Hyperaccumulating plants are characterized by their tolerance and ability to accumulate otherwise toxic concentration of metal(loid)s, yet the role of the microbiome remains poorly understood. In Slovenia, two zinc (Zn) and cadmium (Cd) species occur naturally: Noccaea caerulescens and N. praecox, both of which grow at the non-metalliferous site in Lokovec, while N. praecox also occurs at the metalliferous site in Žerjav, polluted with Zn, Cd and lead (Pb). The aim of this study was to investigate the microbiome, transcriptome, metabolome, and metal accumulation, and to assess the effects of plant host and environment on plant responses under natural and controlled conditions. Two experimental approaches were used: (i) natural populations from non-metalliferous and metalliferous sites and (ii) a transplant experiment in which seeds of both N. praecox ecotypes were planted in Lokovec and Žerjav substrates. Whole plants, including roots and rhizosphere, were sampled for root-associated microbiome, leaf transcriptome and metabolome profiling, and determination of Zn, Cd and Pb in leaves. In natural populations, the root and rhizosphere microbiomes of the two species from Lokovec did not differ, whereas the microbiomes of N. praecox ecotypes were taxonomically and functionally distinct. The leaf transcriptome and metabolome analyses revealed genes and metabolites associated with high metal concentrations, including pathways involved in glutathione metabolism, phenylpropanoid and flavonoid biosynthesis, with species- and environment-specific patterns. In the transplant experiment, transfer to a different substrate led to changes in the diversity and relative abundance of microbial taxa, particularly in the rhizosphere. In the metalliferous substrate, higher Zn concentrations were measured in the leaves of the Lokovec ecotype compared to the Žerjav ecotype, and differences in the spatial distribution of Zn within leaves were also observed. The results of both experiments highlight the complexity of hyperaccumulation and emphasise the important role of ecotype selection for optimising phytoremediation.
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