Abstract
The aims of this study are to investigate whether and how the nitrogen form (nitrate (NO3 –) versus ammonium (NH4 +)) influences cadmium (Cd) uptake and translocation and subsequent Cd phytoextraction by the hyperaccumulator species Sedum plumbizincicola. Plants were grown hydroponically with N supplied as either NO3 – or NH4 +. Short-term (36 h) Cd uptake and translocation were determined innovatively and quantitatively using a positron-emitting 107Cd tracer and positron-emitting tracer imaging system. The results show that the rates of Cd uptake by roots and transport to the shoots in the NO3 – treatment were more rapid than in the NH4 + treatment. After uptake for 36 h, 5.6 (0.056 μM) and 29.0 % (0.290 μM) of total Cd in the solution was non-absorbable in the NO3 – and NH4 + treatments, respectively. The local velocity of Cd transport was approximately 1.5-fold higher in roots (3.30 cm h−1) and 3.7-fold higher in shoots (10.10 cm h−1) of NO3 –- than NH4 +-fed plants. Autoradiographic analysis of 109Cd reveals that NO3 – nutrition enhanced Cd transportation from the main stem to branches and young leaves. Moreover, NO3 – treatment increased Cd, Ca and K concentrations but inhibited Fe and P in the xylem sap. In a 21-day hydroponic culture, shoot biomass and Cd concentration were 1.51 and 2.63 times higher in NO3 –- than in NH4 +-fed plants. We conclude that compared with NH4 +, NO3 – promoted the major steps in the transport route followed by Cd from solution to shoots in S. plumbizincicola, namely its uptake by roots, xylem loading, root-to-shoot translocation in the xylem and uploading to the leaves. S. plumbizincicola prefers NO3 – nutrition to NH4 + for Cd phytoextraction.
Similar content being viewed by others
References
Arnozis PA, Findenegg GR (1986) Electrical charge balance in the xylem sap of beet and Sorghum plants grown with either NO3 or NH4 nitrogen. J Plant Physiol 125:441–449
Baker AJM, Reeves RD, Hajar ASM (1994) Heavy metal accumulation and tolerance in British populations of the metallophyte Thlaspi caerulescens J. and C. Presl (Brassicaceae). New Phytol 127:61–68
Becher M, Talke IN, Krall L, Kramer U (2004) Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri. Plant J 37:251–268
Cataldo DA, Garland TR, Wildung RE (1983) Cadmium uptake kinetics in intact soybean plants. Plant Physiol 73:844–848
Cosio C, DeSantis L, Frey B, Diallo S, Keller C (2005) Distribution of cadmium in leaves of Thlaspi caerulescens. J Exp Bot 56:765–775
Courbot M, Willems G, Motte P, Arvidsson S, Roosens N, Saumitou-Laprade P, Verbruggen N (2007) A major quantitative trait locus for cadmium tolerance in Arabidopsis halleri colocalizes with HMA4, a gene encoding a heavy metal ATPase. Plant Physiol 144:1052–1065
Crawford NM (1995) Nitrate—nutrient and signal for plant-growth. Plant Cell 7:859–868
Crawford NM, Glass ADM (1998) Molecular and physiological aspects of nitrate uptake in plants. Trends Plant Sci 3:389–395
Fujimaki S, Suzui N, Ishioka NS, Kawachi N, Ito S, Chino M, Nakamura S (2010) Tracing cadmium from culture to spikelet: noninvasive imaging and quantitative characterization of absorption, transport, and accumulation of cadmium in an intact rice plant. Plant Physiol 152:1796–1806
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
Ishikawa S, Suzui N, Ito-Tanabata S, Ishii S, Igura M, Abe T, Kuramata M, Kawachi N, Fujimaki S (2011) Real-time imaging and analysis of differences in cadmium dynamics in rice cultivars (Oryza sativa) using positron-emitting 107Cd tracer. BMC Plant Biol 11:172
Jiang JP, Wu LH, Li N, Luo YM, Liu L, Zhao QG, Zhang L, Christie P (2010) Effects of multiple heavy metal contamination and repeated phytoextraction by Sedum plumbizincicola on soil microbial properties. Eur J Soil Biol 46:18–26
Kovacik J, Klejdus B, Stork F, Hedbavny J (2011) Nitrate deficiency reduces cadmium and nickel accumulation in chamomile plants. J Agr Food Chem 59:5139–5149
Krouk G, Crawford NM, Coruzzi GM, Tsay YF (2010) Nitrate signaling: adaptation to fluctuating environments. Curr Opin Plant Biol 13:266–273
