Advertisement

Acta Physiologiae Plantarum

, Volume 31, Issue 2, pp 319–330 | Cite as

A crop tolerating oxidative stress induced by excess lead: maize

  • Yasemin Ekmekçi
  • Deniz Tanyolaç
  • Beycan Ayhan
Original Paper

Abstract

Two 14-day-old seedlings of maize (Zea mays L.) cultivars (3223 and Vero) were exposed to different concentrations of lead [0, 2, 5 and 8 mM Pb(NO3)2·4H2O] for 8 days. Exposure of maize cultivars to excess Pb resulted in a significant root growth inhibition though shoot growth and absolute water content remained less affected. The results of chlorophyll a fluorescence indicated that the highly toxic Pb level affected photochemical efficiency in 3223, while no significant effect was observed in the Vero. At the highly toxic Pb concentration, higher membrane leakage was observed in 3223 leaves than that of Vero. This result was related to the accumulation of Pb. On the other hand, the results suggested that there were similar responses in total soluble POD and GR activities with increasing Pb concentrations between both cultivars. But APX activity significantly decreased at highly toxic Pb level in the Vero while a significant increase observed in the 3223. However, SOD activity in 3223 significantly decreased at the highly toxic Pb concentration compared with that at 2 mM Pb concentration. The results of the present study indicated that, Vero withstands excess Pb with its higher Pb accumulation capacity in roots and better upregulated protective mechanisms compared to 3223. Therefore, Vero is more tolerant to Pb toxicity compared to 3223 which was found to be a less tolerant cultivar.

Keywords

Antioxidant enzymes Lead Accumulation Photochemical activity Maize 

Notes

Acknowledgments

We would like to thank Hacettepe University, Scientific Research Unit (Project no. 02 02 602 013) for the financial support. We are also grateful to Şeniz Ünalan, Chemical Engineering Department, for her assistance in experiments.

