SMNK-1 and VHA-18 are essential for FB-MO complex assembly and transport during spermatogenesis in C. elegans
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The spatiotemporal control of asymmetric positioning of cellular cargoes such as macromolecules and organelles during spermatogenesis is essential to produce functional sperm in most animal species. Yet, the regulatory mechanisms that govern cargo sorting and transport remain largely unknown. Here we show that the casein-like kinase SMNK-1 localized on the surface of membranous organelle (MO) is required to recruit IDR-containing SPE-18 and facilitate the assembly of Major Sperm Protein (MSP) condensate, named Fibrous Body (FB) in spermatocyte during spermatogenesis in C. elegans. Meanwhile, the MO-localized VHA-18, the H subunit of the v-ATPase, is required for pumping the cytoplasmic protons into MOs, generating an alkaline cytoplasmic microenvironment adjacent to MOs, favorable for packaging MSP filaments into fibrous body (FB) and thus guaranteeing the correct cargo sorting during spermatogenesis. Thus, the interplay between membraneless condensate FBs mediated by SMNK-1 and membrane-bound organelle MOs regulated by VHA-18 provides a novel yet uncovered mechanism for cargo sorting and vectorial transport during spermatogenesis in C. elegans.