Plants have a crucial role in providing essential amino acids for human nutrition. Nine of the 20 proteinogenic amino acids are exclusively synthesized de novo in plastids, yet transporters mediating their exchange across the plastid inner envelope remain unknown. Here we identify RETICULATA1 (RE1) as a plastid-localized transporter for basic amino acids-including Arg, Citr, Orn and Lys-in Arabidopsis thaliana. Loss-of-function mutants display a reticulate leaf phenotype, contain lower amounts of basic amino acids and are impaired in amino acid homeostasis. RE1 belongs to a novel class of membrane transport proteins that contain a domain of unknown function 3411 and are found exclusively in plastid-containing organisms. Our results indicate functional overlap with its closest homologue RER1, as the double mutant is lethal. Isotope labelling reveals that loss of RE1 reduces basic amino acid biosynthesis and affects the equilibration of plastidic and cytosolic amino acid pools. These findings uncover a critical role for plastidial amino acid transporters in coordinating primary metabolism, development and nutrient allocation in plants.