Advertisement

Variability of trace element distribution in Noccaea spp., Arabidopsis spp., and Thlaspi arvense leaves: the role of plant species and element accumulation ability

  • Michaela Vašinová Galiová
  • Jiřina SzákováEmail author
  • Lubomír Prokeš
  • Zuzana Čadková
  • Pavel Coufalík
  • Viktor Kanický
  • Vítězslav Otruba
  • Pavel Tlustoš
Article

Abstract

Laser ablation-inductively coupled plasma-mass spectrometry (LA-ICP-MS) was applied for the determination of Cd and Zn distributions within the leaves of Cd- and Zn-hyperaccumulating plants, Noccaea caerulescens, N. praecox, and Arabidopsis halleri, in contrast to nonaccumulator species, Thlaspi arvense and A. thaliana. The elemental mapping of the selected leaf area was accomplished via line scans with a 110-μm-diameter laser beam at a 37-μm s−1 scan speed and repetition rate of 10 Hz. The lines were spaced 180 μm apart and ablated at an energy density of 2 J cm−2. The elemental imaging clearly confirmed that Cd was predominantly distributed within the parenchyma of the T. arvense, whereas in the Noccaea spp. and A. halleri, the highest intensity Cd signal was observed in the veins of the leaves. For Zn, higher intensities were observed in the veins for all the plant species except for A. thaliana. Close relationships between Zn and Ca were identified for the Noccaea spp. leaves. These relationships were not confirmed for A. halleri. Significant correlations were also proved between the Cd and Zn distribution in A. halleri, but not for the Noccaea spp. For both T. arvense and A. thaliana, no relevant significant relationship for the interpretation of the results was observed. Thus, the LA-ICP-MS imaging is proved as a relevant technique for the description and understanding of the elements in hyperaccumulating or highly accumulating plant species, although its sensitivity for the natural element contents in nonaccumulator plant species is still insufficient.

Keywords

Laser ablation Elemental mapping Hyperaccumulating plants Brassicaceae Trace elements 

Notes

Funding information

This study was financially supported by the GAČR project 13-18154S. The results of this research have also been acquired within CEITEC 2020 (LQ1601) project with financial contribution made by the Ministry of Education, Youth and Sports of the Czech Republic within special support paid from the National Programme for Sustainability II Funds.

Supplementary material

10661_2019_7331_MOESM1_ESM.docx (196 kb)
ESM 1 (DOCX 195 kb)

