Biogeochemical Pathways of Phytate-P Utilization in Soil: Plant and Microbial Strategies

Abstract

Phytate (salts of myo-inositol-1,2,3,4,5,6-hexakisphosphate) constitutes a large portion of the organic phosphorus in most soils, but its strong interactions with soil minerals and organic matter limit its availability to plants. Phytate can be used by plants only after it is desorbed from the soil matrix, with the inorganic P being released by phytases via cleavage of its phosphomonoester bonds. While plant phytases function primarily in its internal phytate remobilization, the role of microbial phytases in facilitating phytate-P utilization by plants remains poorly understood. This review focuses on phytase-producing plants and microbes and their uses in improving crop P acquisition from soil phytate. We discuss the behaviors of phytate and phytase in soils, especially their complex interactions with metal oxides, silicate minerals, and organic matter. Strategies to optimize soil phytase activity, including enzyme immobilization, site-directed mutagenesis, and rational protein design are also explored. Besides, we examine the mechanisms and hydrolysis pathways involved in phytase-mediated phytate hydrolysis, identifying situations where phytate utilization is limited by phytate solubility or phytase activity from an evolutionary perspective based on cultivation conditions and plant characteristics. Finally, we summarize strategies to increase plant utilization of soil phytate, including (1) amending soil with phytase-producing microbes, (2) expressing phytase gene in plant roots, (3) coupling phytase and organic acid exudation from plant roots, (4) intercropping phytase-producing plants with organic acid-secreting plants, and (5) incorporating phytase into plants with great organic acid production as cover crops. As these strategies are effective only in specific environments, future studies should focus on: (1) developing novel phytases with high activity and resistance to soil deactivation, (2) cultivating plants that effectively secrete phytase and mobilize soil phytate, and (3) engineering microbial consortia with stable and efficient phytate hydrolysis capabilities. Besides, integrated catalyst systems combining biological and chemical approaches also offer promising solutions for soil phytate hydrolysis. These strategies will exploit stable soil organic P by crop plants while simultaneously decreasing agricultural dependence on P fertilizer and reducing P loss to the environment.