Nutrient transfer in arbuscular mycorrhizas: how are fungal and plant processes integrated?

This review brings together recent work on the coordination of transport processes between fungus and plant symbionts in arbuscular mycorrhizal (AM) symbioses, and focuses on new information on the diversity in structure and function of interfaces and their potential roles in transport processes. We consider the way that fungal activity is polarised to absorb mineral nutrients (especially phosphorus, P) in soil, transport them to the root and release them to the plant. Conversely, the fungal structures within the root appear to be specialised to absorb sugars, which the external mycelium cannot do. The external mycelium depends on a supply of lipid, transported from within the root. High affinity P transporters expressed in the root apices and root hairs of non-mycorrhizal roots, and most probably mycorrhizal roots, absorb P actively. This can result in the development of P depletion zones, so that a low concentration of P at the absorbing surfaces limits further uptake. The external hyphae of AM fungi extend well beyond the depletion zone, accessing supplies of P at a distance and in narrow soil pores, that is absorbed actively by a high affinity P transporter expressed in these small diameter hyphae. Translocation of P within the hyphae and transfer to the plant results in much higher rates of uptake (inflows) by mycorrhizal than non-mycorrhizal roots. The possible role of polyphosphate (polyP) in this process is discussed in the light of new data. Within the root, P is lost from the fungal structures to the interfacial apoplast by an unknown mechanism, and is absorbed by the root cortical cells. The expression of a high affinity P transporter and H + -ATPase in arbuscule-containing cells indicates that these are probably the sites of fungus/plant P transfer. The site of sugar transfer from plant to fungus has not yet been established. At the whole plant level, plant uptake systems located in the youngest regions of the root are positioned to absorb P from undepleted soil, into which the root apex has just grown. In older regions of the roots, colonised by mycorrhizal fungi, the external mycelium will take over the absorptive role and overcome the difficulties posed by the slow diffusion of P in soil.