Abstract
The budding of tubular organs from flat epithelial sheets is a vital morphogenetic process. Cell behaviours that drive such processes are only starting to be unraveled. Using live-imaging and novel morphometric methods, we show that in addition to apical constriction, radially oriented directional intercalation of cells plays a major contribution to early stages of invagination of the salivary gland tube in the Drosophila embryo. Extending analyses in 3D, we find that near the pit of invagination, isotropic apical constriction leads to strong cell-wedging. Further from the pit cells interleave circumferentially, suggesting apically driven behaviours. Supporting this, junctional myosin is enriched in, and neighbour exchanges are biased towards the circumferential orientation. In a mutant failing pit specification, neither are biased due to an inactive pit. Thus, tube budding involves radially patterned pools of apical myosin, medial as well as junctional, and radially patterned 3D-cell behaviours, with a close mechanical interplay between invagination and intercalation.
Highlights
During early embryonic development, simple tissue structures are converted into complex organs through highly orchestrated morphogenetic movements
Apical cell constriction is organised in a radial pattern in the salivary gland placode Upon specification of the placode of cells that will form the embryonic salivary gland at the end of embryonic stage 10, the first apparent change within the apical domain of placodal cells is apical constriction at the point that will form the first point of invagination or pit (Figure 1A,B; [Booth et al, 2014; Myat and Andrew, 2000b])
We have previously shown that apical constriction is clustered around the pit and is important for proper tissue invagination and tube formation (Booth et al, 2014)
Summary
Simple tissue structures are converted into complex organs through highly orchestrated morphogenetic movements. Many developmental processes are similar across organs and even species, and a step could be to explore whether the mechanisms described by Sanchez-Corrales et al are present outside of the fruit fly’s salivary glands If so, this could shed light on what happens when tubes fail to form correctly in an embryo, and on how we could create these structures in the laboratory. We have previously shown that in the salivary gland placode during early tube formation when the cells just start to invaginate, the placodal cells contain prominent junctional and apical-medial actomyosin networks (Booth et al, 2014). Across the placode junctional myosin II is enriched in circumferential junctions, suggesting polarised initiation of cell intercalation through active junction shrinkage This is followed by polarised resolution of exchanges towards the pit, thereby contributing to tissue invagination. Suggest that a tissue-intrinsic mechanical interplay contributes to successful tube budding
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