Pathways, mechanisms and efficiency of phosphate transfer in vesicular-arbuscular mycorrhizal roots

Abstract

The roots of most terrestrial plants are normally colonised by fungi that form beneficial symbioses (mycorrhizas) where a major physiological function is the transfer to the plant of nutrients that are relatively immobile in soil, in exchange for carbohydrates that are used for fungal growth. The most common mycorrhizas are vesicular-arbuscular (VA) mycorrhizas, which are very widespread in wild and cultivated plants. Membrane transport processes are central to the nutritional interactions in VA mycorrhizas. We have estimated that fluxes of P from fungus to root are so high that special mechanisms promoting P efflux from the fungus must be activated by the plant. The fungus may activate transport mechanisms for carbon transfer from the root that are similar to those involved in phloem unloading to the cortical apoplast. It is usually assumed that P transfer to the plant occurs only across the intracellular (arbuscular) interface, simultaneously with carbohydrate transfer from the plant. However, we have obtained evidence that in VA mycorrhizas which have both arbuscular and extensive intercellular phases (Arum-types) the transfer processes are spatially separated. We have suggested that carbohydrate may efflux mainly from cortical cells into the intercellular apoplast, from which it is absorbed into intercellular hyphae, and that the arbuscule is primarily the site of P transfer. Spatial separation between sites of transfer of P and carbohydrates can account for variations in efficiency of nutrient transport (i.e. amount of P transported to the host per amount of carbon transported to the fungus) in different host/fungus combinations or under different environmental conditions. We discuss here the possible functional significance of VA mycorrhizas in which there are different intraradical structures (Arum- versus Paris-types). We suggest that structural differences may be related to differences in nutritional efficiency of the symbiosis. The interesting question of why a plant permits colonisation that may result in little or no nutritional benefit is briefly addressed and the costs and benefits of the VA mycorrhizal association are reviewed. We emphasise the need for integration of structural and functional studies of VA mycorrhizas, and for more research on the mycorrhizas of wild plants.