Centrosome maintains the integrity of and repairs mature olfactory cilia in adult Drosophila

Mechanisms of cilium assembly are well studied; however, how mature metazoan cilia maintain their structures and functions in vivo remains unknown. It is also unclear whether the centrosome-derived basal body (BB) directly contributes to ciliary homeostasis. We combined biochemistry, genetics, high-resolution subcellular imaging, and electrophysiology to investigate long-lived ciliated olfactory sensory neurons (OSNs) and their olfactory behaviour in adult Drosophila. Several centrosome assembly proteins are absent, but another subset persists through dynamic protein exchange at the BBs of mature olfactory cilia. At this ciliary base, pericentriolar material (PCM) components, e.g., {gamma}-Tubulin23C, centrosomin, and pericentrin-like protein form an interconnected network required for ciliary maintenance. Adult- and OSN-specific depletions of these proteins, particularly in combination, disrupt accumulation of the heterotrimeric kinesin-2 at the ciliary base and, subsequently, in the shaft, causing loss of ciliary tubulin, EB1, and odorant receptor co-receptor. These dysregulations cause profound loss of ciliary shaft and impair olfactory function/behaviour. The centrosomal kinases PLK1/POLO and Aurora A also work with this PCM network and are required for mature ciliary homeostasis. Remarkably, these defects in ciliary structure, function, and adult olfactory behaviour are reversible, suggesting that this centrosome-derived BB is a dynamic homeostatic epicentre that regulates trafficking and ciliary structural and compositional integrity in vivo. These findings uncover an active, centrosome-dependent, cell-autonomous mechanism for maintaining and repairing mature metazoan cilia in fully grown organs in adulthood and also provide a possible explanation for how deregulation of conserved ciliary base components could lead to progressive, late-onset cilia-related disorders.