Environmental Science and Pollution Research

, Volume 25, Issue 31, pp 31737–31751 | Cite as

Micro-edaphic factors affect intra-specific variations in trace element profiles of Noccaea praecox on ultramafic soils

  • Tomica MišljenovićEmail author
  • Ksenija Jakovljević
  • Slobodan Jovanović
  • Nevena Mihailović
  • Boško Gajić
  • Gordana Tomović
Research Article


The aim of this study was to compare trace element profiles of Noccaea praecox (Wulfen) F. K. Mey. growing on ultramafic soils in different habitat types and to observe differences in uptake and translocation of trace elements. Physico-chemical characteristics of the soil and concentrations of P2O5, K2O, Ca, Fe, Mn, Zn, Cu, Ni, Cr, Pb, Cd, and Co in plant samples were presented. Biological concentration, accumulation, and translocation factors were calculated to estimate accumulation potential of different N. praecox accessions. All of the studied accessions were Ni hyperaccumulators (with shoot concentrations up to 14,593 mg kg−1), but with notable differences in accumulation and translocation rates. Significant differences in accumulation and translocation patterns of trace elements were observed among accessions from habitats characterized as serpentine steppes on dry, shallow soils in contrast to the accessions from habitats with higher soil moisture, and higher content of organic matter.


Brassicaceae Serpentine soils Hyperaccumulators Heavy metals Nickel 



The authors are very grateful to the editors and anonymous reviewers for their assistance and valuable suggestions, which were helpful in improving the quality of this manuscript.

Funding information

The Ministry of Education, Science and Technological Development of the Republic of Serbia supported this research through Grants 173030 and III 43009.

Supplementary material

11356_2018_3125_MOESM1_ESM.pdf (206 kb)
Online Resource 1 Noccaea praecox a) voucher specimen from Mt. Maljen (SP6); and b) plant sample from SP2. (PDF 206 kb)
11356_2018_3125_MOESM2_ESM.pdf (99 kb)
Online Resource 2 Concentrations of P2O5, K2O, Ca, Mg, Ca/Mg, Fe, Mn, Zn, Cu, Ni, Cr, Pb, Cd, and Co given as mean ± standard deviation in roots and shoots of Noccaea praecox from 6 sites on Mt. Maljen (mg kg−1). *Different letters indicate significant differences using the Dunn’s post hoc procedure. p values <0.05 are marked bold (PDF 98 kb)


