Abstract
The development of highly brilliant synchrotron facilities all around the world is opening the way to new research in biological sciences including speciation studies of trace elements in plants. In this paper, for the first time, iron (Fe) speciation in xylem sap has been assessed by X-ray absorption near-edge structure (XANES) spectroscopy at the highly brilliant synchrotron PETRA III, beamline P06. Both standard organic Fe-complexes and xylem sap samples of Fe-deficient tomato plants were analyzed. The high photon flux provided by this X-ray synchrotron source allows on one side to obtain good XANES spectra in a reasonable amount of time (approx. 15 min for 200 eV scan) at low Fe concentrations (sub parts-per-million), while on the other hand may cause radiation damage to the sample, despite the sample being cooled by a stream of liquid nitrogen vapor. Standard Fe-complexes such as Fe(III)-succinate, Fe(III)-α-ketoglutarate, and Fe(III)-nicotianamine are somehow degraded when irradiated with synchrotron X-rays and Fe(III) can undergo photoreduction. Degradation of the organic molecules was assessed by HPLC-UV/Vis analyses on the same samples investigated by X-ray absorption spectroscopy (XAS). Fe speciation in xylem sap samples revealed Fe(III) to be complexed by citrate and acetate. Nevertheless, artifacts created by radiation damage cannot be excluded. The use of highly brilliant synchrotrons as X-ray sources for XAS analyses can dramatically increase the sensitivity of the technique for trace elements thus allowing their speciation in xylem sap. However, great attention must be paid to radiation damage, which can lead to biased results.
Similar content being viewed by others
References
van Hees PAW, Lundstrom US (2000) Equilibrium models of aluminium and iron complexation with different organic acids in soil solution. Geoderma 94:201–221
Römheld V, Marschner H (1986) Evidence for a specific uptake system for iron phytosiderophores in roots of grasses. Plant Physiol 80:175–180
Tomasi N, De Nobili M, Gottardi S, Zanin L, Mimmo T, Varanini Z, Roemheld V, Pinton R, Cesco S (2013) Physiological and molecular characterization of Fe acquisition by tomato plants from natural Fe complexes. Biol Fert Soils 49:187–200
Tomasi N, Rizzardo C, Monte R, Gottardi S, Jelali N, Terzano R, Vekemans B, De Nobili M, Varanini Z, Pinton R, Cesco S (2009) Micro-analytical, physiological and molecular aspects of Fe acquisition in leaves of Fe-deficient tomato plants re-supplied with natural Fe-complexes in nutrient solution. Plant Soil 325:25–38
Rellan-Alvarez R, Giner-Martinez-Sierra G, Orduna J, Orera I, Rodriguez-Castrillon JA, Garcia-Alonso JI, Abadia J, Alvarez-Fernandez A (2010) Identification of a tri-iron(III), tri-citrate complex in the xylem sap of iron-deficient tomato resupplied with iron: new insights into plant iron long-distance transport. Plant Cell Physiol 51:91–102
Brown GE, Sturchio NC (2002) An overview of synchrotron radiation applications to low temperature geochemistry and environmental science. In: Fenter PA, Rivers ML, Sturchio NC, Sutton SR (eds) Applications of synchrotron radiation in low-temperature geochemistry and environmental science. Reviews in mineralogy and geochemistry, vol. 49. Mineralogical Society of America Washington, DC, USA, pp 1–115
Sarret G, Pilon Smits EAH, Castillo Michel H, Isaure MP, Zhao FJ, Tappero R (2013) Use of synchrotron-based techniques to elucidate metal uptake and metabolism in plants. Adv Agron 119:1–82
