Apo-siderophores promote growth of iron-deficient Arabidopsis plants by mobilizing iron from roots to shoots and reducing oxidative stress in roots

Abstract

Iron (Fe) is an essential micronutrient for most organisms that is, however, poorly bioavailable in the soil. Acquiring this element is therefore a major issue for both plants and microorganisms. Bacteria acquire Fe by secreting siderophores that chelate the ferric ion with a high affinity and that can contribute to Fe nutrition in plants, under certain conditions including stressful ones. Our previous work has shown that pyoverdine, a siderophore purified from a beneficial Pseudomonas sp., leads to plant growth stimulation when supplied in its Fe-free form (apo-pyoverdine/apopyo) to Arabidopsis thaliana plants grown hydroponically under Fe-deficient conditions. To better understand siderophore-mediated growth promotion, we studied the impact of an apo-siderophore with a different structure from pyoverdine, deferoxamine (DFO), on the same model. Here we show that growth stimulation is linked to the ability of siderophores to chelate Fe, as DFO also promotes growth after 3 to 6 days when provided at 25 µM to 4-week-old A. thaliana plants starved for Fe for 1 to 7 days. The extent to which the siderophore stimulates root and shoot growth depends on the amount of Fe stored in the roots prior to the addition of DFO, and likely involves the remobilization of Fe from the roots to the shoots. The promotion of root growth by DFO does not appear to depend on coumarin production or secretion, but is associated with an increase in the expression of genes of the HOMOLOG OF BEE2 INTERACTING WITH IBH1 (HBI1)-dependent brassinosteroid signaling pathway. DFO stimulates lateral root elongation concomitant with a significant decrease in hydrogen peroxide (H2O2) and oxidized glutathione levels and a decrease in stress-related gene expression in roots. In addition, DFO decreases the expression of the UPBEAT (UPB1) gene involved in H2O2-mediated root growth inhibition, and thus lifts the inhibition of the expression of its target genes, the class III peroxidases that stimulate root growth. Overall, this work indicates that growth promotion by apo-siderophores in an iron-poor environment is likely linked to their ability to induce a stronger response to Fe deficiency while decreasing oxidative stress in roots, thus stimulating Fe remobilization from root Fe pools to shoots and promoting secondary root growth.