References

  1. Alvarez-Fernandez, A., Diaz-Benito, P., Abadia, A., Lopez-Millan, A. F., & Abadia, J. (2014). Metal species involved in long distance metal transport in plants. Frontiers in Plant Science, 5, 105.CrossRefGoogle Scholar
  2. Anselin, L. (1995). Local indicators of spatial association – LISA. Geographical Analysis, 27, 93–115.CrossRefGoogle Scholar
  3. Assunção, A. G. L., Ten Bookum, W. M., Nelissen, H. J. M., Vooijs, R., Schat, H., & Ernst, W. H. O. (2003). Differential metal-specific tolerance and accumulation patterns among Thlaspi caerulescens populations originating from different soil types. New Phytologist, 159, 411–419.CrossRefGoogle Scholar
  4. Bartels, B., & Svatoš, A. (2015). Spatially resolved in vivo plant metabolomics by laser ablation-based mass spectrometry imaging (MSI) techniques: LDI-MSI and LA-ESI. Frontiers in Plant Science, 6, 471.CrossRefGoogle Scholar
  5. Basic, N., Keller, C., Fontanillas, P., Vittoz, P., Besnard, G., & Galland, N. (2006). Cadmium hyperaccumulation and reproductive traits in natural Thlaspi caerulescens populations. Plant Biology, 8, 64–72.CrossRefGoogle Scholar
  6. Boughton, B. A., Thinagaran, D., Sarabia, D., Bacic, A., & Roessner, U. (2016). Mass spectrometry imaging for plant biology: a review. Phytochemistry Reviews, 15, 445–488.CrossRefGoogle Scholar
  7. Callahan, D. L., Hare, D. J., Bishop, D. P., Doble, P. A., & Roessner, U. (2016). Elemental imaging of leaves from the metal hyperaccumulating plant Noccaea caerulescens shows different spatial distribution of Ni, Zn and Cd. RSC Advances, 6, 2337–2344.CrossRefGoogle Scholar
  8. Cizdziel, J., Bu, K. X., & Nowinski, P. (2012). Determination of elements in situ in green leaves by laser ablation ICP-MS using pressed reference materials for calibration. Analytical Methods, 4, 564–569.CrossRefGoogle Scholar
  9. Cochran, W. G. (1977). Sampling techniques (Third ed.). New York: Wiley.Google Scholar
  10. Corso, M., Schvartzman, M. S., Guzzo, F., Souard, F., Małkowski, E., Hanikenne, M., & Verbruggen, N. (2018). Contrasting cadmium resistance strategies in two metallicolous populations of Arabidopsis halleri. New Phytologist, 218, 283–297.CrossRefGoogle Scholar
  11. Cosio, C., Martinoia, E., & Keller, C. (2004). Hyperaccumulation of cadmium and zinc in Thlaspi caerulescens and Arabidopsis halleri at the leaf cellular level. Plant Physiology, 134, 716–725.CrossRefGoogle Scholar
  12. Cosio, C., DeSantis, L., Frey, B., Diallo, S., & Keller, C. (2005). Distribution of cadmium in leaves of Thlaspi caerulescens. Journal of Experimental Botany, 56, 765–775.CrossRefGoogle Scholar
  13. de Siqueira Santos, S., Takahashi, D. Y., Nakata, A., & Fujita, A. (2014). A comparative study of statistical methods used to identify dependencies between gene expression signals. Briefings in Bioinformatics, 15, 906–918.CrossRefGoogle Scholar
  14. Dong, Y., Li, B., Malitsky, S., Rogachev, I., Aharoni, A., Kaftan, F., Svatoš, A., & Franceschi, P. (2016). Sample preparation for mass spectrometry imaging of plant tissues: a review. Frontiers in Plant Science, 7, 60.Google Scholar
  15. Etalo, D. W., De Vos, R. C. H., Joosten, M. H. A. J., & Hall, R. D. (2015). Spatially resolved plant metabolomics: some potentials and limitations of laser-ablation electrospray ionization mass spectrometry metabolite imaging. Plant Physiology, 169, 1424–1435.Google Scholar
  16. Frey, B., Keller, C., Zierold, K., & Schulin, R. (2000). Distribution of Zn in functionally different leaf epidermal cells of the hyperaccumulator Thlaspi caerulescens. Plant, Cell & Environment, 23, 675–687.CrossRefGoogle Scholar
  17. Friendly, M. (2002). Corrgrams: exploratory displays for correlation matrices. American Statistician, 56, 316–324.CrossRefGoogle Scholar
