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Natural variation, underlying molecular basis and ecological role of metal hyperaccumulation in Arabidopsis halleri

Subject Area Plant Physiology
Evolution, Anthropology
Ecology and Biodiversity of Plants and Ecosystems
Term from 2011 to 2021
Project identifier Deutsche Forschungsgemeinschaft (DFG) - Project number 197968016
 
The Brassicaceae species Arabidopsis halleri, one of the closest relatives of A. thaliana, exhibits naturally selected extreme traits, namely hyperaccumulation of the essential metal zinc (Zn) as well as the toxic metal cadmium (Cd) to levels several hundred fold higher than other plants, and the ability to colonize metal-rich habitats. We conducted a comprehensive survey of natural diversity of European A. halleri. Multi-element analysis in leaf and soil samples, records of plant developmental stage, habitat and climatic data constitute the largest field dataset of its kind. Our analysis uncovered, for instance, species-wide hyperaccumulation of Zn and tremendous natural variation in Cd accumulation that is strongly dependent on the biogeographic region. We newly discovered in A. halleri the hyperaccumulation of lead (Pb), one of the most problematic environmental pollutants. We transferred more than 900 genotypes from over 170 natural sites into the greenhouse, thus assembling the plant collection that is most comprehensively characterized with respect to characteristics at the sites of plant origin. Phenotyping of this collection under uniform conditions revealed unprecedented natural variation in leaf ionomic profiles. Variation was extreme for Zn and Cd, and metal accumulation was apparently partially suppressed in individuals from metal-contaminated sites. Metal hyperaccumulation is hypothesized to afford protection against herbivory. Indeed, we consistently found that plant elemental defence through Cd and Zn is effective on a wide range of chewing herbivores including potentially adapted field-collected insects. We defined a core collection of 28 individuals for in-depth physiological, molecular, and ecological dissection of (i) the physiological and molecular mechanisms underlying natural diversity in metal hyperaccumulation, and (ii) the ecological role in elemental defence of metal hyperaccumulation, newly including Pb. Metal translocation pathways will be comparatively characterized in the core collection upon cultivation under a variety of edaphic conditions. Metal accumulation will be studied alongside glucosinolate contents as the major classical chemical defence in Brassicaceae to determine the variation in defence investment and its relation with habitat characteristics. Comprehensive transcriptome analysis of the core collection and genome re-sequencing of extreme individuals as well as existing molecular insight will guide the selection of genes to be tested directly for their contribution to natural variation in metal accumulation. Transgenic lines will be generated and phenotyped on native A. halleri soils. Furthermore, the contribution of metal hyperaccumulation as an elemental defence against sucking insects will be determined using appropriate genotypes and transgenic lines differing in metal partitioning. We aim to unravel key steps in the adaptation to an extreme environment.
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