A promoter indel in GmSTOP1a drives soybean adaptation to low-phosphorus acidic soils in low-latitude regions.

Low phosphorus availability is a major barrier to soybean cultivation in tropical and subtropical regions, where phosphate is strongly fixed by highly weathered acidic soils. However, little is known about the genetic basis of soybean adaptation to such low-phosphorus environments. Here, we identify the major quantitative trait locus Superior Phosphate Acquisition 10 (SPA10), which confers enhanced phosphate-acquisition efficiency in low-latitude soils. SPA10 encodes a soybean homolog of SENSITIVE TO PROTON RHIZOTOXICITY 1 (GmSTOP1a), a transcription factor central to low-phosphorus and proton-toxicity responses. A naturally occurring 24-bp insertion in the GmSTOP1a promoter, the haplotype prevalent in high-latitude germplasms, has disrupted a GmAGL12 binding site, attenuating the induction of GmSTOP1a expression under low-phosphorus conditions. By contrast, the promoter haplotype that lacks the 24-bp insertion, which predominates in low-latitude soybean, enables strong GmAGL12-dependent activation of GmSTOP1a and downstream genes involved in organic acid secretion, including several multidrug and toxic compound extrusion transporters. This difference in GmSTOP1a regulation determines the capacity of soybean roots to mobilize fixed phosphorus in acidic soils. Functional validation through CRISPR knockout, overexpression lines, promoter swapping, electrophoretic mobility shift assays, and DNA affinity purification sequencing confirmed that GmSTOP1a is a central regulator of low-phosphorus-responsive transcriptional networks and rhizosphere chemical modification. Field trials showed that overexpression of GmSTOP1a significantly increased seed yield in the absence of P fertilizer, demonstrating its agronomic value in P-deficient soils. Population genetic analysis revealed that the superior haplotype of GmSTOP1a underwent targeted artificial selection during the historical expansion of soybean into low-latitude cultivation zones. Our findings reveal a promoter-based regulatory innovation that has enabled soybean to adapt to acidic, low-phosphorus soils, providing a mechanistic foundation for the breeding of P-efficient cultivars for low-latitude cultivation.