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Comparison of the toxicity and distribution of cadmium and lead in plant cells

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Summary.

The toxicity of heavy metals (Cd, Zn, and Pb) was assessed by in vivo observations of their effect on cytoplasmic streaming in Allium cepa L. bulb scale epidermal cells. On the basis of our results, the order of toxicity of the studied cations is Zn < Pb ≪ Cd. The difference in toxicity between cadmium and lead was found to be very large. When cytoplasmic streaming was assessed, this difference was threefold. When the total content of cadmium and lead (determined by inductively coupled plasma mass spectrometry) was the criterion, the difference in toxicity was 15-fold. Fractionation of the tissue and enzymatic digestion of the cells revealed that the largest proportion of cadmium was located in the cell walls (56%), whereas almost all of the lead (97.6%) was accumulated in an insoluble form. The speciation of water-soluble Pb and Cd fractions is discussed on the basis of analysis by capillary zone electrophoresis interfaced with inductively coupled plasma mass spectrometry of water extracts from epidermal cells. Lead and cadmium appeared to be bound mainly to salts, which explains their toxicity. Cadmium was complexed (detoxified) by organic acids, while thiols were the metal-complexing species for lead. Histidine formed complexes with both cadmium and lead. Ultrastructural analyses showed that lead was encapsulated in small vesicles in the cytoplasm. Fluorescence studies of the endoplasmic reticulum (ER) revealed that it underwent extensive fragmentation under the influence of lead, with numerous ER vesicles appearing in the cells. In other words, the lead deposits in the cytoplasm were contained in vesicles arising from fragmentation of the ER. These observations indicate that epidermal cells have a rapid and effective mechanism for detoxifying lead involving the ER, and this may be one of the mechanisms accounting for the lower toxicity of lead in comparison with cadmium. The suitability of Allium cepa bulb scale epidermal cells for use in ecotoxicological studies is also discussed. Step-by-step directions for this test are given.

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Abbreviations

CZE-ICP-MS:

capillary zone electrophoresis interfaced with inductively coupled plasma mass spectrometry

DiOC6 :

3,3′-dihexyloxacarbocyanine iodide

ER:

endoplasmic reticulum

ICP-MS:

inductively coupled plasma mass spectrometry

References

  • B Alberts D Bray A Johnson J Lewis M Raff K Roberts P Walter (1999) Essential cell biology SeriesTitleAn introduction to molecular cell biology Garland Publishing New York

    Google Scholar 

  • D Antosiewicz M Wierzbicka (1999) ArticleTitleLocalization of lead in Allium cepa L. cells by electron microscopy J Microsc 195 139–149 Occurrence Handle10460677 Occurrence Handle10.1046/j.1365-2818.1999.00492.x Occurrence Handle1:CAS:528:DyaK1MXlvFGlsL8%3D

    Article  PubMed  CAS  Google Scholar 

  • A Baranowska-Morek M Wierzbicka (2004) ArticleTitleLocalization of lead in root tip of Dianthus carthusianorum Acta Biol Cracov Bot 46 45–56

    Google Scholar 

  • RMC Dawson CD Elliott WH Elliott KM Jones (1969) Data for biochemical research EditionNumber2 Oxford University Press Oxford

    Google Scholar 

  • WHO Ernst (1998) Effects of heavy metals in plants at the cellular and organismic level G Schürmann B Markert (Eds) Ecotoxicology John Wiley and Sons, Spektrum Akademischer-Verlag Heidelberg 587–619

    Google Scholar 

  • M Ferrando B Glasmacher G Rau (2002) ArticleTitleThermophysical properties of a monolayer tissue with respect to freeze-drying Biomed Tech 47 IssueIDSuppl 1 390–392 Occurrence Handle10.1515/bmte.2002.47.s1a.390

    Article  Google Scholar 

  • JS Gens C Reuzeau KW Doolittle JG Mcnally BG Pickard (1996) ArticleTitleCovisualization by computational optical-sectioning microscopy of integrin and associated proteins at the plasma membrane of living onion protoplasts Protoplasma 194 215–230 Occurrence Handle11541650 Occurrence Handle10.1007/BF01882029 Occurrence Handle1:CAS:528:DyaK2sXotlOhug%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • S Glińska B Gabara (2002) ArticleTitleInfluence of selenium on lead absorption and localization in meristematic cells of Allium sativum L. and Pisum sativum L. roots Acta Biol Cracov Bot 44 39–48

    Google Scholar 

  • JL Hall (2002) ArticleTitleCellular mechanisms for heavy metal detoxification and tolerance J Exp Bot 53 1–11 Occurrence Handle11741035 Occurrence Handle10.1093/jexbot/53.366.1 Occurrence Handle1:CAS:528:DC%2BD3MXptlKgtLw%3D

