IRONMAN Tunes Responses to Iron Deficiency in Concert with Environmental pH

Iron (Fe) is an essential mineral element which governs the composition of natural plant communities and limits crop yield in agricultural ecosystems due to its extremely low availability in most soils, particularly at alkaline pH. To extract sufficient Fe from the soil under such conditions, some plants including Arabidopsis thaliana secrete Fe-mobilizing phenylpropanoids, which mobilize sparingly soluble Fe hydroxides by reduction and chelation. We show here that ectopic expression of the IRONMAN peptides IMA1 and IMA2 improves growth on calcareous soil by inducing the biosynthesis and secretion of the catecholic coumarin fraxetin (7,8-dihydroxy-6-methoxycoumarin) through increased expression of MYB72 and SCOPOLETIN 8-HYDROXYLASE (S8H), a response which is strictly dependent on elevated environmental pH (pHe). By contrast, transcription of the cytochrome P450 family protein CYP82C4, catalyzing the subsequent hydroxylation of fraxetin to sideretin, which forms less stable complexes with iron, was strongly repressed under such conditions. Luciferase reporter assays in transiently transformed protoplasts showed that IMA1/IMA2 peptides are translated and modulate the expression of CYP82C4 and MYB72 by acting as transcriptional coactivators. It is concluded that IMA peptides regulate processes supporting Fe uptake at both acidic and elevated pH by controlling gene expression upstream of or in concert with a putative pHe signal to adapt the plant to the prevailing edaphic conditions. This regulatory pattern confers tolerance to calcareous soils by extending the pH range in which Fe can be efficiently absorbed from the soil. Altering the expression of IMA peptides provides a novel route for generating plants adapted to calcareous soils. One sentence summaryEctopic expression of IRONMAN peptides improves growth under iron-limiting conditions by inducing responses to limited iron availability in accordance with the environmental pH. 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: Wolfgang Schmidt (wosh@gate.sinica.edu.tw).