McNear DH, Chaney RL, Sparks D (2010) The hyperaccumulator Alyssum murale uses complexation with nitrogen and oxygen donor ligands for Ni transport and storage. Phytochem 71:188–200
Tappero R, Peltier E, Grafe M, Heidel K, Ginder-Vogel M, Livi K, Rivers M, Marcus M, Chaney R, Sparks D (2007) Hyperaccumulator Alyssum murale relies on a different metal storage mechanism for cobalt than for nickel. New Phytol 175:641–654
Sarret G, Willems G, Isaure MP, Marcus MA, Fakra S, Frérot H, Pairis S, Geoffroy N, Manceau A, Saumitou-Laprade P (2009) Zn localization and speciation in Arabidopsis halleri × Arabidopsis lyrata progenies presenting various Zn accumulation capacities. New Phytol 184:581–595
Terzano R, Al Chami Z, Vekemans B, Janssens K, Miano T, Ruggiero P (2008) Zinc distribution and speciation within rocket plants (Eruca vesicaria L. Cavalieri) grown on a polluted soil amended with compost as determined by XRF microtomography and micro-XANES. J Agric Food Chem 56:3222–3231
Kopittke PM, Menzies NW, de Jonge MD, McKenna BA, Donner E, Webb RI, Paterson DJ, Howard DL, Ryan CG, Glover CJ, Scheckel KG, Lombi E (2011) In situ distribution and speciation of toxic copper, nickel, and zinc in hydrated roots of cowpea. Plant Physiol 156:663–673
Huguet S, Bert V, Laboudigue A, Barthès V, Isaure M, Llorens IHS, Sarret G (2012) Cd speciation and localization in the hyperaccumulator Arabidopsis halleri. Environ Exp Bot 82:54–65
Alves S, Nabais C, de Lurdes Simoes Goncalves M, Correia dos Santos M (2011) Nickel speciation in the xylem sap of the hyperaccumulator Alyssum serpyllifolium ssp. lusitanicum growing on serpentine soils of northeast Portugal. J Plant Physiol 168:1715–1722
Kramer U, Cotter-Howells JD, Charnock JM, Baker AJM, Andrew C, Smith J (1996) Free histidine as a metal chelator in plants that accumulate nickel. Nature 379:635–638
Ye WL, Wood BA, Stroud JL, Andralojc PJ, Raab A, McGrath SP, Feldmann J, Zhao FJ (2010) Arsenic speciation in phloem and xylem exudates of castor bean. Plant Physiol 154:1505–1513
Salt DE, Prince RC, Baker AM, Raskin I, Pickering IJ (1999) Zinc ligands in the metal hyperaccumulator Thlaspi caerulescens as determined using X-ray absorption spectroscopy. Environ Sci Technol 33:713–717
Meirer F, Pepponi G, Streli C, Wobrauschek P, Mihucz VG, Záray G, Czech V, Broekaert JAC, Fittschen UEA, Falkenberg G (2007) Application of synchrotron-radiation-induced TXRF-XANES for arsenic speciation in cucumber (Cucumis sativus L.) xylem sap. X-Ray Spectrom 36:408–412
Yoshimura E, Sakaguchi T, Nakanishi H, Nishizawa NK, Nakai I, Mori S (2000) Characterization of the chemical state of iron in the leaves of wild-type tomato and of a nicotianamine-free mutant chloronerva by X-ray Absorption Near-edge Structure (XANES). Phytochem Anal 11:160–162
Jones KW, Marcel Dekker Inc (2002) Synchrotron radiation-induced X-ray Emission. In: Van Grieken RE, Markowicz AA (eds) Handbook of X-ray spectrometry, 2nd edn., pp 501–558
Cesco S, Rombolà AD, Tagliavini M, Varanini Z, Pinton R (2006) Phytosiderophores released by graminaceous species promote 59Fe -uptake in citrus. Plant Soil 287:223–233
López-Millán AF, Morales F, Gogorcena Y, Abadia A, Abadia J (2009) Metabolic responses in iron deficient tomato plants. J Plant Physiol 166:375–384
Lasat MM, Baker AJ, 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
Rellán-Álvarez R, López-Gomollón S, Abadía J, Álvarez-Fernández A (2011) Development of a new high-performance liquid chromatography-electrospray ionization time-of-flight mass spectrometry method for the determination of low molecular mass organic acids in plant tissue extracts. J Agric Food Chem 59:6864–6870
