content, CA, peroxidase (E.C.1.11.1.7), catalase (E.C. 1.11.1.6), superoxide dismutase (E.C. 1.15.1.1), ascorbate peroxidase (E.C. 1.11.1.11), and glutathione reductase (E.C. 1.6.4.2) were enhanced in the plants developed from the seeds soaked with the combination of GA3 (10−6 M), Ca2+, and Ni. The present study showed that pre-sowing seed treatment of GA3 with Ca2+ was more capable in mitigation of adverse effect of Ni toxicity by improving the antioxidant system and Pro accumulation.

Keywords

Antioxidative enzyme Chlorophyll Carbonic anhydrase Proline Triticum aestivum L. 

Notes

Acknowledgements

We thank Professor Govindjee (Professor Emeritus of Biophysics and Plant Biology in the Departments of Plant Biology, Biochemistry and the Center of Biophysics & Computational Biology, University of Illinois at Urbana-Champaign, Urbana, USA) and anonymous reviewers for their valuable suggestions and critical reading of manuscript and Professor Adel Salah Abdul-Jabbar (Director of Attracting Outstanding faculty and Researchers Program) for providing the opportunity to work in Department of Botany and Microbiology, King Saud University, Saud Arabia.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126PubMedCrossRefGoogle Scholar
  2. Ahmad MSA, Hussain M, Ashraf M, Ahmad R, Ashraf MY (2009) Effect of nickel on seed germinability of some elite sunflower (Helianthus Annuus L.) cultivars. Pak J Bot 41:1871–1882Google Scholar
  3. Alam MM, Hayat S, Ali B, Ahmad A (2007) Effect of 28-homobrassinolide treatment on nickel toxicity in Brassica juncea. Photosynthetica 45:139–142CrossRefGoogle Scholar
  4. Alia SPP, Mohanty P (1997) Involvement of proline in protecting thylakoid membranes against free radical-induced photodamage. J Photochem Photobiol B 38:253–257CrossRefGoogle Scholar
  5. Alia MP, Matysik J (2001) Effect of proline on the production of singlet oxygen. Amino Acids 21:195–200PubMedCrossRefGoogle Scholar
  6. Alloway BJ (1995) Soil processes and the behaviour of metals. In: Alloway BJ (ed) Heavy metals in soils. Chapman and Hall, UK, pp 9–38Google Scholar
  7. Al-Whaibi MH, Siddiqui MH, Al-Amri A, Basalah MO (2010) Performance of faba bean under calcium and gibberellic acid application. Int J Plant Develop Biol (in press)Google Scholar
  8. Andreeva IV, Govorina VV, Vinogradova SB, Yagodin BA (2001) Nickel in plants. Agrokhimiya 3:82–94Google Scholar
  9. Antosiewicz DM, Hennig J (2004) Overexpression of LCT1 in tobacco enhances the protective action of calcium against cadmium toxicity. Environ Poll 129:237–245CrossRefGoogle Scholar
  10. Arnon DI (1949) Copper enzymes in isolated chloroplast. Polyphenoloxidases in Beta vulgaris. Plant Physiol 24:1–15PubMedCrossRefGoogle Scholar
  11. Baccouch S, Chaoui A, Ferjani EE (1998) Nickel-induced oxidative damage and antioxidant responses in Zea mays shoots. Plant Physiol Biochem 36:689–694CrossRefGoogle Scholar
  12. Badger MR, Price GD (1994) The role of carbonic anhydrase in photosynthesis. Ann Rev Plant Physiol Plant Mol Biol 45:569–592CrossRefGoogle Scholar
  13. Badr-uz-Zaman, Salim M, Asghar R (2010) Role of Ca2+ on growth of Brassica campestris L. and B. juncea (L.) Czern & Coss under Na+ Stress. J Integ Plant Biol 52:549–555CrossRefGoogle Scholar
  14. Bandurska H (2001) Proline accumulation during hardening and its involvement in reducing membrane injuries in leaves subjected to severe osmotic stress. Acta Physiol Plant 23:483–490CrossRefGoogle Scholar
