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Biological Trace Element Research

, Volume 146, Issue 3, pp 360–368 | Cite as

Arsenic (As) Inhibits Radicle Emergence and Elongation in Phaseolus aureus by Altering Starch-Metabolizing Enzymes Vis-à-Vis Disruption of Oxidative Metabolism

  • Shalinder Kaur
  • Harminder Pal Singh
  • Daizy Rani Batish
  • Asha Negi
  • Priyanka Mahajan
  • Surabhi Rana
  • Ravinder Kumar Kohli
Article

Abstract

The present study investigated the effect of Arsenic (As; 5, 10, 50 μM) on protein and sugar metabolism vis-à-vis oxidative damage during early germination process and radicle emergence (at 12, 24 and 48 h stage) in Phaseolus aureus. As-exposure (50 μM) significantly enhanced protein content (by 40–60%), whereas carbohydrate content declined (by 31–44%) over that in the control. It was associated with a decline in the activities of proteases (47–53%), and increase in the activities of α- and β-amylases, starch phosphorylases, and acid invertases by 3.0, 2.6, 4.8, and 1.7 times after 48 h exposure to 50 μM As. The alteration in protein and carbohydrate metabolic machinery was also accompanied by As-induced reactive oxygen species (ROS)-mediated oxidative damage. As treatment enhanced malondialdehyde and hydrogen peroxide content by 46–252% and 23–216%, and hydroxyl and superoxide ion generation by 15–104% and 17–278%, respectively. As-induced lipid peroxidation and membrane disruption was confirmed by enhanced electrolyte leakage (by 49%) and reduced cell viability (by 43%). Furthermore, in response to 50 μM As, the activities of superoxide dismutases, catalases, ascorbate peroxidases, guaiacol peroxidases, and glutathione reductases increased by 77%, 70%, 116%, 43% and 120%, respectively, in radicles at 48 h stage over that in the control. The study concludes that As inhibits radicle emergence and elongation in germinating P. aureus seeds by altering biochemical processes related to sugar metabolism and inducing an ROS-mediated oxidative damage.

Keywords

Acid invertases As toxicity Emerging radicles Mung bean ROS generation ROS metabolism Starch phosphorylase Sugar metabolism 

