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Joachim Surm Thesis (PDF 9MB) MOLECULAR INSIGHTS INTO THE EVOLUTION OF NOVEL GENES Joachim Maximilian Surm Bachelor of Applied Science/Bachelor of Business Bachelor of Biomedical Science (Honours 1A) Submitted in fulfilment of the requirements for the degree of Doctor of Philosophy School of Biomedical Sciences Faculty of Health Queensland University of Technology 2019 Keywords Acrorhagi, Actinioidea, Actinia tenebrosa, Cnidaria, cnidocyte, convergent evolution, de novo, desaturase, development, diversifying selection, ecology, elongase, Elovl, episodic diversifying selection, evolution, Fad, fatty acid, gene duplication, gene expression, genome, long-chain polyunsaturated fatty acids, lineage-specific, nematocyst, nematocyte, novel cell, ontogeny, phylogenetic, proteome, purifying selection, sea anemone, spatiotemporal expression, toxin, transcriptome, venom. Molecular Insights into the Evolution of Novel Genes i Abstract Understanding the mechanisms that underpin the formation of novel genes is a key research area in molecular evolution. Novel genes can originate through multiple mechanisms (e.g. duplication, horizontal gene transfer and de novo gene formation) and have been associated with phenotypic variation including evolution of venoms, the adaptive immune system, as well as various disease states. Cnidarians represent an excellent model for investigation and characterisation of novel genes as they possess a high number of genes that lack homology with other lineages (10-20 % of the gene set) as well as having genomes more similar to vertebrates than other model species (e.g. Drosophila melanogaster and Caenorhabditis elegans). Moreover, the last common ancestor of cnidarians was venomous, with all extant cnidarian species delivering their venom using a novel, and phylum defining cell – the cnidocyte. These venoms constitute toxin peptides that are often encoded by novel genes. Here I have generated genomic resources (genome, transcriptome) in combination with functional genomics (RNA-seq, proteomics, and fatty acidomics) to elucidate the evolution of novel genes in sea anemone genomes using a comparative phylogenetic approach. Based on the results of the three studies, gene duplication dominates the evolution of novel genes in cnidarians, specifically those that occur within a lineage. This is observed in the first study for both the gene families involved in the biosynthesis of long-chain polyunsaturated fatty acids (LC-PUFAs, ≥ C20), as well as in the second study for multiple toxin families. Finally, the first complete Actinioidea genome confirmed a large gain of novel genes in this lineage, while novel genes in Cnidaria, collectively, appear to undergo an increased frequency of gene duplication events. Broadly, I demonstrate that cnidarian gene families are evolving under a regime of pervasive purifying selection, with some evidence of episodic diversifying selection. These results are consistent with other studies, which report similar observations in cnidarians. Taken together, my data indicates phylogeny constrains much of the evolution of gene complement and gene families in cnidarians, suggesting phylogenetic inertia plays an important role. This is significant, with genes encoding toxins previously reported to be strongly associated with a shift in ecological niche. However, dynamic patterns of spatiotemporal gene expression of toxin genes are observed to meet the functional and ecological requirements of cnidarians. My ii Molecular Insights into the Evolution of Novel Genes results further demonstrate Actinioidea-specific genes have pronounced signatures of gene expression and protein localisation to Actinioidea-specific morphological structures, acrorhagi. This suggests that novel morphological structures evolve in concert with novel genes, and that novel innovations are reliant on a process of gene regulation. Overall, I provide insights into the expression, phylogenetic and molecular evolutionary histories of cnidarian genes and gene families, which has important implications in understanding novel genes and novel innovations. Molecular Insights into the Evolution of Novel Genes iii A Note Regarding Format This dissertation is a thesis by publication. It contains three articles that have either been published or are under blind-peer review by refereed journals. The logical flow of the thesis is maintained by introducing these articles where they fit most appropriately into the thesis structure. All articles have been reformatted using the APA referencing style and reconfigured to Word to provide consistent formatting throughout the thesis. Moreover, tables and figures have been numbered continuously throughout the thesis, for consistency. iv Molecular Insights into the Evolution of Novel Genes Table of Contents Keywords ............................................................................................................................. i Abstract .............................................................................................................................. ii Table of Contents .................................................................................................................v List of Figures .................................................................................................................. viii List of Tables ..................................................................................................................... xi List of Supplementary Figures ........................................................................................... xii List of Supplementary Tables ............................................................................................xiv List of Abbreviations .........................................................................................................xvi List of Publications ..........................................................................................................xvii Acknowledgements ............................................................................................................ xx Chapter 1: Introduction.................................................................................... 1 1.1 Mechanisms of novel gene formation .........................................................................1 1.1.1 Gene duplication...............................................................................................1 1.1.2 Gene fusion and fission.....................................................................................5 1.1.3 Exon shuffling ..................................................................................................6 1.1.4 Horizontal gene transfer ....................................................................................6 1.1.5 de novo gene formation.....................................................................................7 1.2 Frequency, distribution and outcomes of novel genes ..................................................9 1.2.1 Chimeric genes .................................................................................................9 1.2.2 Orphan genes ....................................................................................................9 1.3 Cnidarians ................................................................................................................ 12 1.4 Actinia tenebrosa as a candidate to study the evolution of novel genes ...................... 17 1.5 Aims of the Project ................................................................................................... 18 1.6 Research plan ........................................................................................................... 19 1.6.1 Aim 1/Study 1: Insights into the phylogenetic and molecular evolutionary histories of Fad and Elovl gene families in Actiniaria ...................................... 19 1.6.2 Aim 2/Study 2: A process of convergent amplification and tissue-specific expression dominates the evolution of toxin and toxin-like genes in sea anemones ....................................................................................................... 19 1.6.3 Aim3/Study 3: The draft genome of Actinia tenebrosa reveals innovations in Actinioidea ................................................................................................. 20 Chapter 2: Insights into the phylogenetic and molecular evolutionary histories of Fad and Elovl gene families in Actiniaria ......................................... 21 Abstract ............................................................................................................................. 24 2.1 Introduction .............................................................................................................. 25 2.2 Materials and Methods ............................................................................................. 28 2.2.1 Identification of candidate genes ..................................................................... 28 2.2.2 Phylogenetic analyses ..................................................................................... 29 2.2.3 Selection analyses ........................................................................................... 29 2.2.4 Fatty acid analysis .......................................................................................... 30 Molecular Insights into the Evolution of Novel Genes v 2.3 Results ....................................................................................................................
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