SgPHR1-SgPAE1 module modulates root growth and increases low phosphorus tolerance in Stylosanthes guianensis

Phosphorus (P) deficiency severely limits agricultural productivity in tropical acid soils. Stylosanthes guianensis (stylo), a vital forage legume in the tropics, exhibits high tolerance to low P stress. While numerous phosphate (Pi) starvation response genes have been documented in stylo, its underlying regulatory mechanisms remain unclear. In this study, a coordinated root morphological plasticity was observed in the response of P-tolerant stylo genotypes to P deficiency, achieved through enhanced root growth. SgPHR1 (Phosphate Starvation Response 1) was characterized as a Pi-starvation-induced MYB transcription factor localized to the nucleus. Transgenic studies revealed that SgPHR1 overexpression increased plant dry weight and Pi uptake, especially under low-P conditions, whereas SgPHR1 knockdown suppressed these traits in stylo, likely by modulating root growth. RNA-seq analysis identified many downstream targets of SgPHR1, including SgPAE1, which encodes a pectin acetylesterase. Biochemical analyses confirmed SgPHR1 activated the transcription of SgPAE1 by directly binding to the P1BS cis-element in its promoter region. Furthermore, SgPAE1 overexpression enhanced low-P tolerance by promoting root growth and P accumulation, while its suppression impaired these adaptive responses. Further analysis demonstrated that SgPAE1 mediates pectin deacetylation, likely contributing to root cell wall modification. Notably, genes encoding cell wall-modifying enzymes were significantly enriched in roots of SgPAE1-overexpressing plants under P deficiency. Collectively, this study establishes the SgPHR1-SgPAE1 transcriptional module as a key regulatory framework for low-P adaptation in stylo, which is probably through linking Pi signaling to root cell wall remodeling, thereby optimizing root growth and Pi acquisition.