Breeding and genomics approaches for improving phosphorus-use efficiency in grain legumes

Phosphorus (P) is an essential plant macronutrient, but P sources for plant growth are non-renewable, causing great concern for future sustainable agriculture and global food security. Thus, enhancing plant P-use efficiency (PUE) by improving P-acquisition and P-utilization efficiencies is urgently needed in various crops, including grain legumes, for intensive cropping systems. This review discusses how to harness the genetic variability in PUE traits across grain legume gene pools to improve PUE using various conventional breeding approaches and emerging breeding tools. The genetic architecture of PUE traits is complex, being quantitatively inherited and highly influenced by the environment. Thus, we discuss how the biparental QTL mapping approach has been used to dissect the genetic architecture of PUE traits. Unprecedented advances in legume genomics resources, especially high-throughput single nucleotide polymorphisms, have facilitated uncovering genomic regions related to PUE across the whole genome using a genome-wide association mapping approach. Likewise, the availability of complete genome sequence information, pangenome sequences, and the whole-genome rese-quencing approach have provided novel insights into structural variation, including presence/absence and copy number variations, underpinning PUE. Simultaneously, progress in functional genomics, including tran-scriptomics and computational biology, has facilitated the discovery of various underlying transcription factors and the corresponding downstream P signal perception genes and candidate gene(s) controlling PUE and conferring low-P tolerance in various legumes with putative function. We also discuss updated metabolomics and proteomics approaches that have improved our understanding of various gene networks, P-starvation signaling pathways, and P acquisition and utilization of molecular mechanisms important for PUE. Finally, we summarize how novel breeding schemes, including genomic selection, speed breeding, and emerging CRISPR/Cas9-based genome editing tools, will assist in designing P-use-efficient cultivars and adapting grain legumes to low-P en-vironments. Thus, enhancing PUE by integrating various 'omics' approaches could improve P-acquisition and P -utilization efficiencies in various modern grain legume cultivars grown in intensive cropping systems to restrict P-fertilizer overuse and preserve the declining non-renewable global rock phosphate reservoir for securing an economical and sustainable future agriculture.

Automated summary

Phosphorus (P) is a crucial nutrient for plant growth, but its sources are non-renewable, raising concerns for sustainable agriculture and food security. Improving plant P-use efficiency (PUE) is necessary for intensive cropping systems, and this review explores various breeding approaches and tools to enhance PUE in grain legumes. The genetic architecture of PUE traits is complex, influenced by both genetics and the environment. Advances in genomics and functional genomics have provided insights into the underlying genetic mechanisms and pathways related to PUE, while novel breeding schemes and tools offer opportunities for designing P-use-efficient cultivars in low-P environments.