Rethinking internal phosphorus utilization efficiency: a new approach is needed to improve PUE in grain crops

Grain crops are a key driver of the current global phosphorus (P) cycle through their continued demand for P fertilizer, and the subsequent removal of P from fields in the harvested grain. Breeding crops that can yield well with fewer P inputs (i.e., P-efficient crops) may reduce the impact of grain crops of the P cycle, but to date breeding P-efficient cultivars has focused on enhancing P acquisition efficiency (PAE). While the literature abounds in reported genotypic differences in internal P utilization efficiency (PUE) across a range of crops, there has been little progress in breeding crop cultivars with high PUE. This review critically analyzes why drawing conclusions from the body of research on PUE over the past few decades remains difficult and how progress in breeding crop cultivars high in PUE has been impeded. Four aspects of research on PUE are highlighted as being critical in limiting our understanding and exploitation of PUE in grain crops: (i) poor definition of PUE and inconsistent use of terminology, (ii) inappropriate methods used in genotypic screening for PUE that fail to account for the confounding effects of PAE on PUE, (iii) inadequate discussion on the level of P stress suffered by plants and its influence on potential mechanisms conferring high PUE and their utility in cropping systems, and (iv) a focus on P-stress response mechanisms rather than mechanisms conferring genotypic P-tolerance when investigating PUE. These factors are discussed in detail and new approaches and future areas of research on PUE are proposed.