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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.

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Different root parts with or without increased iron-reducing activities have been studied in iron-deficient and iron-sufficient control sugar beet (Beta vulgaris L. Monohil hybrid). The distal root parts of iron-deficient plants, 0 to 5 mm from the root apex, were capable to reduce Fe(III)-chelates and contained concentrations of flavins near 700 m, two characteristics absent in the 5 to 10 mm sections of iron-deficient plants and the whole root of iron-sufficient plants. Flavin-containing root tips had large pools of carboxylic acids and high activities of enzymes involved in organic acid metabolism. In iron-deficient yellow root tips there was a large increase in carbon fixation associated to an increase in phosphoenolpyruvate carboxylase activity. Part of this carbon was used, through an increase in mitochondrial activity, to increase the capacity to produce reducing power, whereas another part was exported via xylem. Root respiration was increased by iron deficiency. In sugar beet iron-deficient roots flavins would provide a suitable link between the increased capacity to produce reduced nucleotides and the plasma membrane associated ferric chelate reductase enzyme(s). Iron-deficient roots had a large oxygen consumption rate in the presence of cyanide and hydroxisalycilic acid, suggesting that the ferric chelate reductase enzyme is able to reduce oxygen in the absence of Fe(III)-chelates.

The effects of iron deficiency on the composition of the xylem sap and leaf apoplastic fluid have been characterized in sugar beet (Beta vulgaris Monohil hybrid). pH was estimated from direct measurements in apoplastic fluid and xylem sap obtained by centrifugation and by fluorescence of leaves incubated with 5-carboxyfluorescein and fluorescein isothiocyanate-dextran. Iron deficiency caused a slight decrease in the pH of the leaf apoplast (from 6.3 down to 5.9) and xylem sap (from 6.0 down to 5.7) of sugar beet. Major organic acids found in leaf apoplastic fluid and xylem sap were malate and citrate. Total organic acid concentration in control plants was 4.3 mm in apoplastic fluid and 9.4 mm in xylem sap and increased to 12.2 and 50.4 mm, respectively, in iron-deficient plants. Inorganic cation and anion concentrations also changed with iron deficiency both in apoplastic fluid and xylem sap. Iron decreased with iron deficiency from 5.5 to 2.5 m in apoplastic fluid and xylem sap. Major predicted iron species in both compartments were [FeCitOH] Ϫ1 in the controls and [FeCit 2 ] Ϫ3 in the iron-deficient plants. Data suggest the existence of an influx of organic acids from the roots to the leaves via xylem, probably associated to an anaplerotic carbon dioxide fixation by roots.

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The effects of high Zn concentration were investigated in sugar beet (Beta vulgaris L.) plants grown in a controlled environment in hydroponics. High concentrations of Zn sulphate in the nutrient solution (50, 100 and 300 microm) decreased root and shoot fresh and dry mass, and increased root/shoot ratios, when compared to control conditions (1.2 microm Zn). Plants grown with excess Zn had inward-rolled leaf edges and a damaged and brownish root system, with short lateral roots. High Zn decreased N, Mg, K and Mn concentrations in all plant parts, whereas P and Ca concentrations increased, but only in shoots. Leaves of plants treated with 50 and 100 microm Zn developed symptoms of Fe deficiency, including decreases in Fe, chlorophyll and carotenoid concentrations, increases in carotenoid/chlorophyll and chlorophyll a/b ratios and de-epoxidation of violaxanthin cycle pigments. Plants grown with 300 microm Zn had decreased photosystem II efficiency and further growth decreases but did not have leaf Fe deficiency symptoms. Leaf Zn concentrations of plants grown with excess Zn were high but fairly constant (230-260 microg.g(-1) dry weight), whereas total Zn uptake per plant decreased markedly with high Zn supply. These data indicate that sugar beet could be a good model to investigate Zn homeostasis mechanisms in plants, but is not an efficient species for Zn phytoremediation.