Effects of Lead on Activities of Photochemical Reaction and Key Enzymes of Carbon Assimilation in Spinach Chloroplast

  • Wu Xiao
  • Liu Chao
  • Qu Chunxiang
  • Huang Hao
  • Liu Xiaoqing
  • Chen Liang
  • Hong Fashui
Article

Abstract

Photosynthesis is one of the most sensitive processes to lead, but the effects of lead on the transformation of light energy of plants are still not clearly understood. In the present paper, spinach was cultivated in the experimental fields and was sprayed with various concentrations of PbCl2 solution. We investigated the effects of lead on the activities of photochemical reaction and the key enzymes of carbon assimilation in spinach chloroplast. The results showed that Pb2+ treatment could significantly inhibit the Hill reaction activity of spinach chloroplast and photophosphorylation, and it had a more conspicuous effect on cyclic photophosphorylation than non-cyclic photophosphorylation. The activities of ATPase on the thylakoid membrane were severely inhibited under Pb2+-treated condition, and Ca2+ ATPase activity was affected more obviously than Mg2+ ATPase activity. Meanwhile, the activities of the key enzymes of carbon assimilation were also significantly reduced by Pb2+, especially Rubisco activase. The reduction of dry weight of spinach caused by Pb2+ was more significant than that of fresh weight. It implied that Pb2+ could disturb light energy transformation of chloroplast.

Keywords

Pb2+ Photophosphorylation Mg2+ ATPase Ca2+ ATPase Rubisco activase 

Notes

Acknowledgments

This work was supported by the National Natural Science Foundation of China (grant no. 20671067, 30470150) and by the Jiangsu Province Universities Natural Science Foundation (grant no. 06KJB180094).

