Folded gastrulation and T48 drive the evolution of coordinated mesoderm internalization in flies

Abstract

Gastrulation constitutes a fundamental yet diverse morphogenetic process of metazoan development. Modes of gastrulation range from stochastic translocation of individual cells to coordinated infolding of an epithelial sheet. How such morphogenetic differences are genetically encoded and whether they have provided specific developmental advantages is unclear. Here we identify two genes, folded gastrulation and t48, which in the evolution of fly gastrulation acted as a likely switch from an ingression of individual cells to the invagination of the blastoderm epithelium. Both genes are expressed and required for mesoderm invagination in the fruit fly Drosophila melanogaster but do not appear during mesoderm ingression of the midge Chironomus riparius. We demonstrate that early expression of either or both of these genes in C.riparius is sufficient to invoke mesoderm invagination similar to D.melanogaster. The possible genetic simplicity and a measurable increase in developmental robustness might explain repeated evolution of similar transitions in animal gastrulation.DOI: http://dx.doi.org/10.7554/eLife.18318.001

Fog signaling has diverse roles in epithelial morphogenesis in insects

“…In both cases, the mechanism and timing of mesoderm internalization is affected by loss of signaling, but the mesoderm is still able to internalize Zusman and Wieschaus, 1985). The same is also true for the dipteran Chironomus, where disruption of Fog signaling has a measurable impact on mesoderm internalization but the pathway is not strictly required for the process (Urbansky et al, 2016). (Handel et al, 2005).…”

“…The Tribolium genome contains one ortholog each for fog, mist and cta (hereafter referred to as Tc-fog, Tc-mist and Tc-cta). Fog is a fast evolving protein with very low overall sequence conservation within insects and no detectable homologs in currently available noninsect genomes (Figure 1-figure supplement 2) (Urbansky et al, 2016). In contrast, previous research has shown Mist and Cta to be well conserved among insects (de Mendoza et al, 2016;Kozasa et al, 2011;Manning et al, 2013;Parks and Wieschaus, 1991;Urbansky et al, 2016).…”

“…In Drosophila, fog, mist and cta are all maternally expressed (Costa et al, 1994;Manning et al, 2013;Parks and Wieschaus, 1991;Urbansky et al, 2016). In Tribolium, we were unable to detect maternal expression for any of the three genes using conventional whole-mount RNA in situ hybridization (ISH) (for staging and description of wild type development see Handel et al, 2000)).…”

“…While the pathway components have been identified in many lineages, the morphogenetic basis of early development greatly varies between different species (Anderson, 1972a, b;Roth, 2004;Urbansky et al, 2016).…”

“…Recent molecular analysis in the midge Chironomus riparius has also cast doubts about the functional conservation of the pathway for early embryonic development. Rather than forming a highly stereotyped ventral furrow, Chironomus embryos internalize their mesoderm via cell ingression, and this event is only weakly affected by loss of Fog signaling (Urbansky et al, 2016).…”