IRONMAN tunes responses to iron deficiency in concert with environmental pH

Abstract

Abstract Iron (Fe) is an essential mineral element that 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 (Arabidopsis thaliana), secrete Fe-mobilizing phenylpropanoids, which mobilize sparingly soluble Fe hydroxides by reduction and chelation. We show here that ectopic expression of the peptides IRONMAN (IMA1) and IMA2 improves growth on calcareous soil by inducing biosynthesis and secretion of the catecholic coumarin 7,8-dihydroxy-6-methoxycoumarin (fraxetin) via increased expression of MYB72 and SCOPOLETIN 8-HYDROXYLASE, a response that 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. We 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, adapting the plant to 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. Our results further suggest that pHe calibrates the activities of components of the Fe deficiency response, accentuating processes that are most efficient under the prevailing conditions. Altering the expression of IMA peptides provides a route for generating plants adapted to calcareous soils.