Maternal Torso-Like Coordinates Tissue Folding During Drosophila Gastrulation

Abstract

The rapid and orderly folding of epithelial tissue during developmental processes such as gastrulation requires the precise coordination of changes in cell shape. Here, we report that the perforin-like protein Torso-like (Tsl), the key extracellular determinant for embryonic terminal patterning, also functions to control epithelial morphogenesis. We find that null mutants display a ventral cuticular hole phenotype that is independent of the loss of terminal structures, and arises as a consequence of mesoderm invagination defects. We show that the holes are caused by uncoordinated constriction of ventral cell apices, resulting in the formation of an incomplete ventral furrow. Consistent with these data, we find that loss of is sensitive to gene dosage of, a critical mediator of Rho1-dependent ventral cell shape changes during furrow formation, suggesting that Tsl may act in this pathway. In addition, loss of strongly suppressed the effects of ectopic expression of Folded Gastrulation (Fog), a secreted protein that promotes apical constriction. Taken together, our data suggest that Tsl controls Rho1-mediated apical constriction via Fog. Therefore, we propose that Tsl regulates extracellular Fog activity to synchronize cell shape changes and coordinate ventral morphogenesis in Identifying the Tsl-mediated event that is common to both terminal patterning and morphogenesis will be valuable for our understanding of the extracellular control of developmental signaling by perforin-like proteins.

Optogenetic rescue of a developmental patterning mutant

“…All three alleles failed to undergo posterior midgut invagination in the dark, indicative of strong loss-of-function of terminal signaling (Figure S1). Blue light illumination restored tissue invagination in OptoSOS-trk and OptoSOS-Tor RNAi embryos, but not OptoSOS-tsl embryos (Figure S1), consistent with a recent report suggesting that Tsl plays an additional, terminal signaling-independent role in gastrulation (20). These preliminary experiments suggested that OptoSOS-trk and OptoSOS-Tor RNAi embryos are able to transition complete loss of terminal signaling in the dark to a strong gain-of-function phenotype upon illumination.…”

Evolution of the Torso activation cassette, a pathway required for terminal patterning and moulting

“…In some of these species, studies have indicated that terminal patterning occurs in other ways. In Drosophila, Torso-like has other functions, including a role in dorso-ventral patterning (Mineo et al, 2017) and gastrulation (Johnson et al, 2017) The nonterminal patterning phenotypes produced in Torso-like null mutants are reminiscent of those caused by Oncopeltus RNA interference (Weisbrod et al, 2013) and over-expression of aphid torso-like in Drosophila (Duncan et al, 2013), implying these functions, rather than terminal patterning, may be more conserved.…”

Torso-Like Is a Component of the Hemolymph and Regulates the Insulin Signaling Pathway in Drosophila

“…To generate the phm:Tsl construct, a 1.1 kb fragment of the phm promoter region (from Ono et al (2006)) was first cloned from gDNA (F -5'-CTG CAG TGA TGC GCT GCT CCT TTG T-3', R -5'-AGA TCT CAC TTT CGA TTT CCT CCT GC-3') into the pGEM-T Easy vector (Promega), before being sequenced and subcloned into pUASTattB-Tsl:eGFP (Johnson et al 2017) via PstI and BglII sites to delete the UAS sequence. Transgenic lines were made (BestGene) via ΦC31 integrase mediated transformation (Bischof et al 2007) using the ZH-51CE attP-landing site.…”