Diverse nitrogen signals activate convergent ROP2-TOR signaling in Arabidopsis

The evolutionarily conserved target-of-rapamycin (TOR) kinase coordinates cellular and organismal growth in all eukaryotes. Amino acids (AAs) are key upstream signals for mammalian TOR activation, but how nitrogen-related nutrients regulate TOR signaling in plants is poorly understood. Here, we discovered that, independent of nitrogen assimilation, nitrate and ammonium function as primary nitrogen signals to activate TOR in the Arabidopsis leaf primordium. We further identified that a total of 15 proteinogenic AAs are also able to activate TOR, and the first AAs generated from plant specific nitrogen assimilation (glutamine), sulfur assimilation (cysteine), and glycolate cycle (glycine), exhibit the highest potency. Interestingly, nitrate, ammonium, and glutamine all activate the small GTPase Rho-related protein from plants 2 (ROP2), and constitutively active ROP2 restores TOR activation under nitrogen-starvation conditions. Our findings suggest that specific evolutionary adaptations of the nitrogen-TOR signaling pathway occurred in plant lineages, and ROP2 can integrate diverse nitrogen and hormone signals for plant TOR activation.