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Uptake of EDTA-complexed Pb, Cd and Fe by solution- and sand-cultured Brassica juncea

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Abstract

Direct plant uptake of metals bound to chelating agents has important implications for metal uptake and the free-ion activity model. Uptake of hydrophilic solutes such as metal–EDTA complexes is believed to occur via bypass apoplastic flow, but many questions remain about the relative importance and selectivity of this pathway. In this study, Brassica juncea (Indian mustard) plants grown in solution- and sand-culture conditions were exposed to metal–EDTA complexes and to PTS, a hydrophilic fluorescent dye previously used as a tracer of apoplastic flow. The results suggest that there are two general phases of solute uptake. Under normal conditions, xylem sap solute concentrations are relatively low (i.e., <0.5% of concentration in solution) and there is a high degree of selectivity among different solutes, while under conditions of stress, xylem sap concentrations are significantly higher (i.e., >3% of concentration in solution) and the selectivity among solutes is less. In healthy plants, xylem sap metal–EDTA concentrations were generally an order of magnitude higher than those of PTS and differences among complexes were observed, with CdEDTA2− exhibiting slightly higher xylem sap concentrations than PbEDTA2− or FeEDTA−. Metal–EDTA complexes were found to dominate xylem sap metal speciation and the fraction of metal in xylem sap present as metal–EDTA was greater for non-nutrient metals (Pb, Cd) than for the nutrient metal Fe. Despite differences in root morphology between plants grown under solution- and sand-culture conditions, uptake of solutes was similar under both sets of growth conditions.

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Abbreviations

EDTA:

ethylenediaminetetraacetic acid

PTS:

8-hydroxy-1,3,6-pyrenetrisulfonic acid

EDDHA:

ethylenediaminedi(o-hydroxyphenylacetic) acid

MES:

2-(4-morpholino)ethanesulfonic acid

HBED:

N,N′-di-(2-hydroxybenzoyl)-ethylenediamine-N,N′-diacetic acid

References

  • Beckett JT, Anderson WP (1972) Ferric-EDTA absorption by maize roots. Ion Transport in Plants; Proceedings of an International Meeting, Academic Press, Liverpool

  • Bedsworth WW, Sedlak DL (2001) Determination of metal complexes of ethylenediaminetetraacetate in the presence of organic matter by high-performance liquid chromatography. J Chromatogr A 905:157–162

    Article  PubMed  CAS  Google Scholar 

  • Bell PF, Chaney RL, Angle JS (1991) Free metal activity and total metal concentrations as indices of micronutrient availability to barley [Hordeum vulgare (L.) cv. ‘Klages’]. Plant Soil 130:51–62

    Article  CAS  Google Scholar 

  • Bell PF, McLaughlin MJ, Cozens G, Stevens DP, Owens G, South H (2003) Plant uptake of 14C-EDTA, 14C-Citrate, and 14C-Histidine from chelator-buffered and conventional hydroponic solutions. Plant Soil 253:311–319

    Article  CAS  Google Scholar 

  • Bingham FT, Strong JE, Sposito G (1983) Influence of chloride salinity on cadmium uptake by Swiss chard. Soil Sci 135:160–165

    CAS  Google Scholar 

  • Blaylock MJ, Salt DE, Dushenkov S, Zakharova O, Gussman C, Kapulnik Y, Ensley BD, Raskin I (1997) Enhanced accumulation of Pb in Indian mustard by soil-applied chelating agents. Environ Sci Technol 31:860–865

    Article  Google Scholar 

  • Borges R, Miguel EC, Dias JMR, da Cunha M, Bressan-Smith RE, de Oliveira JG, de Souza GA (2004) Ultrastructural, physiological and biochemical analyses of chlorate toxicity on rice seedlings. Plant Sci 166:1057–1062

    Article  CAS  Google Scholar 

  • Cabrera D, Young SD, Rowell DL (1988) The toxicity of cadmium to barley plants as affected by complex formation with humic acid. Plant Soil 105:195–204

    Article  CAS  Google Scholar 

  • Campbell PGC (1995) Interactions between trace metals and aquatic organisms: a critique of the free-ion activity model. In: Tessier A, Turner DR (eds) Metal speciation and bioavailability in aquatic systems. John Wiley & Sons, New York pp. 45–102

  • Chaney RL (1988) Plants can utilize iron from Fe-N,N′-di-(2-hydroxybenzoyl)-ethylene-N,N′-diacetic acid, a ferric chelate with 106 greater formation constant than Fe-EDDHA. J Plant Nutr 11:1033–1050

    CAS  Google Scholar 

  • Checkai RT, Corey RB, Helmke PA (1987) Effects of ionic and complexed metal concentrations on plant uptake of cadmium and micronutrient metals from solution. Plant Soil 99:335–345

    Article  CAS  Google Scholar 

  • Collins RN, Merrington G, McLaughlin MJ, Knudsen C (2002) Uptake of intact zinc-ethylenediaminetetraacetic acid from soil is dependent on plant species and complex concentration. Environ Toxicol Chem 21:1940–1945

