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Enhanced cadmium accumulation in maize roots—the impact of organic acids

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Abstract

Low molecular weight organic acids are important components of root exudates and therefore, knowledge regarding the mechanisms of cadmium (Cd) uptake and distribution within plants under the influence of organic acids, is necessary for a better understanding of Cd behavior in the plant–soil system. In this study, acetic and malic acids increased the uptake of Cd by maize (Zea mays L. cv. TY2) roots and enhanced Cd accumulation in shoots under hydroponic conditions. Concentration-dependent net Cd influx in the presence and absence of organic acids could be resolved into linear and saturable components. The saturable component followed Michaelis–Menten kinetics, which indicated that Cd uptake across the plasma membrane was transporter-mediated. While the K m values were similar, the V max values in the presence of acetic and malic acids were respectively 6.0 and 3.0 times that of the control. Zinc transporters were the most probable pathways for Cd accumulation. It was hypothesized that Cd(II)–organic acid complexes associated with the root zone, could decompose and liberate Cd2+ for subsequent absorption by maize roots; and that in the layer of the roots or within the root free space, depletion of Cd2+ was buffered by the presence of Cd(II)–organic acid complexes. Plant response to elevated Cd levels involved overproduction of organic acids in maize roots as a resistance mechanism to alleviate Cd toxicity.

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References

  • 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 

  • Berne RM, Levy MN (1998) Physiology. Mosby, Inc., St. Louis, MO USA, 1131 pp

    Google Scholar 

  • Chaudhry FM, Loneragan JF (1972) Zinc absorption by wheat seedlings and the nature of its inhibition by alkaline earth cations. J Exp Bot 23:552–560

    CAS  Google Scholar 

  • Cieśliński G, Van Rees KCJ, Szmigielska AM, Krishnamurti GSR, Huang PM (1998) Low-molecular-weight-organic acids in rhizosphere soils of durum wheat and their effect on cadmium bioaccumulation. Plant Soil 203:109–117

    Article  Google Scholar 

  • Clemens S (2001) Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212:475–486

    Article  PubMed  CAS  Google Scholar 

  • Cohen CK, Fox TC, Garvin DF, Kochian LV (1998) The role of iron-deficiency stress responses in stimulating heavy-metal transport in plants. Plant Physiol 116:1063–1072

    Article  PubMed  CAS  Google Scholar 

  • Connolly EL, Fett JP, Guerinot ML (2002) Expression of the IRT1 metal transporter is controlled by metals at the levels of transcript and protein accumulation. Plant Cell 14:1347–1357

    Article  PubMed  CAS  Google Scholar 

  • DiTomaso JM, Hart JJ, Kochian LV (1992) Transport kinetics and metabolism of exogenously applied putrescine in roots of intact maize seedlings. Plant Physiol 98:611–620

    PubMed  CAS  Google Scholar 

  • Dudka S, Miller WP (1999) Accumulation of potentially toxic elements in plants and their transfer to human food chain. J Environ Sci Health, Part B 34:681–708

    CAS  Google Scholar 

  • Essah PA, Davenport R, Tester M (2003) Sodium influx and accumulation in arabidopsis. Plant Physiol 133:307–318

    Article  PubMed  CAS  Google Scholar 

  • Han F, Shan XQ, Zhang J, Xie YN, Pei ZG, Zhang SZ, Zhu YG, Wen B (2005) Organic acids promote the uptake of lanthanum by barley roots. New Phytol 165:481–492

    Article  PubMed  CAS  Google Scholar 

  • Hart JJ, Di Tomaso JM, Linscott DL, Kochian LV (1992) Characterization of the transport and cellular compartmentation of paraquat in roots of intact maize seedlings. Pestic Biochem Physiol 43:212–222

    Article  CAS  Google Scholar 

  • Hart JJ, Welch RM, Norvell WA, Sullivan LA, Kochian LV (1998) Characterization of cadmium binding, uptake, and translocation in intact seedlings of bread and durum wheat cultivars. Plant Physiol 116:1413–1420

    Article  PubMed  CAS  Google Scholar 

  • Hill KA, Lion LW, Ahner BA (2002) Reduced Cd accumulation in Zea mays: a protective role for phytosiderophores. Environ Sci Technol 36:5363–5368

    Article  PubMed  CAS  Google Scholar 

  • Huang JW, Blaylock MJ, Kapulnik Y, Ensley BD (1998) Phytoremediation of uranium-contaminated soils: role of organic acids in triggering uranium hyperaccumulation in plants. Environ Sci Technol 32:2004–2008

