Assessing the Divergent Soil Phosphorus Recovery Strategies in Domesticated and Wild Crops

Abstract

Plant-essential phosphorus (P) is a sparingly available mineral in soils. Phosphorus fertilizers-produced by the transformation of insoluble to soluble phosphates-are thus applied to agroecosystems. With advancements in commercial agriculture, crops have been increasingly adapted to grow in fertile environments. Wild crop relatives, however, are adapted to grow in unfertilized soils. In response to these two conditions of P bioavailability (fertilized agroecosystems and unfertilized natural soils), domesticated crops and wild species employ different strategies to grow and develop. It is essential to understand strategies related to P acquisition that may have been lost to domestication, and here we present, for the first time, that across species, modern cultivars engage in physical (i.e., root morphological) mechanisms while their wild relatives promote ecological (i.e., root-microbial) mechanisms. Domesticated crops showcase shallower root system architecture and engage in topsoil foraging to acquire P from the nutrient-stratified environments common to fertilized agroecosystems. Wild species associate with P-cycling bacteria and AM fungi. This divergence in P recovery strategies is a novel delineation of current research that has implications for enhancing agricultural sustainability. By identifying the traits related to P recovery that have been lost to domestication, we can strengthen the P recovery responses by modern crops and reduce P fertilization.

Keywords: domestication; phosphorus; plant-microbe interaction; pqqC; rhizosphere.

Figure 1

Common forms of loss of soluble phosphorus (P) from soil solution. The form of soluble P varies with pH (blue box). Soluble P is plant available and is taken up by roots. H₂PO₄⁻ is the predominant form of phosphate taken up by plant roots (bolded text in blue box). Soluble P can react with cations to form precipitated secondary minerals (dark yellow box). The solubility of the P forms varies with pH (indicated by the arrows in the dark yellow box). Soluble P can also be immobilized to organic forms (red-orange box) or fixed to clay matrices (light yellow box). Figure generated by the authors with information culled from sources within the article [29,30,31,32].

Figure 2

Prototypical methods of soil phosphorus (P) acquisition in P deplete conditions in wild (left) and modern (right) crops. Relative soil P concentration is illustrated with the arrow on the left (topsoil with high concentration and deeper soil with low concentration). To recover P in low-P soils, modern crops tend to exploit topsoil horizons which have a greater abundance of available P compared to lower soil horizons (A) and show responsive root hair growth that increases in length with decreasing concentration of P (B). Wild crop relatives show strong responsive associations with soil P solubilizing bacteria (C) and with arbuscular mycorrhizal fungi (D). Figure generated by the authors using information culled from sources cited within this article [18,26,27,28,44,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78,79].

Figure 3

Mechanism of phosphorus (P) solubilization by the pqqC gene. The pqqC gene regulates soil P solubilization through biosynthesis of pyrroloquinoline quinone (PQQ) (blue background), subsequent catalyzation of gluconic acid (red background), and dissociation of metal-phosphate compounds (green background). An intermediate of PQQ enters the 7-helix structure of pqqC (steps 1 and 2). Once in the reaction matrix, pqqC undergoes conformational change at the α5b and α6 helices (step 3). PQQ is then released from the reaction matrix (step 4). PQQ functions as a cofactor to glucose dehydrogenase and catalyzes the reaction to form gluconic acid initially from glucose (steps 5 and 6). The acidification and reductant potential of gluconic acid allows it to react with metal-phosphate compounds (step 7). The metal-phosphate compounds dissociate, and bioavailable phosphate is released into the soil solution (step 8). Figure generated by the authors from information cited within this article [98,105].