A dedicated partitioning machinery ensures faithful inheritance of the apicoplast in Toxoplasma gondii

Abstract Toxoplasma gondii tachyzoites divide by endodyogeny, an internal budding process that requires precise machinery for equal partitioning of single-copy organelles into daughter cells. The essential apicoplast is partitioned by temporal association with the centrosome, which is orchestrating various cell division processes. However, the identity of the molecular infrastructure facilitating anchoring of the apicoplast to the centrosome is still unknown. Here, we describe the apicoplast partitioning protein 1 (APP1), which first assembles in a specific basal complex (BC) section and then localizes in close proximity to the apicoplast. Conditional APP1 knockdown results in a specific apicoplast partitioning defect. Reciprocally, upon apicoplast loss through ATG8-depletion, APP1 remains associated with the cytoskeleton, consolidating a role in apicoplast anchoring to the cell division infrastructure. Using APP1 as bait in a proximity biotinylation screen, we identify APP3, which positions APP1 to the specific site on the BC, but has overall a more pleiotropic role in coordinating cell division. In summary, APPs are functional connectors between the apicoplast and the daughter cell scaffold (DCS) critical for apicoplast inheritance. Together our findings provide novel mechanistic insights into this unique aspect of apicomplexan organelle biology.