  1. Alexander EB (2009) Soil and vegetation differences from peridotite to serpentinite. Northeast Nat 16(5):178–192CrossRefGoogle Scholar
  2. Alves S, Trancoso MA, Gonçalves MDLS, dos Santos MMC (2011) A nickel availability study in serpentinised areas of Portugal. Geoderma 164(3–4):155–163CrossRefGoogle Scholar
  3. Assunção AGL, Bookum WM, Nelissen HJM, Vooijs R, Schat H, Ernst WHO (2003a) Differential metal-specific tolerance and accumulation patterns among Thlaspi caerulescens populations originating from different soil types. New Phytol 159:411–419. CrossRefGoogle Scholar
  4. Assunção AGL, Schat H, Aarts MGM (2003b) Thlaspi caerulescens, an attractive model species to study heavy metal hyperaccumulation in plants. New Phytol 159(2):351–360CrossRefGoogle Scholar
  5. Baker AJM (1981) Accumulators and excluders-strategies in the response of plants to heavy metals. J Plant Nutr 3(1–4):643–654CrossRefGoogle Scholar
  6. Baker AJM, Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metallic elements – a review of their distribution, ecology and phytochemistry. Biorecovery 1:81–126Google Scholar
  7. Baker AJM, Walker PL (1990) Ecophysiology of metal uptake by tolerant plants. In: Shaw AJ (ed) Heavy metal tolerance in plants. CRC Press, Boca Raton, pp 155–177Google Scholar
  8. Baker AJM, Reeves RD, Hajar ASM (1994) Heavy metal accumulation and tolerance in British population of the metallophyte Thlaspi caerulescens J. & C. Presl (Brassicaceae). New Phytol 127:61–68CrossRefGoogle Scholar
  9. Baker AJM, McGrath SP, Reeves RD, Smith JAC (2000) Metal hyperaccumulator plants: a review of the ecology and physiology of a biological resource for phytoremediation of metal-polluted soils. In: Terry N, Banuelos G (eds) Phytoremediation of contaminated soils and water. CRC Press, Boca Raton, pp 171–188Google Scholar
  10. Bani A, Pavlova D, Echevarria G, Mullaj A, Reeves RD, Morel J-L, Sulçe S (2010) Nickel hyperaccumulation by the species of Alyssum and Thlaspi (Brassicaceae) from the ultramafic soils of the Balkans. Bot Serb 34:3–14Google Scholar
  11. Bani A, Echevarria G, Montargès-Pelletier E, Gjoka F, Sulçe S, Morel JL (2014) Pedogenesis and nickel biogeochemistry in a typical Albanian ultramafic toposequence. Environ Monit Assess 186(7):4431–4442CrossRefGoogle Scholar
  12. Bini C, Maleci L, Wahsha M (2016) Potentially toxic elements in serpentine soils and plants from Tuscany (Central Italy). A proxy for soil remediation. Catena. CrossRefGoogle Scholar
  13. Boyd R, Martens S (1998) Nickel hyperaccumulation by Thlaspi montanum var. montanum (Brassicaceae): a constitutive trait. Am J Bot 85(2):259–265CrossRefGoogle Scholar
  14. Brady UK, Kruckeberg RA, Bradshaw HD Jr (2005) Evolutionary ecology of plant adaptation to serpentine soils. Annu Rev Ecol Evol Syst 36:243–266CrossRefGoogle Scholar
  15. Brooks RR (1987) Serpentine and its vegetation: a multidisciplinary approach. Dioscorides Press, PortlandGoogle Scholar
  16. Brooks RR (1994) Plants that hyperaccumulate heavy metals. In: Farago ME (ed) Plants and the chemical elements. VCH, Weinheim, pp 87–105CrossRefGoogle Scholar
  17. Brooks RR, Lee J, Reeves RD, Jaffre T (1977) Detection of nickeliferous rocks by analysis of herbarium specimens of indicator plants. J Geochem Explor 7:49–57CrossRefGoogle Scholar
  18. Chen PS Jr, Toribara TT, Warner H (1956) Microdetermination of phosphorus. Anal Chem 28:1756–1758. CrossRefGoogle Scholar