    Article  PubMed  CAS  Google Scholar 

  • Collins RN, Onisko BC, McLaughlin MJ, Merrington G (2001) Determination of metal–EDTA complexes in soil solution and plant xylem by ion chromatography-electrospray mass spectrometry. Environ Sci Technol 35:2589–2593

    Article  PubMed  CAS  Google Scholar 

  • Crowdy SH, Tanton TW (1970) Water pathways in higher plants. J Exp Bot 21:102–111

    CAS  Google Scholar 

  • Degryse F, Smolders E, Merckx R (2006) Labile Cd complexes increase Cd availability to plants. Environ Sci Technol 40:830–836

    Article  PubMed  CAS  Google Scholar 

  • Foote BD, Hanson JB (1964) Ion uptake by soybean root tissue depleted of calcium by ethylenediaminetetraacetic acid. Plant Physiol 39:450–460

    PubMed  CAS  Google Scholar 

  • Grčman H, Velikonja-Bolta S, Vodnik D, Kos B, Leštan D (2001) EDTA enhanced heavy metal phytoextraction: metal accumulation, leaching and toxicity. Plant Soil 235:105–114

    Article  Google Scholar 

  • Hanson PJ, Sucoff EI, Markhart AH (1985) Quantifying apoplastic flux through red pine root systems using trisodium, 3-hydroxy-5,8,10-pyrenetrisulfonate. Plant Physiol 77:21–24

    PubMed  CAS  Google Scholar 

  • Hill-Cottingham DG, Lloyd-Jones CP (1965) The behaviour of iron chelating agents with plants. J Exp Bot 16:233–242

    CAS  Google Scholar 

  • Horst WJ, Klotz F, Szulkiewicz P (1990) Mechanical impedance increases aluminum tolerance of soybean (Glycine max) roots. Plant Soil 124:227–231

    Article  CAS  Google Scholar 

  • McLaughlin MJ, Andrew SJ, Smart MK, Smolders E (1998) Effects of sulfate on cadmium uptake by Swiss chard: I. Effects of complexation and calcium competition in nutrient solutions. Plant Soil 202:211–216

    Article  CAS  Google Scholar 

  • McLaughlin MJ, Smolders E, Merckx R, Maes A (1997) Plant uptake of Cd and Zn in chelator-buffered nutrient solution depends on ligand type. In: Ando T (ed) Plant nutrition––for sustainable food production and environment. Kluwer Academic Publishers, Japan, pp 113–118

  • Moon GJ, Clough BF, Peterson CA, Allaway WG (1986) Apoplastic and symplastic pathways in Avicennia marina (Forsk.) Vierh. roots revealed by fluorescent tracer dyes. Austral. J Plant Physiol 13:637–648

    CAS  Google Scholar 

  • NIST (1998) NIST Critically Selected Stability Constants of Metal Complexes Database, Ver 5.0. Gaithersburg, MD, U.S. Department of Commerce

  • Nowack B, Kari FG, Hilger SU, Sigg L (1996) Determination of dissolved and adsorbed EDTA species in water and sediments by HPLC. Anal Chem 68:561–566

    Article  CAS  Google Scholar 

  • Parker DR, Aguilera JJ, Thomason DN (1992) Zinc-phosphorus interactions in two cultivars of tomato (Lycopersicon esculentum L.) grown in chelator-buffered nutrient solutions. Plant Soil 143:163–177

    Article  CAS  Google Scholar 

  • Parker DR, Norvell WA (1999) Advances in solution culture methods for plant mineral nutrition research. Adv Agron 65:151–213

    CAS  Google Scholar 

  • Parker DR, Norvell WA, Chaney RL (1995) GEOCHEM-PC. A chemical speciation program for IBM and compatible computers. In: Loeppert RH (ed) Chemical equilibrium and reaction models. Soil Science Society of America, Madison, WI, pp 253–269

  • Parker DR, Pedler JF, Ahnstrom ZS, Resketo M (2001) Reevaluating the free-ion activity model of trace metal toxicity toward higher plants: experimental evidence with copper and zinc. Environ Toxicol Chem 20:899–906

    Article  PubMed  CAS  Google Scholar 

  • Pavan MA, Bingham FT (1982) Toxicity of aluminum to coffee seedlings grown in nutrient solution. Soil Sci Soc Am J 46:993–997

    Article  CAS  Google Scholar 

  • Ranathunge K, Steudle E, Lafitte R (2005) A new precipitation technique provides evidence for the permeability of Casparian bands to ions in young roots of corn (Zea mays L.) and rice (Oryza sativa L.). Plant Cell Environ 28:1450–1462

    Article  CAS  Google Scholar 

  • Römheld V, Marschner H (1981) Effect of Fe stress on utilization of Fe chelates by efficient and inefficient plant species. J Plant Nutr 3:551–560

