Organic acids, such as malate, citrate and oxalate, have been proposed to be involved in many processes operating in the rhizosphere, including nutrient acquisition and metal detoxification, alleviation of anaerobic stress in roots, mineral weathering and pathogen attraction. A full assessment of their role in these processes, however, cannot be determined unless the exact mechanisms of plant organic acid release and the fate of these compounds in the soil are more fully understood. This review therefore includes information on organic acid levels in plants (concentrations, compartmentalisation, spatial aspects, synthesis), plant efflux (passive versus active transport, theoretical versus experimental considerations), soil reactions (soil solution concentrations, sorption) and microbial considerations (mineralization). In summary, the release of organic acids from roots can operate by multiple mechanisms in response to a number of well-defined environmental stresses (e.g., Al, P and Fe stress, anoxia): These responses, however, are highly stress- and plant-species specific. In addition, this review indicates that the sorption of organic acids to the mineral phase and mineralisation by the soil's microbial biomass are critical to determining the effectiveness of organic acids in most rhizosphere processes.

Organic acids in the rhizosphere: a critical review

All plants are inhabited internally by diverse microbial communities comprising bacterial, archaeal, fungal, and protistic taxa. These microorganisms showing endophytic lifestyles play crucial roles in plant development, growth, fitness, and diversification. The increasing awareness of and information on endophytes provide insight into the complexity of the plant microbiome. The nature of plant-endophyte interactions ranges from mutualism to pathogenicity. This depends on a set of abiotic and biotic factors, including the genotypes of plants and microbes, environmental conditions, and the dynamic network of interactions within the plant biome. In this review, we address the concept of endophytism, considering the latest insights into evolution, plant ecosystem functioning, and multipartite interactions.

The Hidden World within Plants: Ecological and Evolutionary Considerations for Defining Functioning of Microbial Endophytes

The role of mycorrhizal fungi in acquisition of mineral nutrients by host plants is examined for three groups of mycorrhizas. These are; the ectomycorrhizas (ECM), the ericoid mycorrhizas (EM), and the vesicular-arbuscular mycorrhizas (VAM). Mycorrhizal infection may affect the mineral nutrition of the host plant directly by enhancing plant growth through nutrient acquisition by the fungus, or indirectly by modifying transpiration rates and the composition of rhizosphere microflora.

Nutrient uptake in mycorrhizal symbiosis

Because of their ability to transform atmospheric N2 into ammonia that can be used by the plant, researchers were originally very optimistic about the potential of associative diazotrophic bacteria to promote the growth of many cereals and grasses. However, multiple inoculation experiments during recent decades failed to show a substantial contribution of Biological Nitrogen Fixation (BNF) to plant growth in most cases. It is now clear that associative diazotrophs exert their positive effects on plant growth directly or indirectly through (a combination of) different mechanisms. Apart from fixing N2, diazotrophs can affect plant growth directly by the synthesis of phytohormones and vitamins, inhibition of plant ethylene synthesis, improved nutrient uptake, enhanced stress resistance, solubilization of inorganic phosphate and mineralization of organic phosphate. Indirectly, diazotrophs are able to decrease or prevent the deleterious effects of pathogenic microorganisms, mostly through the synthesis of anti...

Plant Growth-Promoting Effects of Diazotrophs in the Rhizosphere

Roots of grasses in response to iron deficiency markedly increase the release of chelating substances (;phytosiderophores') which are highly effective in solubilization of sparingly soluble inorganic Fe(III) compounds by formation of Fe(III)phytosiderophores. In barley (Hordeum vulgare L.), the rate of iron uptake from Fe(III)phytosiderophores is 100 to 1000 times faster than the rate from synthetic Fe chelates (e.g. Fe ethylenediaminetetraacetate) or microbial Fe siderophores (e.g. ferrichrome). Reduction of Fe(III) is not involved in the preferential iron uptake from Fe(III)phytosiderophores by barley. This is indicated by experiments with varied pH, addition of bicarbonate or of a strong chelator for Fe(II) (e.g. batho-phenanthrolinedisulfonate). The results indicate the existence of a specific uptake system for Fe(III)phytosiderophores in roots of barley and all other graminaceous species. In contrast to grasses, cucumber plants (Cucumis sativus L.) take up iron from Fe(III)phytosiderophores at rates similar to those from synthetic Fe chelates. Furthermore, under Fe deficiency in cucumber, increased rates of uptake of Fe(III)phytosiderophores are based on the same mechanism as for synthetic Fe chelates, namely enhanced Fe(III) reduction and chelate splitting. Two strategies are evident from the experiments for the acquisition of iron by plants under iron deficiency. Strategy I (in most nongraminaceous species) is characterized by an inducible plasma membrane-bound reductase and enhancement of H(+) release. Strategy II (in grasses) is characterized by enhanced release of phytosiderophores and by a highly specific uptake system for Fe(III)phytosiderophores. Strategy II seems to have several ecological advantages over Strategy I such as solubilization of sparingly soluble inorganic Fe(III) compounds in the rhizosphere, and less inhibition by high pH. The principal differences in the two strategies have to be taken into account in screening methods for resistance to ;lime chlorosis'.