References

  1. Ahmed A, Tajmir-Riahi HA (1993) Interaction of toxic metal ions Cd2+, Hg2+ and Pb2+ with light-harvesting proteins of chloroplast thylakoid membranes: an FTIR spectroscopic study. J Inorg Biochem 40:235–243. doi: 10.1016/0162-0134(93)80050-J CrossRefGoogle Scholar
  2. Antosiewicz D, Wierzbicka M (1999) Localization of lead in Allium cepa L. cells by electron misroscopy. J Microsc 195:139–146. doi: 10.1046/j.1365-2818.1999.00492.x PubMedCrossRefGoogle Scholar
  3. Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 85:235–241Google Scholar
  4. Ayhan B, Ekmekçi Y, Tanyolaç D (2007) Investigation of the tolerance to heavy metal (cadmium and lead) stress of some maize cultivars at early seedling stage. Anadolu Univ J Sci Tech 8:411–422 in Turkish with English abstractGoogle Scholar
  5. Bashmakov DI, Lukatkin AS, Revin VV, Duchovskis P, Brazaityte A, Baranauskis K (2005) Growth of maize seedlings affected by different concentrations of heavy metals. Ekologija 3:22–27Google Scholar
  6. Bergmeyer HU (1974) Methods of Enzymatic Analysis, vol II, Section C: Methods for determination of enzyme activity, 2nd edn, pp 685–690Google Scholar
  7. Beyer WF, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161:559–566. doi: 10.1016/0003-2697(87)90489-1 PubMedCrossRefGoogle Scholar
  8. Bigot A, Fontaine F, Clément C, Vaillant-Gaveau N (2007) Effect of the herbicide flumioxazin on photosynthetic performance of grapevine (Vitis vinifera L.). Chemosphere 67:1243–1251. doi: 10.1016/j.chemosphere.2006.10.079 PubMedCrossRefGoogle Scholar
  9. Bilger W, Björkman O (1990) Role of the xanthophyll cycle in photoprotetion eluidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in Hedera canariensis. Photosynth Res 25:173–185. doi: 10.1007/BF00033159 CrossRefGoogle Scholar
  10. Boucher N, Carpentier R (1999) Hg2+, Cu2+, and Pb2+-induced changes in photosystem II photchemical yield and energy storage in isolated thylakoid membranes: a study using simultaneous and photoacoustic measurements. Photosynth Res 59:167–174. doi: 10.1023/A:1006194621553 CrossRefGoogle Scholar
  11. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254. doi: 10.1016/0003-2697(76)90527-3 PubMedCrossRefGoogle Scholar
  12. Briat JF (2002) Metal ion activated oxidative stres and its control. In: Inze D, Montagu MV (eds) Oxidative Stres in Plants. Taylor and Francis, New York, pp 171–189Google Scholar
  13. Brown DH, Slingsby DR (1972) The cellular location of lead and potassium in the lichen Cladonia rangiformis (L.) Hoffman. New Phytol 71:297–305. doi: 10.1111/j.1469-8137.1972.tb04076.x CrossRefGoogle Scholar
  14. Burzyński M (1987) The influence of lead and cadmium on the absorption and distribution of potassium, calcium, magnesium an iron in cucumber seedlings. Acta Physiol Plant 9:229–238Google Scholar
  15. Chakravarty B, Srivastava S (1997) Effect of cadmium andzinc interaction on metal uptake and regeneration of tolerant plants in linseed. Agric Ecosyst Environ 61:45–50. doi: 10.1016/S0167-8809(96)01078-X CrossRefGoogle Scholar
  16. de Abreu CA, de Abreu MF, de Andrade JC (1998) Distribution of lead in the soil profile evaluated by DTPA and Mehlich-3 solutions. Bragantia 57:185–192. doi: 10.1590/S0006-87051998000100021 CrossRefGoogle Scholar
  17. Dietz KJ, Schreiber U, Heber U (1985) The relationship between redox state of QA and photosynthesis in leaves at various carbon-dioxide, oxgen and light regimes. Planta 166:219–226. doi: 10.1007/BF00397352 CrossRefGoogle Scholar
  18. Dou ZX (1988) Lead pollution in soil and its effect on plants. Agro Environ Prot 7:38–39Google Scholar
  19. Draźkiewicz M (1994) Chlorophyllase: accurrence, functions, mechanisim of action, effects of external and internal factors. Photosynthetica 30:321–331Google Scholar
  20. Ekmekçi Y, Tanyolaç D, Ayhan B (2008) Effects of cadmium on antioxidant enzyme and photosynthetic activities in leaves of two maize cultivars. J Plant Physiol 15:600–611. doi: 10.1016/j.jplph.2007.01.017 CrossRefGoogle Scholar
  21. Eun SO, Youn HS, Lee Y (2000) Lead distrubs microtubule organization in the root meristem of Zea mays. Physiol Plant 110:357–365. doi: 10.1034/j.1399-3054.2000.1100310.x CrossRefGoogle Scholar
