Environmental Science and Pollution Research

, Volume 24, Issue 25, pp 20705–20716 | Cite as

Effects of Cd and Zn on physiological and anatomical properties of hydroponically grown Brassica napus plants

  • Martina Benáková
  • Hassan Ahmadi
  • Zuzana Dučaiová
  • Edita Tylová
  • Stephan Clemens
  • Jiří Tůma
Research Article


Clarifying the connection between metal exposure and anatomical changes represents an important challenge for a better understanding of plant phytoextraction potential. A hydroponic screening experiment was carried out to evaluate the effects of combined interactions of Cd and Zn on mineral uptake (Mg, K, Ca, Na) and on the physiological and anatomical characteristics of Brassica napus L cv. Cadeli, Viking, and Navajo. Plants were exposed to 5 μM Cd (CdCl2), 10 μM Zn (ZnSO4), or both Cd + Zn, for 14 days. Cadmium exposure led to a significant reduction in root growth, shoot biomass, and chlorophyll content. After Cd-only and Cd + Zn treatment, primary root tips became thicker and pericycle cells were enlarged compared to the control and Zn-only treatment. No differences between metals were observed under UV excitation, where all treatments showed more intensive autofluorescence connected with lignin/suberin accumulation compared to control conditions. The highest concentrations of Cd and Zn were found in the roots of all tested plants, and translocation factors did not exceed the threshold of 1.0. The root mineral composition was not affected by any treatment. In the shoots, the Mg concentration slightly increased after Cd-only and Cd + Zn treatments, whereas Zn-only treatment caused a sharp decrease in Ca content. Slight increases in K were seen after the addition of Zn. Significantly higher concentrations of Na were induced by Cd- or Zn-only treatment.


Brassica napus Cadmium uptake Mineral uptake Phytoextraction Root anatomy Zinc uptake 



This work was financially supported by the Particular Research Program SV 2103/2015, University of Hradec Kralove, and by the Czech Ministry of Education, Youth and Sports, Project LO1417.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.


  1. Abu-Muriefah SS (2008) Growth parameters and elemental status of cucumber (Cucumus sativus) seedlings in response to cadmium accumulation. Int J Agric Biol 10:261–266 Google Scholar
  2. Agar G, Taspinar M (2003) Effects of calcium, selenium and zinc on cadmium induced chromosomal aberration in roots of Secale cereale. Fresenius Environ Bull 12:1471–1475 Google Scholar
  3. Ali B, Wang B, Ali S et al (2013) 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. doi: 10.1007/s00344-013-9328-6 CrossRefGoogle Scholar
  4. Alkorta I, Epelde L, Mijangos I et al (2006) Bioluminescent bacterial biosensors for the assessment of metal toxicity and bioavailability in soils. Rev Environ Health 21:139–152. doi: 10.1515/REVEH.2006.21.2.139 CrossRefGoogle Scholar
  5. Aravind P, Prasad MNV (2003) Zinc alleviates cadmium-induced oxidative stress in Ceratophyllum demersum L.: a free floating freshwater macrophyte. Plant Physiol Biochem 41:391–397. doi: 10.1016/S0981-9428(03)00035-4 CrossRefGoogle Scholar
  6. Armstrong J, Armstrong W (2001) Rice and Phragmites: effects of organic acids on growth, root permeability, and radial oxygen loss to the rhizosphere. Am J Bot 88:1359–1370 CrossRefGoogle Scholar
