Natural variation in the GmVPE1 promoter contributes to phosphorus re-translocation to seeds and improves soybean yield

Phosphorus (P) is an essential yet frequently deficient plant nutrient. Optimizing P distribution and recycling between tissues is vital for improving P utilization efficiency (PUE). Yet, the mechanisms underlying the transport and re-translocation of P within plants remain unclear. Here, wide-ranging natural diversity in seed P allocation and positive correlations among yield traits were found using 190 soybean accessions in field trials. Among them, the P-efficient genotype BX10 outperformed BD2 in assessments of PUE that were largely explained through differences in P redistribution from pods to seeds under low P stress. Pods of BX10 were therefore subjected to transcriptome analysis, and GmVPE1 was identified as a vacuolar Pi transporter to investigate further. Importantly, significant DNA polymorphism in GmVPE1 promoter regions was remarkably associated with seed weight among soybean accessions grown on P-deficient soils. Further analyses suggested that mRNA abundance of GmVPE1 in haplotype 2 (Hap) is significantly higher than that GmVPE1^Hap1. GmVPE1 was highly upregulated by P deficiency and preferentially expressed in pods, seeds, and seed coats, which was consistent with GUS staining using transgenic soybean plants carrying pGmVPE1^Hap2::GUS. Near-isogenic lines carrying the GmVPE1^Hap2 allele, along with stable transgenic soybeans overexpressing GmVPE1 in a GmVPE1^Hap1 background, had increases in PUE, more seed setting, and greater yields in both greenhouse and field trials than control plants. In summary, natural variation among GmVPE1 alleles determines genetic expression and subsequent P re-translocation phenotypes, which impacts PUE and yield, and thereby makes this an important genetic resource for soybean molecular breeding.