Reduction-based iron uptake revisited

Abstract

With the exception of the grasses, plants rely on a reduction-based iron (Fe) uptake system that is compromised by high soil pH, leading to severe chlorosis and reduced yield in crop plants. We recently reported that iron deficiency triggers the production of secondary metabolites that are beneficial for Fe uptake in particular at high external pH when iron is present but not readily available. The exact function of these metabolites, however, remains enigmatic. Here, we speculate on the mechanism by which secondary metabolites secreted by roots from Fe-deficient plants improve Fe acquisition. We suggest that the production and excretion of Iron Binding Compounds (IBCs) constitute an integrative, pH-insensitive component of the reduction-based iron uptake strategy in plants.Although iron (Fe) is generally present in large amounts, in aerobic soils Fe tends to form oxyhydrates of low solubility, in particular at neutral or high pH. When atmospheric oxygen increased as a result of the evolution of photosynthesis, plants were forced to evolve strategies that improve Fe acquisition, which was chiefly achieved by increasing the solubility of immobile Fe pools. All plant species except the grasses have employed a mechanism that includes reduction of ferric chelates, mediated by a plasma membrane-bound oxidoreductase (FRO2 in Arabidopsis). The reduction of Fe(III) weakens the stability of the chelate and the released Fe(II) is taken up by a ZIP family transporter (IRT1).2 A drawback of this strategy is that it works best at a slightly acidic pH and is strongly impaired in soils with high pH.3 This is partly counteracted by induction of a P-type H + -ATPase that provides a favorable pH environment (AHA2). 4Excretion of organic compounds, mainly phenolics or flavins, have been associated with the Fe deficiency response since the early seventies, 5,6 but were later considered to be of minor importance and, with some notable exceptions (e.g., the massive production of riboflavin and riboflavin derivatives by some species), 7,8 were largely neglected in studies related to iron acquisition processes in model species such as Arabidopsis. Nevertheless, the frequent observation of this phenomenon led to speculations on the function of these compounds in Fe acquisition, comprising effects on the microbiome in the rhizosphere, a function (for flavins) in electron transport during the reduction of Fe(III), chelation of Fe, and chemical reduction of Fe(III). The first clear-cut evidence for a function of Fe deficiency-induced root secretions in Fe uptake was provided by Jin et al. showing that phenolics secreted by red clover roots facilitated the acquisition of Fe bound to anionic residues in the apoplast.9 Similarly, transgenic rice plants overexpressing the phenolic efflux transporter PEZ1 grew better on soils with high pH and poor Fe solubility.10 In Arabidopsis, robust induction of the phenylpropanoid pathway, both at the transcript and protein levels, 11,12 indicating that in roots of Fe-deficient plants phenolic compounds ar...

Gene Expression Profiling of Iron Deficiency Chlorosis Sensitive and Tolerant Soybean Indicates Key Roles for Phenylpropanoids under Alkalinity Stress

“…Iron deficient dicots are known to increase production and efflux of either flavin compounds or fluorescent phenolic compounds, but not both within a single species (Cesco et al, 2010 ; Rodríguez-Celma and Schmidt, 2013 ). Iron deficient Arabidopsis increases production of phenolics of the coumarin class (Rodríguez-Celma et al, 2013 ; Schmid et al, 2014 ; Schmidt et al, 2014 ) by increasing expression of the phenylpropanoid pathway, and our results suggest that soybean has a similar response.…”

Tapping into cyanobacteria electron transfer for higher exoelectrogenic activity by imposing iron limited growth

“…54) and inhibited at high pH. [54][55][56][57][58] Regulated paths which operate optimally at a more acidic pH as a strategy for iron uptake is likely due to the fact that lower pH favours the solubility of ferrous, the product of ferric reduction. 59 The enhanced ferricyanide reduction capacity of iron limited PCC7942 may be indirect evidence of the proposed reductive iron acquisition system involving SomB1-irpAB-r1, overexpressed in iron limited growth.…”

Ethylene Participates in the Regulation of Fe Deficiency Responses in Strategy I Plants and in Rice

“…This includes the capacity to acidify the rhizosphere medium (due to increased expression of plasma membrane proton-ATPase genes, such as AtAHA2, AtAHA7, CsHA1 , and MxHA7 ), which contributes to Fe solubilisation (Santi et al, 2005 ; Waters et al, 2007 ; Zha et al, 2014 ); and the increased synthesis and release of Fe 3+ -related compounds such as flavins and phenolics (Jin et al, 2007 ; Rodríguez-Celma et al, 2013 ; Fourcroy et al, 2014 ; Schmid et al, 2014 ; Schmidt et al, 2014 ). The exact function of flavins and phenolics is not totally clear, but it has been proposed that they could act as “Iron Binding Compounds” contributing to Fe mobilization in the rhizosphere (Rodríguez-Celma and Schmidt, 2013 ). Alternatively, their main function could be related to Fe 3+ reduction, acting as long distance electron shuttle (Rodríguez-Celma and Schmidt, 2013 ).…”

“…The exact function of flavins and phenolics is not totally clear, but it has been proposed that they could act as “Iron Binding Compounds” contributing to Fe mobilization in the rhizosphere (Rodríguez-Celma and Schmidt, 2013 ). Alternatively, their main function could be related to Fe 3+ reduction, acting as long distance electron shuttle (Rodríguez-Celma and Schmidt, 2013 ).…”