Cellular coumarin uptake mediated by CIT1 plays a key role in root iron acquisition of Arabidopsis

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English. Iron (Fe) is essential for a wide range of physiological events in many organisms including plants since it serves as a central component of various types of metalloproteins. However, plants frequently suffer from Fe deficiency because the majority of Fe in natural soil is insoluble ferric (hydr)oxides, which is not bioavailable. To overcome this limitation, plants exudate plant-specialized metabolites capable of ferric Fe solubilization from roots in response to poor Fe environments. Fe-mobilizing coumarins (FMC), such as fraxetin, form a metabolite group contributing to this process in non-grass species. In Arabidopsis, FMC emission from cortex and epidermis into the rhizosphere relies on the the ABC transporter PDR9 (ABCG37). Interestingly, these cell layers were also shown to absorb coumarins exogenously supplied in Fe-limiting conditions. It raises the question of whether a cellular uptake of coumarins in these cells might play an important role in FMC secretion-based Fe acquisition. To answer this question, we aimed to identify membrane transporters involved in FMC uptake and characterized their physiological functions in Arabidopsis. We recently isolated Coumarin Import Transporter1 (CIT1), whose expression responds to Fe deficiency in Arabidopsis roots. Loss-of-function of CIT1 resulted in the disruption of coumarin secretion and seedling growth in Fe-limiting conditions (Figure). CIT1 protein accumulation was strongly induced in root epidermis encountering Fe deficiency, consistent with the major site of PDR9 localization. Transport assay using yeast cells demonstrated an uptake activity of CIT1 against fraxetin and its precursor scopoletin, but not against other compounds related to FMC biosynthesis. Given that coumarins are abundant in both cortex and epidermal cell layers, these results suggest that CIT1 reinforces PDR9-mediated FMC secretion from the epidermis by loading cortex-derived coumarins into the epidermis, leading to intense Fe acquisition.