  15. Basra SMA, Farooq M, Tabassum R (2005) Physiological and biochemical aspects of seed vigor enhancement treatments in fine rice (Oryza sativa L.). Seed Sci Technol 33:623–628Google Scholar
  16. Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207CrossRefGoogle Scholar
  17. Boominathan R, Doran PM (2002) Ni-induced oxidative stress in roots of the Ni hyperaccumulator Alyssum bertolonii. New Phytol 156:205–215CrossRefGoogle Scholar
  18. Braam J (1992) Regulated expression of the calmodulin-related TCH genes in cultured Arabidopsis cells: induction by calcium and heat shock. Proc Natl Acad Sci 89:3213–3216PubMedCrossRefGoogle Scholar
  19. Catalfamo JL, Feinberg JH, Smith GW, Birecka H (1978) Effect of gibberellic acid and ethylene on peroxidase in pea internodes. J Exp Bot 29:347–357CrossRefGoogle Scholar
  20. Chance B, Maehly AC (1955) Assay of catalase and peroxidases. Methods Enzymol 11:764–775CrossRefGoogle Scholar
  21. Chen JC, Ting YY, Lin H, Lian TC (2009) Heavy metal. Concentrations in sea water from grass prawn hatcheries and the coast of Taiwan. J World Maricul Soc 16:316–332CrossRefGoogle Scholar
  22. Choudhary M, Jetley UK, Khan MA, Zutshi S, Fatma T (2007) Effect of heavy metal stress on proline, malondialdehyde, and superoxide dismutase activity in the cyanobacterium Spirulina platensis-S5. Ecotox Environ Safe 66:204–209CrossRefGoogle Scholar
  23. de Souza IRP, MacAdam JW (2001) Gibberellic acid and dwarfism effects on the growth dynamics of B73 maize (Zea mays L.) leaf blades: a transient increase in apoplastic peroxidase activity precedes cessation of cell elongation. J Exp Bot 52:1673–1682PubMedCrossRefGoogle Scholar
  24. Delauney AJ, Verma DPS (1993) Proline biosynthesis and osmoregulation in plants. Plant J 4:215–223CrossRefGoogle Scholar
  25. Dwivedi RS, Randhawa NS (1974) Evaluation of rapid test for hidden hunger of zinc in plants. Plant Soil 40:45–451CrossRefGoogle Scholar
  26. El-Enany AE, Issa AA (2001) Proline alleviates heavy metal stress in Scenedesmus armatus. Folia Microbiol 46:227–230CrossRefGoogle Scholar
  27. Ewais EA (1997) Effects of cadmium, nickel and lead on growth, chlorophyll content and proteins of weeds. Biol Plant 39:403–410CrossRefGoogle Scholar
  28. Farago ME, Mullen WA (1979) Plants which accumulate metals. Part IV. A possible copper-proline complex from the roots of Armeria maritima. Inorg Chim Acta 32:L93–L94CrossRefGoogle Scholar
  29. Foyer C, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25CrossRefGoogle Scholar
  30. Fry SC (1979) Phenolic components of the primary cell wall and their possible role in the hormonal regulation of growth. Planta 146:343–351CrossRefGoogle Scholar
  31. Gajewska E, Skłodowska M (2008) Differential biochemical responses of wheat shoots and roots to nickel stress: antioxidative reactions and proline accumulation. Plant Growth Reg 54:179–188CrossRefGoogle Scholar
  32. Gajewska E, Skłodowska M, Słaba M, Mazur J (2006a) Effect of nickel on antioxidative enzyme activities, proline and chlorophyll contents in wheat shoots. Biol Plant 50:653–659CrossRefGoogle Scholar
  33. Gajewska E, Słaba M, Andrzejewska R, Skłodowska M (2006b) Nickel-induced inhibition of wheat root growth is related to H2O2 production, but not to lipid peroxidation. Plant Growth Regul 49:95–103Google Scholar
  34. Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I. Occurrence in higher plants. Plant Physiol 59:309–314PubMedCrossRefGoogle Scholar
