Sperm Head-Tail Linkage Requires Restriction of Pericentriolar Material to the Proximal Centriole End

The centriole, or basal body, is the center of attachment between the sperm head and tail. While the distal end of the centriole templates the cilia, the proximal end associates with the nucleus. Using Drosophila, we identify a centriole-centric mechanism that ensures proper proximal end docking to the nucleus. This mechanism relies on the restriction of pericentrin-like protein (PLP) and the pericentriolar material (PCM) to the proximal end of the centriole. PLP is restricted proximally by limiting its mRNA and protein to the earliest stages of centriole elongation. Ectopic positioning of PLP to more distal portions of the centriole is sufficient to redistribute PCM and microtubules along the entire centriole length. This results in erroneous, lateral centriole docking to the nucleus, leading to spermatid decapitation as a result of a failure to form a stable head-tail linkage. •The proximal end of the centriole docks to the spermatid nucleus•Proper centriole docking to the nucleus requires proximal restriction of PCM•Pericentrin-like protein (PLP) restricts PCM to the proximal centriole end•PLP is proximally restricted by eliminating its availability during centriole growth Functional sperm require a stable linkage between the sperm head and tail, a linkage mediated by the centriole. Galletta et al. reveal how restriction of pericentriolar material to the proximal end of the centriole—achieved via restriction of the Pericentrin-like protein—ensures proximal end docking to the nucleus.