Secretion of redox-active metabolites as a general strategy for iron acquisition in plants

Abstract

Iron is an essential but often poorly bioavailable nutrient due to its low solubility, especially in alkaline soils. Plants have evolved at least two distinct strategies to extract iron from soil: solubilization of ferric iron by phytosiderophores, and reduction to the ferrous form at the root surface followed by direct import. Here, we describe the discovery of a novel redox-active catecholic metabolite, termed sideretin, which derives from the coumarin fraxetin, and is the primary molecule exuded by Arabidopsis thaliana roots in response to iron deficiency. Using a combination of metabolomics, heterologous expression, and coexpression analysis we have identified two enzymes that complete the biosynthetic pathway of sideretin. Chemical characterization of synthetic sideretin and biological assays with pathway mutants suggest that sideretin is critical for iron nutrition and support a role for small molecule-mediated iron reduction in A. thaliana under iron-limiting growth conditions. Further, we show that sideretin production is evolutionarily ancient and occurs in eudicot species only distantly related to A. thaliana. In addition to sideretin, untargeted metabolomics of the root exudates of various eudicots revealed the production of structurally diverse redox-active molecules in response to iron deficiency. Our results indicate that secretion of small molecule reductants by roots may be a widespread and previously underappreciated component of the reduction-based iron uptake strategy.