Surrounding tissue morphogenesis with disrupted posterior midgut invagination during Drosophila gastrulation

Abstract

Gastrulation involves multiple, physically-coupled tissue rearrangements. During Drosophila gastrulation, posterior midgut (PMG) invagination promotes both germband extension and hindgut invagination, but whether the normal epithelial rearrangement of PMG invagination is required for morphogenesis of the connected tissues has been unclear. In steppke mutants, epithelial organization of the PMG primordium is strongly disrupted. Despite this disruption, germband extension and hindgut invagination are remarkably effective, and involve myosin network inductions known to promote their wild-type remodelling. Known tissue-autonomous signaling could explain the planar-polarized, junctional myosin networks of the germband, but pushing forces from PMG invagination have been implicated in inducing apical myosin networks of the hindgut primordium. To confirm that the wave of hindgut primordium myosin accumulations is due to mechanical effects, rather than diffusive signalling, we analyzed α-catenin RNAi embryos, in which all of the epithelial tissues initially form but then lose cell-cell adhesion, and observed strongly diminished hindgut primordium myosin accumulations. Thus, alternate mechanical changes in steppke mutants seem to circumvent the lack of normal PMG invagination to induce hindgut myosin networks and invagination. Overall, both germband extension and hindgut invagination are robust to experimental disruption of the PMG invagination, and, although the processes occur with some abnormalities in steppke mutants, there is remarkable redundancy in the multi-tissue system. Such redundancy could allow complex morphogenetic processes to change over evolutionary time.