Citric acid enhances the phytoextraction of chromium, plant growth, and photosynthesis by alleviating the oxidative damages in Brassica napus L.

Abstract

Chromium (Cr) toxicity is widespread in crops grown on Cr-contaminated soils and has become a serious environmental issue which requires affordable strategies for the remediation of such soils. This study was performed to assess the performance of citric acid (CA) through growing Brassica napus in the phytoextraction of Cr from contaminated soil. Different Cr (0, 100, and 500 μM) and citric acid (0, 2.5, and 5.0 mM) treatments were applied alone and in combinations to 4-week-old seedlings of B. napus plants in soil under wire house condition. Plants were harvested after 12 weeks of sowing, and the data was recorded regarding growth characteristics, biomass, photosynthetic pigments, malondialdehyde (MDA), electrolytic leakage (EL), antioxidant enzymes, and Cr uptake and accumulation. The results showed that the plant growth, biomass, chlorophyll contents, and carotenoid as well as soluble protein concentrations significantly decreased under Cr stress alone while these adverse effects were alleviated by application of CA. Cr concentration in roots, stem, and leaves of CA-supplied plant was significantly reduced while total uptake of Cr increased in all plant parts with CA application. Furthermore, in comparison with Cr treatments alone, CA supply reduced the MDA and EL values in both shoots and roots. Moreover, the activity of superoxide dismutase (SOD), guaiacol peroxidase (POD), catalase (CAT), and ascorbate peroxidase (APX) in shoots and roots markedly increased by 100 μM Cr exposure, while decreased at 500 μM Cr stress. CA application enhanced the activities of antioxidant enzymes compared to the same Cr treatment alone. Thus, the data indicate that exogenous CA application can increase Cr uptake and can minimize Cr stress in plants and may be beneficial in accelerating the phytoextraction of Cr through hyper-accumulating plants such as B. napus.

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References

  1. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    CAS  Article  Google Scholar 

  2. Ali S, Cai S, Zeng F, Qiu B, Zhang G (2012) Effect of salinity and hexavalent chromium stresses on uptake and accumulation of mineral elements in barley genotypes differing in salt tolerance. J Plant Nutr 35:827–839

    CAS  Article  Google Scholar 

  3. Ali S, Farooq MA, Jahangir MM, Abbas F, Bharwana SA, Zhang GP (2013a) Effect of chromium and nitrogen form on photosynthesis and anti-oxidative system in barley. Biol Plant 57:785–791

    Article  Google Scholar 

  4. Ali B, Wang B, Ali S, Ghani MA, Hayat MT, Yang C, Xu L, Zhou WJ (2013b) 5-Aminolevulinic acid ameliorates the growth, photosynthetic gas exchange capacity, and ultrastructural changes under cadmium stress in Brassica napus L. J Plant Growth Regul 32:604–614

    CAS  Article  Google Scholar 

  5. Anwaar SA, Ali S, Ali S, Ishaque W, Farid M, Farooq MA, Sharif M (2015) Silicon (Si) alleviates cotton (Gossypium hirsutum L.) from zinc (Zn) toxicity stress by limiting Zn uptake and oxidative damage. Environ Sci Pollut Res 22:3441–3450

    CAS  Article  Google Scholar 

  6. Anwer S, Ashraf MY, Hussain M, Ashraf M, Jamil A (2012) Citric acid mediated phytoextraction of cadmium by maize (Zea mays L.). Pak J Bot 44:1831–1836

    CAS  Google Scholar 

  7. Araújo JCT, Nascimento CWA (2010) Phytoextraction of lead from soil from a battery recycling site: the use of citric acid and NTA. Water Air Soil Pollut 211:113–120

    Article  Google Scholar 

  8. Bareen FE (2012) Chelate assisted phytoextraction using oilseed brassicas. Environ Pollut 21:289–311

    Article  Google Scholar 

  9. Boonyapookana B, Parkpian P, Techapinyawat S, Delaune RD, Jugsujinda A (2005) Phytoaccumulation of lead by Sunflower (Helianthus annus), Tobacco (Nicotianatabacum), and Vetiver (Vetiveriazizanioides). J Environ Sci Health 40:117–137

