Vellutini, B. C. | Search bioRxiv

bioRxiv2023

Combinatorial Wnt signaling landscape during brachiopod anteroposterior patterning

BackgroundWnt signaling pathways play crucial roles in animal development. They establish embryonic axes, specify cell fates, and regulate tissue morphogenesis from the early embryo to organogenesis. It is becoming increasingly recognized that these distinct developmental outcomes depend upon dynamic interactions between multiple ligands, receptors, antagonists, and other pathway modulators, consolidating the view that a combinatorial "code" controls the output of Wnt signaling. However, due to the lack of comprehensive analyses of Wnt components in several animal groups, it remains unclear if specific combinations always give rise to specific outcomes, and if these combinatorial patterns are conserved throughout evolution. ResultsIn this work, we investigate the combinatorial expression of Wnt signaling components during the axial patterning of the brachiopod Terebratalia transversa. We find that T. transversa has a conserved repertoire of ligands, receptors, and antagonists. These genes are expressed throughout embryogenesis but undergo significant upregulation during axial elongation. At this stage, Frizzled domains occupy broad regions across the body while Wnt domains are narrower and distributed in partially overlapping patches; antagonists are mostly restricted to the anterior end. Based on their combinatorial expression, we identify a series of unique transcriptional subregions along the anteroposterior axis that coincide with the different morphological subdivisions of the brachiopod larval body. When comparing these data across the animal phylogeny, we find that the expression of Frizzled genes is relatively conserved, whereas the expression of Wnt genes is more variable. ConclusionsOur results suggest that the differential activation of Wnt signaling pathways may play a role in regionalizing the anteroposterior axis of brachiopod larvae. More generally, our analyses suggest that changes in the receptor context of Wnt ligands may act as a mechanism for the evolution and diversification of the metazoan body axis.

developmental biology↗

bioRxiv2023

Pre-patterned epithelial invagination prevents mechanical instability during fly gastrulation

Mechanical forces are crucial for driving and shaping tissue morphogenesis during embryonic development, but their relevance for the evolution of development remains poorly understood. Here, we show that a morphogenetic innovation present in fly embryos--a deep epithelial fold known as the cephalic furrow--plays a mechanical role during Drosophila gastrulation. By integrating in vivo experiments and in silico simulations, we find that the formation of the cephalic furrow prevents mechanical instabilities at the head-trunk epithelium by absorbing the compressive stresses generated by concurrent morphogenetic movements of gastrulation, the expansion of mitotic domains and the germ band extension. Furthermore, by comparing the expression of known and novel genes involved in cephalic furrow formation between fly species, we find that the presence of the cephalic furrow is linked to changes in the expression of buttonhead transcription factor at the head-trunk boundary. These data suggest that the genetic control of cephalic furrow formation was established through the integration of a new player into the ancestral head-trunk patterning system, and that mechanical instability may have been the selective pressure associated with the evolution of the cephalic furrow. Our findings uncover empirical evidence for how mechanical forces can influence the evolution of morphogenetic innovations in early development.

developmental biology↗