Summary Leaf mineral composition, the leaf ionome, reflects the complex interaction between a plant and its environment including local soil composition, an influential factor that can limit species distribution and plant productivity. Here we addressed within‐species variation in plant–soil interactions and edaphic adaptation using Arabidopsis halleri, a well‐suited model species as a facultative metallophyte and metal hyperaccumulator.We conducted multi‐element analysis of 1972 paired leaf and soil samples from 165 European populations of A. halleri, at individual resolution to accommodate soil heterogeneity. Results were further confirmed under standardized conditions upon cultivation of 105 field‐collected genotypes on an artificially metal‐contaminated soil in growth chamber experiments.Soil‐independent between‐ and within‐population variation set apart leaf accumulation of zinc, cadmium and lead from all other nutrient and nonessential elements, concurring with differential hypothesized ecological roles in either biotic interaction or nutrition. For these metals, soil–leaf relationships were element‐specific, differed between metalliferous and nonmetalliferous soils and were geographically structured both in the field and under standardized growth conditions, implicating complex scenarios of recent ecological adaptation.Our study provides an example and a reference for future related work and will serve as a basis for the molecular–genetic dissection and ecological analysis of the observed phenotypic variation.
Nicotianamine (NA) is among the most studied plant metal chelators. A large body of evidence supports its crucial role for Fe distribution in plants and as a precursor of phytosiderophore synthesis in grasses. NA forms stable complexes in vitro not only with Fe(II) and Fe(III) but also with various other divalent metal cations including Zn(II). Early observations indicated a possible contribution of NA to Zn trafficking in plants. Numerous studies on transgenic monocot and dicot plants with modulated NA levels have since then reported Zn accumulation phenotypes. NAS genes were shown to represent promising targets for biofortification efforts. For instance, NA was found to bind Zn in rice grains in a form bioavailable for humans. Recently, additional strong support for the existence of Zn-NA complexes in planta has been obtained in rice, Arabidopsis thaliana and the Zn hyperaccumulating plant A. halleri. We review the evidence for a role of NA in the intercellular and long-distance transport of Zn in plants and discuss open questions.
SummaryElevated nicotianamine synthesis in roots of Arabidopsis halleri has been established as a zinc (Zn) hyperaccumulation factor. The main objective of this study was to elucidate the mechanism of nicotianamine-dependent root-to-shoot translocation of metals.Metal tolerance and accumulation in wild-type (WT) and AhNAS2-RNA interference (RNAi) plants were analysed. Xylem exudates were subjected to speciation analysis and metabolite profiling.Suppression of root nicotianamine synthesis had no effect on Zn and cadmium (Cd) tolerance but rendered plants nickel (Ni)-hypersensitive. It also led to a reduction of Zn rootto-shoot translocation, yet had the opposite effect on Ni mobility, even though both metals form coordination complexes of similar stability with nicotianamine. Xylem Zn concentrations were positively, yet nonstoichiometrically, correlated with nicotianamine concentrations. Two fractions containing Zn coordination complexes were detected in WT xylem. One of them was strongly reduced in AhNAS2-suppressed plants and coeluted with 67 Zn-labelled organic acid complexes. Organic acid concentrations were not responsive to nicotianamine concentrations and sufficiently high to account for complexing the coordinated Zn. We propose a key role for nicotianamine in controlling the efficiency of Zn xylem loading and thereby the formation of Zn coordination complexes with organic acids, which are the main Zn ligands in the xylem but are not rate-limiting for Zn translocation.
Summary Lead (Pb) ranks among the most problematic environmental pollutants. Background contamination of soils is nearly ubiquitous, yet plant Pb accumulation is barely understood. In a survey covering 165 European populations of the metallophyte Arabidopsis halleri, several field samples had indicated Pb hyperaccumulation, offering a chance to dissect plant Pb accumulation. Accumulation of Pb was analysed in A. halleri individuals from contrasting habitats under controlled conditions to rule out aerial deposition as a source of apparent Pb accumulation. Several elemental imaging techniques were employed to study the spatial distribution and ligand environment of Pb. Regardless of genetic background, A. halleri individuals showed higher shoot Pb accumulation than A. thaliana. However, dose–response curves revealed indicator rather than hyperaccumulator behaviour. Xylem sap data and elemental imaging unequivocally demonstrated the in planta mobility of Pb. Highest Pb concentrations were found in epidermal and vascular tissues. Distribution of Pb was distinct from that of the hyperaccumulated metal zinc. Most Pb was bound by oxygen ligands in bidentate coordination. A. halleri accumulates Pb whenever soil conditions render Pb phytoavailable. Considerable Pb accumulation under such circumstances, even in leaves of A. thaliana, strongly suggests that Pb can enter food webs and may pose a food safety risk.
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