Phosphorus Uptake by Plants: From Soil to Cell

Abstract

P is an important plant macronutrient, making up about 0.2% of a plant's dry weight. It is a component of key molecules such as nucleic acids, phospholipids, and ATP, and, consequently, plants cannot grow without a reliable supply of this nutrient. Pi is also involved in controlling key enzyme reactions and in the regulation of metabolic pathways (Theodorou and Plaxton, 1993). After N, P is the second most frequently limiting macronutrient for plant growth. This update focuses on P in soil and its uptake by plants, transport across cell membranes, and compartmentation and redistribution within the plant. We will concentrate on P in higher plants, although broadly similar mechanisms have been shown to apply in algae and fungi. Although the total amount of P in the soil may be high, it is often present in unavailable forms or in forms that are only available outside of the rhizosphere. Few unfertilized soils release P fast enough to support the high growth rates of crop plant species. In many agricultural systems in which the application of P to the soil is necessary to ensure plant productivity, the recovery of applied P by crop plants in a growing season is very low, because in the soil more than 80% of the P becomes immobile and unavailable for plant uptake because of adsorption, precipitation, or conversion to the organic form (Holford, 1997). Plant acquisition of soil P. Plant root geometry and morphology are important for maximizing P uptake, because root systems that have higher ratios of surface area to volume will more effectively explore a larger volume of soil (Lynch, 1995). For this reason mycorrhizae are also important for plant P acquisition, since fungal hyphae greatly increase the volume of soil that plant roots explore (Smith and Read, 1997). In certain plant species, root clusters (proteoid roots) are formed in response to P limitations. These specialized roots exude high amounts of organic acids (up to 23% of net photosynthesis), which acidify the soil and chelate metal ions around the roots, resulting in the mobilization of P and some micronutrients (Marschner, 1995). The uptake of P poses a problem for plants, since the concentration of this mineral in the soil solution is low but plant requirements are high. The form of P most readily accessed by plants is Pi, the concentration of which rarely exceeds 10 μm in soil solutions (Bieleski, 1973). Therefore, plants must have specialized transporters at the root/soil interface for extraction of Pi from solutions of micromolar concentrations, as well as other mechanisms for transporting Pi across membranes between intracellular compartments, where the concentrations of Pi may be 1000-fold higher than in the external solution. There must also be efflux systems that play a role in the redistribution of this precious resource when soil P is no longer available or adequate. The form in which Pi exists in solution changes according to pH. The pKs for the dissociation of H3PO4 into H2PO4−and then into HPO42− are 2.1 and 7.2, respectively. Therefore, below pH 6.0, most Pi will be present as the monovalent H2PO4−species, whereas H3PO4 and HPO42− will be present only in minor proportions. Most studies on the pH dependence of Pi uptake in higher plants have found that uptake rates are highest between pH 5.0 and 6.0, where H2PO4−dominates (Ullrich-Eberius et al., 1984: Furihata et al., 1992), which suggests that Pi is taken up as the monovalent form. Under normal physiological conditions there is a requirement for energized transport of Pi across the plasma membrane from the soil to the plant because of the relatively high concentration of Pi in the cytoplasm and the negative membrane potential that is characteristic of plant cells. This energy requirement for Pi uptake is demonstrated by the effects of metabolic inhibitors, which rapidly reduce Pi uptake. The precise mechanics of membrane transport are still not clear, although cotransport of Pi with one or more protons is the favored option based on the following observations. The addition of Pi to starved roots results in both depolarization of the plasma membrane and acidification of the cytoplasm (Ullrich and Novacky, 1990). The depolarization indicates that Pi does not enter simply as H2PO4− or HPO42−, both of which would lead to membrane hyperpolarization. From these results it is likely that Pi is co-transported with positively charged ions. Cotransport of Pi with a cation involving a stoichiometry of more than 1 C+/H2PO4−or more than 2 C+/HPO42−would result in a net influx of positive charge and hence lead to the observed membrane depolarization. The cytoplasmic acidification associated with Pi transport would suggest that the cation is H+, but acidification would occur regardless of the nature of the cation if the transported species were H2PO4−, since it would undergo a pH-dependent dissociation in the cytoplasm to HPO42− and H+. To verify H+cotransport requires simultaneous or at least compara