Abstract
The effect of N form (NO3 − versus NH4 +) on growth and uptake of Cd and Zn by the hyperaccumulator Thlaspi caerulescens (Ganges ecotype) was investigated in hydroponic and rhizobox experiments. In the hydroponic experiments, NO3 − or NH4 + was supplied to plants with the pH of the nutrient solution being unbuffered or buffered at around 6.0. A moderately contaminated soil was used in the rhizobox experiment with or without additions of NO3 −, NH4 + or NH4 + + DCD (dicyanodiamide, a nitrification inhibitor). A higher biomass was obtained when N was supplied as NO3 − in both experiments, indicating that T. caerulescens prefers NO3 − over NH4 +. In the hydroponic experiments, supplying NO3 − resulted in a doubling of Cd concentration in the shoots compared with the NH4 + treatment, regardless whether solution pH was buffered or not. The form of N also had a noticeable effect on root Zn concentrations. In the rhizosphere box experiment, rhizosphere pH was markedly influenced by the N treatment. The acidification in the NH4 + and NH4 + + DCD treatments increased the concentrations of extractable Cd and Zn, both of which showed a considerable depletion in the rhizosphere. However, total uptake of Cd and Zn were highest in the NO3 − treatment, despite the fact that concentrations of extractable Cd and Zn in the rhizosphere were the lowest in this treatment. The results showed that supplying N as NO3 − promoted growth and phytoextraction of Cd and Zn by T. caerulescens compared with NH4 +.
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Assunção AGL, Bleeker P, ten Bookum WM, Vooijs R, Schat H (2008) Intraspecific variation of metal preference patterns for hyperaccumulation in Thlaspi caerulescens: evidence from binary metal exposures. Plant Soil 303:289–299. doi:10.1007/s11104-007-9508-x
Assunção AGL, Bookum WM, Nelissen HJM, Vooijs R, Schat H, Ernst WHO (2003) Differential metal-specific tolerance and accumulation patterns among Thlaspi caerulescens populations originating from different soil types. New Phytol 159:411–419. doi:10.1046/j.1469-8137.2003.00819.x
Brooks RR (1998) Plants that hyperaccumulate heavy metals. CAB International, Wallingford
Brown SL, Chaney RL, Angle JS, Baker AJM (1994) Phytoremediation potential of Thlaspi caerulescens and Bladder Campion for zinc- and cadmium-contaminated soil. J Environ Qual 23:1151–1157
Chaney RL, Angle JS, Broadhurst CL, Peters CA, Tappero RV, Sparks DL (2007) Improved understanding of hyperaccumulation yields commercial phytoextraction and phytomining technologies. J Environ Qual 36:1429–1443. doi:10.2134/jeq2006.0514
Hammond JP, Bowen HC, White PJ, Mills V, Pyke KA, Baker AJM, Whiting SN, May ST, Broadley MR (2006) A comparison of the Thlaspi caerulescens and Thlaspi arvense shoot transcriptomes. New Phytol 170:239–260. doi:10.1111/j.1469-8137.2006.01662.x
Ju X, Liu X, Zhang F (2004) Nitrogen transformations in a Chinese Aquic Cambisol applied urea with dicyandiamide or plant residues. Commun Soil Sci Plant Anal 35:2397–2416. doi:10.1081/CSS-200030318