    Article  CAS  Google Scholar 

  • Jones DL (1998) Organic acids in the rhizosphere—a critical review. Plant Soil 205:25–44

    Article  CAS  Google Scholar 

  • Jones DL, Darrah PR (1994) Role of root derived organic acids in the mobilization of nutrients from the rhizosphere. Plant Soil 166:247–257

    Article  CAS  Google Scholar 

  • Keller C, Hammer D, Kayser A, Richner W, Brodbeck M, Sennhauser M (2003) Root development and heavy metal phytoextraction efficiency: comparison of different plant species in the field. Plant Soil 249:67–81

    Article  CAS  Google Scholar 

  • Krishnamurti GSR, Cieśliński G, Huang PM, Van Rees KCJ (1997) Kinetics of cadmium release from soils as influenced by organic acids: implication in cadmium availability. J Environ Qual 26:271–277

    Article  CAS  Google Scholar 

  • Küpper H, Lombi E, Zhao FJ, McGrath SP (2000) Cellular compartmentation of cadmium and zinc in relation to other elements in the hyperaccumulator Arabidopsis halleri. Planta 212:75–84

    Article  PubMed  Google Scholar 

  • Lasat MM, Baker AJM, Kochian LV (1996) Physiological characterization of root Zn2+ absorption and translocation to shoots in Zn hyperaccumulator and nonaccumulator species of Thlaspi. Plant Physiol 112:1715–1722

    PubMed  CAS  Google Scholar 

  • Lasat MM, Pence NS, Garvin DF, Ebbs SD, Kochian LV (2000) Molecular physiology of zinc transport in the Zn hyperaccumulator Thlaspi caerulescens. J Exp Bot 51:71–79

    Article  PubMed  CAS  Google Scholar 

  • LIamas A, Ullrich CI, Sanz A (2000) Cd2+ effects on transmembrane electrical potential difference, respiration and membrane permeability of rice (Oryza sativa L.) roots. Plant Soil 219:21–28

    Article  Google Scholar 

  • Lindberg S, Landberg T, Greger M (2004) A new method to detect cadmium uptake in protoplasts. Planta 219:526–532

    Article  PubMed  CAS  Google Scholar 

  • Lombi E, Tearall KL, Howarth JR, Zhao FJ, Hawkesford MJ, McGrath SP (2002) Influence of iron status on cadmium and zinc uptake by different ecotypes of the hyperaccumulator Thlaspi caerulescens. Plant Physiol 128:1359–1367

    Article  PubMed  CAS  Google Scholar 

  • López-Bucio J, Nieto-Jacobo MF, Ramírez-Rodríguez V, Herrera-Estrella L (2000) Organic acid metabolism in plants: from adaptive physiology to transgenic varieties for cultivation in extreme soils. Plant Sci 160:1–13

    Article  PubMed  Google Scholar 

  • Montague MJ (1993) Calcium antagonists inhibit sustained gibberellic acid-induced growth of Avena (oat) stem segments. Plant Physiol 101:399–405

    PubMed  CAS  Google Scholar 

  • Mullins GL, Sommers LE (1986) Cadmium and zinc influx characteristics by intact corn (Zea mays L.) seedlings. Plant Soil 96:153–164

    Article  CAS  Google Scholar 

  • Nigam R, Srivastava S, Prakash S, Srivastava MM (2000) Effect of organic acids on the availability of cadmium in wheat. Chem Spec Bioavailab 12:125–132

    CAS  Google Scholar 

  • Nor YM, Cheng HH (1986) Chemical speciation and bioavailability of copper: uptake and accumulation by Eichornia. Environ Toxicol Chem 5:941–947

    CAS  Google Scholar 

  • Norvell WA, Welch RM (1993) Growth and nutrient uptake by barley (Hordeum vulgare L. cv Herta). Studies using an N-(2-hydroxyethyl)ethylenedinitrilotriacetic acid-buffered nutrient solution technique. Plant Physiol 101:619–625

    PubMed  CAS  Google Scholar 

  • Pellet DM, Grunes DL, Kochian LV (1995) Organic acid exudation as an aluminum-tolerance mechanism in maize (Zea mays L.). Planta 196:788–795

