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Comparative Analysis of Ciliary Gene Regulation in Nematodes

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Comparative Analysis of Ciliary Gene Regulation in Nematodes Comparative analysis of ciliary gene regulation in nematodes by Shirley Yin B.Sc., University of British Columbia, 2014 Dissertation Submitted in Partial Fulfillment of the Requirements for the Degree of Master of Science in the Department of Molecular Biology and Biochemistry Faculty of Science © Shirley Yin 2016 SIMON FRASER UNIVERSITY Fall 2016 All rights reserved. However, in accordance with the Copyright Act of Canada, this work may be reproduced without authorization under the conditions for “Fair Dealing.” Therefore, limited reproduction of this work for the purposes of private study, research, criticism, review and news reporting is likely to be in accordance with the law, particularly if cited appropriately. Approval Name: Shirley Yin Degree: Master of Science Title: Comparative analysis of ciliary gene regulation in nematodes Examining Committee: Chair: Christopher Beh Associate Professor Jack Chen Senior Supervisor Professor David Baillie Supervisor Professor Emeritus Michel Leroux Supervisor Professor Fiona Brinkman Internal Examiner Professor Date Defended: 8 September 2016 ii Abstract Cilia are highly-conserved organelles ubiquitously present in metazoans and some unicellular eu- karyotes. Cilia are responsible for many biological functions, including fluid movement during left- right body development, and sensory functions such as signal transduction in vision and olfaction. In humans, ciliary defects result in a plethora of serious genetic diseases termed ciliopathies. De- spite their diverse morphology and function, cilia share a common microtubule-based structure and are comprised of a core set of proteins, and many ciliary genes share similar but likely not identical regulation mechanisms. Our research aims to understand the variations in cis-regulatory elements in ciliary genes and the impact of such variations on transcriptional regulation. We hypothesize that cis-regulatory elements in different ciliary promoters are unique and that this uniqueness impacts the expression and function of ciliary genes. We focus on a particular cis-regulatory element, the X-box motif, which functions as the binding motif for RFX/DAF-19, a transcription factor that regulates ciliary gene expression. We identify and analyze X-box motifs for a set of 32 well-studied ciliary genes in C. elegans and their orthologs in 25 additional nematodes, including both free-living and parasitic species. My research consists of three modules. First, we curate ciliary gene orthologs using a combined approach, including homology-based gene finding and RNA-seq-based improve- ment. The primary goal of this step is to ensure that the 5’ ends of the genes are accurately defined in order to properly locate ciliary promoters. Second, we search for putative X-box motifs in these promoters using computational tools to identify motifs that resemble the consensus. For the promot- ers from which consensus X-box motifs are not found, we searched for X-box motifs that may show more differences from the consensus using frequency matrix-based search and regular expressions, which we call “atypical” X-box motifs. Third, we analyze the putative atypical X-box motifs, fo- cusing on their sequence similarities, positions in promoter sequences, and flanking sequences, and compare them against the consensus X-box motifs. We find that atypical X-box motifs differ from the consensus but do not have common patterns or characteristics. Our research aims to understand the variations that can occur in X-box motifs despite the highly conserved DNA-binding domain of RFX/DAF-19. Keywords: cilia; bioinformatics; transcriptional regulation; X-box motifs iii Acknowledgements Many people were helpful and influential during my time in graduate school. I am extremely grateful to my senior supervisor, Dr. Jack Chen, for his mentorship and providing valuable advice and support in my research project. I have learned and benefited immensely from his dedication and patience. I am also grateful to Dr. Jiarui Li, who was always willing to provide help and advice and taught me a lot. My gratitude extends to my committee members, Dr. David Baillie and Dr. Michel Leroux, for providing guidance and reviewing the thesis, as well as Dr. Fiona Brinkman and Dr. Christopher Beh for serving on my examining committee. I would like to thank the members of the Chen lab: Zhaozhao Qin, Cyndi Zhao, Jun Wang, Dr. Xi Chen, Dr. Timothy Warrington, Marija Jovanovic, Justin White, Matthew Douglas, Dr. Junxiang Gao, Dr. Jian Ling for creating an enjoyable and productive place to work. Farnaz Bondar and Chander Siddarth were undergraduate volunteers partially under my supervision and contributed to the identification of X-box polymorphisms in C. elegans strains and gene annotation and X-box search in B. xylophilus, respectively. Finally, I am grateful to friends and family for their ongoing encouragement and support throughout these years. iv Table of Contents Approval ii Abstract iii Acknowledgements iv Table of Contents v List of Tables ix List of Figures xii List of Acronyms xx Glossary xxi 1 Introduction 1 1.1 Overview of transcriptional regulation of genes . 