Systemic Regulation of Iron Acquisition by Arabidopsis in Environments with Heterogeneous Iron Distributions

Nutrient distribution within the soil is generally heterogeneous. Plants, therefore, have evolved sophisticated systemic processes enabling them to optimize their nutrient acquisition efficiency. By organ-to-organ communication in Arabidopsis thaliana, for instance, iron starvation in one part of a root drives the upregulation of a high-affinity iron uptake system in other root regions surrounded by sufficient levels of iron. This compensatory response through Fe-starvation-triggered organ-to-organ communication includes the upregulation of Iron-regulated transporter 1 (IRT1) gene expression on the iron-sufficient side of the root, however, the molecular basis underlying this long-distance signaling remain unclear. Here, we analyzed gene expression by RNA-seq analysis of iron-starved split-root cultures. Genome-wide expression analysis showed that localized iron depletion in roots upregulated several genes involved in iron uptake and signaling, such as IRT1, in a distant part of the root exposed to iron-sufficient conditions. This result indicates that long-distance signaling for iron demand alters the expression of a subset of genes responsible for iron uptake and coumarin biosynthesis to maintain a level of iron acquisition sufficient for the entire plant. Loss of IRON MAN /FE-UPTAKE-INDUCING PEPTIDE (IMA/FEP) leads to the disruption of compensatory upregulation of IRT1 in the root surrounded by sufficient iron. In addition, our split-root culture-based analysis provides evidence that the IMA3/FEP1-MYB10/72 pathway mediates long-distance signaling in iron homeostasis through the regulation of coumarin biosynthesis. These data suggest that the signaling of IMA/FEP, a ubiquitous family of metal-binding peptides, is critical for organ-to-organ communication in response to iron starvation under heterogeneous iron conditions in the surrounding environment.