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Assessment of trace element accumulation potential of Noccaea kovatsii from ultramafics of Bosnia and Herzegovina and Serbia

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Abstract

In this work, we present the results of the investigation of trace elements (Fe, Mg, Ni, Zn, Cu, Cr, Co, Cd, Pb) accumulation potential of Noccaea kovatsii (Heuff.) F. K. Mey., from the Balkan Peninsula. The study included eight populations from ultramafic soils, six from Bosnia and Herzegovina, and two from Serbia. Principal component analysis (PCA) was used to reveal relationships of elements in soil, and Pearson’s correlation coefficients for analysing associations of available quantities of elements in soil and those in roots and shoots of N. kovatsii. Uptake and translocation efficiency was assessed by using bioconcentration (BCF) and translocation factors (TF). All the analysed populations of N. kovatsii emerged as strong Ni accumulators, with the highest shoot concentrations of 12,505 mg kg−1. Even thought contents of Zn in plant tissues of N. kovatsii were under the hyperaccumulation level (602 mg kg−1 and 1120 mg kg−1 respectively), BCF was up to 667, indicating that certain surveyed populations have strong accumulative potential for this element.

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References

  • Alexander, E. B., & DuShey, J. (2011). Topographic and soil differences from peridotite to serpentinite. Geomorphology, 135(3-4), 271–276.

    Google Scholar 

  • Anacker, B. L. (2014). The nature of serpentine endemism. American Journal of Botany, 101(2), 219–224.

    Google Scholar 

  • Artelari, R. (2002). Thalspi L. In A. Strid & Kit Tan (Eds.), Flora Hellenica 2 (pp. 253-261). A.R.G. Gantner Velag K, K. Ruggell.

  • Asemaneh, T., Ghaderian, S. M., & Baker, A. J. M. (2007). Responses to Mg/Ca balance in an Iranian serpentine endemic plant, Cleome heratensis (Capparaceae) and a related non-serpentine species. C. foliolosa. Plant and Soil, 293(1-2), 49–59.

    CAS  Google Scholar 

  • Assunção, A. G., Schat, H., & Aarts, M. G. (2003). Thlaspi caerulescens, an attractive model species to study heavy metal hyperaccumulation in plants. New Phytologist, 159(2), 351–360.

    Google Scholar 

  • Assunção, A. G., Bleeker, P., Wilma, M., Vooijs, R., & Schat, H. (2008). Intraspecific variation of metal preference patterns for hyperaccumulation in Thlaspi caerulescens: evidence from binary metal exposures. Plant and Soil, 303(1-2), 289–299.

    Google Scholar 

  • Baker, A. J. (1981). Accumulators and excluders-strategies in the response of plants to heavy metals. Journal of Plant Nutrition, 3(1-4), 643–654.

    CAS  Google Scholar 

  • Baker, A. J. M., Reeves, R. D., & Hajar, A. S. M. (1994). Heavy metal accumulation and tolerance in British populations of the metallophyte Thlaspi caerulescens J. & C. Presl (Brassicaceae). New Phytologist, 127(1), 61–68.

    CAS  Google Scholar 

  • Baker, A. J., & Walker, P. L. (1990). Ecophysiology of metal uptake by tolerant plants. In A. J. Shaw (Ed.), Heavy Metal Tolerance in Plants: Evolutionary Aspects (pp. 155–177). Boca Raton: CRC Press.

    Google Scholar 

  • Bani, A., Pavlova, D., Echevarria, G., Mullaj, A., Reeves, R. D., Morel, J. L., & Sulçe, S. (2010). Nickel hyperaccumulation by the species of Alyssum and Thlaspi (Brassicaceae) from the ultramafic soils of the Balkans. Botanica Serbica, 34(1), 3–14.

    Google Scholar 

  • Boyd, R. S., & Martens, S. N. (1998). Nickel hyperaccumulation by Thlaspi montanum var. montanum (Brassicaceae): a constitutive trait. American Journal of Botany, 85(2), 259–265.

    CAS  Google Scholar 

  • Boyd, R. S., Kruckeberg, A. R., & Rajakaruna, N. (2009). Biology of ultramafic rocks and soils: research goals for the future. Northeastern Naturalist, 16(sp5), 422–440.

    Google Scholar 

  • Brady, K. U., Kruckeberg, A. R., & Bradshaw, H. D., Jr. (2005). Evolutionary ecology of plant adaptation to serpentine soils. Annual Review of Ecology, Evolution, and Systematics, 36, 243–266.