    Article  Google Scholar 

  10. Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    CAS  Article  Google Scholar 

  11. Chigbo C, Batty L (2013) Effect of EDTA and citric acid on phytoremediation of Cr-B [a] P-co-contaminated soil. Environ Sci Pollut Res 20:8955–8963

    CAS  Article  Google Scholar 

  12. Das BC, Panda A, Sahoo PK, Jena S, Padhi P (2014) Effect of chromium (VI) on wheat seedlings and the role of chelating agents. Curr Sci 106:1387–1395

    CAS  Google Scholar 

  13. Dhindsa RS, Plumb-Dhindsa P, Thorne TA (1981) Leaf senescence correlated with increased levels of membrane permeability and lipid peroxidation and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–101

    CAS  Article  Google Scholar 

  14. Dionisio-Sese ML, Tobita S (1998) Antioxidant responses of rice seedlings to salinity stress. Plant Sci 135:1–9

    CAS  Article  Google Scholar 

  15. Diwan H, Ahmad A, Iqbal M (2008) Genotypic variation in the phytoremediation potential of Indian mustard for chromium. Environ Manag 41:734–741

    Article  Google Scholar 

  16. Ehsan S, Ali S, Noureen S, Farid M, Shakoor MB, Aslam A, Bharwana SA, Tauqeer HM (2013) Comparative assessment of different heavy metals in urban soil and vegetables irrigated with sewage/industrial waste water. Ecoterra 35:37–53

    Google Scholar 

  17. Ehsan S, Ali S, Noureen S, Mehmood K, Farid M, Ishaque W, Shakoor MB, Rizwan M (2014) Citric acid assisted phytoremediation of Cd by Brassica napus L. Ecotoxicol Environ Saf 106:164–172

    CAS  Article  Google Scholar 

  18. Evangelou M, Ebel M, Schaeffer A (2007) Chelate assisted phytoextraction of heavy metals from soil. Effect, mechanism, toxicity and fate of chelating agents. Chemosphere 68:989–1003

    CAS  Article  Google Scholar 

  19. Farooq MA, Ali S, Hameed A, Ishaque W, Mahmood K, Iqbal Z (2013) Alleviation of cadmium toxicity by silicon is related to elevated photosynthesis, antioxidant enzymes; suppressed cadmium uptake and oxidative stress in cotton. Ecotoxicol Environ Saf 96:242–249

    CAS  Article  Google Scholar 

  20. Freitas EVS, Nascimento CWA, Silva Sousa A, Silva FB (2013) Citric acid-assisted phytoextraction of lead: a field experiment. Chemosphere 92:213–217

    CAS  Article  Google Scholar 

  21. Gill RA, Zang L, Ali B, Farooq MA, Cui P, Yang S, Ali S, Zhou W (2015) Chromium-induced physio-chemical and ultrastructural changes in four cultivars of Brassica napus L. Chemosphere 120:154–164

    CAS  Article  Google Scholar 

  22. Gunawardana B, Singhal N, Johnson A (2011) Effects of amendments on copper, cadmium, and lead phytoextraction by Lolium perenne from multiple-metal contaminated solution. Int J Phytorem 13:215–232

    CAS  Article  Google Scholar 

  23. Habiba U, Ali S, Farid M, Shakoor MB, Rizwan M, Ibrahim M, Abbasi GH, Hayat T, Ali B (2015) EDTA enhanced plant growth, antioxidant defence system and phytoextraction of copper by Brassica napus L. Environ Sci Pollut Res 22:1534–1544

    CAS  Article  Google Scholar 

  24. Haouari CC, Nasraoui AH, Bouthour D, Houda MD, Daieb CB, Mnai J, Gouia H (2012) Response of tomato (Solanum lycopersicon) to cadmium toxicity: growth, element uptake, chlorophyll content and photosynthesis rate. Afr J Plant Sci 6:1–7

    CAS  Google Scholar 

  25. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    CAS  Article  Google Scholar 

