Roles of Arbuscular Mycorrhizas in Plant Phosphorus Nutrition: Interactions between Pathways of Phosphorus Uptake in Arbuscular Mycorrhizal Roots Have Important Implications for Understanding and Manipulating Plant Phosphorus Acquisition

Abstract

In this Update, we review new findings about the roles of the arbuscular mycorrhizas (mycorrhiza = fungus plus root) in plant growth and phosphorus (P) nutrition. We focus particularly on the function of arbuscular mycorrhizal (AM) symbioses with different outcomes for plant growth (from positive to negative) and especially on the interplay between direct P uptake via root epidermis (including root hairs when present) and uptake via the AM fungal pathway. The results are highly relevant to many aspects of AM symbiosis, ranging from signaling involved in the development of colonization and the regulation of P acquisition to the roles of AM fungi in determining the composition of natural plant assemblages in ecological settings and their changes with time. P is critical for plant growth and makes up about 0.2% of dry weight, but it is one of the most difficult nutrients for plants to acquire. In soil, it may be present in relatively large amounts, but much of it is poorly available because of the very low solubility of phosphates of iron, aluminum, and calcium, leading to soil solution concentrations of 10 μm or less and very low mobility (Schachtman et al., 1998). In consequence, uptake of orthophosphate (Pi) by root epidermal cells including root hairs (the direct pathway) leads to lowering of Pi concentrations in the rhizosphere (so-called depletion zones), because replacement does not keep pace with uptake (Fig. 1). Plants and fungi take up P as negatively charged Pi ions (H2PO4 −), which poses additional problems, because the concentration in cells is about 1,000-fold higher than in the soil solution and the cell membrane has an inside-negative electric potential. Pi uptake, therefore, requires metabolic energy and involves high-affinity transporter proteins in the Pht1 family (Bucher, 2007). Accordingly, plants have evolved a range of strategies that increase either Pi uptake capacity or availability of Pi in soil (Marschner, 1995). The most common of these strategies worldwide is AM symbiosis. Scattered through the plant kingdom are other strategies that enhance Pi availability or uptake, such as the formation of dense “cluster roots” that produce organic anions that release Pi from poorly available inorganic forms, but these are much less common (Cheng et al., 2011; Lambers et al., 2011). In many cases, it appears that cluster root formation may be an alternative strategy to AM formation, as in most Proteaceae and also white lupin (Lupinus albus), but some plants, such as Casuarina, develop both cluster roots and AM (Lambers et al., 2008). The two pathways of P uptake in an AM root involve different regions of the root, different cell types, and different Pi transporters. In the direct pathway (DP), Pi is absorbed from the rhizosphere by plant Pi transporters in epidermis and root hairs (green circles) close to the root surface. Uptake is normally faster than replacement by diffusion from the bulk soil, resulting in reduced Pi concentrations (depletion) close to the roots (callout 1). In the mycorrhizal pathway, Pi is taken up into AM fungal hyphae by fungal Pi transporters (blue circles) several centimeters from the root and translocated to intracellular fungal structures (arbuscules and hyphal coils) in root cortical cells (callout 2). Plant Pi transporters, induced in colonized cells (yellow circle), transfer Pi from the interfacial apoplast to plant cortical cells (callout 3). The majority (probably 70%–80%) of terrestrial plant species are capable of interacting with AM fungi in nature, and the activities of AM fungi and plant roots are closely integrated as a result of coevolution over at least 450 million years (Smith and Read, 2008). The major advantage of the AM symbiosis for plants in acquiring P is that AM fungi provide a very effective pathway (the AM pathway) by which P is scavenged from large volumes of soil and rapidly delivered to cortical cells within the root, bypassing direct uptake. The AM pathway can reduce the impact of Pi depletion in the rhizosphere and so improve plant P nutrition and growth (Fig. 1). The extent to which an AM plant grows better than a nonmycorrhizal (NM) counterpart (as in a pot experiment) depends in part on the size of its root system, including numbers and extent of root hairs. In general, plants with low root-shoot biomass ratios, slow root growth rates, and/or poor development of root hairs show relatively larger growth increases when AM. Conversely, growth differences between AM and NM plants tend to disappear as available soil P is increased, because of lower P depletion in rhizospheres (Smith and Read, 2008). Nevertheless, growth increases of AM plants over NM counterparts are maintained if high total soil P is poorly available (Bolan, 1991). Recent physiological and molecular research has revealed clearly that the AM pathway plays a major role in P uptake, regardless of the extent to which an AM plant benefits in terms of increased growth or P uptake