Defense manifestations of enzymatic and non-enzymatic antioxidants in Ricinus communis L. exposed to lead in hydroponics

Open access


Lead (Pb) is a major inorganic pollutant with no biological significance and has been a global concern. Phytotoxicity of lead induces toxic effects by generating reactive oxygen species (ROS), which inhibits most of the cellular processes in plants. Hydro-ponic experiments were performed with Ricinus communis to investigate the toxicity and antioxidant responses by exposing to different concentrations of lead (0, 200 and 400 µM) for 10 days. Pb stress caused a significant increase in electrolyte leakage, non-enzymatic antioxidants (phenols and flavonoids) and a decrease in the elemental profile of the plant. Histochemical visualization clearly indicates the significant increase of H2O2 production in dose-dependent manner under Pb stress. Likewise, an increase in catalase, guaiacol peroxidase and superoxide dismutase activity was also evident. Ascorbate peroxidase and MDAR, on the other hand, responded biphasically to Pb treatments showing a decrease in concentration. The decline in redox ratio GSH/GSSG was imposed by the indirect oxidative stress of Pb. Hence these findings showed the ameliorative potential of R. communis to sustain Pb toxicity under oxidative stress.

If the inline PDF is not rendering correctly, you can download the PDF file here.

  • 1. Gupta DK Huang HG Corpas FJ. Lead tolerance in plants: strategies for phytoremediation. Environ. Sci. Pollut. Res. 2013; 20: 2150–2161.

  • 2. Obiora SC Chukwu A Toteu SF Davies TC. Assessment of heavy metal contamination in soils around lead (Pb)-zinc (Zn) mining areas in Enyigba south-eastern Nigeria. J. Geol. Soc. 2016; 87: 453–462.

  • 3. Kumar A and Prasad MNV. Plant-lead interactions: Transport toxicity tolerance and detoxification mechanisms. Ecotoxicol. Environ. Saf. 2018; 166 401–418.

  • 4. Mroczek-Zdyrska M Strubińska J Hanaka A. Selenium improves physiological parameters and alleviates oxidative stress in shoots of lead-exposed Vicia faba L. minor plants grown under phosphorus-deficient conditions. J. Plant Growth Regul. 2016: 36; 186–199.

  • 5. Sorrentino MC Capozzi F Giordano S Spagnuolo V. Genotoxic effect of Pb and Cd on in vitro cultures of Sphagnum palustre: an evaluation by ISSR markers. Chemosphere 2017; 181: 208–215.

  • 6. Ashraf U and Tang X. Yield and quality responses plant metabolism and metal distribution pattern in aromatic rice under lead (Pb) toxicity. Chemosphere 2017; 176: 141–155. doi:10.1016/j.chemosphere.2017.02.103.

  • 7. Piwowarczyk B Tokarz K Muszyńska E Makowski W Jędrzejczyk R Gajewski Z Hanus-Fajerska E. The acclimatization strategies of kidney vetch (Anthyllis vulneraria L.) to Pb toxicity. Environ. Sci. Pollut. Res. 2018; 25: 19739–19752.

  • 8. Morel JL Mench M Guckert A. Measurement of Pb Cu and Cd Binding with Mucilage Exudates from Maize (Zea mays L.) Roots Biol. Fertil. Soils 1986; 2: 29–34.

  • 9. Pourrut B Shahid M Dumat C Winterton P Pinelli E. Lead uptake toxicity and detoxification in plants. Rev Environ Conta Toxicol 2011; 213: 113–136.

  • 10. Kaur G Singh HP Batish DR Kohli RK. A time course assessment of changes in reactive oxygen species generation and antioxidant defense in hydroponically grown wheat in response to lead ions (Pb2+). Protoplasma 2012; 249(4): 1091–1100. doi:10.1007/s00709-011-0353-7

  • 11. Mahdavian K Ghaderian SM Schat H. Pb accumulation Pb tolerance antioxidants thiols and organic acids in metallicolous and non-metallicolous Peganum harmala L. under Pb exposure. Environ Exper Bot 2016; 126: 21–31.

  • 12. López-Orenes A Dias MC Ferrer MÁ Calderón A Moutinho-Pereira J Correia C Santos C. Different mechanisms of the metalliferous Zygophyllum fabago shoots and roots to cope with Pb toxicity. Environ. Sci. Pollut. Res. 2018; 25: 1319–1330.

  • 13. Saleem M Asghar HN Zahir ZA Shahid M. Impact of lead tolerant plant growth promoting rhizobacteria on growth physiology antioxidant activities yield and lead content in sunflower in lead contaminated soil. Chemosphere 2018; 195: 606–614.

  • 14. Sidhu GPS Singh HP Batish DR Kohli RK. Effect of lead on oxidative status antioxidative response and metal accumulation in Coronopus didymus. Plant Physiol. Biochem. 2016; 105: 290–296.

