Abstract
The localization, biotransformation, and chemical speciation of copper in root tips of cucumber (Cucumis sativus) were investigated using synchrotron-based micro X-ray fluorescence (μ-XRF) and micro X-ray absorption near edge structure (μ-XANES). The highest content of Cu was found in root cap and meristematic zone whereas low Cu content in elongation and maturation zone. There was a dramatic increase of Cu content in root cap and meristematic zone after treatment with 100 μM CuSO4 for 72 h. The μ-XANES analysis revealed that most of Cu in root tip was bound with alginate, citrate, and cysteine-like ligands whereas rarely deposited in form of CuO. From root cap to maturation zone, the proportion of Cu bound with alginate-like ligands increased whereas that bound with citrate-like ligands decreased. The proportion of Cu bound with cysteine-like ligands increased from root cap to elongation zone but sharply declined in maturation zone. The results suggested that Cu was chelated by S ligands in the cell walls which protect protoplasm against possible damage caused by Cu excess.
Abbreviations
- EXAFS:
-
extended X-ray absorption fine structure
- MTs:
-
metallothioneins
- PCs:
-
phytochelatins
- SRXRF:
-
synchrotron radiation X-ray fluorescence
- SSRF:
-
ShanghHai synchrotron radiation facility
- μ-XRF:
-
micro X-ray fluorescence
- μ-XANES:
-
micro X-ray absorption near edge structure
- XAS:
-
X-ray absorption spectroscopy
References
Bai, J.H., Xiao, R., Cui, B.S., Zhang, K.J., Wang, Q.G., Liu, X.H., Gao, H.F., Huang, L.B.: Assessment of heavy metal pollution in wetland soils from the young and old reclaimed regions in the Pearl River Estuary, South China. — Environ. Pollut. 159: 817–8242, 2011.
Barrett, J.E.S., Taylor, K.G., Hudson-Edwards, K.A., Charnock, J.M.: Solid-phase speciation of Pb in urban road dust sediment: a XANES and EXAFS study. — Environ. Sci. Technol. 44: 2940–2946, 2010.
Clemens, S.: Molecular mechanisms of plant metal tolerance and homeostasis. — Planta 212: 475–486, 2001.
Clemens, S.: Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. — Biochimie 88: 1707–1719, 2006.
Cobbett, C.S.: Phytochelatins and their roles in heavy metal detoxification. — Plant Physiol. 123: 825–832, 2000.
Fukuda, N., Hokura, A., Kitajima, N., Terada, Y., Saito, H., Abe, T., Nakai, I.: Micro X-ray fluorescence imaging and micro X-ray absorption spectroscopy of cadmium hyper- accumulating plant, Arabidopsis halleri ssp. gemmifera, using high-energy synchrotron radiation. — J. Anal. Atom. Spectrometry 23: 1068–1075, 2008.
Giampaoli, P., Tresmondi, F., Lima, G.P.P., Kanashiro, S., Alves, E.S., Domingos, M., Tavares, A.R.: Analysis of tolerance to copper and zinc in Aechmea blanchetiana grown in vitro. — Biol. Plant. 56: 83–88, 2012.
Hall, J.L.: Cellular mechanisms for heavy metal detoxification and tolerance. — J. exp. Bot. 53: 1–11, 2002.
Jeon, C., Park, J.Y., Yoo, Y.J.: Characteristics of metal removal using carboxylated alginic acid. — Water Resour. 36: 1814–1824, 2002.
Kahle, H.: Response of roots of trees to heavy-metals. — Environ. exp. Bot. 33: 99–119, 1993.
Kang, S.X., Sun, X., Ju, X., Huang, Y.Y., Yao, K., Wu, Z.Q., Xian, D.C.: Measurement and calculation of escape peak intensities in synchrotron radiation X-ray fluorescence analysis. — Nucl. Instrument. Methods B 192: 365–369, 2002.
Kopittke, P.M., Menzies, N.W., Jonge, M.D., McKenna, B.A., Donner, E., Webb, R.I., Paterson, D.J., Howard, D.L., Ryan, C.G., Glover, C.J., Scheckel, K.G., Lombi, E.: In situ distribution and speciation of toxic copper, nickel and zinc in hydrated roots of cowpea. — Plant Physiol. 156: 663–673, 2011.
Kramer, U.: Metal hyperaccumulation in plants. — Annu. Rev. Plant Biol. 61: 517–534, 2010.
Lee, D.K., Ahn, J.H., Song, S.K., Choi, Y.D., Lee, J.S.: Expression of an expansin gene is correlated with root elongation in soybean. — Plant Physiol. 131: 985–997, 2003.
Lee, J., Reeves, R.D., Brooks, R.R., Jaffre, T.L.: Relation between nickel and citric-acid in some nickel-accumulating plants. — Phytochemistry 17: 1033–1035, 1978.
Liao, M.T., Hedley, M.J., Woolley, D.J., Brooks, R.R., Nichols, M.A.: Copper uptake and translocation in chicory (Cichorium intybus L. cv. Grasslands Puna) and tomato (Lycopersicon esculentum Mill. cv. Rondy) plants grown in NFT system. I. Copper uptake and distribution in plants. — Plant Soil 221: 135–142, 2000.
