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University of California Riverside UNIVERSITY OF CALIFORNIA RIVERSIDE A Genomic Exploration of Transposable Element and piRNA Occupancy, Abundance, and Functionality A Dissertation submitted in partial satisfaction of the requirements for the degree of Doctor of Philosophy in Genetics, Genomics, and Bioinformatics by Patrick A. Schreiner June 2017 Dissertation Committee: Dr. Peter Atkinson, Chairperson Dr. Thomas Girke Dr. Jason Stajich Copyright by Patrick A. Schreiner 2017 The Dissertation of Patrick A. Schreiner is approved: Committee Chairperson University of California, Riverside Acknowledgements I acknowledge that the content in Chapter 2 has been published within the “The whole genome sequence of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann), reveals insights into the biology and adaptive evolution of a highly invasive pest species” article by Ppanicolaou et. al in Genome Biology on September 22, 2016. Chapter 3 has been published to the Biorxiv preprint server entitled “piClusterBusteR: Software For Automated Classification And Characterization Of piRNA Cluster Loci” with Dr. Peter Atkinson on May 1, 2017. I am very grateful to my research advisor, Dr. Peter Atkinson, for the opportunity to pursue research in his laboratory. His knowledge, experience, and mentorship were critical in guiding the success of this research. The regular, open-minded scientific discussion and resources that Dr. Atkinson provided put me in an excellent position to succeed in graduate school and beyond. I would also like to thank the members of my guidance, oral exam, and dissertation committees, Dr. Thomas Girke and Dr. Jason Stajich. Their knowledge and experience in the field, teaching ability, mentorship, and patience were invaluable in allowing my professional development as a scientist in the field of Bioinformatics. The contributions that Dr. Girke and Dr, Stajich made with regard to project development and execution were critical for the quality and applicability of this research. I cannot thank Dr. Atkinson, Dr. Girke, and Dr. Stajich enough for their support of my career goals and my job search. iv I owe gratitude to my family, friends, and colleagues for their personal and professional support during the pursuit of my degree. My fiancé, Lily Maxham, was a stable, supportive, and understanding partner during a particularly unpredictable and demanding period of time. My parents, Janet and Edward Schreiner, as well as brothers, Timothy and Matthew Schreiner, were extraordinarily helpful in promoting physical, social, and mental well-being during graduate school. I can’t express enough the appreciation that I have in knowing that I have that unwavering support of these individuals at all times. I greatly appreciate my fellow lab members, Michael Han and Lee Doss, for their friendship and establishing the light and fun, yet productive environment that I enjoyed coming to day after day. Their knowledge of the lab and the field, as well as their availability for personal and professional discussion around the clock was extremely helpful. I am also very lucky and appreciative to have additional staff and faculty that supported my career pursuit before, during, and after the pursuit of my Ph.D. at UCR. My undergraduate research advisor and continuing mentor, Dr. Catherine Putonti at Loyola University of Chicago, provided the opportunity to learn from undergraduate research and presentation. In doing so, she supported and facilitated my success before and during my Ph.D. I am grateful for the opportunity to work with the Director of Graduate Student Professional Development, Dr. Margaret Gover, for the final two years at UCR. v Her support, experience, and commitment to my success played a major role in facilitating my degree progress and achieving my career goals directly after graduating with my Ph.D. I owe thanks to Dr. Cheryl Hayashi for allowing independence and the opportunity to excel as a Teaching Assistant in the Biology department. Her personal and formal appreciation provided me the opportunity to succeed in the classroom and take on leadership roles with confidence. vi ABSTRACT OF THE DISSERTATION A Genomic Exploration of Transposable Element Occupancy, Abundance, and Functionality by Patrick A. Schreiner Doctor of Philosophy, Graduate Program in Genetics, Genomics, and Bioinformatics University of California, Riverside, June 2017 Dr. Peter W. Atkinson, Chairperson The research herein aims to promote a better understanding of the occupancy, architecture, and diversity of transposable elements and piRNA clusters across species. Transposable elements are identified, characterized, and classified in an effort to pursue molecular strategies to control a species regarded among the most significant agricultural pests, Ceratitis capitata. I present a software tool available for general use, piClusterBusteR, that is capable of quickly and accurately annotating the contents of piRNA clusters in any species of interest. The conserved architecture, yet tissue-specific vii nature of piRNA clusters is described in the ovaries and testes of 13 Metazoan species. A reproducible and statistically significant metric is also demonstrated regarding the relative utilization of piRNA amplification. This software, TruePaiR, generated benchmark values for comparison and context in notable tissues and species, as well as demonstrated the capability to identify subtle differences in piRNA biogenesis across control and experimental conditions. Finally, a bioinformatic workflow is generated to observe the potential for piRNA-mediated post-transcriptional regulation via poly(A) deadenylation of protein-coding genes. By further understanding the presence, architecture, and targets of transposable elements and piRNAs, this research contributes to knowledge of the organismal evolution and development, as well as the conservation and potential to engineer the piRNA pathway in a therapeutic context across species. viii Table of Contents Chapter 1: Introduction 1.1 Transposable Elements.............................................................................1 1.2 The Mechanics of Transposition.............................................................. 2 1.3 TE-derived Small RNAs.......................................................................... 5 1.4 Maternal Deposition of piRNAs .............................................................11 1.5 Proteins in the piRNA Pathway...............................................................12 1.6 References................................................................................................15 Chapter 2: Genomic Characterization of the Mediterranean Fruit Fly, Ceratitis capitata 2.1 Abstract.................................................................................................... 20 2.2 Introduction.............................................................................................. 20 2.3 Materials and Methods............................................................................. 23 2.4 Results...................................................................................................... 30 2.5 Future Directions......................................................................................40 2.6 References................................................................................................ 43 Chapter 3: piClusterBusteR - Software for Automated Classification and Characterization of piRNA Cluster Loci 3.1 Abstract.................................................................................................... 47 3.2 Introduction.............................................................................................. 48 3.3 Materials and Methods............................................................................. 52 3.4 Results...................................................................................................... 63 3.5 Discussion................................................................................................ 74 3.6 References................................................................................................ 78 3.7 Supplementary Material........................................................................... 81 Chapter 4: TruePaiR - Software for the Accurate Identification of Complementary piRNA Read Pairs in High-Throughput Sequencing Data 4.1 Abstract.................................................................................................... 91 4.2 Introduction.............................................................................................. 92 4.3 Materials and Methods............................................................................. 95 4.4 Results...................................................................................................... 97 4.5 Discussion................................................................................................ 110 4.6 References................................................................................................ 113 4.7 Supplementary Material........................................................................... 116 Chapter 5: A Genomic Exploration of piRNA-mediated Deadenylation of Protein- coding Genes in Drosophila melanogaster 5.1 Abstract.................................................................................................... 126 5.2 Introduction.............................................................................................. 126 5.3 Methods and Results...............................................................................
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