Plant and Soil

, Volume 286, Issue 1–2, pp 377–391 | Cite as

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

  • Laurel A. Schaider
  • David R. Parker
  • David L. Sedlak
Original Paper

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.

Keywords

Bypass flow Free-ion activity model Metal–EDTA Metal uptake Phytoremediation Sand culture 

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

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References

  1. Beckett JT, Anderson WP (1972) Ferric-EDTA absorption by maize roots. Ion Transport in Plants; Proceedings of an International Meeting, Academic Press, LiverpoolGoogle Scholar
  2. 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 905:157–162PubMedCrossRefGoogle Scholar
  3. 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 130:51–62CrossRefGoogle Scholar
  4. 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 253:311–319CrossRefGoogle Scholar
  5. Bingham FT, Strong JE, Sposito G (1983) Influence of chloride salinity on cadmium uptake by Swiss chard. Soil Sci 135:160–165Google Scholar
  6. 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 31:860–865CrossRefGoogle Scholar
  7. 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 166:1057–1062CrossRefGoogle Scholar
  8. Cabrera D, Young SD, Rowell DL (1988) The toxicity of cadmium to barley plants as affected by complex formation with humic acid. Plant Soil 105:195–204CrossRefGoogle Scholar
  9. 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. 45–102Google Scholar
  10. 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 11:1033–1050Google Scholar
  11. 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 99:335–345CrossRefGoogle Scholar
  12. 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 21:1940–1945PubMedCrossRefGoogle Scholar
  13. 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 35:2589–2593PubMedCrossRefGoogle Scholar
  14. Crowdy SH, Tanton TW (1970) Water pathways in higher plants. J Exp Bot 21:102–111Google Scholar
  15. Degryse F, Smolders E, Merckx R (2006) Labile Cd complexes increase Cd availability to plants. Environ Sci Technol 40:830–836PubMedCrossRefGoogle Scholar
  16. Foote BD, Hanson JB (1964) Ion uptake by soybean root tissue depleted of calcium by ethylenediaminetetraacetic acid. Plant Physiol 39:450–460PubMedGoogle Scholar
  17. Grčman H, Velikonja-Bolta S, Vodnik D, Kos B, Leštan D (2001) EDTA enhanced heavy metal phytoextraction: metal accumulation, leaching and toxicity. Plant Soil 235:105–114CrossRefGoogle Scholar
  18. 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 77:21–24PubMedGoogle Scholar
  19. Hill-Cottingham DG, Lloyd-Jones CP (1965) The behaviour of iron chelating agents with plants. J Exp Bot 16:233–242Google Scholar
  20. Horst WJ, Klotz F, Szulkiewicz P (1990) Mechanical impedance increases aluminum tolerance of soybean (Glycine max) roots. Plant Soil 124:227–231CrossRefGoogle Scholar
  21. 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 202:211–216CrossRefGoogle Scholar
  22. 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 113–118Google Scholar
  23. 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 13:637–648Google Scholar
  24. NIST (1998) NIST Critically Selected Stability Constants of Metal Complexes Database, Ver 5.0. Gaithersburg, MD, U.S. Department of CommerceGoogle Scholar
  25. Nowack B, Kari FG, Hilger SU, Sigg L (1996) Determination of dissolved and adsorbed EDTA species in water and sediments by HPLC. Anal Chem 68:561–566CrossRefGoogle Scholar
  26. 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 143:163–177CrossRefGoogle Scholar
  27. Parker DR, Norvell WA (1999) Advances in solution culture methods for plant mineral nutrition research. Adv Agron 65:151–213Google Scholar
  28. 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 253–269Google Scholar
  29. 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 20:899–906PubMedCrossRefGoogle Scholar
  30. Pavan MA, Bingham FT (1982) Toxicity of aluminum to coffee seedlings grown in nutrient solution. Soil Sci Soc Am J 46:993–997CrossRefGoogle Scholar
  31. 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 28:1450–1462CrossRefGoogle Scholar
  32. Römheld V, Marschner H (1981) Effect of Fe stress on utilization of Fe chelates by efficient and inefficient plant species. J Plant Nutr 3:551–560Google Scholar
  33. 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 35:2854–2859PubMedCrossRefGoogle Scholar
  34. Sauvé S, Cook N, Hendershot WH, McBride MB (1996) Linking plant tissue concentrations and soil copper pools in urban contaminated soils. Environ Pollut 94:153–157PubMedCrossRefGoogle Scholar
  35. Schreiber L, Hartmann K, Skrabs M, Zeier J (1999) Apoplastic barriers in roots: chemical composition of endodermal and hypodermal cell walls. J Exp Bot 50:1267–1280CrossRefGoogle Scholar
  36. Skinner RH, Radin JW (1994) The effect of phosphorus nutrition on water flow through the apoplastic bypass of cotton roots. J Exp Bot 45:423–428Google Scholar
  37. Smolders E, Lambrechts RM, McLaughlin MJ, Tiller KG (1998) Effect of soil solution chloride on cadmium availability to Swiss chard. J Environ Qual 27:426–431CrossRefGoogle Scholar
  38. Smolders E, McLaughlin MJ (1996) Chloride increases cadmium uptake in Swiss chard in a resin-buffered nutrient solution. Soil Sci Soc Am J 60:1443–1447CrossRefGoogle Scholar
  39. Steudle E, Peterson CA (1998) How does water get through roots? J Exp Bot 49:775–788CrossRefGoogle Scholar
  40. Tanton TW, Crowdy SH (1971) The distribution of lead chelate in the transpiration stream of higher plants. Pestic Sci 2:211–213Google Scholar
  41. Vassil AD, Kapulnik Y, Raskin I, Salt DE (1998) The role of EDTA in lead transport and accumulation by Indian mustard. Plant Physiol 117:447–453PubMedCrossRefGoogle Scholar
  42. 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 41:1499–1507CrossRefGoogle Scholar
  43. Wallace A, North CP, Mueller RT, Shannon LM, Hemaidan N (1955) Behavior of chelating agents in plants. Proc Am Soc Hortic Sci 65:9–16Google Scholar
  44. Wu J, Hsu FC, Cunningham SD (1999) Chelate-assisted Pb phytoextraction: Pb availability, uptake, and translocation constraints. Environ Sci Technol 33:1898–1904CrossRefGoogle Scholar
  45. 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 19:329–336CrossRefGoogle Scholar
  46. 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 38:1141–1153Google Scholar
  47. 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 16:1569–1592CrossRefGoogle Scholar
  48. 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 210:302–311PubMedCrossRefGoogle Scholar
  49. Zimmermann HM, Steudle E (1998) Apoplastic transport across young maize roots: effect of the exodermis. Planta 206:7–19CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2006

Authors and Affiliations

  • Laurel A. Schaider
    • 1
    • 2
  • David R. Parker
    • 3
  • David L. Sedlak
    • 1
  1. 1.Department of Civil and Environmental EngineeringUniversity of CaliforniaBerkeleyUSA
  2. 2.Department of Environmental HealthHarvard School of Public HealthBostonUSA
  3. 3.Department of Environmental SciencesUniversity of CaliforniaRiversideUSA

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