References

  1. 1.
    Mahimairaja S, Bolan NS, Adriano DC, Robinson B (2005) Arsenic contamination and its risk management in complex environmental settings. Adv Agron 86:1–82CrossRefGoogle Scholar
  2. 2.
    Naidu R, Bhattacharya P (2009) Arsenic in the environment – risks and management strategies. Environ Geochem Health 31:1–8PubMedCrossRefGoogle Scholar
  3. 3.
    Williams PN, Villada A, Deacon C, Raab A, Figuerola J, Green AJ, Feldmann J, Meharg AA (2007) Greatly enhanced arsenic shoot assimilation in rice leads to elevated grain levels compared to wheat and barley. Environ Sci Technol 41:6854–6859PubMedCrossRefGoogle Scholar
  4. 4.
    Polizzotto M, Kocar BD, Benner SG, Sampson M, Fendorf S (2008) Near surface wetland sediments as a source of arsenic release to ground water in Asia. Nature 454:505–508PubMedCrossRefGoogle Scholar
  5. 5.
    Lou-Hing D, Zhang B, Price AH, Meharg AA (2011) Effects of phosphate on arsenate and arsenite sensitivity in two rice (Oryza sativa L.) cultivars of different sensitivity. Environ Exp Bot 72:47–52CrossRefGoogle Scholar
  6. 6.
    Smith E, Naidu R, Alston AM (1998) Arsenic in the soil environment: a review. Adv Agron 64:149–195CrossRefGoogle Scholar
  7. 7.
    Hartley-Whitaker J, Ainsworth G, Meharg AA (2001) Copper and arsenate induced oxidative stress in Holcus lanatus L. clones with differential sensitivity. Plant Cell Environ 24:13–22CrossRefGoogle Scholar
  8. 8.
    Stoeva N, Berova M, Zlatev Z (2005) Effect of arsenic on some physiological parameters in bean plants. Biol Plant 49:293–296CrossRefGoogle Scholar
  9. 9.
    Singh HP, Batish DR, Kohli RK, Arora K (2007) Arsenic-induced root growth inhibition in mung bean (Phaseolus aureus Roxb.) is due to oxidative stress resulting from enhanced lipid peroxidation. Plant Growth Regul 53:65–73CrossRefGoogle Scholar
  10. 10.
    Meharg AA (2003) Variation in arsenic accumulation—hyperaccumulation in ferns and their allies. New Phytol 157:25–31CrossRefGoogle Scholar
  11. 11.
    Singh HP, Kaur S, Batish DR, Sharma VP, Sharma N, Kohli RK (2009) Nitric oxide alleviates arsenic toxicity by reducing oxidative damage in the roots of Oryza sativa (rice). Nitric Oxide 20:289–297PubMedCrossRefGoogle Scholar
  12. 12.
    Ma B, Wan J, Shen Z (2007) H2O2 production and antioxidant responses in seeds and early seedlings of two different rice varieties exposed to aluminum. Plant Growth Regul 52:91–100CrossRefGoogle Scholar
  13. 13.
    Van den Broeck K, Vendecasteele C, Geuns JMC (1998) Speciation by liquid chromatography-inductively coupled plasma-mass spectrometry of arsenic in mung bean seedlings used as a bio-indicator for the arsenic contamination. Anal Chim Acta 361:101–111CrossRefGoogle Scholar
  14. 14.
    Sheppard SC (1992) Summary of phytotoxic levels of soil arsenic. Water Air Soil Pollut 64:539–550CrossRefGoogle Scholar
  15. 15.
    Lowry OH, Rosebrough NT, Farr AL, Randall RJ (1951) Protein measurement with the folin–phenol reagent. J Biol Chem 193:265–275PubMedGoogle Scholar
  16. 16.
    Batish DR, Singh HP, Setia N, Kaur S, Kohli RK (2006) Effect of 2-benzoxazolinone (BOA) on seedling growth and associated biochemical changes in mung bean (Phaseolus aureus). Z Naturforsch C 61:709–714PubMedGoogle Scholar
  17. 17.
    Fiske CH, Subbarow Y (1952) The colorimetric determination of phosphorus. J Biol Chem 56:375Google Scholar
  18. 18.
    Nelson N (1994) A photometric adaptation of the Somogyi method for the determination of glucose. J Biol Chem 153:375–380Google Scholar
  19. 19.
    Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198PubMedCrossRefGoogle Scholar
  20. 20.
    Misra HR, Fridovich I (1972) The univalent reduction of oxygen by reduced flavins and quinines. J Biol Chem 247:188–192PubMedGoogle Scholar
  21. 21.
    Halliwell B, Gutteridge JMC, Auroma O (1987) The deoxyribose method: a simple ‘test tube’ assay for determination of rate constants for reactions of hydroxyl radicals. Ann Biochem 165:215–219CrossRefGoogle Scholar
  22. 22.
    Steponkus PL, Lanphear FR (1967) Refinement of triphenyl tetrazolium chloride method of determining cold injury. Plant Physiol 42:1423–1426PubMedCrossRefGoogle Scholar
  23. 23.
    Beauchamp CO, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicaple to acrylamide gels. Anal Biochem 44:276–287PubMedCrossRefGoogle Scholar
  24. 24.
    Mishra S, Dubey RS (2006) Inhibition of ribonuclease and proteases activities in arsenic exposed rice seedlings: role of proline as enzyme protectant. J Plant Physiol 163:927–936PubMedCrossRefGoogle Scholar
  25. 25.
    Maheshwari R, Dubey RS (2007) Nickel toxicity inhibits ribonuclease and proteases activities in rice seedlings: protective effects of proline. Plant Growth Regul 51:231–243CrossRefGoogle Scholar
  26. 26.