    Article  CAS  Google Scholar 

  • Pence NS, Larsen PB, Ebbs SD, Letham DLD, Lasat MM, Garvin DF, Eide D, Kochian LV (2000) The molecular physiology of heavy metal transporter in the Zn/Cd hyperaccumulator Thlaspi caerulescens. Proc Natl Acad Sci USA 97:4956–4960

    Article  PubMed  CAS  Google Scholar 

  • Piñeros MA, Magalhaes JV, Carvalho Alves VM, Kochian LV (2002) The physiology and biophysics of an aluminum tolerance mechanism based on root citrate exudation in Maize. Plant Physiol 129:1194–1206

    Article  PubMed  CAS  Google Scholar 

  • Qin F, Shan XQ, Wen B (2004) Effects of low-molecular-weight organic acids and residence time on desorption of Cu, Cd, and Pb from soils. Chemosphere 57:253–263

    Article  PubMed  CAS  Google Scholar 

  • Rauser WE (1987) Compartmental efflux analysis and removal of extracellular cadmium from roots. Plant Physiol 85:62–65

    Article  PubMed  CAS  Google Scholar 

  • Rauser WE (1999) Structure and function of metal chelators produced by plants—the case for organic acids, amino acids, phytin and metallothioneins. Cell Biochem Biophys 31:19–48

    Article  PubMed  CAS  Google Scholar 

  • Robinson BH, Leblanc M, Petit D, Brooks RR, Kirkman JH, Gregg PEH (1998) The potential of Thlaspi caerulescens for phytoremediation of contaminated soils. Plant Soil 203:47–56

    Article  CAS  Google Scholar 

  • Schwartz C, Echevarria G, Morel JL (2003) Phytoextraction of cadmium with Thlaspi caerulescens. Plant Soil 249:27–35

    Article  CAS  Google Scholar 

  • Senden MHMN, van der Meer AJGM, Verburg TG, Wolterbeek HTH (1995) Citric acid in tomato plant roots and its effect on cadmium uptake and distribution. Plant Soil 171:333–339

    Article  CAS  Google Scholar 

  • Shan XQ, Lian J, Wen B (2002) Effect of organic acids on adsorption and desorption of rare earth elements. Chemosphere 47:701–710

    Article  PubMed  CAS  Google Scholar 

  • Shan XQ, Wang HO, Zhang SZ, Zhou HF, Zheng Y, Yu H, Wen B (2003) Accumulation and uptake of light rare earth elements in a hyperaccumulator Dicropteris dichotoma. Plant Sci 165:1343–1353

    Article  CAS  Google Scholar 

  • Smith RM, Martell AE, Motekaitis RJ (1997) NIST critically selected stability constants of metals complexes database. Version 4.0. US Department of Commerce, National Institute of Standards and Technology, Gaithersburg, MD

    Google Scholar 

  • Srivastava S, Prakash S, Srivastava MM (1999) Chromium mobilization and plant availability—the impact of organic complexing ligands. Plant Soil 212:203–208

    Article  CAS  Google Scholar 

  • Veltrup W (1978) Characteristics of zinc uptake by barley roots. Physiol Plant 42:190–194

    Article  CAS  Google Scholar 

  • Wang WS, Shan XQ, Wen B, Zhang SZ (2004a) A method for predicting bioavailability of rare earth elements in soils to maize. Environ Toxicol Chem 23:767–773

    Article  CAS  Google Scholar 

  • Wang ZW, Zhang SZ, Shan XQ (2004b) Effects of low-molecular-weight-organic-acids on uptake of lanthanum by wheat roots. Plant Soil 261:163–170

    Article  CAS  Google Scholar 

  • Westall JC, Zachary JL, Morel FMM (1976) MINEQL: a computer program for the calculation of chemical equilibrium composition of aqueous systems. Parsons RM Laboratory, Massachusettes Institute of Technology

  • Zhao FJ, Lombi E, McGrath SP (2003) Assessing the potential for zinc and cadmium phytoextraction with the hyperaccumulator Thlaspi caerulescens. Plant Soil 249:37–43

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was supported by the National Natural Science Foundation of China (Grant 20237010 and 20177030). We thank Prof. Naibing Bai (Institute of Software, Chinese Academy of Sciences) for generous help in Cd speciation calculations.

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Correspondence to Xiaoquan Shan.

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Han, F., Shan, X., Zhang, S. et al. Enhanced cadmium accumulation in maize roots—the impact of organic acids. Plant Soil 289, 355–368 (2006). https://doi.org/10.1007/s11104-006-9145-9

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