Kirkby EA, Knight AH (1977) Influence of level of nitrate nutrition on ion uptake and assimilation, organic-acid accumulation, and cation-anion balance in whole tomato plants. Plant Physiol 60:349–353
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. doi:10.1007/s004250000366
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
Lombi E, Zhao FJ, Dunham SJ, McGrath SP (2000) Cadmium accumulation in populations of Thlaspi caerulescens and Thlaspi goesingense. New Phytol 145:11–20. doi:10.1046/j.1469-8137.2000.00560.x
Lombi E, Zhao FJ, Dunham SJ, McGrath SP (2001a) Phytoremediation of heavy metal-contaminated soils: Natural hyperaccumulation versus chemically enhanced phytoextraction. J Environ Qual 30:1919–1926
Lombi E, Zhao FJ, McGrath SP, Young SD, Sacchi GA (2001b) Physiological evidence for a high-affinity cadmium transporter highly expressed in a Thlaspi caerulescens ecotype. New Phytol 149:53–60. doi:10.1046/j.1469-8137.2001.00003.x
Loosemore N, Straczek A, Hinsinger P, Jaillard B (2004) Zinc mobilisation from a contaminated soil by three genotypes of tobacco as affected by soil and rhizosphere pH. Plant Soil 260:19–32. doi:10.1023/B:PLSO.0000030173.71500.e1
Marschner H (1995) Mineral Nutrition of Higher Plants. Academic, London
Maxted AP, Black CR, West HM, Crout NMJ, McGrath SP, Young SD (2007) Phytoextraction of cadmium and zinc from arable soils amended with sewage sludge using Thlaspi caerulescens: development of a predictive model. Environ Pollut 150:363–372. doi:10.1016/j.envpol.2007.01.021
McGrath SP, Zhao FJ (2003) Phytoextraction of metals and metalloids from contaminated soils. Curr Opin Biotechnol 14:277–282. doi:10.1016/S0958-1669(03)00060-0
McGrath SP, Lombi E, Gray CW, Caille N, Dunham SJ, Zhao FJ (2006) Field evaluation of Cd and Zn phytoextraction potential by the hyperaccumulators Thlaspi caerulescens and Arabidopsis halleri. Environ Pollut 141:115–125. doi:10.1016/j.envpol.2005.08.022
McGrath SP, Zhao FJ, Lombi E (2001) Plant and rhizosphere processes involved in phytoremediation of metal-contaminated soils. Plant Soil 232:207–214. doi:10.1023/A:1010358708525
Parker DR, Norvell WA, Chaney RL (1995) GEOCHEM-PC - A chemical speciation program for IBM and compatible personal computers. In: Loeppert RH (ed) Chemical equilibrium and reaction models, soil science society of America. American Society of Agronomy, Madison, pp 253–269
Pence NS, Larsen PB, Ebbs SD, Letham DLD, Lasat MM, Garvin DF, Eide D, Kochian LV (2000) The molecular physiology of heavy metal transport in the Zn/Cd hyperaccumulator Thlaspi caerulescens. Proc Natl Acad Sci USA 97:4956–4960. doi:10.1073/pnas.97.9.4956
Plette ACC, Nederlof MM, Temminghoff EJM, van Riemsdijk WH (1999) Bioavailability of heavy metals in terrestrial and aquatic systems: a quantitative approach. Environ Toxicol Chem 18:1882–1890. doi:10.1897/1551-5028(1999)018<1882:BOHMIT>2.3.CO;2
Puschenreiter M, Stöger G, Lombi E, Horak O, Wenzel WW (2001) Phytoextraction of heavy metal contaminated soils with Thlaspi goesingense and Amaranthus hybridus: Rhizosphere manipulation using EDTA and ammonium sulfate. J Plant Nutr Soil Sci 164:615–621.
