Rhizosphere Acidification as a Response to Iron Deficiency in Bean Plants

Abstract

Iron deficiency in higher plants causes accumulation of salts of organic acids in the roots, the most characteristic being citrate. We show that citrate and malate accumulate in beans (Phaseolus vulgaris L. var Prelude), not because of a lack of the iron-containing enzyme aconitase (EC 4.2.13), but in close coupling to the extrusion of protons during rhizosphere acidification, one of the 'Fe-efficiency' reactions of dicotyledonous plants. When proton excretion is induced in roots of control bean plants by addition of fusicoccin, only malate, not citrate, is accumulated. We propose that iron deficiency induces production of organic acids in the roots, which in beans leads to both proton excretion and an increased capacity to reduce ferric chelates via the induced electron transfer system in the root epidermis cells.Plants growing under iron deficiency may employ different strategies to increase iron uptake: (a) dicotyledons and non-grass monocotyledons develop a strong ferric reduction activity at the root surface (2); moreover, they may acidify the rhizosphere by active proton extrusion (23); and (b) grasses excrete highly effective siderophores, which are structurally related to the cellular iron carrier nicotianamine (27). Both mono-and dicotyledons are known to accumulate organic acid salts, especially citrate, in roots (6,14,31) and leaves (10,26).Evidence has accumulated which shows that the ferric reduction activity in the roots of Fe-efficient dicotyledons resides in the plasma membrane of the root epidermis cells, where an enzyme system can transfer electrons from cytosolic NADPH to extracellular ferric chelates, with low substrate specificity (2). This enzyme system has not been found in grasses (19).We recently proposed that accumulated citrate, via the activities of aconitase and isocitrate dehydrogenase, is responsible for the strongly reduced redox poise of NADP in cells with high ferric reduction capacity (4). Citrate accumulation, in response to iron deficiency, has been suggested to be caused by lowered levels of the iron-containing enzyme aconitase (1,8,31 Enzyme Assays. Tissue extracts were made by grinding the tissue (roots after washing with 0.5 mm CaSO4) with 50% (w/w) polyvinylpolypyrrolidone, washed sand and an extraction buffer at OC in a porcelain mortar. The resulting brei was centrifuged at 1 lOOg for 5 min and the supernatant at 50.000g for 10 min. From the last supernatant 2.5 ml was brought over 4 ml Sephadex G-25 and the eluate was used for determination of enzyme activity. The extraction buffer for aconitase (EC 4.2.1.3) was 0.1 M Hepes, 10 mM tricarballylate, pH 7.5. The activity was determined in two ways: (a) by following the formation ofcis-aconitate from citrate at 240 nm (1 mM cis-aconitate: A240 = 3.55) (18). The reaction mixture contained, in a final volume of 500 ,ul, 0.1 M Hepes, 10 mM citrate, pH 7.5, and up to 100 Ml enzyme preparation. The reaction was started by addition of citrate; and (b)

Literature review: Phytoaccumulation of chromium, uranium, and plutonium in plant systems

“…Although the detailed mechanisms of Cr translocation are not understood, there are reports that Fe-deficient and P-deficient plants can better translocate Cr from roots to shoots (Cary et al, 1977a;Bonet et al, 1991). These results lead to the hypothesis that Fe-and P-deficiency induced accumulation of organic acids, e.g., citric acid (Landsberg, 1981;De Vos et al, 1986;Johnson et al, 1994), may play an important role in Cr translocation.…”

Phosphorus Stress-Induced Proteoid Roots Show Altered Metabolism in Lupinus albus

“…Exudation of organic acids by other species in response to nutrient stress, particularly P and Fe, has been documented (Landsberg, 1981;Marschner et al, 1986;Ric De Vos et al, 1986;Lipton et al, 1987). Concentrations of malic and citric acids were distinctly higher in acidified rhizosphere segments of P-starved rape (Brassica napus) plants, which coincided with increased malate in the corresponding root tissue (Hoffland et al, 1989).…”

Modulation of iron responsive gene expression and enzymatic activities in response to changes of the iron nutritional status in Cucumis sativus L.

“…In fact, the energy demand in the roots under iron stress deficiency is very high since they necessitate an increased amount of reducing equivalents, energy and tricarboxylic cycle intermediates to sustain all the processes induced by this condition (Zocchi, 2006 and reference therein). Indeed, an increase in the sugar concentration has been demonstrated in the phloem of iron deficient bean plants (De Vos et al, 1986). Whether sugars, or other molecules transported along with them in the phloem, are responsible for a systemic signal in iron deficiency response is still unknown.…”