  35. Gilroy S, Jones RL (1992) Gibberellic acid and abscisic acid coordinately regulated cytoplasmic calcium and secretory activity in barley aleurone protoplasts. Proc Natl Acad Sci 89:3591–3595PubMedCrossRefGoogle Scholar
  36. Gong M, Chen SN, Song YQ, Li ZG (1997a) Effect of calcium and calmodulin on intrinsic heat tolerance in relation to antioxidant systems in maize seedlings. Aust J Plant Physiol 24:371–379CrossRefGoogle Scholar
  37. Gong M, Li YJ, Dai X, Tian M, Li ZG (1997b) Involvement of calcium and calmodulin in the acquisition of HS induced thermotolerance in maize seedlings. J Plant Physiol 150:615–621Google Scholar
  38. Greeger M (1999) Metal availability and bioconcentration in plants. In: Prasad MNV, Hagemeyer J (eds) Heavy metal stress in plants. Springer, New York, pp 1–29Google Scholar
  39. Hare PD, Cress WA (1997) Metabolism implications of stress-induced proline accumulation in plants. Plant Growth Regul 21:79–102CrossRefGoogle Scholar
  40. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198PubMedCrossRefGoogle Scholar
  41. Hirschi KD (2004) The Calcium Conundrum. Both versatile nutrient and specific signal. Plant Physiol 136:2438–2442PubMedCrossRefGoogle Scholar
  42. Jáuregui-Zùñiga D, Ferrer MA, Calderón AA, Muñoz R, Moreno A (2005) Heavy metal stress reduces the deposition of calcium oxalate crystals in leaves of Phaseolus vulgaris. J Plant Physiol 162:1183–1187PubMedCrossRefGoogle Scholar
  43. Jiang Y, Huang B (2001) Effect of calcium on antioxidant activities and water relations associated with heat tolerance in two cool-season grasses. J Exp Bot 355:341–349CrossRefGoogle Scholar
  44. Khan MN, Siddiqui MH, Mohammad F, Naeem M, Khan MMA (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 32:121–132CrossRefGoogle Scholar
  45. Kuznetsov VV, Shevyakova NI (1997) Stress responses of tobacco cells to high temperature and salinity: Proline accumulation and phosphorylation of polypeptides. Physiol Plant 100:320–326CrossRefGoogle Scholar
  46. Lutts S, Kinet JM, Bouharmont J (1995) Changes in plant response to NaCl during development of rice (Oryza sativa L.) varieties differing in salinity resistance. J Exp Bot 46:1843–1852CrossRefGoogle Scholar
  47. Maggio A, Barbieri G, Raimondi G, Pascale SD (2010) Contrasting effects of GA3 treatments on tomato plants exposed to increasing salinity. J Plant Growth Regul 29:63–72CrossRefGoogle Scholar
  48. Matysik J, Alia BB, Mohanty P (2002) Molecular mechanisms of quenching of reactive oxygen species by proline under stress in plants. Curr Sci 82:525–532Google Scholar
  49. McAinsh MR, Clayton H, Mansfield TA, Hetherington AM (1996) Changes in stomatal behavior and guard cell cytosolic free calcium in response to oxidative stress. Plant Physiol 111:1031–1042PubMedGoogle Scholar
  50. Mcllveen WD, Negusanti JJ (1994) Nickel in the terrestrial environment. Sci Total Environ 148:109–138CrossRefGoogle Scholar
  51. Mehta SK, Gaur JP (1999) Heavy-metal-induced proline accumulation and its role in ameliorating metal toxicity in Chlorella vulgaris. New Phytol 143:253–259CrossRefGoogle Scholar
  52. Melgar JC, Benlloch M, Fernández-Escobar R (2006) Calcium increases sodium exclusion in olive plants. Sci Hortic 109:303–305CrossRefGoogle Scholar
  53. Mohanty N, Vass I, Demeter S (1989) Impairment of photosystem 2 activity at the level of secondary quinone electron acceptor in chloroplasts treated with cobalt, nickel and zinc ions. Physiol Plant 76:386–390Google Scholar