Kupper H, Mijovilovich A, Meyer-Klaucke W, Kroneck PMH (2004) Tissue- and age-dependent differences in the complexation of cadmium and zinc in the cadmium/zinc hyperaccumulator Thlaspi caerulescens (Ganges ecotype) revealed by X-ray absorption spectroscopy. Plant Physiol 134:748–757
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
Lasat MM, Baker AJM, Kochian LV (1998) Altered Zn compartmentation in the root symplasm and stimulated Zn absorption into the leaf as mechanisms involved in Zn hyperaccumulation in Thlaspi caerulescens. Plant Physiol 118:875–883
Liu L, Wu LH, Li N, Cui LQ, Li Z, Jiang JP, Jiang YG, Qiu XY, Luo YM (2009) Effect of planting densities on yields and zinc and cadmium uptake by Sedum plumbizincicola. Environ Sci 30:3422–3426 (in Chinese with English abstract)
Liu L, Wu LH, Li N, Luo YM, Li SL, Li Z, Han CL, Jiang YG, Christie P (2011) Rhizosphere concentrations of zinc and cadmium in a metal contaminated soil after repeated phytoextraction by Sedum plumbizincicola. Int J Phytoremediat 13:750–764
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
Lu LL, Tian SK, Yang XE, Wang XC, Brown P, Li TQ, He ZL (2008) Enhanced root-to-shoot translocation of cadmium in the hyperaccumulating ecotype of Sedum alfredii. J Exp Bot 59:3203–3213
Luo BF, Du ST, Lu KX, Liu WJ, Lin XY, Jin CW (2012) Iron uptake system mediates nitrate-facilitated cadmium accumulation in tomato (Solanum lycopersicum) plants. J Exp Bot 63:3127–3136
Ma JF, Ueno D, Zhao FJ, McGrath SP (2005) Subcellular localisation of Cd and Zn in the leaves of a Cd-hyperaccumulating ecotype of Thlaspi caerulescens. Planta 220:731–736
McClure PR, Kochian LV, Spanswick RM, Shaff JE (1990) Evidence for cotransport of nitrate and protons in maize roots 1. Effects of nitrate on the membrane-potential. Plant Physiol 93:281–289
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
Miller AJ, Cookson SJ, Smith SJ, Wells DM (2001) The use of microelectrodes to investigate compartmentation and the transport of metabolized inorganic ions in plants. J Exp Bot 52:541–549
Monsant AC, Tang C, Baker AJM (2008) The effect of nitrogen form on rhizosphere soil pH and zinc phytoextraction by Thlaspi caerulescens. Chemosphere 73:635–642
Monsant AC, Wang YD, Tang CX (2010) Nitrate nutrition enhances zinc hyperaccumulation in Noccaea caerulescens (Prayon). Plant Soil 336:391–404
Monsant AC, Kappen P, Wang YD, Pigram PJ, Baker AJM, Tang CX (2011) In vivo speciation of zinc in Noccaea caerulescens in response to nitrogen form and zinc exposure. Plant Soil 348:167–183
Papoyan A, Kochian LV (2004) Identification of Thlaspi caerulescens genes that may be involved in heavy metal hyperaccumulation and tolerance. Characterization of a novel heavy metal transporting ATPase. Plant Physiol 136:3814–3823
Sarathchandra SU (1978) Nitrification activities and changes in populations of nitrifying bacteria in soil perfused at 2 different H-ion concentrations. Plant Soil 50:99–111
Schwartz C, Echevarria G, Morel JL (2003) Phytoextraction of cadmium with Thlaspi caerulescens. Plant Soil 249:27–35
Stitt M (1999) Nitrate regulation of metabolism and growth. Curr Opin Plant Biol 2:178–186
Suzuki M, Tsukamoto T, Inoue H, Watanabe S, Matsuhashi S, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2008) Deoxymugineic acid increases Zn translocation in Zn-deficient rice plants. Plant Mol Biol 66:609–617
Talke IN, Hanikenne M, Kramer U (2006) Zinc-dependent global transcriptional control, transcriptional deregulation, and higher gene copy number for genes in metal homeostasis of the hyperaccumulator Arabidopsis halleri. Plant Physiol 142:148–167
Tsukamoto T, Nakanishi H, Kiyomiya S, Watanabe S, Matsuhashi S, Nishizawa NK, Mori S (2006) 52Mn translocation in barley monitored using a positron-emitting tracer imaging system. Soil Sci Plant Nutr 52:717–725
Tsukamoto T, Nakanishi H, Uchida H, Watanabe S, Matsuhashi S, Mori S, Nishizawa NK (2009) 52Fe translocation in barley as monitored by a positron-emitting tracer imaging system (PETIS): evidence for the direct translocation of Fe from roots to young leaves via phloem. Plant Cell Physiol 50:48–57
Turan M, Sevimli F (2005) Influence of different nitrogen sources and levels on ion content of cabbage (Brassica oleracea var. capitate). New Zeal J Crop Hort 33:241–249