  22. FAOSTAT Food and Agriculture Organization of the United Nations (FAO) (2006) Statistical databasesGoogle Scholar
  23. Fernandes JC, Henriques FS (1991) Biochemical, physiological and structural effects of excess copper in plants. Bot Rev 57:246–273. doi: 10.1007/BF02858564 CrossRefGoogle Scholar
  24. Fritioff A, Greger M (2006) Uptake and distribution of Zn, Cu, Cd and Pb in an aquatic plant Potamogeton natans. Chemosphere 63:220–227. doi: 10.1016/j.chemosphere.2005.08.018 PubMedCrossRefGoogle Scholar
  25. Foyer CH, Lopez-Oelgado H, Dat JF, Scott JM (1997) Hydrogen peroxide- and glutathione-associated mechanisms of acclimatory stress tolerance and signalling. Physiol Plant 100:241–254. doi: 10.1111/j.1399-3054.1997.tb04780.x CrossRefGoogle Scholar
  26. Genty B, Briantais JM, Baker N (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92Google Scholar
  27. Havaux M, Strasser RJ, Greppin H (1991) A theoretical and experimental analysis of the q P and q N coefficients and chlorophyll fluorescence quenching and their relation to photochemical and nonphotochemical events. Photosynth Res 27:41–45. doi: 10.1007/BF00029975 CrossRefGoogle Scholar
  28. Heidari R, Khayami M, Farboodnia T (2005) Effect of pH and EDTA on Pb accumulation in Zea mays seedlings. J Agron 4:49–54CrossRefGoogle Scholar
  29. Imberty A, Goldberg R, Catesson A-M (1985) Isolation and characterization of Populus isoperoxidases involved in the last step of lignin formation. Planta 164:221–226. doi: 10.1007/BF00396085 CrossRefGoogle Scholar
  30. Johnson MS, Eaton JW (1980) Environmental contamination through residual trace metal dispersal from a derelict lead-zinc mine. J Environ Qual 9:175–179CrossRefGoogle Scholar
  31. Krupa Z, Baszyński T (1995) Some aspects of heavy metals toxicity towards photosynthetic apparatus direct and indirect effects on light and dark reactions. Acta Physiol Plant 17:177–190Google Scholar
  32. Kopittke PM, Asher CJ, Kopittke RA, Menzies NW (2007) Toxic effects of Pb2+ on growth of cowpea (Vigna unguiculata). Environ Pollut 150:280–287. doi: 10.1016/j.envpol.2007.01.011 PubMedCrossRefGoogle Scholar
  33. Lane SD, Martin ES (1977) A histochemical investigation of lead uptake in Raphanus sativus. New Phytol 79:281–286. doi: 10.1111/j.1469-8137.1977.tb02206.x CrossRefGoogle Scholar
  34. Levitt J (1980) Responses of plants to environmental stresses, vol Vol II, 2nd edn. Academic Press, New York, p 607Google Scholar
  35. Lozano R, Azcon R, Palma JM (1996) SOD and drought stress in Lactua sativa. New Phytol 136:329–331Google Scholar
  36. Lu C, Zhang JH (2000) Photosynthetic CO2 assimilation, chlorophyll flouresence and photoinhibition as affected by nitrogen deficiency in maize plants. Plant Sci 151:135–143. doi: 10.1016/S0168-9452(99)00207-1 PubMedCrossRefGoogle Scholar
  37. Lu CM, Chau CW, Zhang JH (2000) Acute toxicity of excess mercury on photosynthetic performance of cyanobacterium, S. platensis—assessment by chlorophyll flourescence analysis. Chemosphere 41:191–196. doi: 10.1016/S0045-6535(99)00411-7 PubMedCrossRefGoogle Scholar
  38. Lummerzheim M, Sandroni M, Castresana C, de Oliveira D, Van Montagu M, Roby D, Timmerman B (1995) Comparative microscopic and enzymatic characterization of the leaf necrosis induced in Arabidopsis thaliana by lead nitrate and by Xanthomanas campestris pv.Campestris after foliar spray. Plant Cell Environ 18:499–509. doi: 10.1111/j.1365-3040.1995.tb00550.x CrossRefGoogle Scholar
  39. Małkowski E, Stolarek J, Karcz W (1996) Toxic effect of Pb2+ ions on extension growth of cereal plants. Pol J Environ Stud 5:41–45Google Scholar
  40. Malkowski E, Kita A, Galas W, Karcz W, Kuperberg J (2002) Lead distrubition in corn seedling (Zea mays L.) and its effect on growth and the concentration of potassium and calcium. Plant Growth Regul 37:69–76. doi: 10.1023/A:1020305400324 CrossRefGoogle Scholar
  41. Mallick N, Mohn FH (2003) Use of chlorophyll fluorescence in metal-stress research: a case study with the gren microalga Scenedesmus. Ecotoxicol Environ Saf 55:64–69. doi: 10.1016/S0147-6513(02)00122-7 PubMedCrossRefGoogle Scholar
  42. Maribel LD, Satoshi T (1998) Antioxidant responses of rice seedlings to salinity stres. Plant Sci 135:1–9. doi: 10.1016/S0168-9452(98)00025-9 CrossRefGoogle Scholar
