Plant strategies to mine iron from alkaline substrates

Abstract

In concert with oxygen, soil alkalinity strongly restricts the availability of iron, an essential nutrient with a multitude of functions in living organisms. In addition to its role in mitochondrial energy metabolism and as a cofactor for enzymes, in plants iron also plays key roles in photosynthesis and is required for chlorophyll biosynthesis. The ability to thrive in calcareous soils, referred to as calcicole behaviour, is the readout of an amalgam of traits of which efficient foraging of iron is a decisive factor. Recently, the well-established concept of two distinct iron uptake strategies, phylogenetically separating grasses from other land plants, was expanded by the discovery of auxiliary mechanisms that extend the range of edaphic conditions to which a species can adapt. Secretion of a tailor-made cocktail of iron-mobilising metabolites into the rhizosphere, the composition of which is responsive to a suite of edaphic and internal cues, allows survival in calcareous soils through a competitive iron acquisition strategy, which includes intricate interactions with the consortium of associated microorganisms in, on, and around the roots. This versatile, reciprocal plant-microbiome interplay affects iron mobilisation directly, but also collaterally by impacting growth, fitness, and health of the host. Here, we review the mechanisms and the multifaceted regulation of iron acquisition in plants, taking into consideration the specific constraints associated with the uptake of iron from alkaline soils. Knowledge on how plants extract iron from such soils sets the stage for a better understanding of essential ecological processes and for combatting iron malnutrition in humans.

Effects of Citric Acid and Humic-like Substances on Yield, Enzyme Activities, and Expression of Genes Involved in Iron Uptake in Tomato Plants

“…Abiotic stress from Fe deprivation is signaled through the phloem from sinks in the root system, where there is an alteration in the absorption and transport of this nutrient [50]. In nongrass monocotyledons and in dicotyledons, such as tomato, that develop under conditions of Fe deprivation and/or in calcareous soils, strategy I presents an enzymatic mechanism for coping with Fe-deficient conditions; according to the results obtained, H + -ATPase and FRO enzymes may be involved in this mechanism and act together with enzymes of the antioxidant system in addition to the regulation of iron transporters (IRT1, ZIP and NRAMP1) and probably coumarin excretion [13]. Although our study does not show a situation of iron deficiency recovery, we can clarify the individual impact of CA and HLS on the enzymatic mechanisms related to iron metabolism in tomato plants grown in calcareous soil.…”

“…The FRO, IRT1, and NRAMP1 genes are regulated transcriptionally by the central basic helix-loop-helix (bHLH) FER-like Fe deficiency-induced transcription factor (FIT) [11]. Similarly, phenolic compounds such as coumarins [12,13] and organic acids [6] are exuded by roots and are involved in the Fe-making machinery by facilitating the solubilization and reduction of unavailable Fe in the soil.…”

Protein Phosphorylation Orchestrates Acclimations ofArabidopsisPlants to Environmental pH

“…From the vast suite of responses to alterations in iron availability, vacuolar iron sequestration appears to be the only process that is responsive to pH e , suggesting that control of the cytosolic iron concentration has priority over mobilization, uptake, and xylem-loading of iron (to ultimately satisfy the demand of sink tissues). Thus, avoidance of iron overload - strictly controlled by pH e – seems to be controlled separately from the responses to low iron availability, which induces a much more pronounced and multi-faceted response (65).…”

Iron sensing in plants

“…Iron is an abundant element in most soils; however, only a minor fraction of the total Fe is available for uptake by plant roots. This shortage is caused by the formation of Fe(III) oxyhydroxides with extremely low solubility, in particular in alkaline soils ( Vélez-Bermúdez and Schmidt, 2022 ). Only in extremely acidic soils or in the absence of oxygen, Fe is available in concentrations that may exceed the requirement of plants and cause oxidative damage due to the formation of radical oxygen species.…”