Uncovering the physiology and distribution of thallium in Tl-hyperaccumulating and Tl-sensitive populations of Biscutella laevigata L.

Background And Aims: Thallium (Tl) is extremely toxic to all life forms and is an emerging pollutant. Plants in the Brassicaceae family, including edible crops, have an enhanced capacity for Tl accumulation, even from soils with low thallium concentration. The most extreme Tl hyperaccumulator is Biscutella laevigata, capable of attaining >32 000 μg Tl g-1 dry weight (DW) in its leaves.

Methods: Biscutella laevigata from a non-metallicolous accession (Feltre, Italy) and a metallicolous accession (Les Malines, France) were subjected to a dosing experiment in hydroponics (0, 5 and 30 μm Tl), followed by synchrotron-based micro-X-ray fluorescence analysis to elucidate tissue- and cellular-level Tl distribution.

Key Results: Flow cytometric data on the two accessions showed that the Feltre accession has a genome size twice of that of the Les Malines accession (256 and 125 pg per 2C, respectively), suggesting that they are phylogenetically distant populations. The Feltre accession did not accumulate Tl (125 μg Tl g-1 DW on average in leaves) at the 5 µm Tl dose level, whereas the Les Malines accession had a mean of 1750 μg Tl g-1 DW, with peaks of 24 130 μg Tl g-1 DW, at the 30 µm Tl dose level. At 30 µm Tl, the non-metallicolous accession did not grow, and at 5 µm Tl it showed reduced biomass compared with the metallicolous one. In the Les Malines accession, the synchrotron-based micro-X-ray fluorescence analysis revealed that Tl was localized in the vacuoles of epidermal cells, especially underneath trichomes and in trichome basal cells. Thallium also occurred in solid crystalline deposits (3-5 µm in size, ~40 wt% Tl) that were found mainly in foliar margins and under trichome bases.

Conclusions: Biscutella laevigata is an attractive model for studying Tl hypertolerance and hyperaccumulation on account of the extreme expression of this trait and its marked intraspecific variability.