  54. Molas J (1997) Changes in morphological and anatomical structure of cabbage (Brassica oleracea L.) outer leaves and in ultrastructure of their chloroplasts caused by an In vitro excess of nickel. Photosynthetica 34:513–522CrossRefGoogle Scholar
  55. Moll C, Jones RL (1981) Calcium and gibberellin-induced elongation of lettuce hypocotyl sections. Planta 152:450–456CrossRefGoogle Scholar
  56. Moya JL, Ros R, Picazo I (1995) Heavy metal-hormone interactions in rice plants: Effects on growth, net photosynthesis, and carbohydrate distribution. J Plant Growth Regul 14:61–67CrossRefGoogle Scholar
  57. Naeem M, Idrees M, Khan MMA (2009) Calcium ameliorates photosynthetic capacity, nitrate reductase, carbonic anhydrase, nitrogen assimilation, yield and quality of Cassia sophera L.—a medicinal legume. Physiol Mol Biol Plants 15:237–247CrossRefGoogle Scholar
  58. Nakano G, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidise in spinach chloroplasts. Plant Cell Physiol 22:867–880Google Scholar
  59. Pandey N, Sharma CP (2002) Effects of heavy metals Co2+, Ni2+ and Cd2+ on growth and metabolism of cabbage. Plant Sci 163:753–758CrossRefGoogle Scholar
  60. Pandolfini T, Gabbrielli R, Comparini C (1992) Nickel toxicity and peroxidase activity in seedlings of Triticum aestivum L. Plant Cell Environ 15:719–725CrossRefGoogle Scholar
  61. Papadopoulos A, Prochaska C, Papadopoulos F, Gantidis N, Metaxa E (2007) Determination and evaluation of cadmium, copper, nickel, and zinc in agricultural soils of western macedonia, Greece. Environ Manag 40:719–726CrossRefGoogle Scholar
  62. Rhodes D, Hanson AD (1993) Quaternary ammonium and tertiary sulfonium compounds in higher plants. Annu Rev Plant Physiol Plant Mol Biol 44:357–384CrossRefGoogle Scholar
  63. Saeidi-Sar S, Khavari-Nejad R, Fahimi H, Ghorbanli M, Majd A (2007) Interactive effects of gibberellin A3 and ascorbic acid on lipid peroxidation and antioxidant enzyme activities in Glycine max seedlings under nickel stress. Russ J Plant Physiol 54:74–79CrossRefGoogle Scholar
  64. Salt DE, Krämer U (2000) Mechanisms of metal hyperaccumulation in plants. In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals—using plants to clean up the environment. Wiley, New York, pp 231–246Google Scholar
  65. Schat H, Sharma SS, Vooijs R (1997) Heavy metal-induced accumulation of free proline in a metal-tolerant and a nontolerant ecotype of Silene vulgaris. Physiol Plant 101:477–482CrossRefGoogle Scholar
  66. Seeman JR, Critchley C (1985) Effects of salt stress on the growth, ion content, stomatal behaviour and photosynthetic capacity of salt-sensitive species, Phaseolus vulgaris (L). Planta 164:151–162CrossRefGoogle Scholar
  67. Seregin IV, Kozhevnikova AD (2006) Physiological role of nickel and its toxic effects on higher plants. Russ J Plant Physiol 53:257–277CrossRefGoogle Scholar
  68. Shah K, Dubey RS (1998) Effect of cadmium on proline accumulation and ribonuclease activity in rice seedlings: role of proline as a possible enzyme protectant. Biol Plant 40:121–130CrossRefGoogle Scholar
  69. Shalygo NV, Kolensikova NV, Voronetskaya VV, Averina NG (1999) Effects of Mn2+, Fe2+, Co2+ and Ni2+ on chlorophyll accumulation and early stages of chlorophyll formation of greening barley seedling. Russ J Plant Physiol 46:496–501Google Scholar
