Control of meiotic chromosomal bouquet and germ cell morphogenesis by the Zygotene cilium

Meiosis is a cellular program essential for haploid gamete production. A hallmark of meiosis is chromosomal pairing via meiotic Cohesins and synaptonemal complex proteins. However, chromosomal pairing also depends on cytoplasmic mechanical forces. In meiosis, chromosomal pairing is facilitated by unique telomere dynamics. Telomeres bind Sun/KASH proteins on the nuclear envelope (NE), associating them with perinuclear microtubules that emanate from the centrosome. This facilitates telomere rotations on the NE that shuffle chromosomes, providing their homology searches. Ultimately, telomeres are pulled towards the centrosome and cluster on the NE, looping their chromosomes to the other side, forming a configuration called the zygotene chromosomal bouquet. The bouquet is universally conserved, was discovered in 1900, and is essential for chromosomal pairing and fertility. However, how cytoplasmic counterparts of bouquet formation are mechanically regulated is unknown. Here, we identified a novel cilium in zebrafish meiosis, that specifically connects to the bouquet centrosome and constitutes a cable system as the cytoplasmic bouquet machinery. Through analyzing multiple ciliary mutants, we demonstrate that the zygotene cilium is essential for chromosomal bouquet formation, germ cell morphogenesis, ovarian development and fertility. We further show that the zygotene cilium is conserved in male meiosis as well as in mammalian oogenesis. Our work uncovers a novel concept of a cilium as a newly identified player in meiosis. We propose a new cellular paradigm that cilia can control chromosomal dynamics.