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

Authors :
Inaki M
Higashi T
Okuda S
Matsuno K
Source :
PLoS genetics [PLoS Genet] 2024 Oct 07; Vol. 20 (10), pp. e1011422. Date of Electronic Publication: 2024 Oct 07 (Print Publication: 2024).
Publication Year :
2024

Abstract

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.<br />Competing Interests: The authors have declared that no competing interests exist.<br /> (Copyright: © 2024 Inaki et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.)

Details

Language :
English
ISSN :
1553-7404
Volume :
20
Issue :
10
Database :
MEDLINE
Journal :
PLoS genetics
Publication Type :
Academic Journal
Accession number :
39374304
Full Text :
https://doi.org/10.1371/journal.pgen.1011422