The <scp>PtoTCP19</scp> – <scp>PtoOBE2</scp> complex orchestrates phosphate deficiency tolerance and biomass production in <i>Populus</i>

Soil inorganic phosphate (Pi) availability critically limits forest primary productivity, necessitating effective adaptation to Pi variation. However, how perennial trees orchestrate Pi deficiency tolerance while maintaining growth under low-phosphate (LP) stress remains unexplored. Combining genome-wide association study (GWAS), RNA sequencing (RNA-seq), DNA affinity purification sequencing (DAP-seq), genetic transformation, and molecular experiments, we investigated how perennial species like Populus orchestrate phosphate deficiency tolerance and biomass production under LP stress. Here, we showed that TCP DOMAIN PROTEIN 19 (PtoTCP19) physically interacted with OBERON2 (PtoOBE2) to form a nuclear transcriptional complex. Genetic evidence supported the complex's functionality: overexpression of either PtoTCP19 or PtoOBE2 (OE-PtoTCP19/PtoOBE2) improved LP tolerance and biomass, while their respective loss-of-function materials (Ri-PtoTCP19 and KO-PtoOBE2) exhibited opposite phenotypes. Mechanistically, the PtoTCP19-PtoOBE2 complex executes a dual-pathway strategy: upregulating PHOSPHATE TRANSPORTER 1;4 (PtoPHT1;4) to boost Pi acquisition and activating the EXPANSIN B2 (PtoEXPB2) promoter to stimulate root growth, as validated by overexpressing-PtoEXPB2 (OE-PtoEXPB2) plants. Together, the PtoTCP19-PtoOBE2 complex is a novel hub that integrates Pi uptake and root development to orchestrate phosphate deficiency tolerance and biomass production in Populus, providing strategic insights for molecular breeding.