  • 15. Khan MM Islam E Irem S Akhtar K Ashraf MY Iqbal J Liu D. Pb-induced phytotoxicity in para grass (Brachiaria mutica) and castor bean (Ricinus communis L.): antioxidant and ultrastructural studies. Chemosphere 2018; 200: 257–265.

  • 16. Maldonado-Magana A Favela-Torres E Rivera-Cabrera F Volke-Sepulveda TL. Lead bioaccumulation in Acacia farnesiana and its effect on lipid peroxidation and glutathione production. Plant Soil 2011; 339(1-2): 377–389.

  • 17. Kumar A Majeti NVP. Proteomic responses to lead-induced oxidative stress in Talinum triangulare Jacq. (Willd.) roots: identification of key biomarkers related to glutathione metabolisms. Environ. Sci. Pollut. Res. 2014; 21: 8750–8764.

  • 18. Kohli SK Handa N Bali S Arora S Sharma A Kaur R Bhardwaj R. Modulation of antioxidative defense expression and osmolyte content by co-application of 24-epibrassinolide and salicylic acid in Pb exposed Indian mustard plants. Ecotoxicol. Environ. Saf 2018; 147: 382–393.

  • 19. Zhou F Wang J Yang N. Growth responses antioxidant enzyme activities and lead accumulation of Sophora japonica and Platycladus orientalis seedlings under Pb and water stress. Plant Growth Regul 2015; 75: 383–389.

  • 20. Rodriguez E da Conceição Santos M Azevedo R Correia C Moutinho-Pereira J Ferreira de Oliveira JMP Dias MC. Photosyn-thesis light-independent reactions are sensitive biomarkers to monitor lead phytotoxicity in a Pb-tolerant Pisum sativum cultivar. Environ. Sci. Pollut. Res. 2015; 22: 574–585.

  • 21. Marques MC Nascimento CWA da Silva AJ Gouviea-Neto AS. Tolerance of an energy crop (Jatropha curcas L.) to zinc and lead assessed by chlorophyll fluorescence and enzyme activity. S Afr J Bot 2017; 112: 275–282.

  • 22. Kiran BR Prasad MNV. Ricinus communis L. (Castor bean) a potential multi-purpose environ-mental crop for improved and integrated phyto-remediation. The Euro Biotech J 2017a; 1(2): 1–16.

  • 23. Olivares AR Carrillo-González R González-Chávez MCA Hernández RMS. Potential of castor bean (Ricinus communis L.) for phytoremediation of mine tailings and oil production. J. Environ. Manag. 2013; 114: 316–323.

  • 24. Kushwaha A Hans N Kumar S Rani R. A critical review on speciation mobilization and toxicity of lead in soil-microbe-plant system and bioremediation strategies. Ecotoxicol. Environ. Saf. 2018;147: 1035–1045.

  • 25. Silva WR da Silva FBV Arauj PRM do Nascimento. Assessing human health risks and strategies for phytoremediation in soils contaminated with As Cd Pb and Zn by slag disposal. Ecotoxicol. Environ. Saf. 2017; 144: 522–530.

  • 26. Wei R Guo Q Yu G Kong J Okoli CP. Stable isotope fractionation during uptake and translocation of cadmium by tolerant Ricinus communis and hyperaccumulator Solanum nigrum as influenced by EDTA. Environ. Pol. 2018; 236: 634–644.

  • 27. Yazdi M Kolahi M Kazemi EM Barnaby AGB. Study of the contamination rate and change in growth features of lettuce (Lactuca sativa Linn.) in response to cadmium and a survey of its phytochelatin synthase gene. Ecotoxicol. Environ. Saf. 2019; 180: 295–308.

  • 28. Huang G Guo G Yao S Zhang N Hu H. Organic Acids Amino acids compositions in the root exudates and Cu-accumulation in castor (Ricinus communis L.) under Cu Stress. Int J Phytoremediation 2016; 18(1): 33–40.doi:10.1080/15226514.2015.1058333.

  • 29. Celik O and Akdas EY. Tissue specific transcriptional regulation of seven heavy metal stress-responsive miRNAs and their putative targets in nickel indicator castor bean (R. communis L.) plants. Ecotoxicol. Environ. Saf. 2019; 170: 682–690.

  • 30. Yang J Yang J Huang J. Role of co-planting and chitosan in phytoextraction of As and heavy metals by Pteris vittata and castor bean – A field case. Ecol. Eng. 2017; 109: 35–40.

  • 31. Kiran BR Prasad MNV. Responses of Ricinus communis L. (Castor bean phytoremediation crop) seedlings to lead (Pb) toxicity in hydroponics. Selcuk J Agr Food Sci 2017b; 31(1): 73–80.

