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Microscopic biomineralization processes and Zn bioavailability: a synchrotron-based investigation of Pistacia lentiscus L. roots

  • Alteration and element mobility at the microbe-mineral interface
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Abstract

Plants growing on polluted soils need to control the bioavailability of pollutants to reduce their toxicity. This study aims to reveal processes occurring at the soil-root interface of Pistacia lentiscus L. growing on the highly Zn-contaminated tailings of Campo Pisano mine (SW Sardinia, Italy), in order to shed light on possible mechanisms allowing for plant adaptation. The study combines conventional X-ray diffraction (XRD) and scanning electron microscopy (SEM) with advanced synchrotron-based techniques, micro-X-ray fluorescence mapping (μ-XRF) and X-ray absorption spectroscopy (XAS). Data analysis elucidates a mechanism used by P. lentiscus L. as response to high Zn concentration in soil. In particular, P. lentiscus roots take up Al, Si and Zn from the rhizosphere minerals in order to build biomineralizations that are part of survival strategy of the species, leading to formation of a Si-Al biomineralization coating the root epidermis. XAS analysis rules out Zn binding to organic molecules and indicates that Zn coordinates Si atoms stored in root epidermis leading to the precipitation of an amorphous Zn-silicate. These findings represent a step forward in understanding biological mechanisms and the resulting behaviour of minor and trace elements during plant-soil interaction and will have significant implications for development of phytoremediation techniques.

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Notes

  1. Error Reporting Recommendations: A Report of the Standards and Criteria Committee, July 26, 2000—www.ixasportal.net/ixas/images/ixas_mat/Error_Reports_2000.pdf)

References

  • Audet P, Charest C (2007) Dynamics of arbuscular1 mycorrhizal symbiosis in heavy metal phytoremediation: meta-analytical and conceptual perspectives. Environ Pollut 147:609–614

    Article  CAS  Google Scholar 

  • Aversa G, Balassone G, Boni M, Amalfitano (2002) Themineralogy of the “Calamine” ores in SW Sardinia (Italy): preliminary results. Period Mineral 71:201–218

    Google Scholar 

  • Bacchetta G, Cao A, Cappai G, Carucci A, Casti M, Fercia ML, Lonis R, Mola F (2012) A field experiment on the use of Pistacia lentiscus L. and Scrophularia canina L. subsp. bicolor (Sibth. Et Sm.) Greuter for the phytoremediation of abandoned mining areas. Plant Biosyst 146:1054–1063

  • Bacchetta G, Cappai G, Carucci A, Tamburini E (2015) Use of native plants for the remediation of abandoned mine sites in Mediterranean semiarid environments. Bull Environ Contam Toxicol. doi:10.1007/s00128-015-1467-y

    Google Scholar 

  • Baker AJM (1981) Accumulators and excluders strategies in the response of plants to heavy metals. J Plant Nutr 3:643–654

    Article  CAS  Google Scholar 

  • Bauer P, Elbaum R, Weiss IM (2011) Calcium and silicon mineralization in land plants: transport, structure and function. Plant Sci 180:746–756

    Article  CAS  Google Scholar 

  • Benfatto M, Meneghini C (2015) A close look into the low energy region of the XAS spectra: the XANES region. In: Mobilio S, Boscherini F, Meneghini C (eds) Synchrotron radiation, basics, methods and applications. Springer, Berlin Heidelberg, pp 213–240

    Google Scholar 

  • Billows E (1941) I minerali della Sardegna ed i loro giacimenti: Rendiconti Università di Cagliari, p 331–335

  • Boni M, Gilg A, Aversa G, Balassone G (2003) The “Calamine” of SW Sardinia (Italy): geology, mineralogy and stable isotope geochemistry of a supergene Zn-mineralisation. Econ Geol 98:731–748

    Article  CAS  Google Scholar 

  • Caldelas C, Dong S, Araus JL, Jakob Weiss D (2011) Zinc isotopic fractionation in Phragmites australis in response to toxic levels of zinc. J Exp Bot 62:2169–2178

    Article  CAS  Google Scholar 

  • Chaoui A, Mazhoudi S, Ghorbal MH, Elferjani E (1997) Cadmium and zinc induction of lipid peroxidation and effects on antioxidant enzyme activities in bean (Phaseolus vulgaris L.). Plant Sci 127:139–147

    Article  CAS  Google Scholar 

  • Concas S, Lattanzi P, Bacchetta G, Barbafieri M, Vacca A (2015, submitted) Zn, Pb and Hg contents of Pistacia lentiscus L. grown on heavy-metal rich soils: implications for phytostabilization. Water Air Soil Poll