  18. Fukuda, N., Hokura, A., Kitajima, N., Terada, Y., Saito, H., Abe, T., & Nakai, I. (2008). Micro X-ray fluorescence imaging and micro X-ray absorption spectroscopy of cadmium hyper-accumulating plant, Arabidopsis halleri ssp. gemmifera, using high-energy synchrotron radiation. Journal of Analytical Atomic Spectrometry, 23, 1068–1075.CrossRefGoogle Scholar
  19. Galiová, M., Kaiser, J., Novotný, K., Hartl, M., Kizek, R., & Babula, P. (2011). Utilization of laser-assisted analytical methods for monitoring of lead and nutrition elements distribution in fresh and dried Capsicum annuum L. leaves. Microscopy Research and Technique, 74, 845–852.Google Scholar
  20. Han, R., Quinet, M., André, E., van Elteren, J. T., Destrebecq, F., Vogel-Mikuš, K., Cui, G., Debeljak, M., Lefèvre, I., & Lutts, S. (2013). Accumulation and distribution of Zn in the shoots and reproductive structures of the halophyte plant species Kosteletzkya virginica as a function of salinity. Planta, 238, 441–457.CrossRefGoogle Scholar
  21. Hanć, A., Malecka, A., Kutrowska, A., Bagniewska-Zadworna, A., Tomaszewska, B., & Baralkiewicz, D. (2016). Direct analysis of elemental biodistribution in pea seedlings by LA-ICP-MS, EDX and confocal microscopy: imaging and quantification. Microchemical Journal, 128, 305–311.CrossRefGoogle Scholar
  22. Hanikenne, M., & Nouet, C. (2011). Metal hyperaccumulation and hypertolerance: a model for plant evolutionary genomics. Current Opinion in Plant Biology, 14, 252–259.CrossRefGoogle Scholar
  23. Hu, P. J., Gan, Y. Y., Tang, Y. T., Zhang, Q. F., Jiang, D., Yao, N., & Qiu, R. L. (2012). Cellular tolerance, accumulation and distribution of cadmium in leaves of hyperaccumulator Picris divaricata. Pedosphere, 22, 497–507.CrossRefGoogle Scholar
  24. Huguet, S., Bert, V., Laboudigue, A., Barthes, V., Isaure, M. P., Llorens, I., Schat, H., & Sarret, G. (2012). Cd speciation and localization in the hyperaccumulator Arabidopsis halleri. Environmental and Experimental Botany, 82, 54–65.CrossRefGoogle Scholar
  25. Isaure, M. P., Huguet, S., Meyer, C. L., Castillo-Michel, H., Testemale, D., Vantelon, D., Saumitou-Laprade, P., Verbruggen, N., & Sarret, G. (2015). Evidence of various mechanisms of Cd sequestration in the hyperaccumulator Arabidopsis halleri, the non-accumulator Arabidopsis lyrata, and their progenies by combined synchrotron-based techniques. Journal of Experimental Botany, 66, 3201–3214.CrossRefGoogle Scholar
  26. ISO 11260. (1994). Standard of soil quality - determination of effective cation exchange capacity and base saturation level using barium chloride solution. Geneve: International Organization for Standardization.Google Scholar
  27. Kaiser, J., Galiová, M., Novotný, K., Červenka, R., Reale, L., Novotný, J., Liška, M., Samek, O., Kanický, V., Hrdlička, A., Stejskal, K., Adam, V., & Kizek, R. (2009). Mapping of lead, magnesium and copper accumulation in plant tissues by laser-induced breakdown spectroscopy and laser-ablation inductively coupled plasma mass spectrometry. Spectrochimica Acta Part B, 64, 67–73.CrossRefGoogle Scholar
  28. Kashem, M. A., Singh, B. R., Kubota, H., Sugawara, R., Kitajima, N., Kondo, T., & Kawai, S. (2010). Zinc tolerance and uptake by Arabidopsis halleri ssp. gemmifera grown in nutrient solution. Environmental Science and Pollution Research, 17, 1174–1176.CrossRefGoogle Scholar
  29. Kizilgoz I (2016) Effects of increasing soil calcium application on growth and uptake of calcium, phosphorus, zinc and boron in durum wheat (Triticum durum L.). Oxid Commun 39: 258–265.Google Scholar
  30. Klug, B., Specht, A., & Horst, W. J. (2011). Aluminium localization in root tips of the aluminium accumulating plant species buckwheat (Fagopyrum esculentum Moench). Journal of Experimental Botany, 62, 5453–5462.CrossRefGoogle Scholar
  31. Kozhevnikova, A. D., Seregin, I. V., Gosti, F., & Schat, H. (2017). Zinc accumulation and distribution over tissues in Noccaea caerulescens in nature and in hydroponics: a comparison. Plant and Soil, 411, 5–16.CrossRefGoogle Scholar
