Motile cilia spin the Reissner fiber, a tensioned and anchored extracellular thread essential for body morphogenesis

Abstract

The Reissner fiber (RF) is an extracellular thread composed of the glycoprotein SCO-spondin (Sspo) that forms within cerebrospinal fluid (CSF) in the brain ventricles and central canal (CC) of vertebrates. Its assembly depends on motile cilia, yet how cilia and CSF flow transform secreted Sspo into a fiber that spans the length of the body axis has remained unknown. Using live imaging in zebrafish, we show that globular Sspo is remodeled into thin fibrils that anchor to the floor plate (FP), elongate, and spin together into a tensioned, posteriorly translocating RF. Fiber assembly draws on a shared CSF pool of Sspo but requires local ciliary activity for globule-to-fibril remodeling. Once assembled, the RF is anchored by dynamic fibrils that stabilize the fiber and preserve its tension. Perturbations that locally disrupt ciliary motility and RF integrity along the CC result in region-specific defects in axial morphogenesis. These findings identify the RF as a flow-responsive extracellular system that converts ciliary beating into mechanical structure, linking fluid dynamics to the large-scale shaping of the vertebrate body. HighlightsO_LIMotile cilia remodel Sspo globules into FP-anchored fibrils that bundle into RF. C_LIO_LIRF assembly draws on a shared CSF Sspo pool but requires local cilia activity. C_LIO_LILaser ablation reveals patterned RF tension constrained by dynamic FP anchors. C_LIO_LIRegional cilia defects cause local RF loss and corresponding body shape defects. C_LI