References

  1. 1.
    Raskin I, Smith RD, Salt DE (1997) Phytoremediation of metals: using plants to remove pollutants from the environment. Curr Opin Biotechnol 8:221–226PubMedCrossRefGoogle Scholar
  2. 2.
    Srivastava AK, Venkatachalam P, Raghothama KG, Sahi SV (2007) Identification of lead-regulated genes by suppression subtractive hybridization in the heavy metal accumulator Sesbania drummondii. Planta 225:1353–1365PubMedCrossRefGoogle Scholar
  3. 3.
    Sahi SV, Bryant NL, Sharma NC, Singh SR (2002) Characterization of lead hyperaccumulator shrub, Sesbania drummondii. Environ Sci Technol 36:4676–4680PubMedCrossRefGoogle Scholar
  4. 4.
    Garbisu C, Alkorta I (2001) Phytoextraction: a cost-effective plant-based technology for the removal of metals from the environment. Bioresour Technol 77:229–236PubMedCrossRefGoogle Scholar
  5. 5.
    Ribeiro Guevara S, Bubach D, Vigliano P, Lippolt G, Arribére M (2004) Heavy metal and other trace elements in native mussel Diplodon chilensis from Nothern Patagonia Lakes, Argentina. Biol Trace Element Res 102(1–3):245–263CrossRefGoogle Scholar
  6. 6.
    Yuan WK, Guo YZ, Da ZW, Shi ZL (2007) Heavy metals in bark of Pinus massoniana (Lamb.) as an indicator of atmospheric deposition near a smeltery at Qujiang, China. Environ Sci Pollut Res 14(4):270–275CrossRefGoogle Scholar
  7. 7.
    Cosson Richard P (1994) Heavy metal intracellular balance and relationship with metallothionein induction in the gills of carp. Biol Trace Element Res 46(3):229–245CrossRefGoogle Scholar
  8. 8.
    Iman Al-Saleh, Neptune S, Abdullah M (2003) Heavy metal concentrations in the breast milk of Saudi women. Biol Trace Element Res 96(1–3):21–37Google Scholar
  9. 9.
    Wong MK, Tan P, Wee YC (1993) Heavy metals in some Chinese herbal plants. Biol Trace Element Res 36(2):135–142CrossRefGoogle Scholar
  10. 10.
    Smith HA, Hidalgo HA, Bryan SE (1982) Heavy metal composition of polysomal fractions following cadmium challenge. Biol Trace Element Res 4(1):57–67CrossRefGoogle Scholar
  11. 11.
    Poland EK, Urszula S (1996) Heavy metals in the brain of long-tailed duck (Clangula hyemalis) wintering in the Pomeranian Bay. Biol Trace Element Res 55(1–2):191–197Google Scholar
  12. 12.
    Shearan IS, Singh R (1993) Effect of heavy metals on photosynthesis in higher plants. In: Abrol YP, Mohanty P, Govindjee (eds) Photosynthesis: photoreactions to plant productivity. Kluwer, Dordrecht, pp 451–468Google Scholar
  13. 13.
    Sinha SK, Srivastava HS, Tripathi RD (1993) Influence of some growth regulators and cations on inhibition of chlorophyll biosynthesis by lead in maize. Bull Environ Contam Toxicol 51:241–246PubMedGoogle Scholar
  14. 14.
    Romanowska E (2002) Gas exchange functions in heavy metal stressed plants. In: Prasad MNV (ed) Physiology and biochemistry of metal toxicity and tolerance in plants. Kluwer, Dordrecht, pp 257–285Google Scholar
  15. 15.
    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 52:199–223CrossRefGoogle Scholar
  16. 16.
    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 20:313–322CrossRefGoogle Scholar
  17. 17.
    Ewais EA (1997) Effect of cadmium, nickel and lead on growth chlorophyll content and proteins of weeds. Biol Plant 39:403–410CrossRefGoogle Scholar
  18. 18.
    Kastori R, Plesnicar MZ, Sakac D, Pankovic I, Arsenijevic-Maksimovic (1998) Effect of excess lead on sunflower growth and photosynthesis. J Plant Nutr 21:75–85.17Google Scholar
  19. 19.
    Romanowska E, Wróblewska B, Droak A, Siedlecka M (2006) High light intensity protects photosynthetic apparatus of pea plants against exposure to lead. Plant Physiol Biochem 44:387–394PubMedCrossRefGoogle Scholar
  20. 20.
    Ruley A, Thomas S, Nilesh C, Sahi Shivendra V (2004) Antioxidant defense in a lead accumulating plant Sesbania drummondii. Plant Physiol Bioch 42:899–906CrossRefGoogle Scholar
  21. 21.
    Van Assche F, Clijsters H (1990) Effects of metals on enzyme activity in plants. Plant Cell Environ 13:195–206CrossRefGoogle Scholar
  22. 22.
    Zacchini M, Rea E, Tullio M, de Agazio M (2003) Increased antioxidative capacity in maize calli during and after oxidative stress induced by a long lead treatment. Plant Physiol Biochem 41:49–54CrossRefGoogle Scholar
  23. 23.
    Ernst WHO, Nielssen HGM, Ten Bookum WM (2000) Combination toxicology of metal-enriched soils: physiological responses of a Zn- and Cd-resistant ecotypes of Silene vulgaris on polymetallic soils. Environ Exp Bot 43:55–71CrossRefGoogle Scholar
  24. 24.
    Kupper H, Kupper F, Spiller M (1996) Environmental relevance of heavy metal substituted chlorophylls using the example of water plants. J Exp Bot 47:259–266CrossRefGoogle Scholar