  19. Chen S, Sun L, Chao L, Zhou Q, Sun T (2009) Estimation of lead bioavailability in smelter-contaminated soils by single and sequential extraction procedure. Bull Environ Contam Toxicol 82(1):43–47CrossRefGoogle Scholar
  20. Clapham AR, Akeroyd JR (1993) Thlaspi L. In: Tutin TG, Burges NA, Chater AO, Edmondson JR, Heywood VH, Moore DM, Valentine DH, Walters SM, Webb DA (eds) Flora Europaea, vol 1. University Press, Cambridge, pp 384–388Google Scholar
  21. Davis RD, Beckett PHT, Wollan E (1978) Critical levels of twenty potentially toxic elements in young spring barley. Plant Soil 49:395–408. CrossRefGoogle Scholar
  22. Deng THB, Cloquet C, Tang YT, Sterckeman T, Echevarria G, Estrade N, Morel JL, Qiu RL (2014) Nickel and zinc isotope fractionation in hyperaccumulating and nonaccumulating plants. Environ Sci Technol 48(20):11926–11933CrossRefGoogle Scholar
  23. Deng THB, van der Ent A, Tang YT, Sterckeman T, Echevarria G, Morel J-L, Qiu RL (2018) Nickel hyperaccumulation mechanisms: a review on the current state of knowledge. Plant Soil 423:1–11CrossRefGoogle Scholar
  24. Ducić V, Milovanović M (2005) Klima Srbije. Zavod za udžbenike i nastavna sredstva, Beograd (in Serbian)Google Scholar
  25. Đurović S, Jakovljević K, Buzurović U, Niketić M, Mihailović N, Tomović G (2016) Differences in trace element profiles of three subspecies of Silene parnassica (Caryophyllaceae) growing on ophiolitic substrate. Aust J Bot 64(3):235–245Google Scholar
  26. Echevarria G (2018) Genesis and behaviour of ultramafic soils and consequences for nickel biogeochemistry. In: van der Ent A, Echevarria G, Baker AJM, Morel JL (eds) Agromining: farming for metals. extracting unconventional resources using plants, Mineral resources series. Springer International Publishing AG, pp 135–156Google Scholar
  27. Egner H, Riehm H, Domingo WR (1960) Untersuchungen uber die chemische Bodenanalyse als Grundlage fur die Beurteilung des Nahrstoffzustandes der Boden II. Chemische Extractionmetoden zu Phosphor- und Kaliumbestimmung, Kunlinga Landboukshogskolans Annaler 26:199–215 (in German)Google Scholar
  28. Escarré J, Lefèbvre C, Gruber W, Leblanc M, Lepart J, Rivière Y, Delay B (2000) Zinc and cadmium hyperaccumulation by Thlaspi caerulescens from metalliferous and non-metalliferous sites in the Mediterranean area: implication for phytoremediation. New Phytol 145:429–437CrossRefGoogle Scholar
  29. FAO (1974) The Euphrates pilot irrigation project. Methods of soil analysis. Gadeb soil laboratory (a laboratory manual). Food and Agriculture OrganizationGoogle Scholar
  30. Filipović I, Pavlović Z, Marković B, Radin V, Marković O, Gagić N, Atin B, Milićević M (1967-1971) Geological map sheet Gornji Milanovac 1:100 000. Geologic map of Yugoslavia. Federal Geological Institute, BelgradeGoogle Scholar
  31. Ghaderian SM, Mohtadi A, Rahiminejad MR, Baker AJM (2007) Nickel and other metal uptake and accumulation by species of Alyssum (Brassicaceae) from the ultramafics of Iran. Environ Pollut 145:293–298CrossRefGoogle Scholar
  32. Grupe M, Kuntze H (1988) Zur Ermittlung der Schwermetallverfügbarkeit lithogen und anthropogen belasteter Standorte. 1. Cd und Cu, Z. Z Pflanzenernaehr Bodenkd 151:319–324 (in German)CrossRefGoogle Scholar
  33. Gupta AK, Sinha S (2006) Chemical fractionation and heavy metal accumulation in the plant of Sesamum indicum (L.) var. T55 grown on soil amended with tannery sludge: selection of single extractants. Chemosphere 64(1):161–173CrossRefGoogle Scholar