  32. Kulhánek, M., Balík, J., Černý, J., Sedlář, O., & Vašák, F. (2016). Evaluating of soil sulfur forms changes under different fertilizing systems during long-term field experiments. Plant, Soil and Environment, 62, 408–415.CrossRefGoogle Scholar
  33. Leitenmaier, B., & Küpper, H. (2013). Compartmentation and complexation of metals in hyper- accumulator plants. Frontiers in Plant Science, 4, 374.CrossRefGoogle Scholar
  34. Likar, M., Pongrac, P., Vogel-Mikuš, K., & Regvar, M. (2010). Molecular diversity and metal accumulation of different Thlaspi praecox populations from Slovenia. Plant and Soil, 330, 195–205.CrossRefGoogle Scholar
  35. Liu, M. Q., Yanai, J., Jiang, R. F., Zhang, F., McGrath, S. P., & Zhao, F. J. (2008). Does cadmium play a physiological role in the hyperaccumulator Thlaspi caerulescens? Chemosphere, 71, 1276–1283.CrossRefGoogle Scholar
  36. Lobinski, R., Moulin, C., & Ortega, R. (2006). Imaging and speciation of trace elements in biological environment. Biochimie, 88, 1591–1604.CrossRefGoogle Scholar
  37. 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, 11–20.CrossRefGoogle Scholar
  38. Lombi, E., Tearall, K. L., Howarth, J. R., Zhao, F. J., Hawkesford, M. J., & McGrath, S. P. (2002). Influence of iron status on cadmium and zinc uptake by different ecotypes of the hyperaccumulator Thlaspi caerulescens. Plant Physiology, 128, 1359–1367.CrossRefGoogle Scholar
  39. Lovy, L., Latt, D., & Sterckeman, T. (2013). Cadmium uptake and partitioning in the hyperaccumulator Noccaea caerulescens exposed to constant Cd concentrations throughout complete growth cycles. Plant and Soil, 362, 345–354.CrossRefGoogle Scholar
  40. Maestri, E., Marmiroli, M., Visioli, G., & Marmiroli, N. (2010). Metal tolerance and hyperaccumulation: cost and trade-offs between traits and environment. Environmental and Experimental Botany, 68, 1–13.CrossRefGoogle Scholar
  41. McGrath, S. P., Lombi, E., Gray, C. W., Caille, N., Dunham, S. J., & Zhao, F. J. (2006). Field evaluation of Cd and Zn phytoextraction potential by the hyperaccumulators Thlaspi caerulescens and Arabidopsis halleri. Environmental Pollution, 141, 115–125.CrossRefGoogle Scholar
  42. Meyer, C. L., Juraniec, M., Huguet, S., Chaves-Rodriguez, E., Salis, P., Isaure, M. P., Goormaghtigh, E., & Verbruggen, N. (2015). Intraspecific variability of cadmium tolerance and accumulation, and cadmium-induced cell wall modifications in the metal hyperaccumulator Arabidopsis halleri. Journal of Experimental Botany, 66, 3215–3227.CrossRefGoogle Scholar
  43. Milner, M. J., & Kochian, L. V. (2008). Investigating heavy-metal hyperaccumulation using Thlaspi caerulescens as a model system. Annals of Botany, 102, 3–13.CrossRefGoogle Scholar
  44. Mingorance, M. D., Barahona, E., & Fernandez-Galvez, J. (2007). Guidelines for improving organic carbon recovery by the wet oxidation method. Chemosphere, 68, 409–413.CrossRefGoogle Scholar
  45. Nunes, M. A. G., Voss, M., Corazza, G., Flores, E. M. M., & Dressler, V. L. (2016). External calibration strategy for trace element quantification in botanical samples by LA-ICP-MS using filter paper. Analytica Chimica Acta, 905, 51–57.CrossRefGoogle Scholar
  46. Oliveira, S. R., & Arruda, M. A. Z. (2015). Application of laser ablation (imaging) inductively coupled plasma mass spectrometry for mapping and quantifying Fe in transgenic and non-transgenic soybean leaves. Journal of Analytical Atomic Spectrometry, 30, 389–395.CrossRefGoogle Scholar
  47. Pearson R.K. (2002) Outliers in process modeling and identification. IEEE Transactions on Control Systems Technology 10, 55–63.Google Scholar
  48. Pellegrini, M., Laugier, A., Sergent, M., Phantanluu, R., Valls, R., & Pellegrini, L. (1993). Interactions between the toxicity of the heavy-metals cadmium, copper, zinc in combinations and the detoxifying role of calcium in the brown alga Cystoseira barbata. Journal of Applied Phycology, 5, 351–361.CrossRefGoogle Scholar
