Mutually Exclusive Alterations in Secondary Metabolism Are Critical for the Uptake of Insoluble Iron Compounds by Arabidopsis and Medicago truncatula

Abstract

ORCID IDs: 0000-0002-7967-5136 (J.R.-C.); 0000-0001-5470-5901 (J.A.); 0000-0002-7850-6832 (W.S.).The generally low bioavailability of iron in aerobic soil systems forced plants to evolve sophisticated genetic strategies to improve the acquisition of iron from sparingly soluble and immobile iron pools. To distinguish between conserved and species-dependent components 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 upregulation of genes coding for enzymes involved in riboflavin biosynthesis in M. truncatula and phenylpropanoid synthesis in Arabidopsis upon iron deficiency. Coexpression and promoter analysis indicated that the synthesis of flavins and phenylpropanoids is tightly linked to and putatively coregulated with other genes encoding proteins involved in iron uptake. We further provide evidence that the production and secretion of phenolic compounds is critical for the uptake of iron from sources with low bioavailability but dispensable under conditions where iron is readily available. In Arabidopsis, homozygous mutations in the Fe(II)-and 2-oxoglutarate-dependent dioxygenase family gene F69H1 and defects in the expression of PLEIOTROPIC DRUG RESISTANCE9, encoding a putative efflux transporter for products from the phenylpropanoid pathway, compromised iron uptake from an iron source of low bioavailability. Both mutants were partially rescued when grown alongside wild-type Arabidopsis or M. truncatula seedlings, presumably by secreted phenolics and flavins. We concluded that production and secretion of compounds that facilitate the uptake of iron is an essential but poorly understood aspect of the reduction-based iron acquisition strategy, which is likely to contribute substantially to the efficiency of iron uptake in natural conditions.

Putrescine Alleviates Iron Deficiency via NO-Dependent Reutilization of Root Cell-Wall Fe in Arabidopsis

“…Rodríguez-Celma et al (2013) showed that secretion of phenolics is critical for Arabidopsis Fe acquisition from low bioavailability sources, and then Fourcroy et al (2014) and Schmidt et al (2014) demonstrated that coumarins are the active compounds in this process. Schmid et al (2014) confirmed that secretion of coumarins is an essential aspect of Arabidopsis Fe acquisition and provided extensive information on metabolomic changes elicited by Fe deficiency.…”

Iron-Binding E3 Ligase Mediates Iron Response in Plants by Targeting Basic Helix-Loop-Helix Transcription Factors

“…Recently, it has been shown that root exudates including phenolics and riboflavin derivatives function as iron-binding compounds in Arabidopsis and Medicago truncatula, similar to those in the chelation-based Strategy II response. The induction of phenylpropanoid and flavin pathway genes is tightly linked to core genes of the iron acquisition machinery, such as FIT, FRO2, IRT1, and AHA2, and thus appears to constitute an integral component of the Strategy I response in Arabidopsis and M. truncatula (Rodríguez-Celma et al, 2013).…”

Iron-Nicotianamine Transporters Are Required for Proper Long Distance Iron Signaling

“…Both these genes are strongly up-regulated by iron deficiency, and regulatory proteins governing the expression of these genes have been the subject of intense investigation (Colangelo and Guerinot, 2004;Jakoby et al, 2004;Yuan et al, 2005Yuan et al, , 2008Bauer et al, 2007;Wang et al, 2007;Long et al, 2010;Selote et al, 2015;Li et al, 2016;Mai et al, 2016). An additional component of iron uptake in nongraminaceous plants is the discovery that iron deficiency induces the secretion of phenolics and flavins (Rodríguez-Celma et al, 2013), later better defined as coumarins (Schmid et al, 2014) that are secreted by the ABCG37/PDR9 transporter (Fourcroy et al, 2014).…”