  7. Armstrong J, Armstrong W (2005) Rice: sulfide-induced barriers to root radial oxygen loss, Fe2+ and water uptake, and lateral root emergence. Ann Bot 96:625–638. doi: 10.1093/aob/mci215 CrossRefGoogle Scholar
  8. Balen B, Tkalec M, Sikić S et al (2011) Biochemical responses of Lemna minor experimentally exposed to cadmium and zinc. Ecotoxicology 20:815–826. doi: 10.1007/s10646-011-0633-1 CrossRefGoogle Scholar
  9. Barker AV, Pilbeam DJ (2015) Handbook of plant nutrition, Second Edition. CRC Press. ISBN: 9781439881972Google Scholar
  10. Brown SL, Chaney RL, Angle JS et al (1998) The phytoavailability of cadmium to lettuce in long-term biosolids-amended soils. J Environ Qual. doi: 10.2134/jeq1998.00472425002700050012x
  11. Chaney RL (2010) Cadmium and zinc. In: Hooda PS (ed) Trace elements in soils. Wiley, Ltd, pp 409–439. ISBN: 9781405160377Google Scholar
  12. Cherif J, Mediouni C, Ben Ammar W et al (2011) Interactions of zinc and cadmium toxicity in their effects on growth and in antioxidative systems in tomato plants (Solanum lycopersicum). J Environ Sci (China) 23:837–844. doi: 10.1016/S1001-0742(10)60415-9 CrossRefGoogle Scholar
  13. Chibuike GU, Obiora SC (2014) Heavy metal polluted soils: effect on plants and bioremediation methods. Appl Environ Soil Sci 2014:12. doi: 10.1155/2014/752708 CrossRefGoogle Scholar
  14. Choppala G, Saifullah, Bolan N et al (2014) Cellular mechanisms in higher plants governing tolerance to cadmium toxicity. Crit Rev Plant Sci 33:374–391. doi: 10.1080/07352689.2014.903747 CrossRefGoogle Scholar
  15. Clemens S, Aarts MGM, Thomine S et al (2013) Plant science: the key to preventing slow cadmium poisoning. Trends Plant Sci 18:92–99. doi: 10.1016/j.tplants.2012.08.003 CrossRefGoogle Scholar
  16. Cojocaru P, Gusiatin ZM, Cretescu I (2016) Phytoextraction of Cd and Zn as single or mixed pollutants from soil by rape (Brassica napus). Environ Sci Pollut Res 23:10693–10701. doi: 10.1007/s11356-016-6176-5 CrossRefGoogle Scholar
  17. Courbot M, Willems G, Motte P et al (2007) A major quantitative trait locus for cadmium tolerance in Arabidopsis halleri colocalizes with HMA4, a gene encoding a heavy metal ATPase. Plant Physiol 144:1052–1065. doi: 10.1104/pp.106.095133 CrossRefGoogle Scholar
  18. Davis-Carter JG, Parker MB, Gaines TP (1991) Interaction of soil zinc, calcium, and pH with zinc toxicity in peanuts. In: Wright RJ, Baligar VC, Murrmann RP (eds) Plant-soil interactions at low pH. Springer Netherlands, pp 339–347. doi:  10.1007/978-94-011-3438-5_39
  19. Emamverdian A, Ding Y, Mokhberdoran F et al (2015) Heavy metal stress and some mechanisms of plant defense response. Sci World J 2015:e756120. doi: 10.1155/2015/756120 CrossRefGoogle Scholar
  20. Eren E, Argüello JM (2004) Arabidopsis HMA2, a divalent heavy metal-transporting P(IB)-type ATPase, is involved in cytoplasmic Zn2+ homeostasis. Plant Physiol 136:3712–3723. doi: 10.1104/pp.104.046292 CrossRefGoogle Scholar
  21. Fageria NK (2008) The use of nutrients in crop plants. CRC Press. ISBN: 9781420075106Google Scholar
  22. Hänsch R, Mendel RR (2009) Physiological functions of mineral micronutrients (Cu, Zn, Mn, Fe, Ni, Mo, B, Cl). Curr Opin Plant Biol 12:259–266. doi: 10.1016/j.pbi.2009.05.006 CrossRefGoogle Scholar
