Dual role of Xenopus Odf2 in multiciliated cell patterning and differentiation

Abstract

In developing tissues, the number, position, and differentiation of cells must be coordinately controlled to ensure the emergence of physiological function. The epidermis of the Xenopus embryo contains thousands of uniformly distributed multiciliated cells (MCCs), which grow hundreds of coordinately polarized cilia that beat vigorously to generate superficial water flow. Using this model, we uncovered a dual role for the conserved centriolar component Odf2, in MCC apical organization at the cell level, and in MCC spatial distribution at the tissue level. Like in other species, Xenopus Odf2 localized to the basal foot of basal bodies. Consistently, Odf2 morpholino-mediated knockdown impaired basal foot morphogenesis. Consequently, the rate of microtubule nucleation by Odf2-deficient basal bodies was reduced, leading to cilia disorientation, reduced beating, and ultimately altered flow production across the embryo. Furthermore, we show that Odf2 is required to maintain MCC motility and homotypic repulsion prior to their emergence into the surface layer. Our data suggest that Odf2 promotes MCC spacing via its role in the modulation of cytoplasmic microtubule dynamics. Mathematical simulations confirmed that reduced migration speed alters the spacing order of MCCs. This study provides a striking example of coupling between organizational scales by a unique effector.