Mechanoregulation of basal body integrity during Plasmodium exflagellation

Constant mechanical stress challenges the structural integrity of cell systems. During malaria Parasite transmission from mammal to mosquito, Plasmodium male gametogenesis features a unique axoneme release pattern characterized by basal body first, axoneme following. Substantial mechanical stress from axonemal beating threatens basal body integrity during axoneme exflagellation. However, how Plasmodium adapts to such mechanical stress and maintains the structural integrity of the basal body remains elusive. In this study, we identified a conserved Plasmodium protein, Calcifer, essential for male gamete formation and mosquito transmission of the Parasite. Calcifer translocates to the basal body after axoneme assembly and persists during exflagellation, which is distinct from canonical basal body proteins. Parasites lacking Calcifer form intact axonemes but show rapid axoneme disintegration during exflagellation, a defect that can be rescued by inhibiting axoneme beating. In vivo and in vitro assays revealed that Calcifer directly stabilizes basal body integrity under mechanical forces generated by axoneme beating. Calcifer forms a wrapping structure around the basal body at the axoneme minus end, providing resistance to mechanical stress. Our findings elucidate a mechanical stabilization mechanism of the basal body that resists axoneme-beating-induced mechanical stress and reveal Calcifer as a key factor safeguarding basal body integrity during Plasmodium axoneme exflagellation.