Plastid-localized amino acid metabolism coordinates rice ammonium tolerance and nitrogen use efficiency

Abstract Ammonium toxicity affecting plant metabolism and development is a worldwide problem impeding crop production. Remarkably, rice (Oryza sativa L) favors ammonium as its major nitrogen source in paddy fields. We set up a forward-genetic screen to decipher the molecular mechanisms conferring rice ammonium tolerance and identified the rohan mutant showing root hyper-sensitivity to ammonium due to a missense mutation in an arginine-succinate lyase-encoding gene. ROHAN localizes to plastids while its expression is induced by ammonium. ROHAN alleviates ammonium-inhibited root elongation by converting the excessive glutamine into arginine. Consequently, arginine leads to auxin accumulation in the root meristem thereby stimulating root elongation under high ammonium. Furthermore, we identified natural variation in the ROHAN allele between Japonica and Indica subspecies explaining their different root sensitivity towards ammonium. Finally, we show that ROHAN expression positively correlates with root ammonium tolerance and that nitrogen use efficiency and yield can be improved through a gain-of-function approach.