  49. Polatajko, A., Feldmann, I., Hayen, H., & Jakubowski, N. (2011). Combined application of a laser ablation-ICP-MS assay for screening and ESI-FTICR-MS for identification of a Cd-binding protein in Spinacia oleracea L. after exposure to Cd. Metallomics, 3, 1001–1008.CrossRefGoogle Scholar
  50. Pongrac, P., Zhao, F. J., Razinger, J., Zrimec, A., & Regvar, M. (2009). Physiological responses to Cd and Zn in two Cd/Zn hyperaccumulating Thlaspi species. Environmental and Experimental Botany, 66, 479–486.CrossRefGoogle Scholar
  51. Przedpełska-Wąsowicz, E., Polatajko, A., & Wierzbicka, M. (2012). The influence of cadmium stress on the content of mineral nutrients and metal-binding proteins in Arabidopsis halleri. Water, Air, and Soil Pollution, 223, 5445–5458.CrossRefGoogle Scholar
  52. Rittner M., Müller W. (2012) 2D mapping of LA-ICPMS trace element distributions using R. Computers & Geosciences 42, 152–161.Google Scholar
  53. Sarret, G., Saumitou-Laprade, P., Bert, V., Proux, O., Hazemann, J. L., Traverse, A., Marcus, M. A., & Manceau, A. (2002). Forms of zinc accumulated in the hyperaccumulator Arabidopsis halleri. Plant Physiology, 130, 1815–1826.CrossRefGoogle Scholar
  54. Schvartzman, M. S., Corso, M., Fataftah, N., Scheepers, M., Nouet, C., Bosman, B., Carnol, M., Motte, P., Verbruggen, N., & Hanikenne, M. (2018). Adaptation to high zinc depends on distinct mechanisms in metallicolous populations of Arabidopsis halleri. New Phytologist, 218, 269–282.CrossRefGoogle Scholar
  55. Silverman, B. W. (1986). Density estimation for statistics and data analysis. London: Chapman & Hall.CrossRefGoogle Scholar
  56. Sitko, K., Rusinowski, S., Kalaji, H. M., Szopiński, M., & Małkowski, E. (2017). Photosynthetic efficiency as bioindicator of environmental pressure in A. halleri. Plant Physiology, 175, 290–302.CrossRefGoogle Scholar
  57. Stein, R. J., Höreth, S., de Melo, J. R. F., Syllwasschy, L., Lee, G., Garbin, M. L., Clemens, S., & Krämer, U. (2016). Relationships between soil and leaf mineral composition are element-specific, environment-dependent and geographically structured in the emerging model Arabidopsis halleri. New Phytologist, 213, 1274–1286.CrossRefGoogle Scholar
  58. 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, 523–540.CrossRefGoogle Scholar
  59. Tian, S., Lu, L., Labavitch, J., Yang, X., He, Z., Hu, H., Sarangi, R., Newville, M., Commisso, J., & Brown, P. (2011). Cellular sequestration of cadmium in the hyperaccumulator plant species Sedum alfredii. Plant Physiology, 157, 1914–1925.CrossRefGoogle Scholar
  60. Tlustoš, P., Břendová, K., Száková, J., Najmanová, J., & Koubová, K. (2016). The long-term variation of Cd and Zn hyperaccumulation by Noccaea spp. and Arabidopsis halleri plants in both pot and field conditions. International Journal of Phytoremediation, 18, 110–115.CrossRefGoogle Scholar
  61. Turková, S., Vašinová Galiová, M., Štůlová, K., Čadková, Z., Száková, J., Otruba, V., & Kanický, V. (2017). Study of metal accumulation in tapeworm section using laser ablation-inductively coupled plasma-mass spectrometry (LA-ICP-MS). Microchemical Journal, 133, 380–390.CrossRefGoogle Scholar
  62. Turnau, K., Ostachowicz, B., Wojtczak, G., Anielska, T., & Sobczyk, Ł. (2010). Metal uptake by xerothermic plants introduced into Zn-Pb industrial wastes. Plant and Soil, 337, 299–311.CrossRefGoogle Scholar
  63. Valentinuzzi, F., Cesco, S., Tomasi, N., & Mimmo, T. (2015). Influence of different trap solutions on the determination of root exudates in Lupinus albus L. Biology and Fertility of Soils, 51, 757–765.CrossRefGoogle Scholar
  64. Vašinová Galiová, M., Fišáková Nývltová, M., Kynický, J., Prokeš, L., Neff, H., Mason, A. Z., Gadas, P., Kosler, J., & Kanický, V. (2013). Elemental mapping in fossil tooth root section of Ursus arctos by laser ablation inductively coupled plasma mass spectrometry (LA-ICP-MS). Talanta, 105, 235–243.CrossRefGoogle Scholar
