Abstract
Multiple nuclei sharing a common cytoplasm are found in diverse tissues, organisms, and diseases. Yet, multinucleation remains a poorly understood biological property. Cytoplasm sharing invariably involves plasma membrane breaches. In contrast, we discovered cytoplasm sharing without membrane breaching in highly resorptive Drosophila rectal papillae. During a six-hour developmental window, 100 individual papillar cells assemble a multinucleate cytoplasm, allowing passage of proteins of at least 62 kDa throughout papillar tissue. Papillar cytoplasm sharing does not employ canonical mechanisms such as incomplete cytokinesis or muscle fusion pore regulators. Instead, sharing requires gap junction proteins (normally associated with transport of molecules < 1 kDa), which are positioned by membrane remodeling GTPases. Our work reveals a new role for apical membrane remodeling in converting a multicellular epithelium into a giant multinucleate cytoplasm.
Highlights
Sharing of cytoplasm in a multinucleate tissue or organism is an important and recurring adaptation across evolution
We discovered that the rectal papilla is a new example of a tissue with cytoplasm sharing
As our dBrainbow approach only identifies cytoplasm sharing events that do not involve failed division/cytokinesis, we examined whether sharing results from fusion pore formation, as in skeletal muscle
Summary
Sharing of cytoplasm in a multinucleate tissue or organism is an important and recurring adaptation across evolution. Despite exhibiting strong cytoplasm sharing defects, shi, Rab, and Rab RNAi papillae appear morphologically normal, with only minor cell number decreases (FigS2C) These results suggest that membrane recycling GTPases regulate a specific developmental event associated with cytoplasm sharing, and not papillar morphogenesis. Using either pan-hindgut or papillae-specific (FigS5C-D, Methods) knockdown of cytoplasm sharing regulators, we find both shiDN and ogreDN animals are extremely sensitive to the high-salt diet (mean survival
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