Environmental Science and Pollution Research

, Volume 23, Issue 20, pp 20408–20430 | Cite as

Molybdenum (Mo) increases endogenous phenolics, proline and photosynthetic pigments and the phytoremediation potential of the industrially important plant Ricinus communis L. for removal of cadmium from contaminated soil

  • Fazal HadiEmail author
  • Nasir Ali
  • Michael Paul Fuller
Research Article


Cadmium (Cd) in agricultural soil negatively affects crops yield and compromises food safety. Remediation of polluted soil is necessary for the re-establishment of sustainable agriculture and to prevent hazards to human health and environmental pollution. Phytoremediation is a promising technology for decontamination of polluted soil. The present study investigated the effect of molybdenum (Mo) (0.5, 1.0 and 2.0 ppm) on endogenous production of total phenolics and free proline, plant biomass and photosynthetic pigments in Ricinus communis plants grown in Cd (25, 50 and 100 ppm) contaminated soils and the potential for Cd phytoextraction. Mo was applied via seed soaking, soil addition and foliar spray. Foliar sprays significantly increased plant biomass, Cd accumulation and bioconcentration. Phenolic concentrations showed significantly positive correlations with Cd accumulation in roots (R 2 = 0.793, 0.807 and 0.739) and leaves (R 2 = 0.707, 721 and 0.866). Similarly, proline was significantly positively correlated with Cd accumulation in roots (R 2 = 0.668, 0.694 and 0.673) and leaves (R 2 = 0.831, 0.964 and 0.930). Foliar application was found to be the most effective way to deliver Mo in terms of increase in plant growth, Cd accumulation and production of phenolics and proline.


Heavy metal Phytoextraction Foliar application of Mo Bioconcentration factor 



The Pakistan Science Foundation (PSF) is highly acknowledged for the full financial support. PSF has funded this project under Pak-US Natural Sciences Linkage Programme (NSLP) vide project No. PSF/NSLP/KP-UM (432).


