Mycorrhizal Fungi Can Dominate Phosphate Supply to Plants Irrespective of Growth Responses

Abstract

Arbuscular mycorrhizal (AM) fungi are vital components of nearly all terrestrial ecosystems, forming mutually beneficial (mutualistic) symbioses with the roots of around 80% of vascular plants and often increasing phosphate (P) uptake and growth. We present novel data showing that AM fungi can provide the dominant route for plant P supply, even when overall growth or P uptake remains unaffected. The results will change our understanding of the roles of AM fungi in agricultural and natural ecosystems; they also predict that mycorrhiza-specific plant P transporters must play a major role in plant P uptake regardless of whether the plants respond to AM colonization by taking up more P per plant or by increased dry weight, compared with nonmycorrhizal (NM) control plants. AM associations are the outcome of 450 million years of co-evolution, which has led to adaptations in both plants and fungi that underpin their symbiotic development and function. The main physiological basis for mutualism is bidirectional nutrient transfer (Smith and Smith, 1990). Plants supply the AM fungi with sugars, and the fungi enhance the ability of the plants to scavenge for scarce and immobile nutrients, particularly P. Different AM fungus-plant combinations are functionally diverse both in effectiveness of the fungi as symbionts and in responsiveness of the plants in terms of total P uptake, growth, and/or reproduction, again compared with NM controls. This diversity has significant influences on plant interactions in ecosystems (Read, 1998; van der Heijden et al., 1998; Jakobsen et al., 2002; van der Heijden and Sanders, 2002) but is poorly understood at physiological or molecular levels. In an AM plant, P (as orthophosphate) can be absorbed both directly at the soil-root interface through root epidermis and root hairs and via the “mycorrhizal” pathway via external AM hyphae in soil (Fig. 1). These hyphae absorb P, translocate it rapidly to AM structures within the roots (intercellular hyphae, intracellular coils, and highly branched intracellular arbuscules; for details, see Smith and Read, 1997), from whence it is released to the interfacial apoplast adjacent to root cortical cells (Smith and Smith, 1990). Quantitative estimates of the fungal contribution to total P uptake have often assumed that the direct and mycorrhizal uptake pathways act in concert, although it is recognized that uptake directly from soil may decrease as the concentration of P in the soil solution adjacent to the roots becomes depleted (Tinker and Nye, 2000). The ability of AM hyphae to grow beyond this depletion zone and deliver P to the root is thought to be the main basis for their positive effects on P uptake and plant growth (Smith and Read, 1997). Where there is no response to symbiosis in terms of these variables (i.e. values for AM plants are not larger than NM plants growing in the same soil), it has been assumed that the mycorrhizal uptake pathway is not functioning and that all of the plant P is absorbed directly through P transporters in the root epidermis and root hairs. Increased growth or success of AM plants is then attributed to other benefits of the symbiosis, such as suppression of pathogens (West et al., 1993; Newsham et al., 1995). Diagrammatic representation (not to scale) of direct and mycorrhizal uptake pathways into plant roots. In the direct pathway, high-affinity plant P transporters (black circles) located in the epidermis and root hairs are involved in uptake of orthophosphate from the soil solution directly into plant cells. If the rate of uptake exceeds the rate of diffusion of P in the soil solution, the concentration of P is reduced leading to 1- to 2-mm zones of depletion (narrow yellow band) close to the root surfaces, which limit the rate of uptake. The mycorrhizal pathway involves uptake of P from the soil solution by AM fungal transporters (blue circles) located in external hyphae. P is then translocated rapidly over considerable distances (1-15 cm) and is delivered to fungus-plant interfaces in the root cortex. Plant P transporters located at these interfaces (black circles) absorb P into root cortical cells. We now present results of an experiment carried out in a low-P soil/sand mix to determine the relative contributions of the direct and mycorrhizal uptake pathways in three plant species of varying responsiveness to mycorrhizas when colonized by three AM fungal species. The plants were flax (Linum usitatissimum L. cv Linetta), tomato (Lycopersicon esculentum Mill. cv Rio-Grande 76R), and medic (Medicago truncatula L. cv Jemalong). The AM fungi Gigaspora rosea Nicolson and Schenck (Banque Européen des Glomales, BEG 9), Glomus intraradices Schenck and Smith (BEG 87), and Glomus caledonium (Nicol. and Gerd.) Trappe and Gerdemann (BEG 20) were grown in pot cultures of Trifolium subterraneum to provide inoculum, because AM fungi are unculturable and must be propagated on host plants. All plant-fungus combinations plus n