The Malaysian state of Sabah on the Island of Borneo has recently emerged as a global hotspot of nickel hyperaccumulator plants. This study focuses on the tissue-level distribution of nickel and other physiologically relevant elements in hyperaccumulator plants with distinct phylogenetical affinities. The roots, old stems, young stems and leaves of Flacourtia kinabaluensis (Salicaceae), Actephila alanbakeri (Phyllanthaceae), Psychotria sarmentosa (Rubiaceae) and young stems and leaves of Glochidion brunneum (Phyllanthaceae) were studied using nuclear microprobe (micro-PIXE and micro-BS) analysis. The tissue-level distribution of nickel found in these species has the same overall pattern as in most other hyperaccumulator plants studied previously, with substantial enrichment in the epidermal cells and in the phloem. This study also revealed enrichment of potassium in the spongy and palisade mesophyll of the studied species. Calcium, chlorine, manganese and cobalt were found to be enriched in the phloem and also concentrated in the epidermis and cortex of the studied species. Although hyperaccumulation ostensibly evolved numerous times independently, the basic mechanisms inferred from tissue elemental localization are convergent in these tropical woody species from Borneo Island.
Globally, the majority of Ni hyperaccumulator plants occur on ultramafic soils in tropical regions, and the genus Phyllanthus, from the Phyllanthaceae family, is globally the most represented taxonomical group. Two species from Sabah (Malaysia) are remarkable because Phyllanthus balgooyi can attain >16 wt% of Ni in its phloem exudate, while Phyllanthus rufuschaneyi reaches foliar concentrations of up to 3.5 wt% Ni, which are amongst the most extreme concentrations of Ni in any plant tissue. Synchrotron X-ray fluorescence microscopy, nuclear microbe (micro-PIXE+BS) and (cryo) scanning electron microscopy with energy dispersive spectroscopy were used to spatially resolve the elemental distribution in the plant organs of P. balgooyi and P. rufuschaneyi. The results show that P. balgooyi has extraordinary enrichment of Ni in the (secondary) veins of the leaves, whereas in contrast, in P. rufuschaneyi Ni occurs in interveinal areas. In the roots and stems, Ni is localized mainly in the cortex and phloem but is much lower in the xylem. The findings of this study show that, even within the same genus, the distribution of nickel and other elements, and inferred processes involved with metal hyperaccumulation, can differ substantially between species.