    Article  PubMed  CAS  Google Scholar 

  • N Harris NJ Chaffey (1985) ArticleTitlePlasmotubules in transfer cells of pea (Pisum sativum L.) Planta 165 191–196 Occurrence Handle10.1007/BF00395041

    Article  Google Scholar 

  • N Harris KJ Oparka DJ Walker-Smith (1982) ArticleTitlePlasmotubules: an alternative to transfer cells? Planta 156 461–465 Occurrence Handle10.1007/BF00393318

    Article  Google Scholar 

  • HG Heumann (2002) ArticleTitleUltrastructural localization of zinc in zinc-tolerant Armeria maritima ssp. halleri by autometallography J Plant Physiol 159 191–203 Occurrence Handle10.1078/0176-1617-00553 Occurrence Handle1:CAS:528:DC%2BD38Xis1Khsb8%3D

    Article  CAS  Google Scholar 

  • VB Ivanov EI Bystrova IV Seregin (2003) ArticleTitleComparative impacts of heavy metals on root growth as related to their specificity and selectivity Russ J Plant Physiol 50 398–406 Occurrence Handle10.1023/A:1023838707715 Occurrence Handle1:CAS:528:DC%2BD3sXjvFyitrk%3D

    Article  CAS  Google Scholar 

  • MD Jarvis DWM Leung (2001) ArticleTitleChelated lead transport in Chamaecytisus proliferus (L.f.) link ssp. proliferus var. palmensis (H. Christ): an ultrastructural study Plant Sci 161 433–441 Occurrence Handle10.1016/S0168-9452(01)00424-1 Occurrence Handle1:CAS:528:DC%2BD3MXls1aqur8%3D

    Article  CAS  Google Scholar 

  • A Kabata-Pendias H Pendias (1999) Biogeochemia pierwiastków śladowych PWN Warszawa

    Google Scholar 

  • L Kłyszejko-Stefanowicz (1998) Cytobiochemia PWN Warszawa

    Google Scholar 

  • J Kopcewicz S Lewak (2002) Fizjologia roślin PWN Warszawa

    Google Scholar 

  • U Kristen (1997) ArticleTitleUse of higher plants as screens for toxicity assessment Toxicol In Vitro 11 181–191 Occurrence Handle10.1016/S0887-2333(97)00005-2 Occurrence Handle1:CAS:528:DyaK2sXjvFKnsrw%3D

    Article  CAS  Google Scholar 

  • I Lang-Pauluzzi (2000) ArticleTitleThe behavior of the plasma membrane during plasmolysis: study by UV microscopy J Microsc 198 188–198 Occurrence Handle10849197 Occurrence Handle10.1046/j.1365-2818.2000.00677.x Occurrence Handle1:STN:280:DC%2BD3czgslyjsQ%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • IK Lichtscheidl WG Url (1990) ArticleTitleOrganization and dynamics of cortical endoplasmic reticulum in inner epidermal cells of onion bulb scales Protoplasma 157 203–215 Occurrence Handle10.1007/BF01322653

    Article  Google Scholar 

  • AG Loewy P Siekevitz JR Menninger JAN Gallant (1991) Cell structure and function SeriesTitleAn integrated approach Saunders College Publishing Philadelphia

    Google Scholar 

  • GR MacFarlane MD Burchett (2000) ArticleTitleCellular distribution of copper, lead and zinc in the grey mangrove, Avicennia marina (Forsk.) Vierh Aquat Bot 68 45–59 Occurrence Handle10.1016/S0304-3770(00)00105-4 Occurrence Handle1:CAS:528:DC%2BD3cXlsVyjtr8%3D

    Article  CAS  Google Scholar 

  • K Mengel EA Kirkby (1978) Copper K Mengel EA Kirkby (Eds) Principles of plant nutrition International Potash Institute Worblaufen-Bern, Switzerland 463–474

    Google Scholar 

  • E Michalak M Wierzbicka (1998) ArticleTitleDifferences in lead tolerance between Allium cepa plants developing from seeds and bulbs Plant Soil 199 251–260 Occurrence Handle10.1023/A:1004321331708 Occurrence Handle1:CAS:528:DyaK1cXjslOgu78%3D

    Article  CAS  Google Scholar 

  • D Neumann U Zur Nieden O Lichtenberger I Leopold (1995) ArticleTitleHow does Armeria maritima tolerate high heavy metal concentrations? J Plant Physiol 146 704–717 Occurrence Handle1:CAS:528:DyaK2MXotlOnsrY%3D