  34. Gupta KD, Corpas JF, Palma MJ (eds) (2013) Heavy metal stress in plants. Springer-Verlag, BerlinGoogle Scholar
  35. Hijmans RJ, Guarino L, Mathur P (2012) DIVA-GIS version 7.5. Accessed 10 Jan 2017
  36. Hobbs RJ, Streit B (1986) Heavy metal concentrations in plants growing on a copper mine spoil in the grand canyon, Arizona. Am Midl Nat 115:277–281CrossRefGoogle Scholar
  37. ISO 11466 (1995) International standard. Soil quality—extraction of trace elements soluble in aqua regia, 03–01Google Scholar
  38. ISO 6636/2 (1981) International standard. Fruits, vegetables and derived products—determination of zinc content—part 2: atomic absorption spectrometric methodGoogle Scholar
  39. Jakovljević K, Buzurović U, Andrejić G, Ðurović S, Niketić M, Mihailović N, Tomović G (2015) Trace elements contents and accumulation in soils and plant species Goniolimon tataricum (L.) Boiss. (Plumbaginaceae) from the ultramafic and dolomitic substrates of the Central Balkans. Carpathian J Earth Environ Sci 10:147–160Google Scholar
  40. James BR, Barlett RJ (1983) Behavior of chromium in soils VII adsorption and reduction of hexavalent forms. J Environ Qual 12:177–181CrossRefGoogle Scholar
  41. Jones JB (1997) Plant nutrition manual. CRC Press, Boca RatonGoogle Scholar
  42. Kabata-Pendias A (2011) Trace elements in soils and plants, 4th edn. CRC Press, Boca RatonGoogle Scholar
  43. Kaiser HF, Rice J (1974) Little jiffy, mark IV. Educ Psychol Meas 34:111–117CrossRefGoogle Scholar
  44. Kazakou E, Dimitrakopoulos PG, Baker AJM, Reeves RD, Troumbis AY (2008) Hypotheses, mechanisms and trade-offs of tolerance and adaptation to serpentine soils: from species to ecosystem level. Biol Rev 83:495–508Google Scholar
  45. Kazakou E, Adamidis GC, Baker AJ, Reeves RD, Godino M, Dimitrakopoulos PG (2010) Species adaptation in serpentine soils in Lesbos Island (Greece): metal hyperaccumulation and tolerance. Plant Soil 332(1–2):369–385CrossRefGoogle Scholar
  46. Kierczak J, Neel C, Bril H, Puziewicz J (2007) Effect of mineralogy and pedoclimatic variations on Ni and Cr distribution in serpentine soils under temperate climate. Geoderma 142(1–2):165–177CrossRefGoogle Scholar
  47. Kierczak J, Pędziwiatr A, Waroszewski J, Modelska M (2016) Mobility of Ni, Cr and co in serpentine soils derived on various ultrabasic bedrocks under temperate climate. Geoderma 268:78–91CrossRefGoogle Scholar
  48. Košanin O, Gajić B (2008) Karakteristike nekih serpentinskih zemljišta u sastojinama crnog bora na području Divčibare-Bukovi. Šumarstvo 4:89–98 (in Serbian)Google Scholar
  49. Kramer U (2010) Metal Hyperaccumulation in plants. Annu Rev Plant Biol 61:517–534CrossRefGoogle Scholar
  50. Kruckeberg AR (1967) Ecotypic response to ultramafic soils by some plant species of northwestern United States. Brittonia 19(2):133–151CrossRefGoogle Scholar
  51. Kruckeberg AR (1984) California’s serpentine. Fremontia 11:1–17Google Scholar
  52. Likar M, Pongrac P, Vogel-Mikuš K, Regvar M (2010) Molecular diversity and metal accumulation of different Thlaspi praecox populations from Slovenia. Plant Soil 330:195–205CrossRefGoogle Scholar
  53. Macnair MR (2003) The hyperaccumulation of metals by plants. Adv Bot Res 40:63–105CrossRefGoogle Scholar
  54. Malik RN, Husain SZ, Nazir I (2010) Heavy metal contamination and accumulation in soil and wild plant species from industrial area of Islamabad, Pakistan. Pak J Bot 42(1):291–301Google Scholar
