A tomato purple acid phosphatase SlPAP26b rewires tissue-specific Pi remobilization through differential perturbation of SlPHL1-SlSPX2 levels

Acid phosphatases, both intracellular and secretory, play a crucial role in maintaining phosphate (Pi) homeostasis in plants. Using an integrated omics approach in Pi-deficient tomato seedlings, we identified SlPAP26b as a prominent candidate potentially involved in Pi remobilization from senescing to developing tissues, supported by its strong transcript accumulation in leaves and roots and pronounced induction during leaf senescence. Both SlPHR1 and SlPHL1, the two main tomato MYB-CC domain transcription factors of the Pi starvation response, directly activated the transcription of SlPAP26b by binding to the P1BS element in its promoter. Functional characterization revealed that silencing of SlPAP26b leads to stunted shoot growth and reduced intracellular acid phosphatase activity. Tracer studies using radioactive P (γ-32P-ATP) confirmed impaired Pi translocation from older to younger leaves, resulting in lower Pi levels in young tissues even under Pi-sufficient conditions in the silenced seedlings. The protein abundance of SlSPX2, a negative regulator of SlPHL1, was markedly reduced in SlPAP26b-silenced seedlings, accompanied by a corresponding increase in SlPHL1 protein abundance. Notably, SlPAP26b silencing reduced SlSPX2 but increased SlPHL1 protein accumulation, accompanied by elevated expression of several Pi starvation-induced (PSI) genes in younger leaves and roots, indicating the misregulated activation of the Pi starvation response (PSR) even under Pi sufficiency. Collectively, these findings identify a previously uncharacterized function of SlPAP26b in mediating tissue-specific Pi remobilization by selectively modulating the SlSPX2-SlPHL1 regulatory module, thereby advancing our understanding of the molecular mechanisms underlying Pi homeostasis in plants.