Distinct cellular and junctional dynamics independently regulate the rotation and elongation of the embryonic gut in Drosophila.

Complex organ structures are formed with high reproducibility. To achieve such intricate morphologies, the responsible epithelium undergoes multiple simultaneous shape changes, such as elongation and folding. However, these changes have typically been assessed separately. In this study, we revealed how distinct shape changes are controlled during internal organ morphogenesis. The Drosophila embryonic hindgut undergoes left-right asymmetric rotation and anteroposterior elongation in a tissue-autonomous manner driven by cell sliding and convergent extension, respectively, in the hindgut epithelia. However, the regulation of these processes remains unclear. Through genetic analysis and live imaging, we demonstrated that cell sliding and convergent extension are independently regulated by Myosin1D and E-cadherin, and Par-3, respectively, whereas both require MyosinII activity. Using a mathematical model, we demonstrated that independently regulated cellular dynamics can simultaneously cause shape changes in a single mechanical system using anisotropic edge contraction. Our findings indicate that distinct cellular dynamics sharing a common apparatus can be independently and simultaneously controlled to form complex organ shapes. This suggests that such a mechanism may be a general strategy during complex tissue morphogenesis. Author summary: Complex organ structures are formed with high reproducibility. To achieve such intricate morphologies, the tissue undergoes multiple shape changes, such as elongation and folding, which are driven by distinct cellular behaviors. However, these changes have been assessed separately and the regulatory mechanisms are not fully understood. In this study, we explored the regulation of multiple tissue deformations using the Drosophila embryonic hindgut as a model system. The hindgut simultaneously undergoes left-right asymmetric rotation and anterior-posterior elongation, driven by cell sliding and intercalation, respectively. Through genetic analysis, live imaging, and mathematical modeling, we reveal that distinct genetic pathways regulate these processes, despite both utilizing common cell boundary contraction. Our findings indicate that distinct cellular dynamics sharing a common apparatus can be independently and simultaneously controlled to form complex organ shapes. These mechanisms might be widely applicable in the morphogenesis of complex organs. [ABSTRACT FROM AUTHOR]