    CAS  Google Scholar 

  • A Ng ML Parker AJ Parr PK Saunders AC Smith KW Waldron (2000) ArticleTitlePhysicochemical characteristics of onion (Allium cepa L.) tissue J Agric Food Chem 48 5612–5617 Occurrence Handle11087527 Occurrence Handle10.1021/jf991206q Occurrence Handle1:CAS:528:DC%2BD3cXntVOmtr8%3D

    Article  PubMed  CAS  Google Scholar 

  • E Nieboer DHS Richardson (1980) ArticleTitleThe replacement of the nondescriptive term heavy metals by a biologically and chemically significant classification of metal ions Environ Pollut 1B 3–26

    Google Scholar 

  • H Quader E Schnepf (1986) ArticleTitleEndoplasmic reticulum and cytoplasmic streaming: fluorescence microscopical observations in adaxial epidermis cells of onion bulb scales Protoplasma 131 250–252 Occurrence Handle10.1007/BF01282989

    Article  Google Scholar 

  • H Quader A Hofmann E Schnepf (1987) ArticleTitleShape and movement of the endoplasmic reticulum in onion bulb epidermis cells: possible involvement of actin Eur J Cell Biol 44 17–26

    Google Scholar 

  • C Reuzeau KW Doolittle JG Mcnally BG Pickard (1997) ArticleTitleCovisualisation in living onion cells of putative integrin, putative spectrin, actin, putative intermediate filaments and other proteins at the plasma membrane and in an endomembranous sheath Protoplasma 199 173–197 Occurrence Handle11541651 Occurrence Handle10.1007/BF01294505 Occurrence Handle1:CAS:528:DyaK1cXnvVOiuw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • ES Reynolds (1963) ArticleTitleThe use of lead citrate of high pH as an electronopaque stain in electron microscopy J Cell Biol 17 208–213 Occurrence Handle13986422 Occurrence Handle10.1083/jcb.17.1.208 Occurrence Handle1:CAS:528:DyaF3sXktVClu70%3D

    Article  PubMed  CAS  Google Scholar 

  • A Scott S Wyatt PL Tsou D Robertson N Strömgren-Allen (1999) ArticleTitleModel system for plant cell biology: GFP imaging in living onion epidermal cells BioTechniques 26 1125–1132 Occurrence Handle10376152 Occurrence Handle1:CAS:528:DyaK1MXjvVanur8%3D

    PubMed  CAS  Google Scholar 

  • IV Seregin VB Ivanov (2001) ArticleTitlePhysiological aspects of cadmium and lead toxic effects on higher plants Russ J Plant Physiol 48 523–544 Occurrence Handle10.1023/A:1016719901147 Occurrence Handle1:CAS:528:DC%2BD3MXlvVSlsrY%3D

    Article  CAS  Google Scholar 

  • AJ Shaw (1990) Heavy metal tolerance in plants: evolutionary aspects CRC Press Boca Raton, Fla

    Google Scholar 

  • J Szpunar R Łobiński A Prange (2003) ArticleTitleHyphenated techniques for elemental speciation in biological systems Appl Spectrosc 57 102A–111A Occurrence Handle14658613 Occurrence Handle10.1366/000370203321558128 Occurrence Handle1:CAS:528:DC%2BD3sXivFajtLc%3D

    Article  PubMed  CAS  Google Scholar 

  • M Terasaki J Song JR Wong MJ Weiss LB Chen (1984) ArticleTitleLocalization of endoplasmic reticulum in living and glutaraldehyde-fixed cells with fluorescent dyes Cell 38 101–108 Occurrence Handle6432338 Occurrence Handle10.1016/0092-8674(84)90530-0 Occurrence Handle1:CAS:528:DyaL2cXmt1KisLs%3D

    Article  PubMed  CAS  Google Scholar 

  • CH Walker SP Hopkin RM Sibly DB Peakall (2002) Principles of ecotoxicology Wydawnictwo Naukowe PWN Warszawa

    Google Scholar 

  • M Wierzbicka (1987a) ArticleTitleLead accumulation and its translocation barriers in roots of Allium cepa L. autoradiographic and ultrastructural studies Plant Cell Environ 10 17–26 Occurrence Handle10.1111/j.1365-3040.1987.tb02075.x Occurrence Handle1:CAS:528:DyaL2sXitFWjtrw%3D

    Article  CAS  Google Scholar 

  • M Wierzbicka (1987b) ArticleTitleLead translocation and localization in Allium cepa roots Can J Bot 65 1851–1860 Occurrence Handle1:CAS:528:DyaL2sXlvFamtro%3D