Rellán-Álvarez R, El-Jendoubi H, Wohlgemuth G, Abadía A, Fiehn O, Abadía J (2011) Metabolite profile changes in xylem sap and leaf extracts of Strategy I plants in response to iron deficiency and resupply. Front Plant Sci 2:1–18
Ambe S (1989) Mössbauer study of iron in the tomato plant. Int J Radiat Appl Instrum Part A 40:671–675
Ressler T (1998) WinXAS: a XAS data analysis program under MS Windows. J Synchrotron Radiat 5:118–122
Ressler T, Wong J, Roos J, Smith IL (2000) Quantitative speciation of Mn-bearing particulates emitted from autos burning (methylcyclopenthadienyl)manganese tricarbonyl-added gasolines using XANES spectroscopy. Environ Sci Technol 34:950–958
Ressler T (2004) Win XAS 3.x. Manual. Available at www.winxas.de
Bennett JH, Lee EH, Krizek DT, Olsen RA, Brown JC (1982) Photochemical reduction of iron. II. Plant related factors. J Plant Nutr 5:335–344
Abrahamson HB, Rezyani AB, Brushmiller JG (1994) Photochemical and spectroscopic studies of complexes of iron(III) with citric acid and other carboxylic acids. Inorg Chim Acta 226:117–127
Manceau A, Marcus MA, Tamura N (2002) Quantitative speciation of heavy metals in soils and sediments by synchrotron X-ray techniques. In: Fenter PA, Rivers ML, Sturchio NC, Sutton SR (eds) Applications of synchrotron radiation in low-temperature geochemistry and environmental science. Reviews in mineralogy and geochemistry, vol. 49. Mineralogical Society of America Washington, DC, USA, pp 341–428
Burmeister WP (2000) Structural changes in a cryo-cooled protein crystal owing to radiation damage. Acta Cryst D56:328–341
Ravelli RBG, McSweeney SM (2000) The “fingerprint” that X-rays can leave on structures. Structure 8:315–328
Weik M, Ravelli RBG, Kryger G, McSweeney S, Raves ML, Harel M, Gros P, Silman I, Kroon J, Sussman JL (2000) Specific chemical and structural damage to proteins produced by synchrotron radiation. Proc Natl Acad Sci USA 97:623–628
Lombi E, Scheckel KG, Kempson IM (2011) In situ analysis of metal(loid)s in plants: state of the art and artefacts. Environ Exp Bot 72:3–17
Lombi E, De Jonge M, Donner E, Kopittke PM, Howard DL, Kirkham R, Ryan CG, Paterson D (2011) Fast X-ray fluorescence microtomography of hydrated biological samples. PLoS One 6:e20626
Terzano R, Alfeld M, Janssens K, Vekemans B, Schoonjans T, Vincze L, Tomasi N, Pinton R, Cesco S (2013) Spatially resolved (semi)quantitative determination of iron (Fe) in plants by means of synchrotron micro X-ray fluorescence. Anal Bioanal Chem 405:3341–3350
Cesco S, Mimmo T, Tonon G, Tomasi N, Pinton R, Terzano R, Neumann G, Weisskopf L (2012) Plant- borne flavonoids released into the rhizosphere: Impact on soil bio-activities related to plant nutrition. A review. Biol Fertil Soils 48:123–149
Acknowledgments
Research was supported by grants from Italian MIUR (FIRB-Programma “Futuro in Ricerca”), Free University of Bolzano (TN5056) and the Autonomous Province of Bolzano (Rhizotyr—TN5218). The Authors would like to thank Dr. Melissa Denecke (INE, KIT, Karlsruhe, Germany) for her critical revision of the manuscript. Bjorn de Samber and Gerd Wellenreuther are acknowledged for their assistance with the cryo-stream system.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(PDF 208 kb)
Rights and permissions
About this article
Cite this article
Terzano, R., Mimmo, T., Vekemans, B. et al. Iron (Fe) speciation in xylem sap by XANES at a high brilliant synchrotron X-ray source: opportunities and limitations. Anal Bioanal Chem 405, 5411–5419 (2013). https://doi.org/10.1007/s00216-013-6959-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00216-013-6959-1