  23. Hassan MJ, Zhang G, Wu F et al (2005) Zinc alleviates growth inhibition and oxidative stress caused by cadmium in rice. J Plant Nutr Soil Sci 168:255–261. doi: 10.1002/jpln.200420403 CrossRefGoogle Scholar
  24. Hernández-Allica J, Becerril JM, Garbisu C (2008) Assessment of the phytoextraction potential of high biomass crop plants. Environ Pollut 152:32–40. doi: 10.1016/j.envpol.2007.06.002 CrossRefGoogle Scholar
  25. Jiang XJ, Luo YM, Liu Q et al (2004) Effects of cadmium on nutrient uptake and translocation by Indian mustard. Environ Geochem Health 26:319–324. doi: 10.1023/B:EGAH.0000039596.15586.b3 CrossRefGoogle Scholar
  26. Küpper H, Küpper F, Spiller M (1998) In situ detection of heavy metal substituted chlorophylls in water plants. Photosynth Res 58:123–133. doi: 10.1023/A:1006132608181 CrossRefGoogle Scholar
  27. Lalor GC (2008) Review of cadmium transfers from soil to humans and its health effects in the Jamaican environment. Sci Total Environ 400:162–172. doi: 10.1016/j.scitotenv.2008.07.011 CrossRefGoogle Scholar
  28. Laskowski MJ, Williams ME, Nusbaum HC, et al (1995) Formation of lateral root meristems is a two-stage process. Development 121:3303–3310. doi:
  29. Li X, Yang Y, Zhang J et al (2012) Zinc induced phytotoxicity mechanism involved in root growth of Triticum aestivum L. Ecotoxicol Environ Saf 86:198–203. doi: 10.1016/j.ecoenv.2012.09.021 CrossRefGoogle Scholar
  30. Lux A, Martinka M, Vaculik M et al (2011) Root responses to cadmium in the rhizosphere: a review. J Exp Bot 62:21–37. doi: 10.1093/jxb/erq281 CrossRefGoogle Scholar
  31. Maathuis FJM (2013) Sodium in plants: perception, signalling, and regulation of sodium fluxes. J Exp Bot 65:849–858. doi: 10.1093/jxb/ert326 CrossRefGoogle Scholar
  32. Marchiol L, Assolari S, Sacco P et al (2004) Phytoextraction of heavy metals by canola (Brassica napus) and radish (Raphanus sativus) grown on multicontaminated soil. Environ Pollut 132:21–27. doi: 10.1016/j.envpol.2004.04.001 CrossRefGoogle Scholar
  33. Mohamed AA, Castagna A, Ranieri A et al (2012) Cadmium tolerance in Brassica juncea roots and shoots is affected by antioxidant status and phytochelatin biosynthesis. Plant Physiol Biochem 57:15–22. doi: 10.1016/j.plaphy.2012.05.002 CrossRefGoogle Scholar
  34. Monteiro M, Santos C, Mann RM et al (2007) Evaluation of cadmium genotoxicity in Lactuca sativa L. using nuclear microsatellites. Environ Exp Bot 60:421–427. doi: 10.1016/j.envexpbot.2006.12.018 CrossRefGoogle Scholar
  35. Morel M, Crouzet J, Gravot A et al (2009) AtHMA3, a P1B-ATPase allowing Cd/Zn/Co/Pb vacuolar storage in Arabidopsis. Plant Physiol 149:894–904. doi: 10.1104/pp.108.130294 CrossRefGoogle Scholar
  36. Nan Z, Li J, Zhang J et al (2002) Cadmium and zinc interactions and their transfer in soil-crop system under actual field conditions. Sci Total Environ 285:187–195. doi: 10.1016/S0048-9697(01)00919-6 CrossRefGoogle Scholar
  37. Nikolic N, Pajevic S, Zupunski M et al (2014) Responses of wheat (Triticum aestivum L.) and maize (Zea mays L.) plants to cadmium toxicity in relation to magnesium nutrition. Acta Bot Croat 73:359–373. doi: 10.2478/botcro-2014-0014 Google Scholar
