Biomechanical control of meiotic chromosomal bouquet and germ cell morphogenesis by the zygotene cilium

The hallmark of meiosis is chromosomal pairing and synapsis via synaptonemal complexes, but chromosomal pairing also depends on cytoplasmic counterparts that tether and rotate telomeres on the nuclear envelope. Telomeres slide on perinuclear microtubules, shuffling chromosomes and mechanically driving their homology searches. Pull of telomeres towards the centrosome drives formation of the “zygotene chromosomal bouquet”. These telomere dynamics are essential for pairing and fertility, and the bouquet, discovered in 1900, is universally conserved. Nevertheless, how cytoplasmic counterparts of bouquet formation are mechanically regulated has remained enigmatic. Here, we report the “zygotene cilium” - a previously unrecognized cilium, in oocytes. We show in zebrafish that this cilium specifically connects to the bouquet centrosome, constituting a cable system of the cytoplasmic bouquet machinery. Furthermore, zygotene cilia extend throughout the germline cyst, a conserved germ cell organization. Using multiple ciliary mutants and laser-induced excision, we demonstrate that the zygotene cilium is essential for chromosomal bouquet and synaptonemal complex formation, germ cell morphogenesis, ovarian development and fertility. Mechanistically, we provide evidence that the cilium functions at least partly via anchoring the bouquet centrosome in order to counterbalance telomere rotation and pulling. We also show that the zygotene cilium is conserved in both male and female meiosis in zebrafish, as well as in mammals. Our work uncovers the novel concept of a cilium as a critical player in meiosis and sheds new light on reproduction phenotypes in ciliopathies. We propose a cellular paradigm that cilia can control chromosomal dynamics.