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DNA methylation memory: Understanding epigenetic reprogramming in vertebrates by Oscar Javier Ortega Recalde A thesis submitted to the University of Otago in fulfilment of the requirement for the degree of Doctor of Philosophy December 2019 This thesis was conducted under the supervision of Dr Timothy A. Hore1 & Professor Neil J. Gemmell1 1Department of Anatomy, University of Otago, Dunedin 9016, New Zealand Declaration Except where specific reference is made to other sources, the work presented in this thesis is the work of the author. It has not been submitted, in whole or in part for any other degree. Oscar Javier Ortega Recalde Abstract DNA methylation is an epigenetic mark critical for vertebrate development and is associated with numerous cellular and organismal processes including X- chromosome inactivation, genomic imprinting, and regulation of gene expression. Importantly, DNA methylation patterns are faithfully inherited during cell division, providing an information memory module additional to the DNA code. This mark, along with other epigenetic modifications, plays an essential role in establishing and maintaining cell identity. DNA methylation dynamics has been studied in detail in eutherian mammals, where two major waves of demethylation, the first in the early embryo and the second during germline development, remove most marks. Erasure of epigenetic memory is associated with cell reprogramming, and in mammals, is inextricably linked to increased developmental potency. For divergent vertebrate models, this dynamic is largely untested and indirect evidence suggests epigenetic memory may be retained in the germline. Furthermore, the role of epigenetic memory and reprogramming in major cell fate transitions, such as sex determination and sex change, is underexplored despite being apparently driven by epigenetic mechanisms in at least some species. In order to understand how epigenetic memory is maintained, erased, and reprogrammed in divergent vertebrates, I have focused on two fish species. I have analysed the epigenome of the germline during gonad development in zebrafish (Danio rerio), and the transcriptome and methylome of bluehead wrasse (Thalassoma bifasciatum) during female-to-male sex change. Using a combination of techniques, including isolation of germline cells, whole genome bisulfite sequencing, and comparative epigenomics and transcriptomics, I explored i Abstract epigenetic memory and reprogramming in these species. This thesis is presented as a collection of research and review papers, as well as a discussion synthesising my results. In the first paper, I assessed the DNA methylation dynamics during zebrafish germline development (Ortega-Recalde, Day, Gemmell, & Hore, 2019). Using a low-coverage whole genome bisulfite sequencing technique, I found that germline DNA methylation levels remain similar to somatic cells throughout development. Additionally, I discovered a remarkable amplification of ribosomal DNA during the critical period of gonad transformation, principally in females, associated with demethylation. Thus, in stark contrast to mammals, the zebrafish germline preserves global levels of DNA methylation and undergoes an enigmatic sex-specific amplification which may be related to sex determination in this species. The broader significance of my findings regarding DNA methylation memory in the zebrafish germline are examined in the second manuscript (Ortega-Recalde & Hore, 2019). In this review, I presented contrasting evidence concerning epigenetic memory and amnesia in vertebrates. In addition to my work, I reviewed new results supporting that non-mammalian species do not undergo DNA methylation erasure, and that epigenetic memory may be an underappreciated reservoir of information between generations. I discuss several hypotheses to explain such divergence and the consequences of retention of germline DNA methylation for transgenerational epigenetic inheritance. The third paper reports a study of socially controlled sex-change in bluehead wrasse (Todd et al., 2019). By using transcriptomic and methylome approaches, ii Abstract this study revealed the molecular events through which a mature ovary is reprogrammed to a functional testis. In addition to identifying the primary triggers and subsequent molecular cascade of this transformation, this study showed that sex change involves a genome-scale epigenetic reprogramming event, including a marked shift in epigenetic molecular machinery, reminiscent of mammalian naïve pluripotent stem cells and primordial germ cells, and extensive changes in DNA methylation patterns. Thus, epigenetic reprogramming plays a central role orchestrating gonad transformation in this species despite not undergoing global DNA methylation erasure. The