Extreme nickel hyperaccumulation in the vascular tracts of the tree Phyllanthus balgooyi from Borneo

Phyllanthus balgooyi (Phyllanthaceae), one of > 20 nickel (Ni) hyperaccumulator plant species known in Sabah (Malaysia) on the island of Borneo, is remarkable because it contains > 16 wt% Ni in its phloem sap, the second highest concentration of Ni in any living material in the world (after Pycnandra acuminata (Sapotaceae) from New Caledonia with 25 wt% Ni in latex). This study focused on the tissue-level distribution of Ni and other elements in the leaves, petioles and stem of P. balgooyi using nuclear microprobe imaging (micro-PIXE). The results show that in the stems and petioles of P. balgooyi Ni concentrations were very high in the phloem, while in the leaves there was significant enrichment of this element in the major vascular bundles. In the leaves, cobalt (Co) was codistributed with Ni, while the distribution of manganese (Mn) was different. The highest enrichment of calcium (Ca) in the stems was in the periderm, the epidermis and subepidermis of the petiole, and in the palisade mesophyll of the leaf. Preferential accumulation of Ni in the vascular tracts suggests that Ni is present in a metabolically active form. The elemental distribution of P. balgooyi differs from those of many other Ni hyperaccumulator plant species from around the world where Ni is preferentially accumulated in leaf epidermal cells.