Surrounding tissue morphogenesis with disrupted posterior midgut invagination during Drosophila gastrulation

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 o...

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Veröffentlicht in:Developmental biology 2025-01, Vol.517, p.168-177
Hauptverfasser: Sabbagh, Sandra, Harris, Tony J.C.
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Sprache:eng
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Zusammenfassung: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. [Display omitted] •The robustness of Drosophila gastrulation is tested using steppke mutants.•The posterior midgut invagination (PMGI) is replaced by an abnormal cell mass.•Surrounding tissues normally affected by PMGI still undergo morphogenesis.•Surrounding tissues form myosin networks known to drive their morphogenesis.•Redundant mechanics seem to substantially circumvent structural disruption of PMGI.
ISSN:0012-1606
1095-564X
1095-564X
DOI:10.1016/j.ydbio.2024.10.001