Hydroxamate siderophores in the iron nutrition of plants

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Abstract
Most fungi and some bacteria respond to Fe deprivation by producing high affinity, ferric‐specific Fe transport ligands called hydroxamate siderophores (HSs). These secondary hydroxamic acids have molecular weights between 500 and 1200 daltons and typically contain three 6‐N‐hydroxyornithine moieties that combine to form ferric chelates with stability constants of approximately 1030. Higher plants under iron‐stressed conditions have been reported to assimilate Fe supplied as Fe(III)‐HSs. This has been confirmed in our laboratories in preliminary studies which demonstrated the uptake and translocation of 55Fe supplied to monooot seedlings as the HS, ferrichrome. Monocot seedlings were also able to absorb and translocate a mixture of fungal HS ligands. These results suggested that the presence of HSs in the vicinity of the root would enhance Fe availability in soil systems. The presence of HSs in a variety of soils was established. Soils from 49 sites representing 22 different taxonomic subgroups were determined by Arthrobacter flavescens JG‐9 bioassay to contain HSs in con‐centrations ranging from 3 nM to 34 nM desferrioxamine B (DFOB) equivalents in aqueous extracts. When corrected to 10% soil moisture the values ranged from 28 nM to 279 nM, chelate concentrations well above the 10 nM concentrations predicted to be necessary to supply Fe to plants by diffusion and mass flow in most soils. A large reservoir of HSs adsorbed to soil particles was also demonstrated by multiple, sequential extraction of natural soil. In bulk soil samples, the adsorption (an average of 98%) of the cationic HS, DFOB, was directly correlated with clay content. Adsorption of this compound was essentially complete within six minutes after addition and appeared to be by a cation exchange reaction. Desorption of natural HSs from soil was a slow reaction and was closely correlated with organic matter content. Adsorption isotherms of both DFOB and mixed fungal HSs and humic acid were linear over a wide concentration range. Adsorption appeared to control the availability of natural HSs in bulk soil, but the 11‐ to 56‐fold higher concentrations found in the rhizosphere soils of ectomycorrhizal pine seedlings suggested that production might temporarily be the determining factor at favorable microsites. The zone of Fe‐HS depletion in the vicinity of the plant root that would result from the low mobility of HSs in soil might be partly compensated for by the accumulation or production of HSs by rhizosphere microorganisms in general and mycorrhizal fungi in particular. Fourteen of 15 ectomycorrhizal fungi investigated produced HSs under Fe‐deficient conditions. The potential for HSs to serve as effective Fe chelators in plant nutrition was established by computer modeling and laboratory experiments which determined the mole fractions of metal chelates for Fe and competing ions in both nutrient solution and soil solution. Under chelate equilibria conditions from pH 4 to 10 in nutrient solution and soil solution, computer modeling predicted that the Fe‐HS chelate formed by DFOB would remain stable over the entire pH range. However, citrate was predicted to occur predominantly as a Ca or Mg chelate above pH 6.0 with less than 0.1% of the ligand chelated to Fe above pH 7. Oxalate, malate, malonate, and succinate were unable to chelate significant Fe above pH 6.0, and less than 10% of these ligands were predicted to be chelated with Fe at pH 5.0. Experimental measurements of chelated Fe in nutrient solution of pH 4 to 10 and.in soil extracts agreed with the predicted values. In contrast to the other organic acids above, as well as pyruvate and α‐ketoglutarate, only DFOB and an ectomycorrhizal fungus‐derived mixture of HSs formed stable Fe chelates above pH 6.0 in nutrient solution. Both DPOB and the HS mixture were predominantly chelated with Fe in a 1:1 (ml H2O/g soil) soil suspension of pH 7.7, whereas no chelated Fe could be detected with the other acids. Since we have found that HSs occur in most soils and are effective Fe chelators over a wide range of pH, are produced by some mycorrhizal fungi which form intimate associations with plant roots, and can be absorbed by plants, we contend that such ligands should be iitportant in Fe nutrition of plants.