ZmPHR1 and ZmPHR2 Mediate Metabolic and Microbial Regulation of Maize Adaptation to Phosphorus Heterogeneity

Spatial heterogeneity of soil phosphorus (P) severely constrains maize productivity, yet the regulatory mechanisms underlying plant adaptation to heterogeneous P supply remain poorly understood. This study reveals the distinct roles of the transcription factors ZmPHR1 and ZmPHR2 in mediating metabolic and rhizosphere microbial responses to heterogeneous P supply in maize (Zea mays L.). Using split-root systems combined with multi-tissue metabolomics and microbiome analysis, we show that mutation of ZmPHR2 severely impaired shoot development, photosynthetic efficiency and systemic P allocation. In contrast, ZmPHR1 mainly influenced root morphological plasticity. Loss of ZmPHR2 led to widespread repression of leaf metabolites, including organic acids and glutathione, and disrupted key pathways such as alanine, aspartate and glutamate metabolism. In root exudates, sphingolipid and histidine metabolism were critical for asymmetric root proliferation. Both mutations abolished differential root growth in P-rich patches and altered bacterial and fungal community composition and network structure. Our findings decipher a ZmPHR1/2-mediated adaptive framework integrating metabolic reprogramming and microbiome assembly, providing a mechanistic basis for breeding P-efficient maize suited to heterogeneous soils.