  • 32. Boda RK Prasad MNV Suthari S. Ricinus communis L. (castor bean) as a potential candidate for revegetating industrial waste contaminated sites in peri-urban Greater Hyderabad: remarks on seed oil. Environ Sci Pollut Res 2017; 24: 1–10. doi 10.1007/s11356-017-9654-5

  • 33. Hoagland DR and Arnon DI The water-culture method for growing plants without soil. Calif Agric Exp Stn Circ 1950; 347: 1–32. doi:citeulike-article-id:9455435.

  • 34. Singleton VL Orthofer R Larnuela-Raventos RM. Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Methods in Enzymology 1999; 299: 152–178.

  • 35. Zhishen J Mengcheng T Jianming W. The determination of flavanoids content in mulberry and their scavenging effects on superoxide radicals. Food Chem. 1999; 64: 555–559.

  • 36. Valentovic P Luxova M Kolarovic L Gasparikova O. Effect of osmotic stress on compatible solutes content membrane stability and water relations in two maize cultivars. Plant Soil Environ 2006; 52: 186-191.

  • 37. Velikova V Yordanov I Edreva A. Oxidative stress and some anti-oxidant systems in acid rain-treated bean plants. Plant Sci 2000; 151(1): 59–66. doi:10.1016/S0168-9452(99)00197-1

  • 38. Lowry OH Rosebrough NJ Farr AL Randall RJ. Protein Measurement with the Folin Phenol Reagent. The Journal of Biological Chemistry 1951; 193(1): 265–275.

  • 39. Beauchamp C and Fridovich I. Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem. 1971; 44(1): 276–287.

  • 40. Aebi H (1984) Catalase in vitro. Meth Enzymol 105:121–126.

  • 41. Nakano Y Asada K. Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 1981; 22(5): 867–880.

  • 42. Putter J. Peroxidase. In: Methods of enzymatic assays. (Ed.H.U. Bergymer) Verlag Chemie Weinhan 1974; 685-690.

  • 43. Drazkiewicz M Skorzynska-Polit E Krupa Z. Response of ascorbate-glutathione cycle to excess copper in Arabidopsis thaliana (L.). Plant Sci 2003; 164(2): 195–202

  • 44. Hissin PJ and Hiff R. A fluorometric method for determination of oxidized and reduced glutathione in tissues. Anal Biochem 1976; 74(1): 214–226.

  • 45. Jiang M and Zhang J. Effect of abscissic acid on active oxygen species antioxidative defense system and oxidative damage in leaves of maize seedlings. Plant Cell Physiol 2001; 42(11): 1265–1273.

  • 46. Liu CW Sung Y Chen BC Lai HY. Effects of nitrogen fertilizers on the growth and nitrate content of Lettuce (Lactuca sativa L.). Int. J. Environ. Res. Public Health. 2014; 11: 4427-4440.

  • 47. Guha A Sengupta D Reddy AR. Polyphasic chlorophyll a fluorescence kinetics and leaf protein analyses to track dynamics of photosynthetic performance in mulberry during progressive drought. J. Photochem. Photobiol. 2013; 119: 71–83.

  • 48. Kumar A and Prasad MNV. Lead-induced toxicity and interference in chlorophyll fluorescence in Talinum triangulare grown hydroponically. Photosynthetica 2015; 53 (1): 66–71.

  • 49. Boguszewska D Zagdanska B. ROS as signaling molecules and enzymes of plant response to unfavorable environmental conditions Oxidative Stress – Molecular Mechanisms and Biological Effects Dr. Volodymyr Lushchak (Ed.) Rijeka Croatia: In Tech 2012; 341-362. DOI: 10.5772/33589

  • 50. Bhattacharjee S. Reactive oxygen species and oxidative burst: roles in stress senescence and signal transduction in plants. Curr Sci 2005; 89(7): 1113–1121.

  • 51. Posmyk MM Kontek R Janas KM. Antioxidant enzymes activity and phenolic compounds content in red cabbage seedlings exposed to copper stress. Ecotoxicol Environ Saf 2009; 72(2): 596–602

  • 52. Shemet SA Fedenko VS. Accumulation of phenolic compounds in maize seedlings under toxic Cd influence. Physiol Biochem Cultiv Plants 2005; 37: 505–512.

  • 53. Sakihama Y Cohen MF Grace SC Yamasaki H. Plant phenolic antioxidant and pro-oxidant activities: phenolics induced oxidative damage mediated by metals in plants. Toxicology 2002; 177(1): 67–80.

  • 54. Kumar A Prasad MNV Achary VMM Panda BB. Elucidation of lead-induced oxidative stress in Talinum triangulare roots by analysis of antioxidant responses and DNA damage at cellular level. Environ Sci Pollut Res 2013; 20(7): 4551–4561.

