Interplay of chelating and reducing root exudates in plant iron acquisition

Iron is an essential nutrient for plants and plant iron deficiency is a widespread problem in agriculture causing significant losses in costs and productivity. Iron deficiency is usually not caused by low iron concentrations in soils. Soils typically inherit the iron of source rocks and the average iron content of the continental crust is 3 % by mass. However, plant iron deficiency typically occurs on well aerated carbonatic soils where the availability of the soil iron is low due to the low solubility of iron bearing mineral phases. Plants adapted to such soils have evolved Fe acquisition strategies that modify the geochemistry of the soil in the direct vicinity of plant roots (i.e. the rhizosphere) in order to increase bioavailability. One such strategy is the production of ligands (so called siderophores) with very high affinity for the formation of soluble iron complexes that can be taken up by plant roots. This strategy is employed by grasses only, but these grasses include agriculturally important crops such as wheat, barley, corn and rice. Other plants rely on the production of smaller ligands with lesser affinity for iron, acidification of the root zone and reduction of iron from soluble complexes. Recently, a new class of coumarin-type ligand has been identified in root exudates that mediate ferric Fe chelation. However, due to their high chemical versatility their mode of action in the rhizosphere is still unclear. Therefore, the present project aims at i) identifying new exudate components with novel or specific Fe acquisition-related functions, in particular regarding the chelation and/or reduction of Fe(III), and characterizing modifications and chemical interactions of these components on their way from the release into the root apoplast to the soil and back; ii) examining synergisms among individual chemical processes involved in Fe mobilization from Fe-bearing phases in the soil; iii) identifying and quantifying the contribution and interplay of chemical and biological processes involved in Fe acquisition via plant-exuded reductants and ligands in the rhizosphere. To address a set of eight sharply defined hypotheses, two German and two Austrian labs from molecular plant nutrition, analytical chemistry, rhizosphere ecology and biogeochemistry will collect root exudates from hydroponic and rhizosphere systems, conduct metal-chelate speciation analysis by advanced MS-coupled techniques, assess Fe chelation and redox reactions of root exudates from wild-type and mutant plants and employ thermodynamic and kinetic modelling approaches. This proposal promises to chemically identify key players in root exudates and to describe their mode of action as chelators, reductants or redox shuttles for an improved Fe nutrition in plants. The understanding of these processes may serve to improve plant traits that support iron efficiency and to inspire cost efficient and environmentally sound fertilization strategies.

Summary research project: 'Interplay of chelating and reducing root exudates in plant iron acquisition' The identification of novel nutrient acquisition processes by crop plants does not occur very often. However, this is what some of the scientists of the current project found a few years ago: a novel mechanism of iron acquisition through the root exudation of so-called coumarins. Iron is an essential nutrient for plants and plant iron deficiency is a widespread problem in agriculture causing significant losses in costs and productivity. Iron deficiency is usually not caused by low iron concentrations in soils. Soils typically inherit the iron of source rocks and the average iron content of the continental crust is 3 % by mass. However, plant iron deficiency typically occurs on well aerated carbonatic soils where the availability of the soil iron is low due to the low solubility of iron bearing mineral phases. Plants adapted to such soils have evolved Fe acquisition strategies that modify the geochemistry of the soil in the direct vicinity of plant roots (i.e. the rhizosphere) in order to increase bioavailability. One such strategy is the production of ligands with high affinity for the formation of soluble iron complexes that can be taken up by plant roots, or the production of smaller ligands with lesser affinity for iron, acidification of the root zone and reduction of iron from soluble complexes. Coumarins have the potential to both ligate iron in soluble complexes and to reduce iron to Fe(II). In this context, the exudation and reactivity of coumarins was investigated In this project the exudation of coumarins by Arabidopsis was demonstrated and quantified not only under hydroponic conditions but also from soil grown plants. The coumarin exudation rates increased with decreasing Fe availability in carbonatic soils. Mutants defective in coumarin synthesis could not grow on these soils. Regarding the mechanism of iron mobilization, it was shown that coumarins mobilized Fe by both reductive dissolution (at low pH) and by a combination of reductive and ligand controlled dissolution at elevated pH (such as in carbonatic soils). Interestingly, the combined mechanisms at elevated pH were autocatalytic: ligand-controlled dissolution mechanism was autocatalytically accelerated by the presence of Fe(II) that was produced due to the reductive properties of coumarins. This efficient catalysis was observed even in presence of oxygen due to a stabilization of Fe(II) by coumarins. In summary, this project identified and elucidated new modes of Fe nutrition in plants and elucidated mechanisms by which these compounds act as chelators and reductants in order to catalytically promote iron mobilization. The understanding of these processes may serve to improve plant traits that support iron efficiency and to inspire cost efficient and environmentally sound fertilization strategies.