Abstract
How genetic programs generate cell-intrinsic forces to shape embryos is actively studied, but less so how tissue-scale physical forces impact morphogenesis. Here we address the role of the latter during axis extension, using Drosophila germband extension (GBE) as a model. We found previously that cells elongate in the anteroposterior (AP) axis in the extending germband, suggesting that an extrinsic tensile force contributed to body axis extension. Here we further characterized the AP cell elongation patterns during GBE, by tracking cells and quantifying their apical cell deformation over time. AP cell elongation forms a gradient culminating at the posterior of the embryo, consistent with an AP-oriented tensile force propagating from there. To identify the morphogenetic movements that could be the source of this extrinsic force, we mapped gastrulation movements temporally using light sheet microscopy to image whole Drosophila embryos. We found that both mesoderm and endoderm invaginations are synchronous with the onset of GBE. The AP cell elongation gradient remains when mesoderm invagination is blocked but is abolished in the absence of endoderm invagination. This suggested that endoderm invagination is the source of the tensile force. We next looked for evidence of this force in a simplified system without polarized cell intercalation, in acellular embryos. Using Particle Image Velocimetry, we identify posteriorwards Myosin II flows towards the presumptive posterior endoderm, which still undergoes apical constriction in acellular embryos as in wildtype. We probed this posterior region using laser ablation and showed that tension is increased in the AP orientation, compared to dorsoventral orientation or to either orientations more anteriorly in the embryo. We propose that apical constriction leading to endoderm invagination is the source of the extrinsic force contributing to germband extension. This highlights the importance of physical interactions between tissues during morphogenesis.
Highlights
During development, many tissues extend in one orientation while narrowing in the orthogonal one
We address this question for the anteroposterior elongation of the body axis of Drosophila embryos
We had previously shown that during elongation, the germband cells stretch along the anteroposterior axis, in addition to undergoing active rearrangements; this suggested that extrinsic tensile forces might be at play
Summary
Many tissues extend in one orientation while narrowing in the orthogonal one These so-called convergence and extension movements elongate the anteroposterior axis in bilateral animals during gastrulation, where they have been most studied [1,2,3,4]. The cell biology of this process has since been extensively characterized, and planar polarization of several other components including Bazooka (the homologue of Par-3) and Ecadherin have been found to be required for active cell rearrangements [11,12,13,14,15,16,17,18,19,20] These polarities are controlled by the anteroposterior (AP) segmentation cascade in Drosophila, the most downstream genes being the pair-rule genes, encoding transcription factors such as Evenskipped and Runt [9,10,21]. Actomyosin-driven shortening of cell contacts has been shown to be essential for convergence and extension movements in vertebrates [7, 23,24,25]
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