  38. Nouairi I, Ammar WB, Youssef NB et al (2006) Comparative study of cadmium effects on membrane lipid composition of Brassica juncea and Brassica napus leaves. Plant Sci 170:511–519. doi: 10.1016/j.plantsci.2005.10.003 CrossRefGoogle Scholar
  39. Nouairi I, Ammar WB, Youssef NB et al (2008) Antioxidant defense system in leaves of Indian mustard (Brassica juncea) and rape (Brassica napus) under cadmium stress. Acta Physiol Plant 31:237–247. doi: 10.1007/s11738-008-0224-9 CrossRefGoogle Scholar
  40. Oomen RJFJ, Wu J, Lelièvre F et al (2009) Functional characterization of NRAMP3 and NRAMP4 from the metal hyperaccumulator Thlaspi caerulescens. New Phytol 181:637–650. doi: 10.1111/j.1469-8137.2008.02694.x CrossRefGoogle Scholar
  41. Pandey N, Pathak GC, Sharma CP (2006) Zinc is critically required for pollen function and fertilisation in lentil. J Trace Elem Med Biol 20:89–96. doi: 10.1016/j.jtemb.2005.09.006 CrossRefGoogle Scholar
  42. Qadir S, Qureshi MI, Javed S et al (2004) Genotypic variation in phytoremediation potential of Brassica juncea cultivars exposed to Cd stress. Plant Sci 167:1171–1181. doi: 10.1016/j.plantsci.2004.06.018 CrossRefGoogle Scholar
  43. Rodríguez-Serrano M, Romero-Puertas MC, Zabalza A et al (2006) Cadmium effect on oxidative metabolism of pea (Pisum sativum L.) roots. Imaging of reactive oxygen species and nitric oxide accumulation in vivo. Plant Cell Environ 29:1532–1544. doi: 10.1111/j.1365-3040.2006.01531.x CrossRefGoogle Scholar
  44. Romero-Puertas MC, Palma JM, Gómez M et al (2002) Cadmium causes the oxidative modification of proteins in pea plants. Plant Cell Environ 25:677–686. doi: 10.1046/j.1365-3040.2002.00850.x CrossRefGoogle Scholar
  45. Roschzttardtz H, Conéjéro G, Curie C et al (2009) Identification of the endodermal vacuole as the iron storage compartment in the Arabidopsis embryo. Plant Physiol 151:1329–1338. doi: 10.1104/pp.109.144444 CrossRefGoogle Scholar
  46. Saifullah, Sarwar N, Bibi S et al (2014) Effectiveness of zinc application to minimize cadmium toxicity and accumulation in wheat (Triticum aestivum L.) Environ Earth Sci 71:1663–1672. doi: 10.1007/s12665-013-2570-1 CrossRefGoogle Scholar
  47. Shahid M, Dumat C, Khalid S, et al (2016) Cadmium bioavailability, uptake, toxicity and detoxification in soil-plant system. In: Reviews of environmental contamination and toxicology volume 241. Springer International Publishing, pp 73–137Google Scholar
  48. Sharma SS, Schat H, Vooijs R et al (1999) Combination toxicology of copper, zinc, and cadmium in binary mixtures: concentration-dependent antagonistic, nonadditive, and synergistic effects on root growth in Silene vulgaris. Environ Toxicol Chem 18:348–355. doi: 10.1002/etc.5620180235 CrossRefGoogle Scholar
  49. Siddiqui MH, Al-Whaibi MH, Sakran AM et al (2012) Effect of calcium and potassium on antioxidant system of Vicia faba L. under cadmium stress. Int J Mol Sci 13:6604–6619. doi: 10.3390/ijms13066604 CrossRefGoogle Scholar
  50. Simonova E, Henselova M, Masarovicova E et al (2007) Comparison of tolerance of Brassica juncea and Vigna radiata to cadmium. Biol Plant 51:488–492. doi: 10.1007/s10535-007-0103-z CrossRefGoogle Scholar
  51. Sinclair SA, Krämer U (2012) The zinc homeostasis network of land plants. Biochim Biophys Acta 1823:1553–1567. doi: 10.1016/j.bbamcr.2012.05.016 CrossRefGoogle Scholar
  52. Singh VP (2005) Toxic metals and environmental issues. Sarup & Sons. ISBN: 8176255491Google Scholar
