Exploring the bZIP regulatory network in the sponge Amphimedon queenslandica: insights into the ancestral animal regulatory genome

Jindrich, Katia (2017). Exploring the bZIP regulatory network in the sponge Amphimedon queenslandica: insights into the ancestral animal regulatory genome PhD Thesis, School of Biological Sciences, The University of Queensland. doi:10.14264/uql.2017.443

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Author Jindrich, Katia
Thesis Title Exploring the bZIP regulatory network in the sponge Amphimedon queenslandica: insights into the ancestral animal regulatory genome
Formatted title
Exploring the bZIP regulatory network in the sponge Amphimedon queenslandica: insights into the ancestral animal regulatory genome
School, Centre or Institute School of Biological Sciences
Institution The University of Queensland
DOI 10.14264/uql.2017.443
Publication date 2017-03-27
Thesis type PhD Thesis
Supervisor Bernard Degnan
Milos Tanurdzic
Total pages 217
Total colour pages 87
Total black and white pages 130
Language eng
Subjects 0603 Evolutionary Biology
0604 Genetics
060802 Animal Cell and Molecular Biology
Formatted abstract
What genomic innovations supported the emergence of multicellular animals, over 600 million years ago, remains one of the most fundamental questions in evolutionary biology. Increasing evidence suggests that the elaboration of the regulatory mechanisms controlling gene expression, rather than gene innovation, underlies this transition. Since transcriptional regulation is largely achieved through the binding of specific transcription factors to specific cis-regulatory DNA, understanding the early evolution of these master orchestrators is key to retracing the origin of animals (metazoans). Basic leucine zipper (bZIP) transcription factors constitute one of the most ancient and conserved families of transcriptional regulators. They play a pivotal role in multiple pathways that regulate cell decisions and behaviours in all kingdoms of life. Here, I explore the early evolution and putative roles of bZIPs in a representative of one of the oldest surviving animal phyla, the marine sponge Amphimedon queenslandica.

Using recently sequenced genomes from across the Eukaryota, and in particular the Metazoa, I first reconstruct the evolution of bZIPs, and document that this transcription factor superfamily has undergone multiple independent kingdom-level expansions. I present here a thorough analysis of the whole superfamily of bZIP transcription factors across the main eukaryotic clades and the putative bZIP network that was in place in the ancestor of all extant animals. To then explore the putative role of bZIP transcription factors in the metazoan ancestor, I identify the bZIP complement in the demosponge Amphimedon queenslandica (phylum Porifera). As expected for regulatory molecules, a majority of the 17 A. queenslandica bZIPs display high temporal specificity, cell-type specific localisation and are dynamically expressed throughout development. Along with bZIPs high expression across developmental stages, these characteristics point towards bZIPs having a fundamental role in this sponge. Given the consistent central role of these transcription factors in the functioning of extant animals, I infer that were already integrated in developmental and cell specific regulatory networks in the ancestral regulatory genome and supported the emergence of multicellularity.

The PAR and ATF4 orthologues particularly stand out: they are highly expressed throughout Amphimedon life cycle and peak in expression at key developmental transitions. A. queenslandica PAR-bZIP AqPARa is part of the sponge circadian network. In this thesis, I establish that AqPARa is both spatially and temporally co-expressed with A. queenslandica cryptochrome AqCRY2, and that expression of both genes is entrained by light. I also explore the involvement of circadian genes that are conserved in other phyla in A. queenslandica response to light. This work provides insights on the animal ancestral circadian regulatory network, and the evolution of PAR-bZIPs implication in the regulation of environmentally cued behaviours.

A. queenslandica ATF4 orthologue, AqATF4, is highly expressed in larval archeocytes. Using chromatin immunoprecipitation followed by deep sequencing (ChIP-Seq) of AqATF4 and five histone H3 post-translational modifications (H3K4me3, H3K4me1, H3K27ac, H3K36me3 and H3K27me3), I explore AqATF4 putative target genes and binding sites in A. queenslandica larva, and the complexity of A. queenslandica regulatory landscape. I conclude that many of the roles bZIPs play in bilaterians have a more ancient origin, and were present in the last common ancestor of all contemporary animals.
Keyword Transcription factor
Gene regulatory networks
Gene regulation
Evolution of multicellularity
Additional Notes Colour pages: This document begins with Roman numerals, but the PDF numbering begins from page 1. Thus the 10th page of the document says page 'x' but can be accessed by page '10' in the PDF search function. I have listed both sets of numbers below: PDF pages: 34-40, 54-59, 85-115, 129-136, 156-166, 194-217 Numbering at bottom of pages: 10-16, 30-35, 61-91, 105-112, 132-142, 170-193

Document type: Thesis
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Created: Wed, 15 Mar 2017, 16:48:17 EST by Katia Jindrich on behalf of Learning and Research Services (UQ Library)