Morphogenesis of a complex glial niche requires an interplay between cellular growth and fusion

Neural stem cells (NSCs) are found in a tailored, intricate cellular microenvironment, the niche, which supports and regulates their activity. Whilst niche architecture is indissociable from its function, the morphogenetic aspects of niche development have been poorly explored. Here, we use the formation of the cortex glia (CG) network in Drosophila as a paradigm of acquisition of architectural complexity of a NSC niche. CG are essential for normal neurogenesis and build a reticular network spanning the entire central nervous system while encasing each NSC linage. We first show that individual CG cells grow tremendously to enwrap several NSC linages, ultimately covering and tiling the entire tissue. Several proliferative mechanisms, including endoreplication and mitosis, in part acytokinetic, support such growth and result in the formation of multinucleated, syncytial CG cells, that we call units. We then reveal that CG units are able to fuse to each other, resulting in the exchange of several subcellular compartments, such as membrane, cytoplasm and organelles. This process relies on well-known molecular players of cell fusion, involving cell surface communication molecules and actin regulators, while being atypical by its extent, dynamics and partial nature. Ultimately, the coordination in time and space of growth, proliferation and fusion mechanisms is required for the remarkable, multi-level architecture of the Drosophila NSC niche.