Evidence for a specific uptake system for iron phytosiderophores in roots of grasses.

Although iron is abundant in soils (1–6%), it is often unavailable to plants because its solubility is dependent on pH and controlled by the low solubility of ferric oxides. Iron availability to plant roots may thus depend on organic chelators which Lindsay reports would maintain an adequate iron supply by diffusion and mass flow at concentrations as low as 10−8 M1,2. Hydroxamate siderophores (HS), microbially produced, ferric-specific, iron transport molecules with stability constants3 as high as 1032, may represent the chelators which maintain these soil iron concentrations. Such peptide derivatives were shown to control iron availability in aquatic ecosystems4, but little is known about their soil role beyond their function as microbial growth factors5,6. We report here the occurrence of HS in aqueous extracts of a variety of soils in concentrations (10−7 M–10−8 M after correction to 10% soil moisture) sufficient to affect plant nutrition1,2.

Occurrence of hydroxamate siderophore iron chelators in soils

Numerous ectomycorrhizal fungi were surveyed for their ability to produce iron-chelating, hydroxamate siderophores (HS). Production of HS was determined by a bioassay based on the stimulation of th...

Production of Hydroxamate Siderophore Iron Chelators by Ectomycorrhizal Fungi

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 w...

Hydroxamate siderophores in the iron nutrition of plants

Comparison of the Abilities of Hydroxamic, Synthetic, and Other Natural Organic Acids to Chelate Iron and Other Ions in Nutrient Solution1

When Fe was supplied at 100 micromolar in nutrient solution of pH 7.5, 10 and 1 micromolar levels of the siderophore desferrioxamine B (DFOB), a microbial iron transport compound, significantly (α = 0.05) enhanced growth and reduced chlorosis of an Fe-inefficient variety of sorghum ( Sorghum bicolor L.). Although significantly adverse effects resulted when both Fe and desferrioxamine B (DFOB) were added at 100 micromolar as FeDFOB, the plants were relatively healthy when grown with 100 micromolar DFOB plus 200 micromolar Fe. It was concluded that sorghum absorbed Fe from the pool of nonchelated, solubilized Fe, and utilized DFOB as a shuttle agent, in equilibrium with this pool, to transport Fe from finely suspended solid phase Fe particles to the membrane of absorbing root cells. In contrast to sorghum, absorption of Fe by the Fe-efficient species sunflower ( Helianthus annuus L.) was related to the level of FeDFOB and independent of the level of solubilized, nonchelated Fe. The latter was decreased whenever the concentration of DFOB was equal to or greater than the concentration of total Fe. For an Fe concentration of 10 micromolar, significantly larger and greener plants were obtained when DFOB was present at 1, 10, or 100 micromolar than in the absence of DFOB. When grown with 100 micromolar FeDFOB, sunflower plants appeared larger and less chlorotic than those supplied with 100 micromolar Fe and no DFOB. Sunflower apparently was able to utilize FeDFOB more directly than was sorghum. It is suggested that sunflower acquires Fe after binding FeDFOB at membrane sites and/or by producing sufficient reductants in the rhizosphere to reduce biologically significant levels of Fe(III)DFOB to the less stable Fe(II)DFOB.

P. E. Powell

Papers

Occurrence of hydroxamate siderophore iron chelators in soils

Production of Hydroxamate Siderophore Iron Chelators by Ectomycorrhizal Fungi

Hydroxamate siderophores in the iron nutrition of plants

Comparison of the Abilities of Hydroxamic, Synthetic, and Other Natural Organic Acids to Chelate Iron and Other Ions in Nutrient Solution1

Effects of a Hydroxamate Siderophore on Iron Absorption by Sunflower and Sorghum