Lin, S.L., Wum, L.: Effects of copper concentration on mineral nutrient-uptake and copper accumulation in protein of copper-tolerant and copper-nontolerant Lotus purshianus L. — Ecotoxicol. Environ. Safe 29: 214–228, 1994.
Maksymiec, W., Baszyński, T.: The role of Ca ions in changes induced by excess Cu2+ in bean plants. Growth parameters. — Acta Physiol. Plant. 20: 411–417, 1998.
Min, H.L., Cai, S.J., Rui, Z., Sha, S., Xie, K.B., Xu, Q.S.: Calcium-mediated enhancement of copper tolerance in Elodea canadensis. — Biol. Plant. 56: 337–343, 2012.
Murphy, A., Zhou, J.M., Goldsbrough, P.B., Taiz, L.: Purification and immunological identification of metallothioneins 1 and 2 from Arabidopsis thaliana. — Plant Physiol. 113: 1293–1301, 1997.
Newman, I.A.: Ion transport in roots: measurement of fluxes using ion-selective microelectrodes to characterize transporter function. — Plant Cell Environ. 24: 1–14, 2001.
Nishizono, H., Ichikawa, H., Suziki, S., Ishii, F.: The role of the root cell-wall in the heavy-metal tolerance of Athyrium yokoscense. — Plant Soil 101: 15–20, 1987.
Pahlsson, A.M.B.: Toxicity of heavy-metals (Zn, Cu, Cd, Pb) to vascular plants — a literature-review. — Water Air Soil Pollut. 47: 287–319, 1989.
Paktunc, D., Foster, A., Heald, S., Laflamme, G.: Speciation and characterization of arsenic in gold ores and cyanidation tailings using X-ray absorption spectroscopy. — Geochim. cosmochim. Acta 68: 969–983, 2004.
Pickering, I.J., Wright, C., Bubner, B., Ellis, D., Persans, M.W., Yu, E.Y., George, G.N., Prince, R.C., Salt, D.E.: Chemical form and distribution of selenium and sulfur in the selenium hyperaccumulator Astragalus bisulcatus. — Plant Physiol. 131: 1460–1467, 2003.
Ressler, T.: WinXAS: A new software package not only for the analysis of energy-dispersive XAS data. — J. Phys. IV. 7: 269–270, 1997.
Sarret, G., Vangronsveld, J., Manceau, A., Musso, M., D’Haen, J., Menthonnex, J.J., Hazemann, J.L.: Accumulation forms of Zn and Pb in Phaseolus vulgaris in the presence and absence of EDTA. — Environ. Sci. Technol. 35: 2854–2859, 2001.
Shi, J.Y., Chen, Y.X., Huang, Y.Y., He, W.: SRXRF microprobe as a technique for studying elements distribution in Elsholtzia splendens. — Micron 35: 557–564, 2004.
Shi, J.Y., Yuan, X.F., Chen, X.C., Wu, B., Huang, Y.Y., Chen, Y.X.: Copper uptake and its effect on metals distribution in root growth zones of Commelina communis revealed by SRXRF. — Biol. trace Element Res. 141: 294–304, 2011.
Tian, S.K., Lu, L.L., Yang, X.O., Webb, S.M., Du, Y.H., Brown, P.H.: Spatial imaging and speciation of lead in the accumulator plant Sedum affredii by microscopically focused synchrotron X-ray investigation. — Environ. Sci. Technol. 44: 5920–5926, 2010.
Tao, S., Liu, W.X., Chen, Y.J., Xu, F.L., Dawson, R.W., Li, B.G., Cao, J., Wang, X.J., Hu, J.Y., Fang, J.Y.: Evaluation of factors influencing root-induced changes of copper fractionation in rhizosphere of a calcareous soil. — Environ. Pollut. 129: 5–12, 2004.
Verbruggen, N., Hermans, C., Schat, H.: Molecular mechanisms of metal hyperaccumulation in plants. — New Phytol. 181: 759–776, 2009.
Walker, T.S., Bais, H.P., Grotewold, E., Vivanco, J.M.: Root exudation and rhizosphere biology. — Plant Physiol. 132: 44–51, 2003.
Yamaoka, W., Takada, S., Takehisa, H., Hayashi, Y., Hokura, A., Terada, Y., Abe, T., Nakai, I.: Study on accumulation mechanism of cadmium in rice (Oriza sativa L.) by micro-XRF imaging and X-ray absorption fine structure analysis utilizing synchrotron radiation. — Bunseki Kagaku 59: 463–475, 2010.
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Acknowledgements: This work was supported by Zhejiang Provincial Natural Science Foundation of China (R5110031), the National Natural Science Foundation of China (21177109, 11179025), Program for New Century Excellent Talents in University (NCET-11-0455), and the Fundamental Research Funds for the Central Universities. This research was carried out at the Shanghai Synchrotron Radiation Facility (SSRF), China. The authors thank Dr. Hua Wang, Chengwen Mao, and Yang Ke for data collection.
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Song, J., Yang, Y.Q., Zhu, S.H. et al. Spatial distribution and speciation of copper in root tips of cucumber revealed by μ-XRF and μ-XANES. Biol Plant 57, 581–586 (2013). https://doi.org/10.1007/s10535-013-0317-1
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DOI: https://doi.org/10.1007/s10535-013-0317-1