    Google Scholar 

  • Brković, D. L., Tomović, G. M., Niketić, M. S., & Lakušić, D. V. (2015). Diversity analysis of serpentine and non-serpentine flora–or, is serpentinite inhabited by a smaller number of species compared to different rock types? Biologia, 70(1), 61–74.

    Google Scholar 

  • Brooks, R. R. (1987). Serpentine and its vegetation: a multidisciplinary approach. Portland, Oregon, USA: Dioscorides Press.

    Google Scholar 

  • Chen, P. S., Toribara, T. T., & Warner, H. (1956). Microdetermination of phosphorus. Analytical Chemistry, 28(11), 1756–1758.

    CAS  Google Scholar 

  • Deng, T. H. B., Cloquet, C., Tang, Y. T., Sterckeman, T., Echevarria, G., Estrade, N., Morel, J.-L., & Qiu, R. L. (2014). Nickel and zinc isotope fractionation in hyperaccumulating and nonaccumulating plants. Environmental Science & Technology, 48(20), 11926–11933.

    CAS  Google Scholar 

  • Deng, T. H. B., van der Ent, A., Tang, Y. T., Sterckeman, T., Echevarria, G., Morel, J.-L., & Qiu, R. L. (2018). Nickel hyperaccumulation mechanisms: a review on the current state of knowledge. Plant and Soil, 423, 1–11.

    CAS  Google Scholar 

  • Diklić, N. (1972). Thlaspi L. In M. Josifović (Ed.), Flora SR Srbije 3 (pp. 341-355). Srpska akademija nauka i umetnosti. Beograd.

  • 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. Australian Journal of Botany, 64(3), 235–245.

    Google Scholar 

  • Egnér, H. A. N. S., Riehm, H., & Domingo, W. R. (1960). Untersuchungen über die chemische Bodenanalyse als Grundlage für die Beurteilung des Nährstoffzustandes der Böden. II. Chemische Extraktionsmethoden zur Phosphor-und Kaliumbestimmung. Kungliga Lantbrukshögskolans Annaler, 26, 199–215.

    Google Scholar 

  • FAO (1974). The Euphrates pilot irrigation project. Methods of soil analysis. Gadeb soil laboratory (a laboratory manual). Food and Agriculture Organization

  • Fones, H. N., Eyles, C. J., Bennett, M. H., Smith, J. A. C., & Preston, G. M. (2013). Uncoupling of reactive oxygen species accumulation and defence signalling in the metal hyperaccumulator plant Noccaea caerulescens. New Phytologist, 199(4), 916–924.

    CAS  Google Scholar 

  • Ghaderian, S. M., Movahedi, M., & Ghasemi, R. (2009). Uptake and accumulation of cobalt by Alyssum bracteatum, an endemic Iranian Ni hyperaccumulator. Northeastern Naturalist, 16(sp5), 131–138.

    Google Scholar 

  • Ghasemi, R., Ghaderian, S. M., & Krämer, U. (2009). Interference of nickel with copper and iron homeostasis contributes to metal toxicity symptoms in the nickel hyperaccumulator plant Alyssum inflatum. New Phytologist, 184(3), 566–580.

    CAS  Google Scholar 

  • Gonneau, C., Genevois, N., Frérot, H., Sirguey, C., & Sterckeman, T. (2014). Variation of trace metal accumulation, major nutrient uptake and growth parameters and their correlations in 22 populations of Noccaea caerulescens. Plant and Soil, 384(1-2), 271–287.

    CAS  Google Scholar 

  • Hermans, C., Conn, S. J., Chen, J., Xiao, Q., & Verbruggen, N. (2013). An update on magnesium homeostasis mechanisms in plants. Metallomics, 5(9), 1170–1183.

    CAS  Google Scholar 

  • Holman, W. I. M. (1943). A new technique for the determination of phosphorus by the molybdenum blue method. Biochemical Journal, 37(2), 256–259.

    CAS  Google Scholar 

  • ISO 6636/2 1981. Fruits, vegetables and derived products -- determination of zinc content -. Part 2: Atomic absorption spectrometric method. International Organization for Standardization.

  • ISO 11466 1995. Soil quality -- Extraction of trace elements soluble in aqua regia. International Organization for Standardization.

  • Jakovljević, K., Buzurović, U., Andrejić, G., Đurović, 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 Journal of Earth and Environmental Sciences, 10, 147–160.

    Google Scholar 

  • Jenny, H. (1980). The Soil Resource: Origin and Behaviour. New York Heidelberg Berlin: Springer-Verlag.

