Abstract
The role of the cellular microenvironment in enabling metazoan tissue genesis remains obscure. Ctenophora has recently emerged as one of the earliest-branching extant animal phyla, providing a unique opportunity to explore the evolutionary role of the cellular microenvironment in tissue genesis. Here, we characterized the extracellular matrix (ECM), with a focus on collagen IV and its variant, spongin short-chain collagens, of non-bilaterian animal phyla. We identified basement membrane (BM) and collagen IV in Ctenophora, and show that the structural and genomic features of collagen IV are homologous to those of non-bilaterian animal phyla and Bilateria. Yet, ctenophore features are more diverse and distinct, expressing up to twenty genes compared to six in vertebrates. Moreover, collagen IV is absent in unicellular sister-groups. Collectively, we conclude that collagen IV and its variant, spongin, are primordial components of the extracellular microenvironment, and as a component of BM, collagen IV enabled the assembly of a fundamental architectural unit for multicellular tissue genesis.
Highlights
A pivotal event in metazoan evolution was the transition from single-cell organisms to multicellular tissues (Figure 1A)
We characterized the extracellular matrix in Ctenophora and the other non-bilaterian animal phyla through a combination of immunohistochemistry (IHC), electron microscopy (EM), RNA sequencing, and genomic and transcriptomic analyses
Expression of NC1 domains without collagenous tails is novel (Figure 4C). These findings show that the extracellular matrix (ECM) of ctenophores contain both collagen IV and standalone NC1 genes, and that the number and diversity collagen IV genes exceeds that of any other metazoan group
Summary
A pivotal event in metazoan evolution was the transition from single-cell organisms to multicellular tissues (Figure 1A). The basement membrane (BM), a specialized form of extracellular matrix (ECM), is a hallmark morphological feature of the microenvironment of epithelial. Developmental Biology and Stem Cells Genomics and Evolutionary Biology eLife digest The emergence of the diversity of multicellular animals involved cells joining together to form tissues and organs. The ‘glue’ that enabled the cells to work together is made of rope-like molecules called collagen, which assemble into scaffolds. These smart scaffolds tether proteins forming basement membranes that connect cells, provide strength to tissues, and transmit information that influences how the cells behave
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