  65. Verbruggen, N., Juraniec, M., Baliardini, C., & Meyer, C. L. (2013). Tolerance to cadmium in plants: the special case of hyperaccumulators. Biometals, 26, 633–638.CrossRefGoogle Scholar
  66. Vogel-Mikuš, K., Simcic, J., Pelicon, P., Budnar, M., Kump, P., Necemer, M., Mesjasz-Przybyłowicz, J., Przybyłowicz, W. J., & Regvar, M. (2008a). Comparison of essential and non-essential element distribution in leaves of the Cd/Zn hyperaccumulator Thlaspi praecox as revealed by micro-PIXE. Plant, Cell & Environment, 31, 1484–1496.CrossRefGoogle Scholar
  67. Vogel-Mikuš, K., Regvar, M., Mesjasz-Przybyłowicz, J., Przybyłowicz, W. J., Simcic, J., Pelicon, P., & Budnar, M. (2008b). Spatial distribution of cadmium in leaves of metal hyperaccumulating Thlaspi praecox using micro-PIXE. New Phytologist, 179, 712–721.CrossRefGoogle Scholar
  68. Vondráčková, S., Hejcman, M., Száková, J., Müllerová, V., & Tlustoš, P. (2014). Soil chemical properties affect the concentration of elements (N, P, K, Ca, Mg, As, Cd, Cr, Cu, Fe, Mn, Ni, Pb, and Zn) and their distribution between organs of Rumex obtusifolius. Plant and Soil, 379, 231–245.CrossRefGoogle Scholar
  69. Walker, D. J., & Bernal, M. P. (2004). The effects of copper and lead on growth and zinc accumulation of Thlaspi caerulescens J. and C. Presl: implications for phytoremediation of contaminated soils. Water, Air, and Soil Pollution, 151, 136–372.CrossRefGoogle Scholar
  70. Wu, B., & Becker, J. S. (2012). Imaging techniques for elements and element species in plant science. Metallomics, 4, 403–416.CrossRefGoogle Scholar
  71. Wu, B., Chen, Y., & Becker, J. S. (2009). Study of essential element accumulation in the leaves of a Cu-tolerant plant Elsholtzia splendens after Cu treatment by imaging laser ablation inductively coupled plasma mass spectrometry (LA-ICP-MS). Analytica Chimica Acta, 633, 165–172.CrossRefGoogle Scholar
  72. Wu, B., Andersch, F., Weschke, W., Weber, H., & Becker, J. S. (2013). Diverse accumulation and distribution of nutrient elements in developing wheat grain studied by laser ablation inductively coupled plasma mass spectrometry imaging. Metallomics, 5, 1276–1284.CrossRefGoogle Scholar
  73. Yang, H. X., Zhao, L. H., Liu, W., & Li, B. (2014). Bioimaging and distribution of Cd, P, S, K, Ca, Cu and Zn elements in Indian Mustard stem. Chinese Journal of Analytical Chemistry, 42, 355–359.CrossRefGoogle Scholar
  74. Zar, J. H. (1999). Biostatistical analysis (Fourth ed.). Upper Saddle River: Prentice Hall.Google Scholar
  75. Zemanová, V., Pavlík, M., Pavlíková, D., & Tlustoš, P. (2013). The changes of contents of selected free amino acids associated with cadmium stress in Noccaea caerulescens and Arabidopsis halleri. Plant, Soil and Environment, 59, 417–422.CrossRefGoogle Scholar
  76. Zhao, F. J., Moore, K. L., Lombi, E., & Zhu, Y. G. (2014). Imaging element distribution and speciation in plant cells. Trends in Plant Science, 19, 183–192.CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Michaela Vašinová Galiová
    • 1
    • 2
  • Jiřina Száková
    • 3
    Email author
  • Lubomír Prokeš
    • 1
  • Zuzana Čadková
    • 4
  • Pavel Coufalík
    • 1
    • 5
  • Viktor Kanický
    • 1
    • 2
  • Vítězslav Otruba
    • 1
    • 2
  • Pavel Tlustoš
    • 3
  1. 1.Department of Chemistry, Faculty of ScienceMasaryk UniversityBrnoCzech Republic
  2. 2.Central European Institute of TechnologyMasaryk UniversityBrnoCzech Republic
  3. 3.Department of Agro-Environmental Chemistry and Plant Nutrition, Faculty of Agrobiology, Food and Natural ResourcesCzech University of Life Science PraguePrague–SuchdolCzech Republic
  4. 4.Department of Zoology and Fisheries, Faculty of Agrobiology, Food and Natural ResourcesCzech University of Life Science PraguePrague–SuchdolCzech Republic
  5. 5.Institute of Analytical ChemistryThe Czech Academy of Sciences, v.v.i.BrnoCzech Republic

Personalised recommendations