  26. Kanwal U, Ali S, Shakoor MB, Farid M, Hussain S, Yasmeen T, Adrees M, Bharwana SA, Abbas F (2014) EDTA ameliorates phytoextraction of lead and plant growth by reducing morphological and biochemical injuries in Brassica napus L. under lead stress. Environ Sci Pollut Res 21:9899–9910

    CAS  Article  Google Scholar 

  27. Katz SA, Salem H (1994) The biological and environmental chemistry of chromium. VCH Publishers, New York

    Google Scholar 

  28. Laaniste P, Joudu J, Eremeev V (2004) Oil content of spring oilseed rape seeds according to fertilization. Agron Res 2:83–86

    Google Scholar 

  29. Lesage E, Meers E, Vervaeke P, Lamsal S, Hopgood M, Tack FMG, Verloo MG (2005) Enhanced phytoextraction: II. Effect of EDTA and citric acid on heavy metal uptake by Helianthus annuus from a calcareous soil. Int J Phytorem 7:143–152

    CAS  Article  Google Scholar 

  30. Lichtenthaler HK (1987) Chlorophyll and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:331–382

    Google Scholar 

  31. Mahmood T, Ejaz-ul-Hasan MA, Hussain M (2012) Faisal canola: a new high yielding canola variety for general cultivation in Punjab. J Agric Res 50:321–328

    Google Scholar 

  32. Meers E, Lesage E, Lamsal S, Hopgood M, Vervaeke P, Tack FMG, Verloo MG (2005) Enhanced phytoextraction: I. Effect of EDTA and citric acid on heavy metal mobility in a calcareous soil. Int J Phytorem 7:129–142

    CAS  Article  Google Scholar 

  33. Melo EEC, Guilherme LRG, Nascimento CWA, Penha HGV (2012) Availability and accumulation of arsenic in oilseeds grown in contaminated soils. Water Air Soil Pollut 223:233–240

    CAS  Article  Google Scholar 

  34. Meng H, Hua S, Shamsi IH, Jilani G, Li Y, Jiang L (2009) Cd-induced stress on the seed germination and seedling growth of Brassica napus L. and its alleviation through exogenous plant growth regulators. Plant Growth Regul 58:47–59

    CAS  Article  Google Scholar 

  35. Metzner H, Rau R, Senger H (1965) Untersuchungen zur synchronisierbarkeit einzelner pigmentmangel-mutanten von Chlorella. Planta 65:186–194

    CAS  Article  Google Scholar 

  36. Mishra S, Srivastava S, Tripathi RD, Govindarajan R, Kuriakose SC, Prasad MNV (2006) Phytochelatin synthesis and response of antioxidants during cadmium stress in Bacopa monnieri L. Plant Physiol Biochem 44:25–37

    CAS  Article  Google Scholar 

  37. Mittler R, Vanderauwera S, Gollery M, Breusegem FV (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498

    CAS  Article  Google Scholar 

  38. Muhammad D, Chen F, Zhao J, Zhang G, Wu F (2009) Comparison of EDTA- and citric acid-enhanced phytoextraction of heavy metals in artificially metal contaminated soil by Typha angustifolia. Int J Phytorem 11:558–574

    CAS  Article  Google Scholar 

  39. Najeeb U, Xu L, Ali S, Jilani G, Gong HJ, Shen WQ, Zhou WJ (2009) Citric acid enhances the phytoextraction of manganese and plant growth by alleviating the ultrastructural damages in Juncus effuses L. J Hazard Mater 170:1156–1163

    CAS  Article  Google Scholar 

  40. Najeeb U, Jilani G, Ali S, Sarwar M, Xu L, Zhou WJ (2011) Insight into cadmium induced physiological and ultra-structural disorders in Juncus effusus L. and its remediation through exogenous citric acid. J Hazard Mater 186:565–574

    CAS  Article  Google Scholar 

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

    CAS  Google Scholar 

  42. Park H, McGinn PJ, Morel FMM (2008) Expression of cadmium carbonic anhydrase of diatoms in seawater. Aquat Microb Ecol 51:183–193

    Article  Google Scholar 

  43. Raziuddin F, Hassan G, Akmal M, Shah SS, Mohammad F, Shafi M, Bakht J, Zhou W (2011) Effects of cadmium and salinity on growth and photosynthesis parameters of Brassica species. Pak J Bot 43:333–340