  25. 25.
    Miles CD, Brandle JR, Daniel DJ, Chu-Der O, Schnare PD, Uhlik DJ (1972) Inhibition of photosystem II in isolated chloroplasts by lead. Plant Physiol 49:820–825PubMedGoogle Scholar
  26. 26.
    Kajsa GV, Sigfridsson Gábor B, Fikret M, Stenbjörn S (2004) Molecular interference of Cd2+ with photosystem II. BBA 1659:19–31Google Scholar
  27. 27.
    Peter F, Katharina K, Anja KL (2005) Mechanism of Cd2+ toxicity: Cd2+ inhibits photoactivation of photosystem II by competitive binding to the essential Ca2+ site. BBA 1706:158–164Google Scholar
  28. 28.
    Wu X, Hong FS, Liu C, Su MY, Zheng L, Gao FQ, Yang F (2008) Effects of Pb2+ on energy distribution and photochemical activity of spinach chloroplast. Spectrochim Acta A 69:738–742CrossRefGoogle Scholar
  29. 29.
    Van de Loo FJ, Salvucci ME (1996) Activation of ribulose-1, 5-bisphosphate carboxylase/ oxygenase (Rubisco) mivolves Rubisco activase trp 16. Biochem 35:8143–8148CrossRefGoogle Scholar
  30. 30.
    Salvucci ME, Ogren WL (1996) The mechanism of Rubisco activase: insights from studies of the properties and structure of the enzyme. Photosynth Res 47:1–11CrossRefGoogle Scholar
  31. 31.
    Du YQ, He JH, Chen JJ, Wei XG, Yang XQ, Wang SY, He WB (2003) Effects of heavy metals of Pb, Cd and Cr on the growth of vegetables and their uptake. Acta Horticulture Sinica 30(1):51–55 (in Chinese)Google Scholar
  32. 32.
    Arnon DI (1949) Copper enzymes in isolated chloroplasts: polyphenol oxidase in Beta vulgaris. Plant Physiol 24:1–15PubMedGoogle Scholar
  33. 33.
    Allen JF, Holmes NG (1986) Electron transport and redox titration. In: Hipkins MF, Baker NR (eds) Photosynthesis, energy transduction: a practical approach. IRL, Oxford, pp 103–141Google Scholar
  34. 34.
    Allnutt FCT, Ewy RG, Renganathan M, Pan RS, Dilley RA (1991) Nigericin and hexylamine effects on localized proton gradients in thylakoid. BBA 1059:28–36CrossRefGoogle Scholar
  35. 35.
    McCarty RE, Racker E (1968) Partial resolution of the enzymes catalyzing photophosphorylation. J Biol Chem 243:129–137PubMedGoogle Scholar
  36. 36.
    Ames BN (1966) Assay of inorganic phosphate, Pi total phosphate and phosphatases (edited by Colowick and Kaplan). Methods Enzymol 8:115CrossRefGoogle Scholar
  37. 37.
    Li SJ, Cai JP, Wan GQ, Wang MQ, Zhao HY (1978) Studies on structure and function of chloroplasts isolation and interchangeability of pure coupling factors. Acta Bot Sin 20(2):103–107 (in Chinese)Google Scholar
  38. 38.
    Shi XB, Wei JM, Shen YK (2001) Effects of sequential deletions of residues from the N- or C-terminus on the function of e subunit of the chloroplast ATP synthase. Biochemistry 40:10825–10831PubMedCrossRefGoogle Scholar
  39. 39.
    Lan Y, Mott KA (1991) Determination of apparent Km values for ribulose 1, 5-bisphosphate carboxylase/oxygenase (Rubisco) activase using the spectrophotometric assay of Rubisco activity. Plant Physiol 95:604–609PubMedGoogle Scholar
  40. 40.
    Madigan MT, Martinko JM, Brock PJ (1997) Biology of microorganisms. Prentice Hall, Upper Saddle River, NJGoogle Scholar
  41. 41.
    Chase MW (1993) Phylogenetics of seed plants: an analysis of nucleotide sequences from the plastid gene rbcL. Ann Mo Bot Gard 80:528–580CrossRefGoogle Scholar
  42. 42.
    Liley RM, Portis AR Jr (1990) Activation of ribulose-1,5-bisphosphate carboxylase/oxygenase by Rubisco activase. Plant Physiol 94:245–250CrossRefGoogle Scholar
  43. 43.
    Portis AR Jr (1995) The regulation of Rubisco by Rubisco activase. J Expt Bot 46:1285–1291Google Scholar
  44. 44.
    Buchanan BB, Gruissem W, Jones RL (2002) Biochemistry and molecular biology of plants. Science Press, American Society of Plant Physiologists, Beijing, pp 568–675Google Scholar
  45. 45.
    Van Assche F, Clijsters H (1983) Multiple effects of heavy metal toxicity on photosynthesis. In: Marcelle R, Clijsters H, van Poucke M (eds) Effects of Stress on photosynthesis. Martinus Nijhoff/Dr. W. Junk, The Hague, pp 371–382Google Scholar
  46. 46.
    Stiborova M, Doubravova M, Brezninova A, Friedrich A (1986) Effect of heavy metal ions on growth and biochemical characteristics of photosynthesis of barley Hordeum vulgare L. Photosynthetica 20:418–425Google Scholar

Copyright information

© Humana Press Inc. 2008

Authors and Affiliations

  • Wu Xiao
    • 1
  • Liu Chao
    • 1
  • Qu Chunxiang
    • 1
  • Huang Hao
    • 1
  • Liu Xiaoqing
    • 1
  • Chen Liang
    • 1
  • Hong Fashui
    • 1
  1. 1.Medical College of Soochow UniversitySuzhouPeople’s Republic of China

Personalised recommendations