Forming mutualistic symbioses with arbuscular mycorrhizae (AMs) improves the acquisition of mineral nutrients for most terrestrial plants. However, the formation of AM symbiosis usually occurs under phosphate (Pi)-deficient conditions. Here, we identify SlSPX1 (SYG1 (suppressor of yeast GPA1) /Pho81(phosphate 81)/XPR1 (xenotropic and polytropic retrovirus receptor 1) as the major repressor of the AM symbiosis in tomato (Solanum lycopersicum) under phosphate-replete conditions. Loss of SlSPX1 function promotes direct Pi uptake and enhances AM colonization under phosphate-replete conditions. We determine that SlSPX1 integrates Pi signaling and AM symbiosis by directly interacting with a set of arbuscule-induced SlPHR proteins (SlPHR1, SlPHR4, SlPHR10, SlPHR11, and SlPHR12). The association with SlSPX1 represses the ability of SlPHR proteins to activate AM marker genes required for the arbuscular mycorrhizal symbiosis. SlPHR proteins exhibit functional redundancy, and no defective AM symbiosis was detected in the single mutant of SlPHR proteins. However, silencing SlPHR4 in the Slphr1 mutant background led to reduced AM colonization. Therefore, our results support the conclusion that SlSPX1-SlPHRs form a Pi-sensing module to coordinate the AM symbiosis under different Pi-availability conditions.

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