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

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.

Mineralogy and Zn Chemical Speciation in a Soil-Plant System from a Metal-Extreme Environment: A Study on Helichrysum microphyllum subsp. tyrrhenicum (Campo Pisano Mine, SW Sardinia, Italy)

“…In this study, SEM and EDS analysis showed the presence of a mineral rim made up of Al-silicates coating the epidermis of H. tyrrhenicum roots (Figure 2), as previously observed in other autochthonous plant species growing in similar environments, like E. pithyusa subsp. cupanii, P. lentiscus, P. australis, and J. acutus [23,[76][77][78]109]. This structure was also detected by STXM ( Figure 6), also showing that Zn is mainly stored in the root epidermis.…”

“…XAS spectra for each sample were collected at least in triplicate for averaging and statistics. According to literature data [23,26,50,52,[74][75][76][77][78], in the soil-plant system, Zn can occur in different coordination environments, both bound to organic compounds (e.g., organic acids, phytochelatins, metallothioneins, etc.) and to inorganic molecules (e.g., sulfur, sulfate, carbonate, etc.)…”

“…Quartz and dolomite were found in roots, stems, and leaves of H. tyrrhenicum. These minerals can occur in roots as residual grains not completely dissolved by plant physiological activities [23,99]. However, their occurrence in leaves and stems has to be ascribed to a biologically-driven mineralization [11,100,101].…”

Zinc Homeostasis and isotopic fractionation in plants: a review

“…The magnitude of both isotopic effects was larger than reported for hydroponically grown crops (Δ Znroot-solution -0.02 to 0.16‰, and Δ 66 Znshoot-root -0.25 to -0.56‰) (Weiss et al 2005;Jouvin et al 2012;Smolders et al 2013). Excess Zn can precipitate with insoluble phosphates or silicates at the root epidermis, the intercellular spaces, and the cell walls of the roots, a process termed biomineralization that might reduce Zn influx into the symplast (Neumann and zur Nieden 2001;Straczek et al 2008;Medas et al 2015;De Giudici et al 2015). In tobacco, Zn binds to the carboxyl and hydroxyl groups of pectin and to the hydroxyl groups of cellulose in the cell walls of roots (Straczek et al 2008).…”

Historical mine pollution and environmental resilience: biomineralization processes and biogeochemical barriers

“…Mineral and microscopic analysis in this work were conducted by X-ray Powder Diffraction (XRPD), Scanning Electron Microscopy (SEM), and synchrotron-based techniques such as X-ray Absorption Spectroscopy (XAS) and Scanning Transmission Xray Microscopy (STXM) [15][16][17][18].…”