Tissue homeostasis at the root of Metazoa: transcriptional control of whole-body regeneration in sponges

Summary:Multicellular animals arose along with complex gene programs controlling tissue integrity. A comprehensive understanding of the core mechanisms underlying tissue maintenance in metazoans is impossible without studying early-branching animal groups. Here, we present reaggregation from single cells in sponges (phylum Porifera) as a promising model for exploring conserved mechanisms maintaining tissue homeostasis in Metazoa. We describe major morphological changes in tissue composition and cell morphology following the mechanical dissociation of intact tissues of a demosponge Halisarca dujardinii and link them to differential transcript expression using bulk RNA sequencing. Reaggregation is accompanied by a massive shift in the expression of transcripts related to cell adhesion, cell polarity, proliferation, and stem cell maintenance. Major signaling pathways are heavily implicated in both reaggregation sensu stricto and further progressive development of the primmorphs. The expression of identified transcription factors in H. dujardinii challenges the conventional views on the regulation of epithelial-mesenchymal transition (EMT).Highlights:Most transcripts show early response to the dissociationExpression of cell adhesion/polarity transcripts precedes the emergence of epithelial cellsGene programs controlling pluripotency and proliferation are transcriptionally decoupledFactors involved in EMT and key components of major signaling pathways are differentially expressed during reaggregation