  55. Manouchehri N, Bermond A (2009) EDTA in soil science: a review of its application in soil trace metal studies. TAET 3:1–15Google Scholar
  56. Matko Stamenković U, Andrejić G, Mihailović N, Šinžar-Sekulić J (2017) Hyperaccumulation of Ni by Alyssum murale Waldst. & kit. From ultramafics in Bosnia and Herzegovina. Appl Ecol Environ Res 15(3):359–372CrossRefGoogle Scholar
  57. McGrath D (1996) Application of single and sequential extraction procedures to polluted and unpolluted soils. Sci Total Environ 178(1):37–44CrossRefGoogle Scholar
  58. McKeague JA (1978) Manual on soil sampling and methods of analysis. Canadian Society of Soil ScienceGoogle Scholar
  59. Micó C, Recatalá L, Peris M, Sánchez J (2006) Assessing heavy metal sources in agricultural soils of an European Mediterranean area by multivariate analysis. Chemosphere 65(5):863–872CrossRefGoogle Scholar
  60. Milić S, Vasin J, Ninkov J, Zeremski T, Brunet B, Sekulić P (2011) Fertility of privately owned Plowland used for field crop production in Vojvodina. Serbia. Field Veg Crop Res 48:359–368Google Scholar
  61. Mojsilović S, Filipović I, Baklajić D, Đoković I, Navala M (1971) Geological map sheet Valjevo 1:100 000. Geologic map of Yugoslavia. Federal Geological Institute, BelgradeGoogle Scholar
  62. Nagajyoti PC, Lee KD, Sreekanth TVM (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8(3):199–216CrossRefGoogle Scholar
  63. O’Dell RE, Rajakaruna N (2011) Intraspecific variation, adaptation, and evolution. In: Harrison SP, NRajakaruna N (eds) Serpentine: evolution and ecology in a model system. University of California Press, Berkeley, pp 97–137Google Scholar
  64. Pędziwiatr A, Kierczak J, Waroszewski J, Ratié G, Quantin C, Ponzevera E (2018) Rock-type control of Ni, Cr, and co phytoavailability in ultramafic soils. Plant Soil 423(1–2):339–362CrossRefGoogle Scholar
  65. Pongrac P, Zhao FJ, Razinger J, Zrimec A, Regvar M (2009) Physiological responses to cd and Zn in two cd/Zn hyperaccumulating Thlaspi species. Environ Exp Bot 66:479–486CrossRefGoogle Scholar
  66. Raskin I, Kumar PN, Dushenkov S, Salt DE (1994) Bioconcentration of heavy metals by plants. Curr Opin Biotechnol 5(3):285–290CrossRefGoogle Scholar
  67. Reeves RD (2006) Hyperaccumulation of trace elements by plants. In: Morel J-L, Echevarria G, Goncharova N (eds) Phytoremediation of metal-contaminated soils. Springer, Dordrecht, pp 25–52CrossRefGoogle Scholar
  68. Reeves RD, Baker AJM (2000) Metal-accumulating plants. In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals: using plants to clean up the environment. Wiley, New York, pp 193–229Google Scholar
  69. Reeves RD, Brooks RR (1983a) European species of Thlaspi L. (Cruciferae) as indicators of nickel and zinc. J Geochem Explor 18:275–283CrossRefGoogle Scholar
  70. Reeves RD, Brooks RR (1983b) Hyperaccumulation of lead and zinc by two metallophytes from mining areas of Central Europe. Environ Pollut 31:277–285CrossRefGoogle Scholar
  71. Reeves RD, Baker AJM, Borhidi A, Berazain R (1999) Nickel hyperaccumulation in the serpentine flora of Cuba. Ann Bot 83:29–38CrossRefGoogle Scholar
  72. Reeves RD, Schwartz C, Morel J-L, Edmondson J (2001) Distribution and metal-accumulating behavior of Thlaspi caerulescens and associated Metallophytes in France. Int J Phytoremediation 3:1–28. CrossRefGoogle Scholar
  73. Robinson BH, Brooks RR, Howes AW, Kirkman JH, Gregg PEH (1997) The potential of the high-biomass nickel hyperaccumulator Berkheya coddii for phytoremediation and phytomining. J Geochem Explor 60:115–126CrossRefGoogle Scholar
