Mutually Exclusive Alterations in Secondary MetabolismAre Critical for the Uptake of Insoluble Iron Compoundsby Arabidopsis and Medicago truncatula

Abstract

The generally low bioavailability of iron in aerobic soil systems forced plants to evolve sophisticated genetic strategies to improvethe acquisition of iron from sparingly soluble and immobile iron pools. To distinguish between conserved and species-dependentcomponents of such strategies, we analyzed iron deficiency-induced changes in the transcriptome of two model species,Arabidopsis (Arabidopsis thaliana) and Medicago truncatula. Transcriptional profiling by RNA sequencing revealed a massive upregulationof genes coding for enzymes involved in riboflavin biosynthesis in M. truncatula and phenylpropanoid synthesis inArabidopsis upon iron deficiency. Coexpression and promoter analysis indicated that the synthesis of flavins and phenylpropanoidsis tightly linked to and putatively coregulated with other genes encoding proteins involved in iron uptake. We further provideevidence that the production and secretion of phenolic compounds is critical for the uptake of iron from sources with lowbioavailability but dispensable under conditions where iron is readily available. In Arabidopsis, homozygous mutations in theFe(II)- and 2-oxoglutarate-dependent dioxygenase family gene F69H1 and defects in the expression of PLEIOTROPIC DRUGRESISTANCE9, encoding a putative efflux transporter for products from the phenylpropanoid pathway, compromised ironuptake from an iron source of low bioavailability. Both mutants were partially rescued when grown alongside wild-typeArabidopsis or M. truncatula seedlings, presumably by secreted phenolics and flavins. We concluded that production andsecretion of compounds that facilitate the uptake of iron is an essential but poorly understood aspect of the reduction-basediron acquisition strategy, which is likely to contribute substantially to the efficiency of iron uptake in natural conditions