Ueno D, Ma JF, Iwashita T, Zhao FJ, McGrath SP (2005) Identification of the form of Cd in the leaves of a superior Cd-accumulating ecotype of Thlaspi caerulescens using 113Cd-NMR. Planta 221:928–936
Ueno D, Iwashita T, Zhao FJ, Ma JF (2008) Characterization of Cd translocation and identification of the Cd form in xylem sap of the Cd-hyperaccumulator Arabidopsis halleri. Plant Cell Physiol 49:540–548
Uraguchi S, Mori S, Kuramata M, Kawasaki A, Arao T, Ishikawa S (2009) Root-to-shoot Cd translocation via the xylem is the major process determining shoot and grain cadmium accumulation in rice. J Exp Bot 60:2677–2688
Wu LH, Zhou SB, Bi D, Guo XH, Qin WH, Wang H, Wang GJ, Luo YM (2006) Sedum plumbizincicola, a new species of the Crassulaceae from Zhejiang. Soils 38:632–633 (in Chinese with English abstract)
Wu LH, Li N, Bi D, Luo YM (2007) Zn and Cd hyperaccumulator in Sedum plumbizincicola under different soil contamination levels and intercropping systems. In: Zhu YG, Lepp N, Naidu R (eds) Biogeochemisry of trace elements: environmental protection, remediation and human health. Tsinghua University Press, Beijing, pp 934–935
Wu LH, Li N, Luo YM (2008) Phytoextraction of heavy metal contaminated soil by Sedum plumbizincicola under different agronomic strategies. In: Proc 5th Int Phytotech Conf, Nanjing, China, pp. 49–50
Wu LH, Li Z, Akahane I, Liu L, Han CL, Makino T, Luo YM, Christie P (2012) Effects of organic amendments on Cd, Zn and Cu bioavailability in soil with repeated phytoremediation by Sedum plumbizincicola. Int J Phytoremediat 14:1024–1038
Wu LH, Liu YJ, Zhou SB, Guo FG, Bi D, Guo XH, Baker AJM, Smith JAC, Luo YM (2013a) Sedum plumbizincicola X.H. Guo et S.B. Zhou ex L.H. Wu (Crassulaceae): a new species from Zhejiang Province, China. Plant Syst Evol 299(3):487–498
Wu LH, Zhong DX, Du YZ, Lu SY, Fu DQ, Li Z, Li XD, Chi Y, Luo YM, Yan JH (2013b) Emission and control characteristics for incineration of Sedum plumbizincicola biomass in a laboratory-scale entrained flow tube furnace. Int J Phytoremediat 15:219–231
Xie HL, Jiang RF, Zhang FS, McGrath SP, Zhao FJ (2009) Effect of nitrogen form on the rhizosphere dynamics and uptake of cadmium and zinc by the hyperaccumulator Thlaspi caerulescens. Plant Soil 318:205–215
Yang XE, Li TQ, Long XX, Xiong YH, He ZL, Stoffella PJ (2006) Dynamics of zinc uptake and accumulation in the hyperaccumulating and non-hyperaccumulating ecotypes of Sedum alfredii Hance. Plant Soil 284:109–119
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
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
Zhao FJ, Jiang RF, Dunham SJ, McGrath SP (2006) Cadmium uptake, translocation and tolerance in the hyperaccumulator Arabidopsis halleri. New Phytol 172:646–654
Zhu E, Liu D, Li JG, Li TQ, Yang XE, He ZL, Stoffella PJ (2011) Effect of nitrogen fertilizer on growth and cadmium accumulation in Sedum alfredii Hance. J Plant Nutr 34:115–126
Acknowledgements
This research was supported by the National Natural Science Foundation of China (Projects 40930739, 41201300 and 41230858), by a grant from the Strategic International Cooperative Program, Japanese Science and Technology Agency (JST) and in part by the Japanese Society for the Promotion of Science (Grant-in-Aid for Scientific Research No. 23380155). We thank Mr. H. Suto (Tokyo Nuclear Services Co. Ltd.) and Dr. S. Ishii (Japanese Atomic Energy Agency) for the technical assistance in 107Cd production, and Prof C. X. Tang (La Trobe University, Australia) for helps on experimental design and paper improvement.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Stuart Simpson
P. J. Hu and Y.-G. Yin contributed equally to this work.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplementary Video S1
Animation film of 107Cd dynamics in S. plumbizincicola fed with NO3 – (left) and NH4 + (right). (MOV 10,489 kb)
Rights and permissions
About this article
Cite this article
Hu, P., Yin, YG., Ishikawa, S. et al. Nitrate facilitates cadmium uptake, transport and accumulation in the hyperaccumulator Sedum plumbizincicola . Environ Sci Pollut Res 20, 6306–6316 (2013). https://doi.org/10.1007/s11356-013-1680-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-013-1680-3