  • De Giudici G, Lattanzi P, Medas D (2015) Synchrotron radiation and environmental sciences synchrotron radiation. In: Mobilio S, Boscherini F, Meneghini C (eds) Synchrotron radiation, basics, methods and applications. Springer, Berlin Heidelberg, pp 661–676

    Google Scholar 

  • De Vivo B, Boni M, Costabile S (1998) Formational anomalies versus mining pollution: geochemical risk maps of Sardinia, Italy. J Geochem Explor 64:321–337

    Article  Google Scholar 

  • De Vos CHR, Schat H, De Waal MAM, Voorja R, Ernst WHO (1991) Increased resistance to copper-induced damage of root cell plasmalemma in copper tolerant Silene cucubalus. Physiol Plant 82:523–528

    Article  Google Scholar 

  • Doncheva S, Stoyanova Z, Velikova V (2001) The influence of succinate on zinc toxicity of pea plant. J Plant Nutr 24:789–806

    Article  CAS  Google Scholar 

  • Dong J, Mao WH, Zhang GP, Cai Y (2007) Root excretion and plant tolerance to cadmium toxicity. Plant Environ J 53:193–200

    CAS  Google Scholar 

  • dos Reis SP, Lima AM, de Souza CRBS (2012) Recent molecular advances on downstream plant responses to abiotic stress. Int J Mol Sci 13:8628–8647

    Article  Google Scholar 

  • Gardea-Torresdey JL, Arteaga S, Tiemann KJ, Chianelli R, Pingitore N, Mackay W (2001) Absorption of copper(II) by creosote bush (Larrea tridentata): use of atomic and x-ray absorption spectroscopy. Environ Toxicol Chem 20:2572–2579

    Article  CAS  Google Scholar 

  • Gardea-Torresdey JL, Videa JRP, Rosa GD, Parsons J (2005) Phytoremediation of heavy metals and study of the metal coordination by X-ray absorption spectroscopy. Coord Chem Rev 249:1797–1810

    Article  CAS  Google Scholar 

  • Gianoncelli A, Morrison GR, Kaulich B, Bacescu D, Kovac J (2006) A fast read-out CCD camera system for scanning X-ray microscopy. Appl Phys Lett 89:251117–251119

    Article  Google Scholar 

  • Gianoncelli A, Kaulich B, Alberti R, Klatka T, Longoni A, de Marco A, Marcello A, Kiskinova M (2009) Simultaneous soft X-ray transmission and emission microscopy. Nucl Instrum Methods 608:195–198

    Article  CAS  Google Scholar 

  • Gianoncelli A, Kourousias G, Stolfa A, Kaulich B (2013) Recent developments at the TwinMic beamline at ELETTRA: an 8 SDD detector setup for low energy X-ray. J Phys Conf Ser 425:182001

    Article  Google Scholar 

  • ICSD (Inorganic Crystal Structure Database) http://icsd.ill.eu/icsd/index.php, 2011

  • Jenks MA, Hasegawa PM (2014) Plant abiotic stress, 2nd edn. Wiley-Blackwell Publishing Inc, Oxford

    Google Scholar 

  • Joner EJ, Briones R, Leyval C (2000) Metal-binding capacity of arbuscular mycorrhizal mycelium. Plant Soil 226:227–234

    Article  CAS  Google Scholar 

  • Kaulich B, Bacescu D, Susini J, David C, Di Fabrizio E, Morrison GR, Charalambous P, Thieme J, Wilhein T, Kovac J, Cocco D, Salome M, Dhez O, Weitkamp T, Cabrini S, Cojoc D, Gianoncelli A, Vogt U, Podnar M, Zangrando M, Zacchigna M, Kiskinova M (2006) Proc. 8th Int. Conf. X-ray Microscopy IPAP Conf. Series 7, 22

  • Kidd PS, Barceló J, Bernal MP, Navari-Izzo F, Poschenrieder C, Shilev S, Clemente R, Monterroso C (2009) Trace element behaviour at the root-soil interface: implications in phytoremediation. Environ Exp Bot 67:243–259

    Article  CAS  Google Scholar 

  • Larcher W (2003) Physiological plant ecology: ecophysiology and stress physiology of functional groups. Springer, Germany

    Book  Google Scholar 

  • Majumdar S, Peralta-Videa JR, Castillo-Michel H, Hong J, Rico CM, Gardea-Torresdey JL (2012) Applications of synchrotron μ-XRF to study the distribution of biologically important elements in different environmental matrices: a review. Anal Chim Acta 755:1–16

    Article  CAS  Google Scholar 

  • Malamy JE (2005) Intrinsic and environmental response pathways that regulate root system architecture. Plant Cell Environ 28:67–77

