A PHR transcription factor-directed gene network reveals key regulators of phosphate metabolism and starvation responses in tomato

Abstract Phosphorus (P) is an essential nutrient for plants, and its scarcity, especially in the form of soluble phosphate (Pi), induces phosphate starvation responses (PSRs). Our research delves into the molecular mechanisms that regulate tomato (Solanum lycopersicum) plant adaptation to Pi deficiency, highlighting the role of 2 PHOSPHATE STARVATION RESPONSE (PHR) transcription factors, SlPHR3 and SlPHR4, as central regulators of Pi metabolism and related developmental/physiological processes, particularly PSRs. Notably, our investigation into the SlPHR3- and SlPHR4-regulated transcriptional network led to the discovery of 3 previously unidentified regulators of Pi metabolism and PSRs: SlGRAS47, SlBHLH48, and SlMYB28. We substantiated the important roles of SlMYB28 in mediating SlPHR3 and SlPHR4 function by demonstrating that SlMYB28 suppression reduces Pi and P accumulation, ameliorates PSR-related phenotypes, and decreases the expression of genes involved in Pi metabolism and PSRs in SlPHR3 and SlPHR4 overexpression plants. Our findings shed light on the adaptive strategies of plants to Pi starvation and open avenues for the identification of important genes involved in Pi metabolism and PSRs, which can be leveraged to improve Pi use efficiency in agricultural crops.