  1. Ahmad A, Hadi F, Ali N (2015) Effective phytoextraction of cadmium (Cd) with increasing concentration of total phenolics and free proline in Cannabis sativa (L) plant under various treatments of fertilizers, plant growth regulators and sodium salt. Int J Phytoremed 17:56–65CrossRefGoogle Scholar
  2. Ali N, Hadi F (2015) Phytoremediation of cadmium improved with the high production of endogenous phenolics and free proline contents in Parthenium hysterophorus plant treated exogenously with plant growth regulator and chelating agent. Environ Sci Pollut Res 22:13305–13318CrossRefGoogle Scholar
  3. Allen SE (1974) Chemical Analysis of Ecological Materials. Blackwell Scientific, Oxford (London)Google Scholar
  4. Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water stress studies. J Plant Soil 39:205–207CrossRefGoogle Scholar
  5. Bavi K, Kholdebarin B, Moradshah A (2011) Effect of cadmium on growth, protein content and peroxidase activity in pea plants. Pak J Bot 43:1467–1470Google Scholar
  6. Bhattacharjee S, Mukherjee AK (1994) Influence of cadmium and lead on physiological and biochemical responses of Vigna unguiculata (L). Walp. Seedling germination behaviour, total protein, proline content and protease activity. Pollut Res 13:269–277Google Scholar
  7. Citterio S, Santagostino A, Fumagalli P, Prato N, Ranalli P, Sgorbati S (2003) Heavy metal tolerance and accumulation of Cd, Cr and Ni by Cannabis sativa L. Plant Soil 256:243–252CrossRefGoogle Scholar
  8. Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88:1707–1719CrossRefGoogle Scholar
  9. De B, Mukherjee AK (1998) Mercury induced metabolic changes in seedlings and cultured cells of tomato. Geobios 23:83–88Google Scholar
  10. Falkowska M, Pietryczuk A, Piotrowska A, Bajguz A, Grygoruk A, Czerpak R (2011) The effect of gibberellic acid (GA3) on growth, metal biosorption and metabolism of the green algae Chlorella vulgaris (chlorophyceae) Beijerinck exposed to cadmium and lead stress. Pol J Environ Stud 20:53–59Google Scholar
  11. Genrich I, Burd D, George D, Glick BR (2000) Plant growth promoting bacteria that decrease heavymetal toxicity in plants. Can J Microbiol 46:237–245CrossRefGoogle Scholar
  12. Gouia H, Ghorbala HH, Meyer C (2000) Effects of cadmium on activity of nitrate reductase and on other enzymes of the nitrate assimilation pathway in bean. Plant Physiol Biochem 38:629–638CrossRefGoogle Scholar
  13. Gupta UC (1997) Symptoms of molybdenum deficiency and toxicity in crops. In: Gupta UC (ed) Molybdenum in agriculture. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  14. Hadi F, Bano A (2009) Utilization of Parthenium hysterophorus for the remediation of lead-contaminated soil. Weed Biol Manag 9(4):307–314CrossRefGoogle Scholar
  15. Hadi F, Asghari B, Fuller MP (2010) The improved phytoextraction of lead (Pb) and the growth of maize (Zea mays L.): the role of plant growth regulators (GA3 and IAA) and EDTA alone and in combinations. Chemosphere 80:457–462CrossRefGoogle Scholar
  16. Hadi F, Ali N, Ahmad A (2014) Enhanced phytoremediation of cadmium-contaminated soil by Parthenium hysterophorus plant: effect of gibberellic acid (GA3) and synthetic chelator, alone and in combinations. Bioremed J 18(1):46–55CrossRefGoogle Scholar
  17. Handique GK, Handique AK (2009) Proline accumulation in lemongrass (Cymbopogon flexuosus Stapf.) due to heavy metal stress. J Environ Biol 30:299–302Google Scholar
  18. 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. African J Plant Sci 6:1–7Google Scholar
  19. Hesberg C, Haensch R, Mendel RR, Bittner F (2004) Tandem orientation of duplicated xanthine dehydrogenase genes from Arabidopsis thaliana. J Biol Chem 279:13547–13554CrossRefGoogle Scholar
  20. Hristozkova M, Geneva M, Stancheva I (2006) Response of pea plants (Pisum sativum L.) to reduced supply with molybdenum and copper. Int J Agric Biol 8(2):218–220Google Scholar
  21. Huang D, Zhang Y, Qi Y, Chen C, Weihong J (2008) Global DNA hypomethylation, rather than reactive oxygen species (ROS), a potential facilitator of cadmium-stimulated K562 cell proliferation. Toxicol Lett 179:43–47CrossRefGoogle Scholar
  22. John R, Ahmad P, Gadgil K, Sharma S (2009) Heavy metal toxicity: effect on plant growth, biochemical parameters and metal accumulation by Brassica juncea L. Intl J Agron Plant Prod 3:65–76Google Scholar
  23. Joseph P (2009) Mechanisms of cadmium carcinogenesis. Toxicol Appl Pharm 238:272–279CrossRefGoogle Scholar
  24. Kaiser BN, Gridley KL, Brady JN, Phillips T, Tyerman SD (2005) The role of molybdenum in agricultural plant production. Ann Bot 96:745–754CrossRefGoogle Scholar
