Breeding, genetics, and physiology of improving phosphorus use efficiency in food legumes

Phosphorus (P) is a crucial plant macronutrient, but the non-renewable nature of P sources for plant growth in soils globally limits crop productivity, causing great concern for future sustainable agriculture and global food security. Thus, improving plant phosphorus use efficiency (PUE) by increasing P-utilization and P-acquisition efficiencies is immediately needed in various crops, including legumes, for intensive cropping systems. This review explores how to harness genetic variability in PUE traits across grain legume gene pools using various conventional breeding and emerging breeding approaches. The role of phytohormones in root architecture development, importance of root exudates secretion, and microbe-assisted breeding represent important strategies for improving PUE, considering the non-renewable nature of P resources and its essential role in plant growth. The genetic makeup of PUE is intricate, orchestrated by quantitative traits and significantly affected by environmental factors. Biparental quantitative trait locus (QTL) mapping has been employed to decipher the genetic basis of PUE traits. Progress in legume genomics, particularly high-throughput single nucleotide polymorphism (SNP) genotyping, has enabled genome-wide identification of regions associated with PUE. Concurrently, advancements in multi-omics approaches (functional genomics, transcriptomics, metabolomics and proteomics) have facilitated the identification of key genes, transcription factors and pathways regulating PUE, P transport, recycling and low-P tolerance. This study also elucidated gene networks, signaling pathways, and molecular mechanisms governing P acquisition and utilization essential for improving PUE. We also evaluate the carbon and metabolic costs associated with P-acquisition traits and critically synthesize consistent findings, discrepancies and knowledge gaps across studies. Lastly, we summarize how to formulate innovative breeding strategies, including genomic selection, accelerated breeding, rhizosphere engineering and emerging clustered regularly interspaced short palindromic repeats/CRISPR-associated protein 9 (CRISPR/Cas9)-based genome editing technologies. This may aid in developing P-use-efficient cultivars and adapting grain legumes to low-P environments. Consequently, enhancing PUE by integrating various "omics" approaches could boost P-acquisition and P-utilization efficiencies in modern grain legume cultivars in intensive cropping systems, thereby mitigating P-fertilizer overuse and safeguarding the diminishing non-renewable global rock phosphate resources for ensuring a sustainable and economically viable agrarian future.