  43. Mishra A, Choudhari MA (1998) Amelioration of lead and mercury effects on germination and rice seedling growth by antioxidants. Biol Plant 41:469–473. doi: 10.1023/A:1001871015773 CrossRefGoogle Scholar
  44. Munzuroğlu O, Geckil H (2002) Effects of metals on seed germination, root elongation, and coleoptile and hypocotyl growth in Triticum aestivum and Cucumis sativus. Arch Environ Contam Toxicol 43:203–213. doi: 10.1007/s00244-002-1116-4 PubMedCrossRefGoogle Scholar
  45. Obroucheva NV, Bystrova EI, Ivanov VB, Anupova OV, Seregin IV (1998) Root growth responses to lead in young maize seedlings. Plant Soil 200:55–61. doi: 10.1023/A:1004204605833 CrossRefGoogle Scholar
  46. Paivoke AEA (2002) Soil lead alters phytase activitiy and mineral nutrient balance of Pisum sativum. Environ Exp Bot 48:61–73. doi: 10.1016/S0098-8472(02)00011-4 CrossRefGoogle Scholar
  47. Pandolfini T, Gabbrielli R, Comparini C (1992) Nickel toxicity and peroxidase activity in seedlings of Triticum aestivum L. Plant Cell Environ 15:719–725. doi: 10.1111/j.1365-3040.1992.tb01014.x CrossRefGoogle Scholar
  48. Parys E, Romanowska E, Siedlecka M, Poskuta JW (1998) The effect of lead on photosynthesis and respiration in detached leaves and in mesophyll protoplasts of Pisum sativum. Acta Physiol Plant 20:313–322. doi: 10.1007/s11738-998-0064-7 CrossRefGoogle Scholar
  49. Patra M, Bhowmik N, Bandopadhyay B, Sharma A (2004) Comparison of mercury, lead and arsenic with respect to genotoxic effects on plant systems and the development of genetic tolerance. Environ Exp Bot 52:199–223. doi: 10.1016/j.envexpbot.2004.02.009 CrossRefGoogle Scholar
  50. Pinto E, Sigaud-Kutner TCS, Leitão MAS, Okamoto AK, Morse D, Colepicolo P (2003) Heavy metal-induced oxidative stress in algae. J Phycol 39:1008–1018. doi: 10.1111/j.0022-3646.2003.02-193.x CrossRefGoogle Scholar
  51. Poskuta JW, Parys E, Romanowaska E (1996) Toxicity of lead to photosynthesis, accumulation of chlorophyll, respiration and growth of Chlorella pyrenoidosa. Protective role of dark respiration. Acta Physiol Plant 18:165–171Google Scholar
  52. Prasad MNV (1997) Trace metals. In: Plant ecophysiology, Wiley, New YorkGoogle Scholar
  53. Radotic′ K, Ducˇic′ T, Mutavdzˇic′ D (2000) Changes in peroxidase activity and isoenzymes in spruce needles after exposure to different concentrations of cadmium. Environ Exp Bot 44:105–113. doi: 10.1016/S0098-8472(00)00059-9 CrossRefGoogle Scholar
  54. Rao VM, Hale BA, Omrod DP (1995) Amelioation of ozone induced oxidative damage in wheat plants grown under high carbon dioxide. Plant Physiol 109:421–432PubMedGoogle Scholar
  55. Rashid A, Camm EL, Ekramoddoullah KM (1994) Molecular mechanism of action of Pb and Zn2+ on water oxidizing complex of photosystem II. FEBS Lett 350:296–298. doi: 10.1016/0014-5793(94)00789-6 PubMedCrossRefGoogle Scholar
  56. Reddy AM, Kumar SG, Jyothsnakumari G, Thimmanaik S, Sudhakar C (2005) Lead induced changes in antioxidant metabolism of horsegram (Macrotyloma uniflorum (Lam.) verdc.) and bengalgram (Cicer arietinum L.). Chemosphere 60:97–104. doi: 10.1016/j.chemosphere.2004.11.092 PubMedCrossRefGoogle Scholar
  57. Romanowska E, Wróblewska B, Drozak A, Siedlecka M (2006) High light intensity protects photosynthetic apparatus of pea plants against exposure to lead. Plant Physiol Biochem 44:387–394. doi: 10.1016/j.plaphy.2006.06.003 PubMedCrossRefGoogle Scholar
  58. Rudakova EV, Karakis KD, Sidorshina ET (1988) The role of plant cell walls in the uptake and accumulation of metal ions. Fiziol Biochim Kult Rast 20:3–12Google Scholar
  59. Scardelis S, Cook CM, Pantis JD, Lanaras T (1994) Comparison of chlorophyll fluorescence and some heavy metal concentration in Sonchus spp. Taraxacum spp. Along an urban pollution gradient. Sci Total Environ 158:157–164. doi: 10.1016/0048-9697(94)04246-J CrossRefGoogle Scholar
  60. Schreiber U, Schliwa U, Bilger W (1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new modulation fluorometer. Photosynth Res 10:51–62. doi: 10.1007/BF00024185 CrossRefGoogle Scholar
  61. Sgherri CLM, Liggini B, Puliga S, Navari-Izzo F (1994) Antioxidant system in Sporobolus stapianus: changes in response to desiccation and rehydration. Phytochemistry 35:561–565. doi: 10.1016/S0031-9422(00)90561-2 CrossRefGoogle Scholar