    Article  CAS  Google Scholar 

  • Manara A (2012) Plant responses to heavy metal toxicity. In: Antonella F (ed) Plants and Heavy Metals, SpringerBriefs in Molecular Science. Springer, Netherlands, pp 27–53

    Chapter  Google Scholar 

  • Medas D, Lattanzi P, Podda F, Meneghini C, Trapananti A, Sprocati A, Casu MA, Musu E, De Giudici G (2014) The amorphous Zn biomineralization at Naracauli stream, Sardinia: electron microscopy and X-ray absorption spectroscopy. Environ Sci Pollut R 21:6775–6782

    Article  CAS  Google Scholar 

  • Medas D, De Giudici G, Casu MA, Musu E, Gianoncelli A, Iadecola A, Meneghini C, Tamburini E, Sprocati AR, Turnau K, Lattanzi P (2015) Microscopic processes ruling Zn bioavailability to roots of Euphorbia pithyusa L. pioneer plant. Environ Sci Technol 49:1400–1408

    Article  CAS  Google Scholar 

  • Meneghini C, Bardelli F, Mobilio S (2012) ESTRA-FitEXA: a software package for EXAFS data analysis. Nucl Inst Methods B 285:153–157

    Article  CAS  Google Scholar 

  • Moore JMCM (1972) Supergene mineral deposits and physiographic development in southwest Sardinia, Italy. T I Min Metall B 71:B59–B66

    Google Scholar 

  • Morrison GR, Gianoncelli A, Kaulich B, Bacescu D, Kovac J (2006) A fast read-out CCD system for configured-detector imaging in STXM. Conf Proc Series IPAP 7:277–379

    Google Scholar 

  • Neumann D, De Figueiredo C (2002) A novel mechanism of silicon uptake. Protoplasma 220:59–67

    Article  CAS  Google Scholar 

  • Neumann D, zur Nieden U (2001) Silicon and heavy metal tolerance of higher plants. Phytochemistry 56:685–692

    Article  CAS  Google Scholar 

  • Padmavathiamma PK, Li LY (2007) Phytoremediation technology: hyper-accumulation metals in plants. Water Air Soil Poll 184:105–126

    Article  CAS  Google Scholar 

  • Rehr JJ, Albers RC (2000) Theoretical approaches to X-ray absorption fine structure. Rev Mod Phys 72:621–654

    Article  CAS  Google Scholar 

  • Rufyikiri G, Thiry Y, Declerck S (2003) Contribution of hyphae and roots to uranium uptake and translocation by arbuscular mycorrhizal carrot roots under root-organ culture conditions. New Phytol 158:391–399

    Article  CAS  Google Scholar 

  • Sole A, Papillon E, Cotte M, Walter P, Susini J (2007) A multiplatform code for the analysis of energy-dispersive X-ray fluorescence spectra. Spectrochim Acta B 62:63–68

    Article  Google Scholar 

  • Stara P, Rizzo R, Tanca GA (1996) Iglesiente-Arburese, miniere e minerali. Ente Minerario Sardo I

  • Sun F, Zhang W, Hu H, Li B, Wang Y, Zhao Y, Li K, Liu M, Li X (2008) Salt modulates gravity signalling pathway to regulate growth direction of primary roots in Arabidopsis. Plant Physiol 146:178–188

    Article  CAS  Google Scholar 

  • Turnau K, Ryszka P, Wojtczak G (2010) Metal tolerant mycorrhizal plants: a review from the perspective on industrial waste in temperate region. In: Koltai H, Kapulnik Y (eds) Arbuscular mycorrhizas: physiology and function. Springer, Netherlands, pp 257–276

    Chapter  Google Scholar 

  • van der Ent A, Baker AJ, Reeves RD, Chaney RL, Anderson CW, Meech JA, Erskine PD, Simonnot MO, Vaughan J, Morel JL, Echevarria G, Fogliani B, Rongliang Q, Mulligan DR (2015) Agromining: farming for metals in the future? Environ Sci Technol. doi:10.1021/es506031u

    Google Scholar 

Download references

Acknowledgments

The study was financially supported by Regione Autonoma Sardegna (LR 7/2007 grant to P.L., Biophyto and SMERI projects) and MIUR (PRIN 2010–2011 Minerals-biosphere interaction).

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Correspondence to D. Medas.

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Responsible editor: Philippe Garrigues

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De Giudici, G., Medas, D., Meneghini, C. et al. Microscopic biomineralization processes and Zn bioavailability: a synchrotron-based investigation of Pistacia lentiscus L. roots. Environ Sci Pollut Res 22, 19352–19361 (2015). https://doi.org/10.1007/s11356-015-4808-9

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