The origins of cell communication in the animal kingdom: Notch signalling during embryogenesis and metamorphosis of the demosponge Amphimedon queenslandica.

Gemma Richards (2010). The origins of cell communication in the animal kingdom: Notch signalling during embryogenesis and metamorphosis of the demosponge Amphimedon queenslandica. PhD Thesis, School of Biological Sciences, The University of Queensland.

       
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Author Gemma Richards
Thesis Title The origins of cell communication in the animal kingdom: Notch signalling during embryogenesis and metamorphosis of the demosponge Amphimedon queenslandica.
School, Centre or Institute School of Biological Sciences
Institution The University of Queensland
Publication date 2010-03
Thesis type PhD Thesis
Supervisor Bernard Degnan
David Merritt
Total pages 212
Total colour pages 30
Total black and white pages 182
Subjects 06 Biological Sciences
Abstract/Summary Intercellular communication is an essential aspect of multicellular life. In the animal kingdom, molecular signalling pathways fulfil this requirement and provide a conduit for information transfer between cells. The origins and ancestral conditions of these signalling pathways can be inferred via comparisons of their structure and deployment in living species. As sponges are one of the earliest branching metazoan phyla, investigations within this lineage provide an important outgroup to which the extensive data on bilaterian intercellular signalling pathways can be compared. Of the handful of signalling pathways that direct animal development, I focus on the Wnt, Notch, Transforming growth factor-β (TGF-β), and Hedgehog signalling mechanisms. To determine their origins, I employ a comparative genomics approach and annotate the incidence and domain architectures of core pathway components in the genomes of representative species across the Holozoa. From this analysis I infer that the Notch, Wnt, and TGF-β pathways are metazoan synapomorphies, whereas the Hedgehog pathway is restricted to the Eumetazoa sensu stricto. Of note, I identify pre-existing functional modules within these pathways that may have provided a foundation for their emergence in the metazoan lineage. The Notch signalling pathway is a key regulator of cell fate decisions during bilaterian development, but has been little studied in non-bilaterian organisms. I report that the genome of the emerging model demosponge Amphimedon queenslandica encodes orthologues of many canonical Notch signalling genes, and further, that these genes also possess many of the short functional motifs and domains that underwrite pathway functionality. Notably, Amphimedon possesses an expanded repertoire of Notch ligands and of Fringe glycosyltransferases. These additions indicate that significant modifications to the ancestral regulation and activity of the Notch pathway may have occurred in the demosponge lineage. To place this inventory of Amphimedon Notch signalling genes into an organismal context, I assay the spatial expression of the Amphimedon Notch receptor and five Delta ligands across a developmental series. I reveal that these genes are differentially expressed during embryogenesis and development of the Amphimedon parenchymella larva. In order to assess the significance of these expression patterns, it was necessary to undertake a descriptive study of Amphimedon developmental morphology. To this end, I sectioned developmental stages and stained them with haematoxylin and eosin. This enabled me to track the ontogeny of diverse cell types and infer the relative timing of morphogenetic events. Utilising this cytological information, the expression of Notch ligands can be linked to the development of the ciliated posterior pigment ring, the anterior pole cells and the intra-epithelial flask cells and globular cells. The cell-type specific expression of Notch ligands leads me to propose that Notch signalling is involved in the determination and differentiation of multiple cell lineages during Amphimedon development – a role that is comparable to the proposed ancestral function of this pathway in the Eumetazoa. Of note, many of the cells expressing Notch ligands in Amphimedon larvae have putative sensory functions. If these cells are directly related to the sensory cells of eumetazoans, this may indicate that Notch signalling has been active in sensory development since the dawn of the Metazoa. Notch signalling is also active in Amphimedon post-embryonic development – during larval settlement and metamorphosis. I demonstrate that Notch ligands are expressed in multiple domains in competent larvae, most notably in the anterior pole cells, which are the primary sites of contact between a larva and the benthos. Using a chemical inhibitor of the Notch pathway, I show that blocking Notch signalling significantly perturbs the ability of Amphimedon larvae to settle and undergo metamorphosis. These experiments suggest an additional role for the Notch pathway in regulating the critical transition between free-swimming larvae and benthic adults in Amphimedon.
Keyword Notch
Amphimedon queenslandica
metazoan developmental signalling pathways
parenchymella
evolution
Additional Notes Colour pages: (30 in total) 21, 35, 72, 74, 75, 85-92, 94, 95, 97, 98, 110, 111, 113-115, 117, 120, 123, 134, 144, 210-212. Landscape pages: (12 in total) 58-60, 72, 74, 75, 198-203.

 
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Created: Mon, 23 Aug 2010, 20:12:41 EST by Gemma Richards on behalf of Library - Information Access Service