1 1.2 Discovery of X-box motifs and RFX genes . 2 1.3 More recent efforts to identify RFX genes, X-box motifs, and ciliary genes . 3 1.4 RFX genes in nematodes . 4 1.5 Overview of cilia and ciliary components/genes . 5 1.6 Ciliopathies . 8 1.7 Thesis aims and organization . 9 2 Development of a bioinformatics pipeline for annotating ciliary genes and identifying X-box motifs 13 2.1 Introduction . 13 2.2 Criteria for a high-confidence ciliary gene set . 13 2.3 Searching for ciliary gene orthologs in nematode species . 17 2.4 Annotation of 5’ start sites of ciliary genes . 17 2.5 Identification of X-box motifs . 18 2.5.1 Identification of typical X-box motifs using HMMER . 18 2.5.2 Identification of atypical X-box motifs using TFM-scan . 19 v 2.5.3 Identification of atypical X-box motifs using regular expressions . 20 2.5.4 Identification of atypical X-box motifs using manual inspection . 20 2.6 Reconstructing gene models with RNA-seq (TBLASTN) analysis . 21 2.7 Discussion . 21 3 Curation of ciliary genes in pathogenic and non-pathogenic nematodes 23 3.1 Introduction . 23 3.2 Phylogenetic analysis of nematodes . 23 3.3 Identification and annotation of ciliary gene orthologs . 28 3.3.1 Curation of arl-6 orthologs in nematodes . 28 3.3.2 Curation of bbs-1 orthologs in nematodes . 32 3.3.3 Curation of bbs-2 orthologs in nematodes . 35 3.3.4 Curation of bbs-4 orthologs in nematodes . 38 3.3.5 Curation of bbs-5 orthologs in nematodes . 41 3.3.6 Curation of bbs-8 orthologs in nematodes . 44 3.3.7 Curation of bbs-9 orthologs in nematodes . 48 3.3.8 Curation of che-2 orthologs in nematodes . 51 3.3.9 Curation of che-11 orthologs in nematodes . 54 3.3.10 Curation of che-13 orthologs in nematodes . 58 3.3.11 Curation of dyf-1 orthologs in nematodes . 61 3.3.12 Curation of dyf-2 orthologs in nematodes . 64 3.3.13 Curation of dyf-3 orthologs in nematodes . 68 3.3.14 Curation of dyf-5 orthologs in nematodes . 71 3.3.15 Curation of dyf-11 orthologs in nematodes . 75 3.3.16 Curation of dyf-13 orthologs in nematodes . 78 3.3.17 Curation of dyf-18 orthologs in nematodes . 82 3.3.18 Curation of dylt-2 orthologs in nematodes . 85 3.3.19 Curation of ift-20 orthologs in nematodes . 88 3.3.20 Curation of ifta-1 orthologs in nematodes . 91 3.3.21 Curation of mks-1 orthologs in nematodes . 94 3.3.22 Curation of mks-6 orthologs in nematodes . 97 3.3.23 Curation of mksr-1 orthologs in nematodes . 100 3.3.24 Curation of mksr-2 orthologs in nematodes . 103 3.3.25 Curation of nphp-2 orthologs in nematodes . 106 3.3.26 Curation of odr-4 orthologs in nematodes . 109 3.3.27 Curation of osm-1 orthologs in nematodes . 112 3.3.28 Curation of osm-5 orthologs in nematodes . 115 3.3.29 Curation of osm-6 orthologs in nematodes . 118 3.3.30 Curation of osm-12 orthologs in nematodes . 121 vi 3.3.31 Curation of tub-1 orthologs in nematodes . 124 3.3.32 Curation of xbx-1 orthologs in nematodes . 127 3.3.33 Summary of gene annotation efforts . 131 3.4 Tracing the missing ciliary genes through gene model reconstruction using RNA-seq analysis . 132 3.4.1 Reconstructing C. elegans osm-5 using C. elegans RNA-seq reads . 133 3.4.2 Reconstructing C. elegans osm-5 using a C. briggsae query . 135 3.4.3 Case study: Reconstruction of M. incognita osm-5 . 138 3.5 Discussion . 140 4 Identification and comparative analysis of X-box motifs in nematodes 141 4.1 Introduction . 141 4.2 Identification of putative X-box motifs in nematodes . 142 4.2.1 X-box motifs in the arl-6 promoter . 142 4.2.2 X-box motifs in the bbs-1 promoter . 144 4.2.3 X-box motifs in the bbs-2 promoter . 146 4.2.4 X-box motifs in the bbs-4 promoter . 148 4.2.5 X-box motifs in the bbs-5 promoter . 150 4.2.6 X-box motifs in the bbs-8 promoter . 152 4.2.7 X-box motifs in the bbs-9 promoter . 155 4.2.8 X-box motifs in the che-2 promoter . 156 4.2.9 X-box motifs in the che-11 promoter . 158 4.2.10 X-box motifs in the che-13 promoter . 159 4.2.11 X-box motifs in the dyf-1 promoter . 161 4.2.12 X-box motifs in the dyf-2 promoter .
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