A mycorrhiza-inducible phosphate transporter SlPT3 regulates phosphate uptake, iron homeostasis, and arbuscule development in tomato under combined nutrient stress conditions.

Interactions between phosphate (Pi) and zinc (Zn) or iron (Fe) nutrition in plants have been widely studied; however, the underlying mechanisms of their cross-talks in arbuscular mycorrhizal (AM) plants remain obscure. Here, we examine the physiological and molecular responses of tomato (Solanum lycopersicum L.) to the combination of Pi, Zn and/or Fe nutrient stresses during symbiosis with Rhizophagus irregularis, revealing the existence of a tripartite Pi-Zn-Fe cross-talk in AM symbiosis. Interestingly, the mycorrhiza-activated SlPT3, a member of the PHOSPHATE TRANSPORTER 1 (PHT1) gene family in tomato, is remarkably induced upon the simultaneous Pi and Zn deficiencies. Reverse genetics analysis revealed that SlPT3 not only contributes to Pi transport but is also essential for arbuscule development during Zn deficiency. Moreover, knockdown of SlPT3 leads to reduced Fe accumulation and arbuscule degeneration in mycorrhizal roots by integration of Pi and Zn deficiencies. In silico analysis indicated that the SlPT3 and its homologs contain the IRT (Iron-regulated transporter) domain across dicot and monocot species. Further heterogeneous expression of SlPT3 in yeasts can restore the Δpho84 defects in high-affinity Pi uptake and regulate iron (Fe+2) homeostasis in the fet3fet4 mutant. Collectively, SlPT3 serves as a context-dependent transporter that reshapes nutrient transport priorities in response to combined stresses, revealing a sophisticated mechanism for maintaining symbiosis under fluctuating soil nutrient conditions. These findings provide new avenues for exploring how arbuscular mycorrhizas integrate multiple nutrient stress signals into intricate plant development.