Abstract
The article provides a biomechanical analysis of ventral furrow formation in the Drosophila melanogaster embryo. Ventral furrow formation is the first large-scale morphogenetic movement in the fly embryo. It involves deformation of a uniform cellular monolayer formed following cellularisation, and has therefore long been used as a simple system in which to explore the role of mechanics in force generation. Here we use a quantitative framework to carry out a systematic perturbation analysis to determine the role of each of the active forces observed. The analysis confirms that ventral furrow invagination arises from a combination of apical constriction and apical–basal shortening forces in the mesoderm, together with a combination of ectodermal forces. We show that the mesodermal forces are crucial for invagination: the loss of apical constriction leads to a loss of the furrow, while the mesodermal radial shortening forces are the primary cause of the internalisation of the future mesoderm as the furrow rises. Ectodermal forces play a minor but significant role in furrow formation: without ectodermal forces the furrow is slower to form, does not close properly and has an aberrant morphology. Nevertheless, despite changes in the active mesodermal and ectodermal forces lead to changes in the timing and extent of furrow, invagination is eventually achieved in most cases, implying that the system is robust to perturbation and therefore over-determined.
Highlights
Ventral furrow invagination in Drosophila melanogaster provides a model system uniquely suited for investigating the cellular and molecular mechanisms of morphogenesis [1], [2]
A combination of active forces is required to drive ventral furrow invagination Our quantification and digitisation of the wild type invagination starts during the fast phase of cellularisation and shows that it finishes in the mesoderm before the ectoderm, with the mesodermal cells beginning to radially lengthen before cellularisation is complete in the ectoderm, see Fig. 3 and Video V1
The results show that while ectodermal forces are not essential for furrow formation they do affect the shape of the furrow and the speed at which is it developed
Summary
Ventral furrow invagination in Drosophila melanogaster provides a model system uniquely suited for investigating the cellular and molecular mechanisms of morphogenesis [1], [2]. The process begins as soon as cellularisation is complete and the embryo is composed of a relatively uniform single layer of columnar epithelial cells, surrounded by a shell composed of a vitelline membrane which contains a liquid yolk. This organisation can be readily appreciated in cross–section, where the epithelial blastoderm forms a circular array of columnar cells with their apical–basal axes aligned radially, and their apical surfaces facing outwards, see Fig. 1a. A combination of local twist–induced expression of mesodermal genes and snail–mediated repression of ectodermal cell fate appears to bring about ventral furrow invagination, via cell biological events such as apical flattening, apical constriction, apical–basal lengthening, apical–basal shortening and basal expansion
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