Responses of sugar beet roots to iron deficiency. Changes in carbon assimilation and oxygen use

Abstract

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 microM, 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.

Figure 1

Scanning electron micrographs showing the root distal segments of iron-deficient plants 5 to 10 mm from the apex (A), 0 to 5 mm from the apex (B), and iron-sufficient sugar beet plants 5 to 10 mm from the apex (C), and 0 to 5 mm from the apex (D).

Figure 2

Separation of organic acids (A), quinones (B), and flavins (C) by HPLC. Organic acids (detected at 210 nm) were oxalate, cis-aconitate, citrate, 2-oxoglutarate, ascorbate, malate, succinate, and fumarate. Flavins (detected at 445 nm) were FAD, FMN, SI, SII, and riboflavin. Reduced Q₉ and Q₁₀ were detected at 290 nm and oxidized Q₉ and Q₁₀ at 275 nm.

Figure 3

Changes in O₂ consumption rates in yellow, iron-deficient (A) and iron-sufficient root tips (B) with different concentrations of SHAM (○), CN⁻ (●), and CN⁻ + SHAM (▴). Data are means ± se of three different replications. Actual O₂ consumption rates are shown in Table V.

Figure 4

Metabolic model for carbon assimilation in sugar beet roots under iron deficiency. Iron deficiency would cause an approximately 50-fold enhancement in carbon assimilation (C.A.) in the cytosol through the increase in PEPC activity, and approximately 5-fold increases in the Krebs cycle (K.C.) and respiratory chain (R.C.) in the mitochondria. Part of the malate and the citrate would be exported via xylem, thus providing respiratory substrates to the shoot. ACoA, Acetyl coenzyme A; CIT, citrate; FUM, fumarate; ISC, isocitrate; MAL, malate; OXA, oxalacetate; OXG, oxoglutarate; PYR, pyruvate; SCoA, succinyl coenzyme A; SUC, succinate.

Figure 5

Proposed electron transport pathways in iron-deficient sugar beet roots. Reduced pyridine nucleotides would reduce flavins (Flv), which are oxidized and in large amounts in the cytosol (up to 700 μm). Flavins would finally provide electrons to the FC-R enzyme of the PM. This enzyme would be able to reduce not only Fe(III)-chelates, but also oxygen when Fe(III)-chelates are absent.