Root exudation of phytosiderophores from soil-grown wheat

Abstract

For the first time, phytosiderophore (PS) release of wheat (Triticum aestivum cv Tamaro) grown on a calcareous soil was repeatedly and nondestructively sampled using rhizoboxes combined with a recently developed root exudate collecting tool. As in nutrient solution culture, we observed a distinct diurnal release rhythm; however, the measured PS efflux was c. 50 times lower than PS exudation from the same cultivar grown in zero iron (Fe)-hydroponic culture. Phytosiderophore rhizosphere soil solution concentrations and PS release of the Tamaro cultivar were soil-dependent, suggesting complex interactions of soil characteristics (salinity, trace metal availability) and the physiological status of the plant and the related regulation (amount and timing) of PS release. Our results demonstrate that carbon and energy investment into Fe acquisition under natural growth conditions is significantly smaller than previously derived from zero Fe-hydroponic studies. Based on experimental data, we calculated that during the investigated period (21-47 d after germination), PS release initially exceeded Fe plant uptake 10-fold, but significantly declined after c. 5 wk after germination. Phytosiderophore exudation observed under natural growth conditions is a prerequisite for a more accurate and realistic assessment of Fe mobilization processes in the rhizosphere using both experimental and modeling approaches.

Keywords: 2′-deoxymugineic acid (DMA); Triticum aestivum cv Tamaro; iron deficiency; phytosiderophore; rhizosphere; strategy II; trace elements.

Fig. 1

2′-Deoxymugineic acid (DMA) exudation rates of wheat (Triticum aestivum cv Tamaro) grown in rhizoboxes filled with calcareous soil (Santomera) and sampled by the root exudate collecting (REC) tool. (a) Plant age-dependent exudation rates sampled for an 8 h period starting at the onset of light (left axis) and concurrent changes in the SPAD index (right axis) (b) Plant age-dependent diurnal rhythm of DMA release. Values represent means ± SE (DMA, n = 5; SPAD, n = 18).

Fig. 2

2′-Deoxymugineic acid (DMA) exudation rates (a) and total carbon (C) exudation rates (b) (nmol C g⁻¹ root DW s⁻¹, derived from total dissolved organic C analyzed) of wheat (Triticum aestivum cv Tamaro) grown on seven different calcareous soils. White numbers represent DMA-derived C as a percentage of total C released. Exudation was sampled hydroponically at 44 d after germination (DAG). Values represent means ± SE (n = 3). Letters indicate significant differences of DMA and total C release, with P < 0.05. Letters a, b: ANOVA including all soils, letters x, y: ANOVA excluding the saline soil Nadec. Sant, Santomera; Xer T, Xeraco topsoil; Xer L, Xeraco subsoil; Bol, Bologna; Nad, Nadec; Lass, Lassee; SL 10%, Siebenlinden + 10% CaCO₃.

Fig. 3

Differences (Δ) in soluble metal concentrations between the sampled bulk and rhizosphere soil solution calculated by subtracting metal rhizosphere from average bulk soil concentrations, averaged across both sampling events. Values represent means ± SE (n = 6). Statistically significant differences are highlighted: *, P < 0.05. Sant, Santomera; Xer T, Xeraco topsoil; Xer L, Xeraco subsoil; Bol, Bologna; Nad, Nadec; Lass, Lassee; SL 10%, Siebenlinden + 10% CaCO₃.

Fig. 4

Maximum theoretical soil solution concentrations of 2′-deoxymugineic acid (DMA, μM) after 24 h in the close vicinity of wheat (Triticum aestivum cv Tamaro) roots (0.5 mm distance from the root surface) grown on the calcareous Santomera soil, calculated based on exudation rates obtained in the 24 h stepwise sampling at 33 and 46 d after germination (DAG) and assuming a uniform root diameter (0.5 mm). Closed symbols, theoretical DMA concentrations around root tips assuming hotspot exudation behavior (i.e. active proportion of root biomass is only 20%); open symbols, averaged theoretical DMA concentration across the total root system (TRS i.e. active proportion of root biomass is 100%).