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PDF, English - main document Download (77MB) | Lizenz: The roles of basement membrane during larva-polyp morphogenesis of the starlet sea anemone Nematostella vectensis by Basu, Soham underlies the terms of Creative Commons Attribution-NonCommercial-NoDerivatives 4.0

Abstract

Living systems attain their shape and size through morphogenesis, which spans across several magnitudes of spatial and temporal scales. The pursuit to understand the driving elements that control morphogenesis has primarily focused its attention on the living matter, on the cells and its underlying genetic information. Evidences over the last few centuries has established deeper insights into how cells can self-organize or can be genetically programmed to achieve emergent properties that drive morphogenesis, however, the deeper impact from its internal environment is often ignored or avoided. In case of embryonic development, what starts as a single cell eventually ends up in a multicellular context with several specialized cell types that are crucial to life and its functions, but also builds up an internal niche created by its extracellular matrix in the process. How does an organism build its own native matrix, and how does that integrate with its morphogenesis? In this thesis, I utilize the simple yet complex biology of the sea anemone Nematostella vectensis as a model species to investigate the connection between the extracellular matrix and the development of an organism, at the tissue and the organismal scales. In a phase known as the larva-polyp transition, Nematostella experiences a shift from an ellipsoidal larva to a tubular polyp featuring four tentacles, post-embryonically. Using immunostaining, generation of endogenous knock-in transgenic lines and photoconversions, I establish the spatiotemporal dynamics of the basement membrane, and focus particularly on collagen IV. Through pharmacological perturbations, I found out that a steady state of collagen IV density across the body axis is crucial for the animal to maintain its organismal morphogenesis. Also, I uncover that the basement membrane is produced by the endoderm and is organized by the muscles. Furthermore, I account for the origins of tissue remodeling that drives the larva-polyp morphogenesis and propose a dominant regime that is modulated through novel muscle-ECM coordination. These findings address the origin of deformations that modulate the larva-polyp morphogenesis, highlighting a key feedback between the active musculature and passive extracellular matrix in a developing organism. I also focus on tissue-specific morphogenesis at the aboral end of the transitioning animal, where a weaker ECM permits the formation of a secondary pore in a cnidarian, which itself a debatable topic in evolutionary biology. Using detailed cellular and molecular descriptions, combined with biophysical experiments, I identify key steps controlled by upstream FGF signaling that lead to the development of an aboral pore. My doctoral thesis sheds light on the coordination of the extracellular matrix with the tissue, and how these interactions are important to modulate morphogenesis across largely different spatial scales.