  25. Kaznina NM, Laiidinen GF, Titov AF (2006) The effect of cadmium on shoot apicalmeristems of barley. Ontogenez 37:444–448Google Scholar
  26. Khatamipour M, Piri E, Esmaeilian Y, Tavassoli A (2011) Toxic effect of cadmium on germination, seedling growth and proline content of milk thistle (Silybum marianum). Ann Biol Res 2(5):527–532Google Scholar
  27. Krocova Z, Macela A, Kroca M, Hernychova L (2000) The immunomodulatory effect(s) of lead and cadmium on the cells of immune system in vitro. Toxicol in Vitro 14:33–40CrossRefGoogle Scholar
  28. Lalk I, Dorfling K (1985) Hardening, ABA, proline and freezing resistance in the winter wheat varieties. Physiol Plant 63:287–229CrossRefGoogle Scholar
  29. Linger P, Ostwald A, Haensler J (2005) Cannabis sativa L. growing on heavy metal contaminated soil: growth, cadmium uptake and photosynthesis. Biol Plant 49(4):567–576CrossRefGoogle Scholar
  30. Mendel RR, Haensch R (2002) Molybdoenzymes and molybdenum cofactor in plants. J Exp Bot 53:1689–1698CrossRefGoogle Scholar
  31. Michalak A (2006) Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. Pol J Environ Stud 15:523–530Google Scholar
  32. Rana M, Dhamija H, Prashar B, Sharma S (2012) Ricinus communis L.–a review. Int J Pharm Tech Res 4(4):1706–1711 Google Scholar
  33. Rix RM (1999) Annuals and biennials. Macmillan, London, p. 106Google Scholar
  34. Rogers NJ, Franklin NM, Apte SC, Batley GE (2007) The importance of physical and chemical characterization in nanoparticle toxicity studies. Integr Environ Assess Manag 3:303–304CrossRefGoogle Scholar
  35. Sagi M, Scazzocchio C, Fluhr R (2002) The absence of molybdenum cofactor sulfuration is the primary cause of the flacca phenotype in tomato plants. Plant J 31:305–317CrossRefGoogle Scholar
  36. Sakishima Y, Yamasaki H (2002) Lipid peroxidation induces by phenolics in conjunction with aluminium ions. Biol Plant 45:249–254CrossRefGoogle Scholar
  37. Sheirdil RA, Bashir K, Hayat R, Akhtar MS (2012) Effect of cadmium on soybean (Glycine max L) growth and nitrogen fixation. Afr J Biotechnol 11:1886–1891Google Scholar
  38. Singleton VL, Rossi JA (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am J Enol Vitic 16:144–158Google Scholar
  39. Sumanta N, Haque CI, Nishika J, Suprakash R (2014) Spectrophotometric analysis of chlorophylls and carotenoids from commonly grown fern species by using various extracting solvents. Res J Chem Sci 4(9):63–69Google Scholar
  40. Sun RL, Zhou QX, Sun FH, Jin CX (2007) Antioxidative defense and proline/phytochelatin accumulation in a newly discovered Cd-hyperaccumulator, Solanum nigrum. Environ Exp Bot 60:468–476CrossRefGoogle Scholar
  41. Takiguchi M, Achanzar W, Qu W, Li G, Waalkes M (2003) Effects of cadmium on DNA-(-cytosine-5) methyltransferase activity and DNA methylation status during cadmium induced cellular transformation. Exp Cell Res 286:355–365CrossRefGoogle Scholar
  42. Tassi E, Pouget J, Petruzzelli G, Barbafieri M (2008) The effects of exogenous plant growth regulators in the phytoextraction of heavy metals. Chemosphere 71:66–73CrossRefGoogle Scholar
  43. Uraguchi S, Watanabe I, Yoshitomi A, Kiyono M, Kuno K (2006) Characteristics of cadmium accumulation and tolerancein novel Cd-accumulating crops, Avena strigosa and Crotalaria juncea. J Exp Bot 57:2955–2965CrossRefGoogle Scholar
  44. Varalakshmi LR, Ganeshamurthy LN (2009) Effect of cadmium on plant biomass and cadmium accumulation in amaranthus (Amaranthus tricolor) cultivars. Indian J Agri Sci 79:226–250Google Scholar
  45. Williams RJ, Frausto da Silva JJR (2002) The involvement of molybdenum in life. Biochem Biophys Res Commun 292:293–299CrossRefGoogle Scholar
  46. Zadeh BM, Savaghebi-Firozabadi GR, Alikhani HA, Hosseini HM (2008) Effect of sunflower and Amaranthus culture and application of inoculants on phytoremediation of the soils contaminated with cadmium. Amer-Eurasian J Agric Environ Sci 4:93–103Google Scholar
  47. Zengin FK, Munzuroglu O (2006) Toxic effects of cadmium (Cd++) on metabolism of sunflower (Helianthus annuus L.) seedlings. Acta Agric Scand Sect B Plant Soil Sci 56:224–229Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Department of BiotechnologyUniversity of MalakandDir LowerPakistan
  2. 2.Department of Biotechnology and MicrobiologySarhad University of Science and Information TechnologyPeshawarPakistan
  3. 3.School of Biological SciencePlymouth UniversityDevonUK

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