Phytosiderophore Efflux Transporters Are Crucial for Iron Acquisition in Graminaceous Plants

Abstract

Eukaryotic organisms have developed diverse mechanisms for the acquisition of iron, which is required for their survival. Graminaceous plants use a chelation strategy. They secrete phytosiderophore compounds, which solubilize iron in the soil, and then take up the resulting iron-phytosiderophore complexes. Bacteria and mammals also secrete siderophores to acquire iron. Although phytosiderophore secretion is crucial for plant growth, its molecular mechanism remains unknown. Here, we show that the efflux of deoxymugineic acid, the primary phytosiderophore from rice and barley, involves the TOM1 and HvTOM1 genes, respectively. Xenopus laevis oocytes expressing TOM1 or HvTOM1 released 14C-labeled deoxymugineic acid but not 14C-labeled nicotianamine, a structural analog and biosynthetic precursor of deoxymugineic acid, indicating that the TOM1 and HvTOM1 proteins are the phytosiderophore efflux transporters. Under conditions of iron deficiency, rice and barley roots express high levels of TOM1 and HvTOM1, respectively, and the overexpression of these genes increased tolerance to iron deficiency. In rice roots, the efficiency of deoxymugineic acid secretion was enhanced by overexpression of TOM1 and decreased by its repression, providing further evidence that TOM1 encodes the efflux transporter of deoxymugineic acid. We have also identified two genes encoding efflux transporters of nicotianamine, ENA1 and ENA2. Our identification of phytosiderophore efflux transporters has revealed the final piece in the molecular machinery of iron acquisition in graminaceous plants.

Nutritionally Enhanced Staple Food Crops

“…The higher amount of both Fe and Zn in Aegilops species compared with that of wheat cultivars under deficient conditions reveal that Aegilops species possess an efficient system for the uptake and translocation of these micronutrients to the leaves and ultimately to seeds. Nozoye et al (2011) report that the efflux of DMA, the primary phytosiderophore from rice and barley, involves the TOM1 and HvTOM1 genes, respectively, the missing piece in the mechanics of the Fe acquision by graminaceous plants, which reveals that the TOM1 and HvTOM1 proteins are the phytosiderophore efflux transporters. Under conditions of iron deficiency, rice and barley roots express high levels of TOM1 and HvTOM1, respectively, and the overexpression of these genes increased tolerance to iron deficiency.…”

Improved iron acquisition ofAstragalus sinicusunder low iron-availability conditions by soil-borne bacteriaBurkholderia cepacia

“…Strategy II plants exhibit greater growth traits than strategy I plants under alkaline conditions. Since the PS-Fe 3+ complexes are directly taken up by roots, without requirement for Fe-reduction of strategy I plants (Nozoye et al 2011). Differing from the reduction-based Fe acquisition, the chelation-based system is much insensitive to alkaline conditions (Römheld and Marschner 1986).…”

Enrichment of ⁶⁵Zn in two contrasting rice genotypes under varying methods of zinc application

“…Similar genotypic variation in translocation and accumulation of 65 Zn was also reported earlier by Shankhdhar et al (2000). Translocation efficiency depends on expression of the efflux transporter genes of nicotianamine (ENA1 and ENA2) which are likely to play role in Zn uptake and transport inside plants (Nozoye et al 2011). Increased amounts of nicotianamine and deoxymugineic acid are involved in the efficient translocation of Zn and Fe into rice grains (Kobayashi and Nishizawa 2012).…”