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ENVIRONMENTAL STRESS AND ADAPTATION TO STRESS

The FRD3-Mediated Efflux of Citrate into the Root Vasculature Is Necessary for Efficient Iron Translocation^1,[OA]

Department of Biochemistry (T.P.D., E.E.R.), Division of Plant Sciences (W.G.), Department of Nutritional Sciences (E.E.R.), and C.S. Bond Life Sciences Center (T.P.D., W.G., E.E.R.), University of Missouri, Columbia, Missouri 65211

Iron, despite being an essential micronutrient, becomes toxic if present at high levels. As a result, plants possess carefully regulated mechanisms to acquire iron from the soil. The ferric reductase defective3 (frd3) mutant of Arabidopsis (Arabidopsis thaliana) is chlorotic and exhibits constitutive expression of its iron uptake responses. Consequently, frd3 mutants overaccumulate iron; yet, paradoxically, the frd3 phenotypes are due to a reduction in the amount of iron present inside frd3 leaf cells. The FRD3 protein belongs to the multidrug and toxin efflux family, members of which are known to export low-M_r organic molecules. We therefore hypothesized that FRD3 loads an iron chelator necessary for the correct distribution of iron throughout the plant into the xylem. One such potential chelator is citrate. Xylem exudate from frd3 plants contains significantly less citrate and iron than the exudate from wild-type plants. Additionally, supplementation of growth media with citrate rescues the frd3 phenotypes. The ectopic expression of FRD3-GFP results in enhanced tolerance to aluminum in Arabidopsis roots, a hallmark of organic acid exudation. Consistent with this result, approximately 3 times more citrate was detected in root exudate from plants ectopically expressing FRD3-GFP. Finally, heterologous studies in Xenopus laevis oocytes reveal that FRD3 mediates the transport of citrate. These results all strongly support the hypothesis that FRD3 effluxes citrate into the root vasculature, a process important for the translocation of iron to the leaves, as well as confirm previous reports suggesting that iron moves through the xylem as a ferric-citrate complex. Our results provide additional answers to long-standing questions about iron chelation in the vasculature and organic acid transport.

² Present address: Department of Plant Biology, Michigan State University, East Lansing, MI 48824.

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Elizabeth E. Rogers (rogersee{at}missouri.edu).

^[OA] Open Access articles can be viewed online without a subscription.

www.plantphysiol.org/cgi/doi/10.1104/pp.107.097162

^* Corresponding author; e-mail rogersee{at}missouri.edu; fax 573–884–9676.

Received February 1, 2007; accepted February 26, 2007; published March 9, 2007.

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