    CAS  Google Scholar 

  • M Wierzbicka (1988) ArticleTitleMitotic disturbance induced by low doses of inorganic lead Caryologia 41 143–160 Occurrence Handle1:CAS:528:DyaL1MXptVeqsg%3D%3D

    CAS  Google Scholar 

  • M Wierzbicka (1989) ArticleTitleDisturbances in cytokinesis caused by inorganic lead Environ Exp Bot 29 123–133 Occurrence Handle10.1016/0098-8472(89)90044-0 Occurrence Handle1:CAS:528:DyaL1MXktVagtbo%3D

    Article  CAS  Google Scholar 

  • M Wierzbicka (1994) ArticleTitleThe resumption of mitotic activity in Allium cepa L. root tips during treatment with lead salts Environ Exp Bot 34 179–180 Occurrence Handle10.1016/0098-8472(94)90036-1

    Article  Google Scholar 

  • M Wierzbicka (1995) ArticleTitleHow lead loses its toxicity to plants Acta Soc Bot Pol 64 81–90

    Google Scholar 

  • M Wierzbicka (1998) ArticleTitleLead in the apoplast of Allium cepa L. root tips: ultrastructural studies Plant Sci 133 105–119 Occurrence Handle10.1016/S0168-9452(98)00023-5 Occurrence Handle1:CAS:528:DyaK1cXis1yis7o%3D

    Article  CAS  Google Scholar 

  • M Wierzbicka (1999a) ArticleTitleThe effect of lead on the cell cycle in the root meristem of Allium cepa L Protoplasma 207 186–194 Occurrence Handle10.1007/BF01282999 Occurrence Handle1:CAS:528:DyaK1MXmtVSnsb8%3D

    Article  CAS  Google Scholar 

  • M Wierzbicka (1999b) ArticleTitleComparison of lead tolerance in Allium cepa with other plant species Environ Pollut 104 41–52 Occurrence Handle10.1016/S0269-7491(98)00156-0 Occurrence Handle1:CAS:528:DyaK1MXpsFGrtA%3D%3D

    Article  CAS  Google Scholar 

  • M Wierzbicka D Antosiewicz (1993) ArticleTitleHow lead can easily enter the food chain: a study of plant roots Sci Total Environ Suppl Part 1 423–429 Occurrence Handle10.1016/S0048-9697(05)80043-9

    Article  Google Scholar 

  • M Wierzbicka M Pielichowska (2004) ArticleTitleAdaptation of Biscutella laevigata L, a metal hyperaccumulator, to growth on a zinc-lead waste heap in southern Poland. I: Differences between waste-heap and mountain populations Chemosphere 54 1663–1674 Occurrence Handle14675845 Occurrence Handle10.1016/j.chemosphere.2003.08.031 Occurrence Handle1:CAS:528:DC%2BD3sXpvVWgsbc%3D

    Article  PubMed  CAS  Google Scholar 

  • M Wierzbicka A Rostański (2002) ArticleTitleMicroevolutionary changes in the ecotypes of calamine waste heap vegetation near Olkusz, Poland: a review Acta Biol Cracov Bot 44 7–19

    Google Scholar 

  • RH Wilson AC Smith M Kacurakova PK Saunders N Wellner KW Waldron (2000) ArticleTitleThe mechanical properties and molecular dynamics of plant cell wall polysaccharides studied by Fourier-transform infrared spectroscopy Plant Physiol 124 397–405 Occurrence Handle10982452 Occurrence Handle10.1104/pp.124.1.397 Occurrence Handle1:CAS:528:DC%2BD3cXmvVGhtb0%3D

    Article  PubMed  CAS  Google Scholar 

  • A Woźny B Zatorska F Młodzianowski (1982) ArticleTitleInfluence of lead on the development of lupin seedlings and ultrastructural localization of this metal in the roots Acta Soc Bot Pol 51 345–351

    Google Scholar 

  • A Woźny J Michejda L Ratajczyk (2001) Basic plant cell biology Wydawnictwo Naukowe AM Poznań, Poland

    Google Scholar 

Download references

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Correspondence to M. H. Wierzbicka.

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Correspondence and reprints: Department of Ecotoxicology, Institute of Experimental Plant Biology, Faculty of Biology, University of Warsaw, Miecznikowa 1, 02-096 Warsaw, Poland.

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Wierzbicka, M., Przedpełska, E., Ruzik, R. et al. Comparison of the toxicity and distribution of cadmium and lead in plant cells. Protoplasma 231, 99–111 (2007). https://doi.org/10.1007/s00709-006-0227-6

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  • DOI: https://doi.org/10.1007/s00709-006-0227-6

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