  70. Sheoran IS, Singal HR, Singh R (1990) Effect of cadmium and nickel on photosynthesis and the enzymes of the photosynthetic carbon reduction cycle in pigeonpea (Cajanuscajan L.). Photosynth Res 23:345–351CrossRefGoogle Scholar
  71. Siddiqui MH, Khan MN, Mohammad F, Khan MMA (2008) Role of nitrogen and gibberellins (GA3) in the regulation of enzyme activities and in osmoprotectant accumulation in Brassica juncea L. under salt stress. J Agron Crop Sci 194:214–224CrossRefGoogle Scholar
  72. Siddiqui MH, Firoz M, Khan MN (2009) Morphological and physio-biochemical characterization of Brassica juncea L. Czern. & Coss. genotypes under salt stress. J Plant Interact 4:67–80CrossRefGoogle Scholar
  73. Siripornadulsil S, Traina S, Verma DPS, Sayre RT (2002) Molecular mechanisms of proline-mediated tolerance to toxic heavy metals in transgenic microalgae. Plant Cell 14:2837–2847PubMedCrossRefGoogle Scholar
  74. Smirnoff N, Cumbes QJ (1989) Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry 28:1057–1060CrossRefGoogle Scholar
  75. Smith GS, Johnston CM, Cornforth IS (1983) Comparison of nutrient solutions for growth of plants in sand culture. New Phytologist 94:537–548CrossRefGoogle Scholar
  76. Soussi M, Ocana A, Lluch C (1998) Effects of salt stress on growth, photosynthesis and nitrogen fixation in chick-pea (Cicer arietinum L.). J Exp Bot 49:1329–1337CrossRefGoogle Scholar
  77. Taylor CB (1996) Proline and water deficit: ups, downs, ins and outs. Plant Cell 8:1221–1224CrossRefGoogle Scholar
  78. Verma DPS (1999) Osmotic stress tolerance in plants: role of proline and sulfur metabolisms. In: Shinozaki K, Yamaguchi-Shinozaki K (eds) Molecular responses to cold, drought, heat and salt stress in higher plants. R.G. Landers, Austin, pp 153–168Google Scholar
  79. Viet HN, Frontasyeva MV, Thi TMT, Gilbert D, Bernard N (2010) Atmospheric heavy metal deposition in Northern Vietnam: Hanoi and Thainguyen case study using the moss biomonitoring technique, INAA and AAS. Environ Sci Poll Res 17(5):1045–1052. doi:10.1007/s11356-009-0258-6 CrossRefGoogle Scholar
  80. Walker CD, Graham RD, Madison JT, Cary EE, Welch RM (1985) Effects of Ni deficiency on some nitrogen metabolites in cowpeas (Vignaunguiculata L. Walp.). Plant Physiol 79:474–479PubMedCrossRefGoogle Scholar
  81. Welch RM (1981) The Biological significance of nickel. J Plant Nutr 3:345–356CrossRefGoogle Scholar
  82. White PJ, Broadley MR (2003) Calcium in plants. Ann Bot 92:487–511PubMedCrossRefGoogle Scholar
  83. Wu JT, Chang SJ, Chou TL (1995) Intracellular proline accumulation in some algae exposed to copper and cadmium. Bot Bull Acad Sinica 36:89–93Google Scholar
  84. Yan F, Schubert S, Mengel K (1992) Effect of low root medium pH on net proton release, root respiration and root growth of corn (Zea mays L.) and broad bean (Vicia faba L.). Plant Physiol 99:415–421PubMedCrossRefGoogle Scholar
  85. Zarcinas BA, Ishak CF, McLaughlin MJ, Cozens G (2004a) Heavy metals in soils and crops in Southeast Asia 1. Environ Geochem Health 26:343–357PubMedCrossRefGoogle Scholar
  86. Zarcinas BA, Pongsakul P, McLaughlin MJ, Cozens G (2004b) Heavy metals in soils and crops in Southeast Asia 2. Thailand. Environ Geochem Health 26:359–371PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Manzer H. Siddiqui
    • 1
  • Mohamed H. Al-Whaibi
    • 1
  • Mohammed O. Basalah
    • 1
  1. 1.Department of Botany, College of ScienceKing Saud UniversityRiyadhSaudi Arabia

Personalised recommendations