Iron Nutrition in Plants: Towards a New Paradigm?

Abstract

Iron (Fe) is an essential micronutrient for plant growth and development. Fe availability affects crops' productivity and the quality of their derived products and thus human nutrition. Fe is poorly available for plant use since it is mostly present in soils in the form of insoluble oxides/hydroxides, especially at neutral to alkaline pH. How plants cope with low-Fe conditions and acquire Fe from soil has been investigated for decades. Pioneering work highlighted that plants have evolved two different strategies to mine Fe from soils, the so-called Strategy I (Fe reduction strategy) and Strategy II (Fe chelation strategy). Strategy I is employed by non-grass species whereas graminaceous plants utilize Strategy II. Recently, it has emerged that these two strategies are not fully exclusive and that the mechanism used by plants for Fe uptake is directly shaped by the characteristics of the soil on which they grow (e.g., pH, oxygen concentration). In this review, recent findings on plant Fe uptake and the regulation of this process will be summarized and their impact on our understanding of plant Fe nutrition will be discussed.

Keywords: Arabidopsis; bHLH; dicots; grass; iron homeostasis; transcription factor.

Figure 1

Iron uptake strategies in plants, not so different after all. (a) Strategy I, also called the reduction-based strategy, was first described as specific to non-grass species. In Arabidopsis, AHA2 (H⁺-ATPase) secretes protons into the rhizosphere to solubilise Fe³⁺ which is then reduced into Fe²⁺ by the ferric reductase FRO2. Fe²⁺ is then uptaken into the plant root via IRT1 and to a lesser extent NRAMP1. Recent findings highlighted that the solubilization/reduction steps can be achieved in rice via the secretion of protocatechuic (PCA) and catechuic (CA) acids via the PEZ2 transporter. Fe²⁺ uptake into the root is then insured by IRT1, IRT2, NRAMP1 and NRAMP5 activities. (b) Strategy II, also called the chelation strategy, was first described as specific to grass species. In rice, mugineic acids (MAs) are secreted via the TOM transporter and Fe³⁺-MA complexes are taken up into the root via the YSL15 transporter. In Arabidopsis, it has recently been shown that Fe mobilizing coumarins (FMC) can chelate Fe³⁺ following their secretion into the rhizosphere via the PDR9 transporter and that Fe³⁺-FMC complexes are taken up into the plant root via an ATP-dependent mechanism.

Figure 2

Transcriptional regulation of iron homeostasis: conserved mechanisms between grass and non-grass species. Upstream from the Fe homeostasis transcriptional regulatory network is clade IVc bHLH transcription factors (i.e., the Arabidopsis IDT1/bHLH34, bHLH104, ILR3/bHLH105 and bHLH115, and the rice OsPRI1/OsbHLH60, OsPRI2/bHLH58, OsPRI3/OsbHLH59 and bHLH57). Among the conserved target genes of clade IVc bHLH between grass and non-grass species are: (i) Clade Ib bHLHs (i.e., bHLH38, bHLH39, bHLH100 and bHLH101, and the rice OsIRO2/OsbHLH56) whose encoded proteins interact with FIT/OsFIT to activate the expression of Fe uptake genes. (ii) Clade IVb bHLHs (the Arabidopsis PYE, and rice OsIRO3 and OsIRO4) whose encoded proteins interact with clade IVc bHLH (i.e., the Arabidopsis ILR3/bHLH105 and bHLH115, and the rice OsPRI1 and OsPRI2) to negatively regulate Fe homeostasis and their own expression. These interactions allow balancing Fe uptake and Fe storage to meet the Fe demand of the plant for its growth and development. (iii) Hemerythrin E3-ubiquitin (E3-ubi) ligases (i.e., the Arabidopsis BTS, and the rice HRZ1 and HRZ2) that are involved in the degradation of clade IVc bHLH transcription factors (i.e., the Arabidopsis ILR3/bHLH105 and bHLH115, and the rice OsPRI1 and OsPRI2). (iv) IMAs that encode peptides that interact with and negatively modulate the hemerythrin E3-ubiquitin ligase activities (i.e., the Arabidopsis BTS, and the rice HRZ1 and HRZ2) that participate in the inter-organ signalling of cellular Fe status for fine-tuning Fe uptake in roots.