significance of the third paper is discussed alongside other contemporary work in the fourth manuscript (Ortega-Recalde, Goikoetxea, Hore, Todd, & Gemmell, 2019). This exhaustive review presents current evidence regarding the genetic and epigenetic basis of natural sex change in fish. The extraordinary sexual plasticity behind such phenomena shows that sexual fate is a reversible process, initiated by male and female signalling networks, with sexual identity likely preserved long-term by epigenetic modifications in the absence of any underlying genetic changes. Finally, in the last chapter I discuss the broader implications of my results, consider the limitations of my research, and integrate my findings into a comprehensive body of work. Together, my research shows that epigenetic memory dynamics, in particular DNA methylation, is heterogeneous in the germline of vertebrates, but likely plays a central role in defining sexual fate for at least some fish species. iii iv Acknowledgments First and foremost, I would like to thank my primary supervisor Tim. It has been a great honour to be his first Ph.D. student and I will always be grateful for his guidance, support, and patience during my studies. Tim’s enthusiasm and passion for science is a source of inspiration. I greatly enjoyed each of our discussions about new ideas, intriguing results and challenging experiments. Even during tough times, he always found the right words to encourage me to continue. He is an excellent mentor and I greatly admire him as a scientist and as a person. I would also like to thank my supervisor Neil Gemmell. He is genuinely enthusiastic about science, and his support and scientific advice were critical for the development of my research project. I would like to especially thank two members of Gemmell’s lab, Erica and Alex. Erica is an exceptional scientist who is always keen to help and collaborate. I appreciate her for introducing me to the wonderful world of sex-changing fish and allowing me to participate in such an amazing research field. Alex is a dedicated and incredible researcher and, above all, a good friend. I enjoyed our time discussing fish, science, and all those meaningful things that make everyday life so enjoyable. None of my work would have been possible without the incredible support of the people who trained me in the lab: Noel Jhinku who was patient enough to teach me how to take care of the zebrafish and not flood the facility in the process, Michelle Wilson for her incredible patience helping me with the cell sorting process and always being enthusiastic about my work and results, Olga v Acknowledgments Kardailsky who trained me in library preparation techniques and was my scientific guru in the lab, Rob Day for introducing me to the sequencing process and trusting me to do it by myself, and Hugh Cross for his help in the bioinformatic analyses and our talks about scripts and other helpful advice. I arrived in New Zealand when Tim’s lab had just started, and I have seen the group grow and flourish over the years. I would like to thank the old members of the Hore laboratory: Morgan Jones, Andrew Wang, Michael Collins and Brooke Williams. They were my first siblings in science in New Zealand. Additionally, all the current members of the Hore’s lab: Donna Bond, Melanie Laird, Michael Dunnet, Victoria Sugrue, Tim Moser and Claudia Davies. They have all my gratitude. Far from home, I felt like part of a team with them. I was fortunate enough to have great friends at my office: Gert-Jan Jeunen, Denise Martini, Natalie Forsdick, Clare Turdle, Allison Miller, Jeremy McCallum and Rami Al-jiab. They have helped me enjoy my time in the department and we supported each other in the long and arduous journey of science. I would also like to thank my friends in New Zealand Sindy Luu, Ming Williams, Mithun Muraleedharan, Sulagna Banerjee, Sophie Gangl, Elizabeth Yarnall, Connor Seddon, Lucía Malone, Nils Birkholz, Aroa Rey, Kiyas Seyitmuhammedov, Leah Smith and many others who made this time unforgettable. I would like to thank my friends in Colombia who have supported me all these years. Despite the distance, they cheered me up and kept me going on this long journey. Finally, I would like to thank my family, my mother Rosalba, my father vi Acknowledgments Luis Humberto, and my brothers, Betho and Diego, for their support and encouragement. vii viii This thesis is dedicated to my parents and brothers ix x We shall not cease from exploration, and the end of all our exploring will be to arrive where we started and know the place for the first time T.S Eliot (1942) xi xii Table of contents Abstract ............................................................................................................................ i Acknowledgments
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