Induction of de novo centriole biogenesis in planarian stem cells

Abstract

The centriole is a fundamental organelle templating cilia formation and ensuring genomic stability. While most cells assemble centrioles using a pre-existing mother as a template, the de novo pathway allows for assembly in their absence. However, the physiological role and regulation of de novo biogenesis in vivo remain poorly understood. The planarian Schmidtea mediterranea, with its abundant somatic stem cells (neoblasts) and dependence on a massive ciliated epithelium for locomotion, presents a unique model to address this gap. We demonstrate that quiescent neoblasts are acentriolar, lacking the templates for canonical duplication. Upon tissue injury, neoblasts are activated and initiate a programmed de novo centriole biogenesis pathway. Super-resolution microscopy and transmission electron microscopy reveal the formation of cytoplasmic procentriolar foci and mature centrioles, independent of any parental structure. Crucially, genetic ablation of Sas-6 or pharmacological inhibition of PLK4—interventions that effectively block the canonical pathway—fail to prevent the formation of new centrioles and functional basal bodies in the regenerating ciliated epithelium. This work provides the first in vivo evidence in a whole organism for an induced de novo centriole biogenesis pathway in adult somatic stem cells. We propose this pathway is a key evolutionary adaptation, enabling rapid, large-scale ciliogenesis essential for planarian regeneration, and represents a distinct, genetically regulated program separable from canonical duplication.