  53. Solhi M, Shareatmadari H, Hajabbasi MA (2005) Lead and zinc extraction potential of two common crop plants, Helianthus annuus and Brassica napus. Water Air Soil Pollut 167:59–71. doi: 10.1007/s11270-005-8089-7 CrossRefGoogle Scholar
  54. Song Y, Jin L, Wang X (2017) Cadmium absorption and transportation pathways in plants. Int J Phytoremediation 19:133–141. doi: 10.1080/15226514.2016.1207598 CrossRefGoogle Scholar
  55. Sridhar BBM, Han FX, Diehl SV et al (2007) Effects of Zn and Cd accumulation on structural and physiological characteristics of barley plants. Braz J Plant Physiol 19:15–22. doi: 10.1590/S1677-04202007000100002 CrossRefGoogle Scholar
  56. Stoyanova Z, Doncheva S (2002) The effect of zinc supply and succinate treatment on plant growth and mineral uptake in pea plant. Braz J Plant Physiol 14:111–116. doi: 10.1590/S1677-04202002000200005 CrossRefGoogle Scholar
  57. Suzuki N (2005) Alleviation by calcium of cadmium-induced root growth inhibition in Arabidopsis seedlings. Plant Biotechnol 22:19–25. doi: 10.5511/plantbiotechnology.22.19 CrossRefGoogle Scholar
  58. Szulc PM, Kobierski M, Majtkowski W (2014) Evaluation of the use of spring rapeseed in phytoremediation of soils contaminated with trace elements and their effect on yield parameters. Plant Breed Seed Sci 69:81–95. doi: 10.1515/plass-2015-0008 Google Scholar
  59. Tammam AA, Hatata MM, Sadek OA (2016) Efect of Cd and Zn interaction on reactive oxygen species and antioxidant machinery of broad bean plants (Vicia faba L). Egypt J Exp Biol Bot 12:193–209. doi: 10.5455/egyjebb.20160819020621 Google Scholar
  60. Tang L, Qiu R, Tang Y et al (2014) Cadmium-zinc exchange and their binary relationship in the structure of Zn-related proteins: a mini review. Met Integr Biometal Sci 6:1313–1323. doi: 10.1039/c4mt00080c CrossRefGoogle Scholar
  61. Taspinar MS, Agar G, Alpsoy L et al (2011) The protective role of zinc and calcium in Vicia faba seedlings subjected to cadmium stress. Toxicol Ind Health 27:73–80. doi: 10.1177/0748233710381888 CrossRefGoogle Scholar
  62. Tkalec M, Stefanić PP, Cvjetko P et al (2014) The effects of cadmium-zinc interactions on biochemical responses in tobacco seedlings and adult plants. PLoS One 9:e87582. doi: 10.1371/journal.pone.0087582 CrossRefGoogle Scholar
  63. Touiserkani T, Haddad R (2012) Cadmium-induced stress and antioxidative responses in different Brassica napus cultivars. J Agric Sci Technol 14:929–937 Google Scholar
  64. Tran TA, Popova LP (2013) Functions and toxicity of cadmium in plants: recent advances and future prospects. Turk J Bot 37:1–13. doi: 10.3906/bot-1112-16 Google Scholar
  65. Turan M, Esringu A (2007) Phytoremediation based on canola (Brassica napus L.) and Indian mustard (Brassica juncea L.) planted on spiked soil by aliquot amount of Cd, Cu, Pb, and Zn. Plant Soil Environ 53:7 CrossRefGoogle Scholar
  66. Van Belleghem F, Cuypers A, Semane B et al (2007) Subcellular localization of cadmium in roots and leaves of Arabidopsis thaliana. New Phytol 173:495–508. doi: 10.1111/j.1469-8137.2006.01940.x CrossRefGoogle Scholar
  67. Vatehova Z, Kollarova K, Zelko I et al (2012) Interaction of silicon and cadmium in Brassica juncea and Brassica napus. Biologia 67:498–504. doi: 10.2478/s11756-012-0034-9 CrossRefGoogle Scholar