    Google Scholar 

  • Kabata-Pendias, A. (2011). Trace Elements in Soils and Plants. CRC Press Taylor & Francis Group.

  • Kaiser, H. F., & Rice, J. (1974). Little jiffy, mark IV. Educational and Psychological Measurement, 34(1), 111–117.

    Google Scholar 

  • Kazakou, E., Adamidis, G. C., Baker, A. J., Reeves, R. D., Godino, M., & Dimitrakopoulos, P. G. (2010). Species adaptation in serpentine soils in Lesbos Island (Greece): metal hyperaccumulation and tolerance. Plant and Soil, 332(1-2), 369–385.

    CAS  Google Scholar 

  • 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), 165–177.

    CAS  Google Scholar 

  • 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, 78–91.

    CAS  Google Scholar 

  • Koch, M. A., & German, D. (2013). Taxonomy and systematics are key to biological information: Arabidopsis, Eutrema (Thellungiella), Noccaea and Schrenkiella (Brassicaceae) as examples. Frontiers in Plant Science, 4, 267.

    Google Scholar 

  • Koch, M., Mummenhoff, K., & Hurka, H. (1998). Systematics and evolutionary history of heavy metal tolerant Thlaspi caerulescens in Western Europe: evidence from genetic studies based on isozyme analysis. Biochemical Systematics and Ecology, 26(8), 823–838.

    CAS  Google Scholar 

  • Krämer, U. (2010). Metal hyperaccumulation in plants. Annual Review of Plant Biology, 61, 517–534.

    Google Scholar 

  • Lange, B., van der Ent, A., Baker, A. J. M., Echevarria, G., Mahy, G., Malaisse, F., Meerts, P., Pourret, O., Verbruggen, N., & Faucon, M. P. (2016). Copper and cobalt accumulation in plants: a critical assessment of the current state of knowledge. New Phytologist, 213, 537–551.

    Google Scholar 

  • Lazarus, B. E., Richards, J. H., Claassen, V. P., O’Dell, R. E., & Ferrell, M. A. (2011). Species specific plant-soil interactions influence plant distribution on serpentine soils. Plant and Soil, 342(1-2), 327–344.

    CAS  Google Scholar 

  • Lombi, E., Zhao, F. J., Dunham, S. J., & McGrath, S. P. (2000). Cadmium accumulation in populations of Thlaspi caerulescens and Thlaspi goesingense. New Phytologist, 145(1), 11–20.

    CAS  Google Scholar 

  • 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. Applied Ecology and Environmental Research, 15(3), 359–372.

    Google Scholar 

  • Marhold, K. (2011). Brassicaceae. EURO+MED (2006–). Euro+Med PlantBase – the information resource for Euro Mediterranean plant diversity. Published on the Internet http://ww2.bgbm.org/EuroPlusMed/.

  • Martos, S., Gallego, B., Sáez, L., López-Alvarado, J., Cabot, C., & Poschenrieder, C. (2016). Characterization of zinc and cadmium hyperaccumulation in three Noccaea (Brassicaceae) populations from non-metalliferous sites in the eastern Pyrenees. Frontiers in Plant Science, 7, 128.

    Google Scholar 

  • McGrath, D. (1996). Application of single and sequential extraction procedures to polluted and unpolluted soils. Science of the Total Environment, 178(1-3), 37–44.

    CAS  Google Scholar 

  • McKeague, J.A. (1978). Manual on soil sampling and methods of analysis. Canadian Society of Soil Science.

  • Milner, M. J., & Kochian, L. V. (2008). Investigating heavy-metal hyperaccumulation using Thlaspi caerulescens as a model system. Annals of Botany, 102(1), 3–13.

  • Mišljenović, T., Jakovljević, K., Jovanović, S., Mihailović, N., Gajić, B., & Tomović, G. (2018). Micro-edaphic factors affect intra-specific variations in trace element profiles of Noccaea praecox on ultramafic soils. Environmental Science and Pollution Research, 25(31), 31737–31751.

    Google Scholar 

  • Mizuno, T., Usui, K., Horie, K., Nosaka, S., Mizuno, N., & Obata, H. (2005). Cloning of three ZIP/Nramp transporter genes from a Ni hyperaccumulator plant Thlaspi japonicum and their Ni2+-transport abilities. Plant Physiology and Biochemistry, 43(8), 793–801.

    CAS  Google Scholar 

  • O'Dell, R. E., & Claassen, V. P. (2009). Serpentine revegetation: a review. Northeastern Naturalist, 16(sp5), 253–271.

