GENOME CONTENT AND DEVELOPMENTAL EXPRESSION OF TRANSCRIPTION FACTOR GENES IN THE DEMOSPONGE AMPHIMEDON QUEENSLANDICA: INSIGHTS INTO THE FIRST MULTICELLULAR ANIMAL

Abstract

Recent phylogenetic insights suggest that the body plan and life cycle of the oldest metazoans, sponges, may resemble the last common ancestor to all animals. While their adult body plan differs drastically from other animals, sponge development displays many metazoan hallmarks. Enabling a framework for the spatial organisation of a variety of cell types, the invention of a basic developmental program may have been the key step allowing the transition to multicellularity in animals. Novel transcription factors were likely to have been crucial to the increase in regulatory complexity that must have accompanied this step. Many developmental regulatory pathways are conserved throughout animal evolution and investigations into the molecular basis of eumetazoan development have led to reconstruction of ancestral developmental states. In this study, I investigate the genomic and developmental innovations that occurred at the base of Metazoa in view of reconstructing the first metazoan developmental program and identifying fundamental characters that enabled the transition to multicellularity in animals. As in other metazoans, in the haplosclerid demosponge Amphimedon queenslandica, fertilisation, cleavage, and gastrulation yield a larva with various cell types patterned along an anteriorposterior axis and into germ layers. Non-neural sensory structures enable the larva to respond to environmental conditions. Drawing on the recently sequenced genome of A. queenslandica, I show that this demosponge has a limited set of homeobox, Sox, Fox, T-box, and nuclear receptor transcription factors, which have important roles during eumetazoan development. Using in situ hybridisation on sponge developmental stages for the first time, I also analyse the expression of a subset of these genes during development. Remarkably, A. queenslandica possesses a clear NK cluster of ANTP genes but lacks Hox, ParaHox, or EHGBox genes. This suggests that an NK cluster was present in the metazoan last common ancestor and that a protoHox gene - progenitor to Hox, ParaHox, and EHGBox genes - arose from within this cluster after demosponges had branched off the main metazoan lineage. Importantly, this implies that Hox genes were co-opted into an existing system for anteriorposterior axial patterning. Using the completed genomes of A. queenslandica and the cnidarian Nematostella vectensis as well as preliminary genome traces of the choanoflagellate Monosiga brevicollis, I have analysed the origin and early evolution of transcription factors through phylogenetic analyses. Metazoanspecific transcription factor classes seem to have evolved before demosponges departed from the main metazoan lineage. It appears that these classes gradually diversified by duplication in different ways, particularly in the periods preceding and following the demosponge/metazoan split. Largely unlike cnidarians, sponges seem to constitute an intermediate stage in the evolution of the metazoan genome and, as such, the transcription factor genes present in their genome may have been part of a core developmental program sufficient for the transition to multicellularity. Many transcription factor genes are expressed during A. queenslandica development and a subset of these genes seems to display some conservation in their developmental expression between sponges and other metazoans. AmqHNF4 expression suggests that epithelium evolution went through a stage without a basement membrane. Based on AmqLim3 and AmqSoxB expression, neurons may be related to pre-neural cells associated with photo- and chemosensory structures. AmqBsh and AmqSoxF were probably involved in regulation of cell adhesion and extracellular matrix molecules during the development of the metazoan ancestor. AmqProx2, AmqPaxB, and AmqPoul expression is only detected in early embryogenesis while AmqSoxC, like most other genes in this study, may be involved in fate determination and differentiation of a specific migrating cell lineage throughout development. Expression data paint the picture of an ancestral metazoan developmental program where asymmetric cleavage participates in early cell fate determination and differentiation and where specified cells respond in different ways to signalling cues by following complex migratory trajectories throughout embryogenesis. From a genomic and developmental perspective, sponges appear to be an intermediate in metazoan evolution. The developmental program seems to have gradually increased in complexity in pre-Cambrian animals. However, the last common ancestor of all extant metazoans may have already utilised many of the same molecular tools during development in the same way as most contemporary animals. The evolutionary steps that occurred at the base of Metazoa and led to a relatively complex core developmental program do not seem to have been recorded until present day

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