The kinase SPE-55 promotes localized assembly of the major sperm protein in Caenorhabditis elegans spermatocytes.

The crawling motility of nematode sperm is driven by the unconventional cytoskeletal protein, Major Sperm Protein (MSP). In developing spermatocytes, MSP assembles on the cytosolic side of Golgi-derived membranous organelles (MOs) in structures called Fibrous Bodies (FBs). These MSP-laden FB-MO complexes facilitate the subsequent segregation of MSP to budding spermatids and away from central residual bodies. Here we identify SPE-55 as a key FB assembly factor. In spe-55 spermatocytes, MSP remains diffusely cytosolic, and minimal MSP segregates to spermatids. The resulting spe-55 spermatozoa are motility-defective. SPE-55 localizes directly to MOs where it recruits the intrinsically disordered protein SPE-18 to initiate FB assembly, yet unlike SPE-6 or SPE-18, SPE-55 is required neither to complete meiosis nor to produce spermatids. Our study reveals an essential interplay between localized kinases and intrinsically disordered proteins in assembling large cytoskeletal complexes.