    Google Scholar 

  • Sarret G, Vangronsveld J, Manceau A, Musso M, D’Haen J, Menthonnex JJ, Hazemann JL (2001) Accumulation forms of Zn and Pb in Phaseolus vulgaris in the presence and absence of EDTA. Environ Sci Technol 35:2854–2859

    Article  PubMed  CAS  Google Scholar 

  • Sauvé S, Cook N, Hendershot WH, McBride MB (1996) Linking plant tissue concentrations and soil copper pools in urban contaminated soils. Environ Pollut 94:153–157

    Article  PubMed  Google Scholar 

  • Schreiber L, Hartmann K, Skrabs M, Zeier J (1999) Apoplastic barriers in roots: chemical composition of endodermal and hypodermal cell walls. J Exp Bot 50:1267–1280

    Article  CAS  Google Scholar 

  • Skinner RH, Radin JW (1994) The effect of phosphorus nutrition on water flow through the apoplastic bypass of cotton roots. J Exp Bot 45:423–428

    CAS  Google Scholar 

  • Smolders E, Lambrechts RM, McLaughlin MJ, Tiller KG (1998) Effect of soil solution chloride on cadmium availability to Swiss chard. J Environ Qual 27:426–431

    Article  Google Scholar 

  • Smolders E, McLaughlin MJ (1996) Chloride increases cadmium uptake in Swiss chard in a resin-buffered nutrient solution. Soil Sci Soc Am J 60:1443–1447

    Article  CAS  Google Scholar 

  • Steudle E, Peterson CA (1998) How does water get through roots? J Exp Bot 49:775–788

    Article  CAS  Google Scholar 

  • Tanton TW, Crowdy SH (1971) The distribution of lead chelate in the transpiration stream of higher plants. Pestic Sci 2:211–213

    CAS  Google Scholar 

  • Vassil AD, Kapulnik Y, Raskin I, Salt DE (1998) The role of EDTA in lead transport and accumulation by Indian mustard. Plant Physiol 117:447–453

    Article  PubMed  CAS  Google Scholar 

  • Villagarcia MR, Carter TE, Rufty TW, Niewoehner AS, Jennette MW, Arrellano C (2001) Genotypic rankings for aluminum tolerance of soybean roots grown in hydroponics and sand culture. Crop Science 41:1499–1507

    Article  Google Scholar 

  • Wallace A, North CP, Mueller RT, Shannon LM, Hemaidan N (1955) Behavior of chelating agents in plants. Proc Am Soc Hortic Sci 65:9–16

    CAS  Google Scholar 

  • Wu J, Hsu FC, Cunningham SD (1999) Chelate-assisted Pb phytoextraction: Pb availability, uptake, and translocation constraints. Environ Sci Technol 33:1898–1904

    Article  CAS  Google Scholar 

  • Yadav R, Flowers TJ, Yeo AR (1996) The involvement of the transpirational bypass flow in sodium uptake by high- and low-sodium-transporting lines of rice developed through intravarietal selection. Plant Cell Environ 19:329–336

    Article  CAS  Google Scholar 

  • Yeo AR, Yeo ME, Flowers TJ (1987) The contribution of an apoplastic pathway to sodium uptake by rice roots in saline conditions. J Exp Bot 38:1141–1153

    CAS  Google Scholar 

  • Zaiter H, Mahfouz B (1993) Salinity effect on root and shoot characteristics of common and tepary beans evaluated under hydroponic solution and sand culture. J Plant Nutr 16:1569–1592

    Article  Google Scholar 

  • Zimmermann HM, Hartmann K, Schreiber L, Steudle E (2000) Chemical composition of apoplastic transport barriers in relation to radial hydraulic conductivity of corn roots (Zea mays L.). Planta 210:302–311

    Article  PubMed  CAS  Google Scholar 

  • Zimmermann HM, Steudle E (1998) Apoplastic transport across young maize roots: effect of the exodermis. Planta 206:7–19

    Article  CAS  Google Scholar 

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Acknowledgements

The authors gratefully acknowledge David Thomason for his assistance in performing the sand culture experiments. L.A.S. was funded by a training fellowship from the University of California Toxic Substances Research and Teaching Program.

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Authors and Affiliations

  1. Department of Civil and Environmental Engineering, University of California, Berkeley, CA, 94720, USA

    Laurel A. Schaider & David L. Sedlak

  2. Department of Environmental Health, Harvard School of Public Health, 401 Park Drive, Landmark Center West, 404B, Boston, MA, 02215, USA

    Laurel A. Schaider

  3. Department of Environmental Sciences, University of California, Riverside, CA, 92521, USA

    David R. Parker

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  1. Laurel A. Schaider
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  2. David R. Parker
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Correspondence to Laurel A. Schaider.

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Schaider, L.A., Parker, D.R. & Sedlak, D.L. Uptake of EDTA-complexed Pb, Cd and Fe by solution- and sand-cultured Brassica juncea . Plant Soil 286, 377–391 (2006). https://doi.org/10.1007/s11104-006-9049-8

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