  62. Sharma P, Dubey RS (2004) Ascorbate peroxidase from rice seedlings: properties of enzyme isoforms, effects of stresses and protective roles of osmolytes. Plant Sci 167:541–550. doi: 10.1016/j.plantsci.2004.04.028 CrossRefGoogle Scholar
  63. Sharma P, Dubey RS (2005) Lead toxicity in plants. Braz J Plant Physiol 17:35–52. doi: 10.1590/S1677-04202005000100004 CrossRefGoogle Scholar
  64. Sinha P, Dube BK, Srivastava P, Chatterjee C (2006) Alteration in uptake and translocation of essential nutrients in cabbage by excess lead. Chemosphere 65:651–656. doi: 10.1016/j.chemosphere.2006.01.068 PubMedCrossRefGoogle Scholar
  65. Skórzyńska-Polit E, Baszyński T (1997) Differences in sensitivity of the photosynthetic apparatus in Cd-stressed runner bean plants in relation to their age. Plant Sci 128:11–21. doi: 10.1016/S0168-9452(97)00126-X CrossRefGoogle Scholar
  66. Stefanov K, Seizova K, Popova I, Petkov VL, Kimenov G, Popov S (1995) Effects of lead ions on the phospholipid composition in leaves Zea mays and Phaseolus vulgaris. J Plant Physiol 147:243–246Google Scholar
  67. Sobotik M, Ivanov VB, Obroucheva NV, Seregin IV, Martin ML, Antipova OV, Bergmann H (1998) Barrier role in root systems in lead exposed plants. J Appl Bot 72:144–147Google Scholar
  68. Tanyolaç D, Ekmekçi Y, Ünalan Ş (2007) Changes in photochemical and antioxidant enzyme activities in maize (Zea mays L.) leaves exposed to excess copper. Chemosphere 67:89–98. doi: 10.1016/j.chemosphere.2006.09.052 PubMedCrossRefGoogle Scholar
  69. Tsang EWT, Bowler C, Herouart D, Van Camp W, Willarroel R, Genetello C, Van Montagu M, Inze D (1991) Differential regulation of superoxide dismutases in plants exposed to environmental stress. Plant Cell 3:783–792PubMedCrossRefGoogle Scholar
  70. Van Assche F, Cardinales C, Clijsters H (1988) Induction of enzyme capacity in plants as a result of heavy metal toxicity: dose–response relations in Phaseolus vulgaris L. treated with zinc and cadmium. Environ Pollut 52:103–115. doi: 10.1016/0269-7491(88)90084-X PubMedCrossRefGoogle Scholar
  71. Verma S, Dubey RS (2003) Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Sci 164:645–655. doi: 10.1016/S0168-9452(03)00022-0 CrossRefGoogle Scholar
  72. Walker WM, Miller JE, Hassett JJ (1977) Effect of lead and cadmium upon the calcium, magnesium, potassium and phosphorus concentration in young corn plants. Soil Sci 124:145–151. doi: 10.1097/00010694-197709000-00004 CrossRefGoogle Scholar
  73. Wang SY, Jiao H, Faust M (1991) Changes in ascorbate, glutathione and related enzyme activity, during thidiazuron-induced bud break of apple. Plant Physiol 82:231–236. doi: 10.1111/j.1399-3054.1991.tb00086.x CrossRefGoogle Scholar
  74. Wierzbicka M (1994) Resumption of mitotic activitiy in Allium cepa root tips during treatment with lead salts. Environ Exp Bot 34:173–180. doi: 10.1016/0098-8472(94)90036-1 CrossRefGoogle Scholar
  75. Wierzbicka M, Obidzińska J (1998) The effect of lead on seed imbibition and germination in different plant species. Plant Sci 137:155–171. doi: 10.1016/S0168-9452(98)00138-1 CrossRefGoogle Scholar
  76. Wu X, Hong F, Liu C, Su M, Zheng L, Gao F, Yang F (2008) Effects of Pb2+ on energy distribution and photochemical activity of spinach chloroplast. Spectrochim Acta A Mol Biomol Spectrosc 69:738–742PubMedCrossRefGoogle Scholar
  77. Yang YY, Jung JY, Song WY, Suh HS, Lee Y (2000) Identification of rice varieties with high tolerance or sensitivity to lead and characterization of the mechanism of tolerance. Plant Physiol 124:1019–1026. doi: 10.1104/pp.124.3.1019 PubMedCrossRefGoogle Scholar
  78. Zacchini M, Rea E, Tullio M, Agazio M (2003) Increased antioxidative capacity in maize calli during and after oxidative stress induced by a long lead treatment. Plant Physiol Biochem 41:49–54. doi: 10.1016/S0981-9428(02)00008-6 CrossRefGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2008

Authors and Affiliations

  • Yasemin Ekmekçi
    • 1
  • Deniz Tanyolaç
    • 2
  • Beycan Ayhan
    • 1
  1. 1.Department of Biology, Faculty of ScienceHacettepe UníversityAnkaraTurkey
  2. 2.Department of Chemical Engineering, Faculty of EngineeringHacettepe UníversityAnkaraTurkey

Personalised recommendations