  68. Versieren L, Evers S, AbdElgawad H et al (2017) Mixture toxicity of copper, cadmium, and zinc to barley seedlings is not explained by antioxidant and oxidative stress biomarkers. Environ Toxicol Chem 36:220–230. doi: 10.1002/etc.3529 CrossRefGoogle Scholar
  69. Vig K, Megharaj M, Sethunathan N et al (2003) Bioavailability and toxicity of cadmium to microorganisms and their activities in soil: a review. Adv Environ Res 8:121–135. doi: 10.1016/S1093-0191(02)00135-1 CrossRefGoogle Scholar
  70. Wang H, Jin JY (2005) Photosynthetic rate, chlorophyll fluorescence parameters, and lipid peroxidation of maize leaves as affected by zinc deficiency. Photosynthetica 43:591–596. doi: 10.1007/s11099-005-0092-0 CrossRefGoogle Scholar
  71. Welch RM, Norvell WA (1999) Mechanisms of cadmium uptake, translocation and deposition in plants. In: McLaughlin MJ, Singh BR (eds) Cadmium in soils and plants. Springer, Dordrecht, pp 125–150. doi: 10.1007/978-94-011-4473-5_6
  72. Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313. doi: 10.1016/S0176-1617(11)81192-2 CrossRefGoogle Scholar
  73. White PJ, Broadley MR (2003) Calcium in plants. Ann Bot 92:487–511. doi: 10.1093/aob/mcg164 CrossRefGoogle Scholar
  74. Wojcik M, Tukiendorf A (2004) Phytochelatin synthesis and cadmium localization in wild type of Arabidopsis thaliana. Plant Growth Regul 44:71–80. doi: 10.1007/s10725-004-1592-9 CrossRefGoogle Scholar
  75. Wu F, Zhang G, Yu J (2003) Interaction of cadmium and four microelements for uptake and translocation in different barley genotypes. Commun Soil Sci Plant Anal 34:2003–2020. doi: 10.1081/CSS-120023233 CrossRefGoogle Scholar
  76. Yamaguchi N, Mori S, Baba K et al (2011) Cadmium distribution in the root tissues of solanaceous plants with contrasting root-to-shoot Cd translocation efficiencies. Environ Exp Bot 71:198–206. doi: 10.1016/j.envexpbot.2010.12.002 CrossRefGoogle Scholar
  77. Yan H, Filardo F, Hu X et al (2016) Cadmium stress alters the redox reaction and hormone balance in oilseed rape (Brassica napus L.) leaves. Environ Sci Pollut Res 23:3758–3769. doi: 10.1007/s11356-015-5640-y CrossRefGoogle Scholar
  78. Yang Y-J, Cheng L-M, Liu Z-H (2007) Rapid effect of cadmium on lignin biosynthesis in soybean roots. Plant Sci 172:632–639. doi: 10.1016/j.plantsci.2006.11.018 CrossRefGoogle Scholar
  79. Yu R, Ji J, Yuan X et al (2012) Accumulation and translocation of heavy metals in the canola (Brassica napus L.)—soil system in Yangtze River Delta, China. Plant Soil 353:33–45. doi: 10.1007/s11104-011-1006-5 CrossRefGoogle Scholar
  80. Zong H, Liu S, Xing R et al (2017) Protective effect of chitosan on photosynthesis and antioxidative defense system in edible rape (Brassica rapa L.) in the presence of cadmium. Ecotoxicol Environ Saf 138:271–278. doi: 10.1016/j.ecoenv.2017.01.009 CrossRefGoogle Scholar

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© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Department of Biology, Faculty of ScienceUniversity of Hradec KrálovéHradec KrálovéCzech Republic
  2. 2.Department of Plant PhysiologyUniversity of BayreuthBayreuthGermany
  3. 3.Department of Experimental Plant BiologyCharles UniversityPragueCzech Republic

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