PIN FORMED 2 facilitates the transport of Arsenite in Arabidopsis thaliana

Abstract

Arsenic contamination is a major environmental issue as it may lead to serious health hazard. Reduced trivalent form of inorganic arsenic, arsenite, is in general more toxic to plants compared with the fully oxidized pentavalent arsenate. The uptake of arsenite in plants has been shown to be mediated through a large subfamily of plant aquaglyceroporins, nodulin 26-like intrinsic proteins (NIPs). However, the efflux mechanisms, as well as the mechanism of arsenite-induced root growth inhibition, remain poorly understood. Using molecular physiology, synchrotron imaging, and root transport assay approaches, we show that the cellular transport of trivalent arsenicals in Arabidopsis thaliana is strongly modulated by PIN FORMED 2 (PIN2) auxin efflux transporter. Direct transport assay using radioactive arsenite, X-ray fluorescence imaging (XFI) coupled with X-ray absorption spectroscopy (XAS), and ICP-MS analysis revealed that pin2 plants accumulate higher concentrations of arsenite in root compared to wild-type. At the cellular level, arsenite specifically targets intracellular cycling of PIN2 and thereby alters the cellular auxin homeostasis. Consistently, loss of PIN2 results in aresenite hypersensitivity in root. XFI coupled with XAS further revealed that loss of PIN2 results in specific accumulation of arsenical species, but not the other metals like iron, zinc or calcium in the root tip. Collectively, these results demonstrate that PIN2 serves as a putative transporter of arsenical species in planta.