    Kevresan S, Petrovic N, Popovic M, Kandrac J (1998) Effect of heavy metals on nitrate and protein metabolism in sugar beet. Biol Plant 41:235–240CrossRefGoogle Scholar
  27. 27.
    Singh HP, Kaur G, Batish DR, Kohli RK (2011) Lead (Pb)-inhibited radicle emergence in Brassica campestris involves alterations in starch-metabolizing enzymes. Biol Trace Elem Res. doi: 10.1007/s12011-011-9129-3
  28. 28.
    Demirevska-Kepova K, Simova-Stoilova L, Stoyanova Z, Hölzer R, Feller U (2003) Biochemical changes in barley plants after excessive supply of copper and manganese. Environ Exp Bot 52:253–266CrossRefGoogle Scholar
  29. 29.
    Xiong ZT, Wang T, Liu K, Zhang ZZ, Gan JH, Huang Y, Li MJ (2008) Differential invertase activity and root growth between Cu-tolerant and non-tolerant populations in Kummerowia stipulacea under Cu stress and nutrient deficiency. Environ Exp Bot 62:17–27CrossRefGoogle Scholar
  30. 30.
    Sturm A (1999) Invertases. Primary structures, functions, and roles in plant development and sucrose partitioning. Plant Physiol 121:1–7PubMedCrossRefGoogle Scholar
  31. 31.
    Verma S, Dubey RS (2001) Effect of cadmium on soluble sugars and enzymes of their metabolism in rice. Biol Plant 44:117–123CrossRefGoogle Scholar
  32. 32.
    Roitsch T, Gonzalez MC (2004) Function and regulation of plant invertases: sweet sensations. Trends Plant Sci 9:606–613PubMedCrossRefGoogle Scholar
  33. 33.
    Sinniah UR, Ellis RH, John P (1998) Irrigation and seed quality development in rapid recycling Brassica, soluble carbohydrates and heat stable protein. Ann Bot 82:647–655CrossRefGoogle Scholar
  34. 34.
    Deryabin AN, Sińkevich MS, Dubinina IM, Burakhanova EA, Trunova TI (2007) Effect of sugars on the development of oxidative stress induced by hypothermia in potato plants expressing yeast invertase gene. Russ J Plant Physiol 54:32–38CrossRefGoogle Scholar
  35. 35.
    Huang W-X, Cao Y, Huang L-J, Ren C, Xiong ZT (2011) Differential expression of acid invertase genes in roots of metallicolous and non-metallicolous populations of Rumex japonicus under copper stress. Chemosphere 84:1432–1439Google Scholar
  36. 36.
    Bolouri-Moghaddam MR, Le Roy K, Xiang L, Rolland F, Van den Ende W (2010) Sugar signalling and antioxidant network connections in plant cells. FEBS J 277:2022–2037PubMedCrossRefGoogle Scholar
  37. 37.
    Saleh M, Al-Garni S (2006) Increased heavy metal tolerance of cowpea plants by dual inoculation of an arbuscular mycorrhizal fungi and nitrogen-fixer Rhizobium bacterium. Afr J Biotechnol 5:133–142Google Scholar
  38. 38.
    Terwelle HF, Slater EC (1967) Uncoupling of respiratory chain phosphorylation by arsenate. Biochim Biophys Acta 143:1–17CrossRefGoogle Scholar
  39. 39.
    Meharg AA (1994) Integrated tolerance mechanisms: constitutive and adaptive plant responses to elevated metal concentrations in the environment. Plant Cell Environ 17:989–993CrossRefGoogle Scholar
  40. 40.
    Gunes A, Inal A, Bagci EG, Pilbeam DJ (2007) Silicon-mediated changes of some physiological and enzymatic parameters symptomatic for oxidative stress in spinach and tomato grown in sodic-B toxic soil. Plant Soil 290:103–114CrossRefGoogle Scholar
  41. 41.
    Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410PubMedCrossRefGoogle Scholar
  42. 42.
    Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930PubMedCrossRefGoogle Scholar
  43. 43.
    Ruiz-Lozano JM, Azcon R, Palma JM (1996) Superoxide dismutase activity in arbuscular mycorrhizal Lactuca sativa plants subjected to drought stress. New Phytol 134:327–333CrossRefGoogle Scholar
  44. 44.
    Cao X, Ma LQ, Tu C (2004) Antioxidant responses to arsenic in the arsenic-hyperaccumulator Chinese brake fern (Pteris vittata L.). Environ Pollut 128:317–325PubMedCrossRefGoogle Scholar
  45. 45.
    Ekmekci Y, Tanyolac D, Ayhana B (2008) Effects of cadmium on antioxidant enzyme and photosynthetic activities in leaves of two maize cultivars. J Plant Physiol 165:600–611PubMedCrossRefGoogle Scholar
  46. 46.
    Schmöger MEV, Oven M, Grill E (2000) Detoxification of arsenic by phytochelatins in plants. Plant Physiol 122:793–801PubMedCrossRefGoogle Scholar
  47. 47.
    Gajewska E, Slaba M, Andrzejewska R, Sklodowska M (2006) Nickel-induced inhibition of wheat root growth is related to H2O2 production, but not to lipid peroxidation. Plant Growth Regul 49:95–103Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Shalinder Kaur
    • 1
  • Harminder Pal Singh
    • 1
  • Daizy Rani Batish
    • 2
  • Asha Negi
    • 1
  • Priyanka Mahajan
    • 2
  • Surabhi Rana
    • 1
  • Ravinder Kumar Kohli
    • 2
  1. 1.Department of Environment StudiesPanjab UniversityChandigarhIndia
  2. 2.Department of BotanyPanjab UniversityChandigarhIndia

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