    CAS  Google Scholar 

  44. Rodriguez E, Santos C, Azevedo R, Moutinho-Pereira J, Correia C, Dias MC (2012) Chromium (VI) induces toxicity at different photosynthetic levels in pea. Plant Physiol Biochem 53:94–100

    CAS  Article  Google Scholar 

  45. Schiavon M, Pilon-Smits EA, Wirtz M, Hell R, Malagoli M (2008) Interactions between chromium and sulfur metabolism. J Environ Qual 37:1536–1545

    CAS  Article  Google Scholar 

  46. Schiavon M, Galla G, Wirtz M, Pilon-Smits EA, Telatin V, Quaggiotti S, Malagoli M (2012) Transcriptome profiling of genes differentially modulated by sulfur and chromium identifies potential targets for phytoremediation and reveals a complex S–Cr interplay on sulfate transport regulation in B. juncea. J Hazard Mater 239:192–205

    Article  Google Scholar 

  47. Sharma P, Pandey S (2014) Status of phytoremediation in world scenario. Int J Environ Bioremed Biodeg 2:178–191

    Google Scholar 

  48. Singh HP, Mahajan P, Kaur S, Batish DR, Kohli RK (2013) Chromium toxicity and tolerance in plants. Environ Chem Lett 11:229–254

    CAS  Article  Google Scholar 

  49. Su DC, Wong JWC (2004) Selection of mustard oilseed rape (Brassica juncea l.) for phytoremediation of cadmium contaminated soil. Bull Environ Contam Toxicol 72:991–998

    CAS  Article  Google Scholar 

  50. Szczygłowska M, Piekarska A, Konieczka P, Namiesnik J (2011) Use of brassica plants in the phytoremediation and biofumigation processes. Int J Mol Sci 12:7760–7771

    Article  Google Scholar 

  51. Tsetimi GO, Okieimen FE (2011) Chelate-assisted phytoextraction of metals from chromated copper arsenate (CCA) contaminated soil. J Environ Chem Ecotoxicol 3:214–224

  52. Vamerali T, Bandiera M, Mosca G (2010) Field crops for phytoremediation of metal-contaminated land. Environ Chem Lett 8:1–17

    CAS  Article  Google Scholar 

  53. Yeh TY, Pan CT (2012) Effect of chelating agents on copper, zinc, and lead uptake by sunflower, Chinese cabbage, cattail, and reed for different organic contents of soils. J Environ Anal Toxicol 2:2161–0525

  54. Zeng F, Zhou W, Qiu B, Ali S, Wu F, Zhang G (2011) Subcellular distribution and chemical forms of chromium in rice plants suffering from different levels of chromium toxicity. J Plant Nutr Soil Sci 174:249–256

    CAS  Article  Google Scholar 

  55. Zhang J, Kirkham MB (1994) Drought-stress induced changes in activities of superoxide dismutase, catalase and peroxidases in wheat leaves. Plant Cell Physiol 35:785–791

    CAS  Google Scholar 

  56. Zhang XZ (1992) The measurement and mechanism of lipid peroxidation and SOD POD and CAT activities in biological system. In: Zhang XZ (ed) Research Methodology of Crop Physiology, Beijing Agriculture Press, pp 208–211

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Acknowledgments

Authors thank the Higher Education Commission of Pakistan for the financial support. The results presented in this paper are a part of MPhil studies of Sehar Afshan.

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Correspondence to Shafaqat Ali.

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Responsible editor: Elena Maestri

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Afshan, S., Ali, S., Bharwana, S.A. et al. Citric acid enhances the phytoextraction of chromium, plant growth, and photosynthesis by alleviating the oxidative damages in Brassica napus L.. Environ Sci Pollut Res 22, 11679–11689 (2015). https://doi.org/10.1007/s11356-015-4396-8

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Keywords

  • Biomass
  • Brassica napus
  • Chromium
  • Citric acid
  • Electrolyte leakage
  • Guaiacol peroxidase
  • Phytoextractions