    Google Scholar 

  • Oze, C., Fendorf, S., Bird, D. K., & Coleman, R. G. (2004). Chromium geochemistry of serpentine soils. International Geology Review, 46(2), 97–126.

    Google Scholar 

  • Palm, E., Brady, K., & Van Volkenburgh, E. (2012). Serpentine tolerance in Mimulus guttatus does not rely on exclusion of magnesium. Functional Plant Biology, 39(8), 679–688.

    CAS  Google Scholar 

  • Pavlova, D., Karadjova, I., & Ganeva, A. (2013). Nickel accumulation screening of the ultramafic flora of Bulgaria. OT Sistematik Botanik Dergisi, 20(2), 41–52.

    Google Scholar 

  • 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 and Soil, 423(1-2), 339–362.

    Google Scholar 

  • Pollard, A. J., Reeves, R. D., & Baker, A. J. (2014). Facultative hyperaccumulation of heavy metals and metalloids. Plant Science, 217, 8–17.

    Google Scholar 

  • R Core Team. (2018). R: A language and environment for statistical computing. In R Foundation for Statistical Computing. Vienna: Austria URL https://www.R-project.org/.

    Google Scholar 

  • Rajakaruna, N., & Baker, A. J. (2004). Serpentine: a model habitat for botanical research in Sri Lanka. Ceylon Journal of Science, 32, 1–19.

    Google Scholar 

  • Rakić, T., Ilijević, K., Lazarević, M., Gržetić, I., Stevanović, V., & Stevanović, B. (2013). The resurrection flowering plant Ramonda nathaliae on serpentine soil–coping with extreme mineral element stress. Flora-Morphology, Distribution, Functional Ecology of Plants, 208(10-12), 618–625.

    Google Scholar 

  • Reeves, R. D., & Adigüzel, N. (2008). The nickel hyperaccumulating plants of the serpentines of Turkey and adjacent areas: a review with new data. Turkish Journal of Biology, 32(3), 143–153.

    CAS  Google Scholar 

  • Reeves, R. D., & Baker, A. J. M. (1984). Studies on metal uptake by plants from serpentine and non-serpentine populations of Thlaspi goesingense Hálácsy (Cruciferae). New Phytologist, 98(1), 191–204.

    CAS  Google Scholar 

  • Reeves, R. D., & Baker, A. J. M. (2000). Metal-accumulating plants. In I. Raskin & B. D. Ensley (Eds.), Phytoremediation of toxic metals: using plants to clean up the environment (pp. 193–230). New York: John Wiley & Sons, Inc..

    Google Scholar 

  • Reeves, R. D., Baker, A. J., Jaffré, T., Erskine, P. D., Echevarria, G., & van der Ent, A. (2018). A global database for plants that hyperaccumulate metal and metalloid trace elements. New Phytologist, 218(2), 407–411.

    Google Scholar 

  • Reeves, R. D., & Brooks, R. R. (1983). European species of Thlaspi L.(Cruciferae) as indicators of nickel and zinc. Journal of Geochemical Exploration, 18(3), 275–283.

    CAS  Google Scholar 

  • Rune, O. (1953). Plant life on serpentines and related rocks in the north of Sweden. Acta Phytogeographica Suecica 31, Upsala.

  • Sinclair, S. A., & Krämer, U. (2012). The zinc homeostasis network of land plants. Biochimica et Biophysica Acta (BBA)-Molecular Cell Research, 1823(9), 1553–1567.

    CAS  Google Scholar 

  • Salehi-Eskandari, B., Ghaderian, S. M., & Schat, H. (2018). Differential interactive effects of the Ca/Mg quotient and PEG-simulated drought in Alyssum inflatum and Fortuynia garcinii. Plant and Soil, 428(1-2), 213–222.

    CAS  Google Scholar 

  • Salihaj, M., Bani, A., Shahu, E., Benizri, E., & Echevarria, G. (2018). Metal accumulation by the ultramafic flora of Kosovo. Ecological Research, 33(4), 687–703.

    CAS  Google Scholar 

  • Shanker, A. K., Cervantes, C., Loza-Tavera, H., & Avudainayagam, S. (2005). Chromium toxicity in plants. Environment International, 31(5), 739–753.

    CAS  Google Scholar 

  • Sillanpää, M., & Jansson, H. (1992). Status of cadmium, lead, cobalt and selenium in soils and plants of thirty countries (No. 65). Food & Agriculture Organization of the United Nations.

  • Sterckeman, T., Cazes, Y., Gonneau, C., & Sirguey, C. (2017). Phenotyping 60 populations of Noccaea caerulescens provides a broader knowledge of variation in traits of interest for phytoextraction. Plant and Soil, 418(1-2), 523–540.