Puschenreiter M, Schnepf A, Millan IM, Fitz WJ, Horak O, Klepp J, Schrefl T, Lombi E, Wenzel WW (2005) Changes of Ni biogeochemistry in the rhizosphere of the hyperaccumulator Thlaspi goesingense. Plant Soil 271:205–218. doi:10.1007/s11104-004-2387-5
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. doi:10.1023/A:1004328816645
Roosens N, Verbruggen N, Meerts P, Ximenez-Embun P, Smith JAC (2003) Natural variation in cadmium tolerance and its relationship to metal hyperaccumulation for seven populations of Thlaspi caerulescens from western Europe. Plant Cell Environ 26:1657–1672. doi:10.1046/j.1365-3040.2003.01084.x
Schwartz C, Morel JL, Saumier S, Whiting SN, Baker AJM (1999) Root development of the Zinc-hyperaccumulator plant Thlaspi caerulescens as affected by metal origin, content and localization in soil. Plant Soil 208:103–115. doi:10.1023/A:1004519611152
van de Mortel JE, Villanueva LA, Schat H, Kwekkeboom J, Coughlan S, Moerland PD, van Themaat EVL, Koornneef M, Aarts MGM (2006) Large expression differences in genes for iron and zinc homeostasis, stress response, and lignin biosynthesis distinguish roots of Arabidopsis thaliana and the related metal hyperaccumulator Thlaspi caerulescens. Plant Physiol 142:1127–1147. doi:10.1104/pp.106.082073
Wang AS, Angle JS, Chaney RL, Delorme TA, Reeves RD (2006) Soil pH effects on uptake of Cd and Zn by Thlaspi caerulescens. Plant Soil 281:325–337. doi:10.1007/s11104-005-4642-9
Wang MY, Glass ADM, Shaff JE, Kochian LV (1994) Ammonium uptake by rice roots. 3. Electrophysiology. Plant Physiol 104:899–906
Wenzel WW, Unterbrunner R, Sommer P, Sacco P (2003) Chelate-assisted phytoextraction using canola (Brassica napus L.) in outdoors pot and lysimeter experiments. Plant Soil 249:83–96. doi:10.1023/A:1022516929239
Whiting SN, Broadley MR, White PJ (2003) Applying a solute transfer model to phytoextraction: Zinc acquisition by Thlaspi caerulescens. Plant Soil 249:45–56. doi:10.1023/A:1022542725880
Whiting SN, Leake JR, McGrath SP, Baker AJM (2000) Positive responses to Zn and Cd by roots of the Zn and Cd hyperaccumulator Thlaspi caerulescens. New Phytol 145:199–210. doi:10.1046/j.1469-8137.2000.00570.x
Xing JP, Jiang RF, Ueno D, Ma JF, Schat H, McGrath SP, Zhao FJ (2008) Variation in root-to-shoot translocation of Cd and Zn among different accessions of the hyperaccumulators Thlaspi caerulescens and Thlaspi praecox. New Phytol 178:315–325. doi:10.1111/j.1469-8137.2008.02376.x
Yanai J, Zhao FJ, McGrath SP (2006) Effect of soil characteristics on Cd uptake by the hyperaccumulator Thlaspi caerulescens. Environ Pollut 139:167–175. doi:10.1016/j.envpol.2005.03.013
Zaccheo P, Crippa L, Pasta VD (2006) Ammonium nutrition as a strategy for cadmium mobilisation in the rhizosphere of sunflower. Plant Soil 283:43–56. doi:10.1007/s11104-005-4791-x
Zhao FJ, Hamon RE, Lombi E, McLaughlin MJ, McGrath SP (2002) Characteristics of cadmium uptake in two contrasting ecotypes of the hyperaccumulator Thlaspi caerulescens. J Exp Bot 53:535–543. doi:10.1093/jexbot/53.368.535
Zhao FJ, Hamon RE, McLaughlin MJ (2001) Root exudates of the hyperaccumulator Thlaspi caerulescens do not enhance metal mobilization. New Phytol 151:613–620. doi:10.1046/j.0028-646x.2001.00213.x
Zhao FJ, Lombi E, McGrath SP (2003) Assessing the potential for zinc and cadmium phytoremediation with the hyperaccumulator Thlaspi caerulescens. Plant Soil 249:37–43. doi:10.1023/A:1022530217289
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We thank the Changjiang Scholars Programme and the Innovative Research Team in the University Scheme (IRT0511) and the “863 Project” (2007AA061001) for financial support. Rothamsted Research receives grant-aided support from the UK Biotechnology and Biological Sciences Research Council.
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Xie, H.L., Jiang, R.F., Zhang, F.S. et al. Effect of nitrogen form on the rhizosphere dynamics and uptake of cadmium and zinc by the hyperaccumulator Thlaspi caerulescens . Plant Soil 318, 205–215 (2009). https://doi.org/10.1007/s11104-008-9830-y
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DOI: https://doi.org/10.1007/s11104-008-9830-y