  • 55. Kabata-Pendias A. Trace elements in soils and plants. 4th edn. CRC Press. Boca Rato. London. Pp 2010; 407–505

  • 56. Kopittke PM Asher CJ Blamey FPC Menzies NW. Toxic effects of Pb2+ on the growth and mineral nutrition of signal grass (Brachiaria decumbens) and Rhodes grass (Chloris gayana). Plant Soil 2007; 300(1-2): 127–136.

  • 57. Qiao X Shi G Jia R Chen L Tian X Xu J. Physiological and biochemical responses induced by lead stress in Spirodela polyrhiza. Plant Growth Regul. 2012; 67: 217–225.

  • 58. Sharma P Dubey RS. Lead Toxicity in Plants. Brazilian J Plant Physiol 2005; 17: 35–52. doi:10.1590/S1677-04202005000100004

  • 59. Aravind P Prasad MNV. Zinc alleviates cadmium-induced oxidative stress in Ceratophyllum demersum L.: a free floating freshwater macrophyte. Plant Physiol Biochem 2003; 41(4): 391–397.

  • 60. Meitei M Kumar A Prasad M Malec P Waloszek A Maleva G Strzalka K. Photosynthetic pigments and pigment-protein complexes of aquatic plants under heavy metal stress. Photosynthetic pigments: chemical structure biological function and ecology. Russian Academy of Sciences St. Petersburg Nauka Russia 2014; 314–329.

  • 61. Parys E Wasilewska W Siedlecka M Zienkiewicz M Drożak A Romanowska E. Metabolic responses to lead of metallicolous and nonmetallicolous populations of Armeria maritima. Arch. Environ. Contam. Toxicol. 2014; 67: 565–577.

  • 62. Yang L Fan T Guan L Ren Y Han Y Liu Q et al. CMDH4 encodes a protein that is required for lead tolerance in Arabidopsis. Plant Soil 2016; 412: 317–330.

  • 63. Chen Q Zhang X Liu Y Wei J Shen W Shen Z Cui J. Hemin-mediated alleviation of zinc lead and chromium toxicity is associated with elevated photosynthesis antioxidative capacity; suppressed metal uptake and oxidative stress in rice seedlings. Plant Growth Regul. 2016; 81: 253–264.

  • 64. Nautiyal N Sinha P. Lead induced antioxidant defense system in pigeon pea and its impact on yield and quality of seeds. Acta Physiol. Planta 2012; 34: 977–983.

  • 65. Wang P Zhang S Wang C Lu J. Effects of Pb on the oxidative stress and antioxidant response in a Pb bioaccumulator plant Vallisneria natans. Ecotoxicol. Environ. Saf. 2012; 78: 28–34.

  • 66. Asada K. Ascorbate peroxidase - a hydrogen peroxide scavenging enzyme in plants. Physiol Plant 1992; 85(2): 235–241.

  • 67. Mishra S Srivastava S Tripathi RD Kumar R Seth CS Gupta DK. Lead detoxification by coontail (Ceratophyllum demersum L.) involves induction of phytochelatins and antioxidant system in response to its accumulation. Chemosphere 2006; 65(6): 1027–1039.

  • 68. Wang C Gu X Wang X Guo H Geng J Yu H Sun J. Stress response and potential biomarkers in spinach (Spinacia oleracea L.) seedlings exposed to soil lead. Ecotoxicol Environ Saf 2011; 74(1): 41–47.

  • 69. Li Y Zhou C Huang M Luo J Hou X Wu P Ma X. Lead tolerance mechanism in Conyza canadensis: subcellular distribution ultra-structure antioxidative defense system and phytochelatins. J. Plant Res. 2016; 129: 251–262.

  • 70. Anjum NA Ahmad I Mohmood I Pacheco M Duarte AC Pereira E Umar S Ahmad A Khan NA Iqbal M Prasad MNV. Modulation of glutathione and its related enzymes in plants’ responses to toxic metals and metalloids – a review. Environ Exp Bot 2012; 75: 307–324.

  • 71. Strubińska J Hanaka A. Adventitious root system reduces lead up-take and oxidative stress in sunflower seedlings. Biol. Plant 2011; 55: 771.

  • 72. Ali B Mwamba TM Gill AR Yang C Ali S Daud MK Wu Y Zhou W. Improvement of element uptake and antioxidative defense in Brassica napus under lead stress by application of hydrogen sulfide. Plant Growth Regul 2014; 74: 261–273. DOI 10.1007/s10725-014-9917-9.

  • 73. Hattab S Hattab S Flores-Casseres ML Boussetta H Doumas P Hernandez LE Banni M. Characterisation of lead-induced stress molecular biomarkers in Medicago sativa plants. Environ. Exp. Bot. 2016; 123: 1–12.

Journal information
All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 79 79 36
PDF Downloads 60 60 21