  74. Robinson BH, Brooks RR, Clothier BE (1999) Soil amendments affecting nickel and cobalt uptake by Berkheya coddii: potential use for phytomining and phytoremediation. Ann Bot London 84:689–694CrossRefGoogle Scholar
  75. Rowell DL (1997) Soil science. Research methods and their applications. Springer, Berlin (in German)Google Scholar
  76. Rune O (1953) Plant life on serpentines and related rocks in the north of Sweden. Acta Phytogeographica Suecica 31:1–139Google Scholar
  77. Shahid M, Shamshad S, Rafiq M, Khalid S, Bibi I, Niazi NK, Dumat C, Rashid MI (2017) Chromium speciation, bioavailability, uptake, toxicity and detoxification in soil-plant system: a review. Chemosphere 178:513–533CrossRefGoogle Scholar
  78. Teptina A, Paukov A (2015) Nickel accumulation by species of Alyssum and Noccaea (Brassicaceae) from ultramafic soils in the Urals, Russia. Aust J Bot 63:78–84Google Scholar
  79. Tomović GM, Mihailović NL, Tumi AF, Gajić BA, Mišljenović TD, Niketić MS (2013) Trace metals in soils and several Brassicaceae plant species from serpentine sites of Serbia. Arch Environ Prot 39:29–49. CrossRefGoogle Scholar
  80. Tomović GM, Buzurović U, Đurović S, Vicić D, Mihailović NL, Jakovljević K (2018) Strategies of heavy metal uptake by three Armeria species growing on different geological substrates in Serbia. Environ Sci Pollut Res 25(1):507–522CrossRefGoogle Scholar
  81. Tumi AF, Mihailović NL, Gajic BA, Niketić MS, Tomović GM (2012) Comparative study of hyperaccumulation of nickel by Alyssum murale s.L. populations from the ultramafics of Serbia. Pol J Environ Stud 21:1855–1866Google Scholar
  82. van der Ent A, Baker AJM, Reeves RD, Pollard AJ, Schat H (2013) Hyperaccumulators of metal and metalloid trace elements: facts and fiction. Plant Soil 362:319–334CrossRefGoogle Scholar
  83. van Reeuwijk LP (ed) (1995) Procedures for soil analysis, Technical paper 8, 5th edn. International Soil Reference and Information Centre, WageningenGoogle Scholar
  84. van Reeuwijk LP (ed) (2002) Procedures for soil analysis, Technical paper 9, 6th edn. International Soil Reference and Information Centre, WageningenGoogle Scholar
  85. Verbruggen N, Hermans C, Schat H (2009) Molecular mechanisms of metal hyperaccumulation in plants. New Phytol 181(4):759–776CrossRefGoogle Scholar
  86. Vogel-Mikuš K, Drobne D, Regvar M (2005) Zn, cd and Pb accumulation and arbuscular mycorrhizal colonisation of pennycress Thlaspi praecox Wulf. (Brassicaceae) from the vicinity of a lead mine and smelter in Slovenia. Environ Pollut 133:233–242CrossRefGoogle Scholar
  87. Xing JP, Jiang RF, Ueno D, Ma JF, Schat H, McGrath SP, Zhao FJ (2008) Variation in root-to-shoot translocation of cadmium and zinc among different accessions of the hyperaccumulators Thlaspi caerulescens and Thlaspi praecox. New Phytol 178:315–325. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Tomica Mišljenović
    • 1
    Email author
  • Ksenija Jakovljević
    • 1
  • Slobodan Jovanović
    • 1
  • Nevena Mihailović
    • 2
  • Boško Gajić
    • 3
  • Gordana Tomović
    • 1
  1. 1.Faculty of Biology, Institute of Botany and Botanical GardenUniversity of BelgradeBelgradeSerbia
  2. 2.Institute for the Application of Nuclear Energy–INEPUniversity of BelgradeBelgradeSerbia
  3. 3.Faculty of Agriculture, Institute of Land Management, Laboratory of Soil PhysicsUniversity of BelgradeBelgradeSerbia

Personalised recommendations