    CAS  Google Scholar 

  • Stevanović, V., Tan, K., & Iatrou, G. (2003). Distribution of the endemic Balkan flora on serpentine I.–obligate serpentine endemics. Plant Systematics and Evolution, 242(1-4), 149–170.

    Google Scholar 

  • Tappero, R., Peltier, E., Gräfe, M., Heidel, K., Ginder-Vogel, M., Livi, K. J. T., Rivers, M. L., Marcus, M. A., Chaney, R. L., & Sparks, D. L. (2007). Hyperaccumulator Alyssum murale relies on a different metal storage mechanism for cobalt than for nickel. New Phytologist, 175(4), 641–654.

    CAS  Google Scholar 

  • Taylor, S. I., & Macnair, M. R. (2006). Within and between population variation for zinc and nickel accumulation in two species of Thlaspi (Brassicaceae). New Phytologist, 169(3), 505–514.

    CAS  Google Scholar 

  • Tomović, G. M., Mihailović, N. L., Tumi, A. F., Gajić, B. A., Mišljenović, T. D., & Niketić, M. S. (2013). Trace metals in soils and several Brassicaceae plant species from serpentine sites of Serbia. Archives of Environmental Protection, 39(4), 29–49.

    Google Scholar 

  • Tumi, A. F., Mihailović, N., Gajić, B. A., Niketić, M., & Tomović, G. (2012). Comparative study of hyperaccumulation of nickel by Alyssum murale sl populations from the ultramafics of Serbia. Polish Journal of Environmental Studies, 21(6), 1855–1866.

    CAS  Google Scholar 

  • Tomović, G., Buzurović, U., Đurović, S., Vicić, D., Mihailović, N., & Jakovljević, K. (2018). Strategies of heavy metal uptake by three Armeria species growing on different geological substrates in Serbia. Environmental Science and Pollution Research, 25(1), 507–522.

    Google Scholar 

  • Van der Ent, A., Baker, A. J., Reeves, R. D., Pollard, A. J., & Schat, H. (2013). Hyperaccumulators of metal and metalloid trace elements: facts and fiction. Plant and Soil, 362(1-2), 319–334.

    Google Scholar 

  • Van Reeuwijk, L. P. (2002). Procedures for soil analysis. In Technical Paper 9. Wageningen: ISRIC.

    Google Scholar 

  • Vithanage, M., Rajapaksha, A. U., Oze, C., Rajakaruna, N., & Dissanayake, C. B. (2014). Metal release from serpentine soils in Sri Lanka. Environmental Monitoring and Assessment, 186(6), 3415–3429.

    CAS  Google Scholar 

  • 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. Environmental Pollution, 133(2), 233–242.

    Google Scholar 

  • White, P. J., & Broadley, M. R. (2009). Biofortification of crops with seven mineral elements often lacking in human diets–iron, zinc, copper, calcium, magnesium, selenium and iodine. New Phytologist, 182(1), 49–84.

    CAS  Google Scholar 

  • Yoon, J., Cao, X., Zhou, Q., & Ma, L. Q. (2006). Accumulation of Pb, Cu, and Zn in native plants growing on a contaminated Florida site. Science of the Total Environment, 368(2-3), 456–464.

    CAS  Google Scholar 

  • Zayed, A., Lytle, C. M., Qian, J. H., & Terry, N. (1998). Chromium accumulation, translocation and chemical speciation in vegetable crops. Planta, 206(2), 293–299.

    CAS  Google Scholar 

  • Zitka, O., Krystofova, O., Hynek, D., Sobrova, P., Kaiser, J., Sochor, J., Zehnalek, J., Babula, P., Ferrol, N., Kizek, R., & Adam, V. (2013). Metal transporters in plants. In D. K. Gupta, F. J. Corpas, & J. M. Palma (Eds.), Heavy metal stress in plants (pp. 19–41). Berlin, Heidelberg: Springer.

    Google Scholar 

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Acknowledgements

Authors are grateful to dr Marjan Niketić (Natural History Museum, Belgrade, Serbia) for revision of the plant material.

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This work was supported by Ministry of Education, Science, and Technological Development of the Republic of Serbia (grant no. 173030).

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Šinzar-Sekulić, J., Stamenković, U.M., Tomović, G. et al. Assessment of trace element accumulation potential of Noccaea kovatsii from ultramafics of Bosnia and Herzegovina and Serbia. Environ Monit Assess 191, 540 (2019). https://doi.org/10.1007/s10661-019-7711-x

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