The RALF1-FERONIA complex interacts with and activates TOR signaling in response to low nutrients.

Target of rapamycin (TOR) kinase is an evolutionarily conserved major regulator of nutrient metabolism and organismal growth in eukaryotes. In plants, nutrients are remobilized and reallocated between shoots and roots under low-nutrient conditions, and nitrogen and nitrogen-related nutrients (e.g., amino acids) are key upstream signals leading to TOR activation in shoots under low-nutrient conditions. However, how these forms of nitrogen can be sensed to activate TOR in plants is still poorly understood. Here we report that the Arabidopsis receptor kinase FERONIA (FER) interacts with the TOR pathway to regulate nutrient (nitrogen and amino acid) signaling under low-nutrient conditions and exerts similar metabolic effects in response to nitrogen deficiency. We found that FER and its partner, RPM1-induced protein kinase (RIPK), interact with the TOR/RAPTOR complex to positively modulate TOR signaling activity. During this process, the receptor complex FER/RIPK phosphorylates the TOR complex component RAPTOR1B. The RALF1 peptide, a ligand of the FER/RIPK receptor complex, increases TOR activation in the young leaf by enhancing FER-TOR interactions, leading to promotion of true leaf growth in Arabidopsis under low-nutrient conditions. Furthermore, we showed that specific amino acids (e.g., Gln, Asp, and Gly) promote true leaf growth under nitrogen-deficient conditions via the FER-TOR axis. Collectively, our study reveals a mechanism by which the RALF1-FER pathway activates TOR in the plant adaptive response to low nutrients and suggests that plants prioritize nutritional stress response over RALF1-mediated inhibition of cell growth under low-nutrient conditions.