Localized mRNA translation mediates maturation of cytoplasmic cilia in Drosophila spermatogenesis

Abstract

Cytoplasmic cilia, a specialized type of cilia in which the axoneme resides within the cytoplasm rather than within the ciliary compartment, are proposed to allow the efficient assembly of very long cilia. Despite being found diversely in male gametes (e.g. Plasmodium microgametocytes and human and Drosophila sperm), very little is known about cytoplasmic cilia assembly. Here we show that a novel RNP granule containing the mRNAs for axonemal dynein motor proteins becomes highly polarized to the distal end of the cilia during cytoplasmic ciliogenesis in Drosophila sperm. This allows for the localized translation of these axonemal dyneins and their incorporation into the axoneme directly from the cytoplasm. We found that this RNP granule contains the proteins Reptin and Pontin, loss of which perturbs granule formation and prevents incorporation of the axonemal dyneins, leading to sterility. We propose that cytoplasmic cilia require the local translation of key protein constituents such that these proteins are incorporated efficiently into the axoneme. Author SummaryCytoplasmic cilia, which are found in human and Drosophila sperm, are unique in that the axoneme is exposed to the cytoplasm. The authors show that a novel RNP granule containing axonemal dynein mRNAs facilitates localized translation of these axonemal proteins, facilitating cytoplasmic cilia formation.