A soil bacterium regulates plant acquisition of iron via deficiency‐inducible mechanisms

Abstract

Despite the abundance of iron in nature, it is the third most limiting nutrient for plants due to its minimal solubility in most soils. While certain soil microbes produce chelating agents that enhance the solubility of iron, the effectiveness of such siderophores in the assimilation of iron by plants is debated. With an increasing understanding that select soil microbes play a signaling role in activating growth and stress responses in plants, the question arises as to whether such symbionts regulate iron assimilation. Here we report a previously unidentified mechanism in which the growth-promoting bacterium Bacillus subtilis GB03 activates the plant's own iron acquisition machinery to increase assimilation of metal ions in Arabidopsis. Mechanistic studies reveal that GB03 transcriptionally up-regulates the Fe-deficiency-induced transcription factor 1 (FIT1), which is necessary for GB03-induction of ferric reductase FRO2 and the iron transporter IRT1. In addition, GB03 causes acidification of the rhizosphere by enhancing root proton release and by direct bacterial acidification, thereby facilitating iron mobility. As a result, GB03-exposed plants have elevated endogenous iron levels as well as increased photosynthetic capacity compared with water-treated controls. In contrast, loss-of-function fit1-2 mutants are compromised in terms of enhanced iron assimilation and photosynthetic efficiency triggered by GB03. In all studies reported herein, a physical partition separating roots from bacterial media precludes non-volatile microbial siderophores from contributing to GB03-stimulated iron acquisition. These results demonstrate the potential of microbes to control iron acquisition in plants and emphasize the sophisticated integration of microbial signaling in photosynthetic regulation.