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Genome Duplication and the Evolution of Gene Clusters in Teleost Fishes

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Genome Duplication and the Evolution of Gene Clusters in Teleost Fishes Genome duplication and the evolution of gene clusters in teleost fishes Dissertation zur Erlangung des akademischen Grades des Doktors der Naturwissenschaften (Dr. rer. nat.) an der Universität Konstanz, Mathematisch-naturwissenschaftliche Sektion Fachbereich Biologie vorgelegt von Dipl. Biol. Simone Högg Konstanz, März 2007 Prüfungskommission: Prof. Iwona Adamska Prof. Axel Meyer Prof. Yves Van de Peer Acknowledgements First, I would like to thank my advisor Prof. Axel Meyer for giving me the opportunity to complete a doctoral degree in his lab. During my undergraduate as well as my graduate time in his group, I acquired a wide basis of knowledge also exceeding my direct work focus. I particularly want to thank Walter Salzburger, who was always helpful for advice on lab work, but also did not get tired of reading single pieces of this thesis and giving valuable comments and improvements. I am grateful to my past and current colleagues of the Meyer Lab and in particular I want to thank, in no particular order, Dirk Steinke, Nils Offen, Ylenia Chiari, Arie van der Meijden, Jing Luo, Ingo Braasch, Kai Stölting, Nicol Siegel, Dave T. Gerrard, and Gerrit Begemann for support and advice for lab work as well as interesting discussion. I also thank Prof. Dr. Miguel Vences for providing me interesting side projects, which are not subject of this thesis. Beside the work times in the lab, I am very grateful to many of my colleagues, who became good friends during our time in the Meyer Lab and shared with me many happy hours. Especially I would like to mention here the Friday-afternoon-tea group and the Badminton people. I especially thank my parents who always supported me in continuing my interest in science and gave me fresh motivation to continue this work to the end. I am also grateful to Jochen Schönthaler, who made the last year of my PhD so much more enjoyable. Thank you for showing so much patience. 2 Table of contents General Introduction................................................................................................................ 4 Genome evolution in actinopterygian fish .......................................................................... 5 Gene duplication in housekeeping pathways ...................................................................... 7 Hox clusters and gene duplication....................................................................................... 9 Evolution of a non-developmental gene cluster ................................................................ 10 East-African cichlids: a natural mutagenesis screen? ....................................................... 11 ParaHox paralogons in teleost fish.................................................................................... 13 Hox cluster and regulatory evolution in teleost fish.......................................................... 14 1. Three rounds (1R/2R/3R) of genome duplications and the evolution of the glycolytic pathway in vertebrates.................................................................................................. 16 1.1. Abstract ................................................................................................................. 16 1.2. Background ........................................................................................................... 17 1.3. Results ................................................................................................................... 20 1.4. Discussion ............................................................................................................. 27 1.5. Conclusion............................................................................................................. 33 1.6. Methods................................................................................................................. 34 2. Hox clusters as models for vertebrate genome evolution.............................................. 38 2.1. Hox genes – quo vadis?......................................................................................... 38 2.2. Hox-cluster evolution in vertebrates ..................................................................... 40 2.3. The fish-specific genome duplication (3R) and Hox-cluster evolution ................ 40 2.4. Evolution of non-coding sequences in gnathostome Hox clusters........................ 41 2.5. Concluding remarks .............................................................................................. 43 3. Phylogenomic analyses of KCNA gene clusters in vertebrates .................................... 45 3.1. Abstract ................................................................................................................. 45 3.2. Background ........................................................................................................... 46 3.3. Results ................................................................................................................... 48 3.4. Discussion ............................................................................................................. 56 3.5. Conclusion............................................................................................................. 59 3.6. Methods................................................................................................................. 59 4. Comparative genomics of ParaHox clusters of teleost fishes: gene cluster breakup and the retention of gene sets following whole genome duplications................................. 62 4.1. Abstract ................................................................................................................. 62 4.2. Background ........................................................................................................... 63 4.3. Results and Discussion.......................................................................................... 68 4.4. Conclusions ........................................................................................................... 80 4.5. Methods................................................................................................................. 81 5. Comparative phylogenomic analyses of teleost fish Hox gene clusters: lessons from the cichlid fish Astatotilapia burtoni .................................................................................. 85 5.1. Abstract ................................................................................................................. 85 5.2. Introduction ........................................................................................................... 86 5.3. Materials and Methods .......................................................................................... 89 5.4. Results ................................................................................................................... 92 5.5. Discussion ........................................................................................................... 103 5.6. Conclusions ......................................................................................................... 106 Summary ............................................................................................................................. 107 Zusammenfassung............................................................................................................... 110 Results produced by collaborators ...................................................................................... 114 Literature cited .................................................................................................................... 115 Appendix ............................................................................................................................. 138 3 General Introduction General Introduction Modern biology in general and molecular biology in particular have contributed substantially to our understanding of the basic processes of life on earth. The ability to determine DNA and protein sequences as well as three-dimensional structures of proteins, and the functional consequences of changes at the amino acid level, provide us with a plethora of information. For the last fifty years, first amino acid, and later also DNA, sequences have been used for the inference of phylogenetic relationships among organisms (Zuckerkandl and Pauling 1965), resolving unknown branches in the tree of life. As a consequence, it is now possible to reconstruct the evolution of biological structures and morphological and behavioral characters, and to study adaptation at the molecular level. Advances in sequencing technologies as well as in computer algorithms made it possible to sequence the complete genomes of model organisms such as the fruit fly ( Drosophila melanogaster ) (Adams et al. 2000) and a nematode ( Caenorhabditis elegans ) (C. elegans Sequencing Consortium 1998) in the beginning, followed by many more species including human ( Homo sapiens ) (Lander et al. 2001; Venter et al. 2001), mouse ( Mus musculus ) (Waterston et al. 2002), rat ( Rattus norvegicus ) (Gibbs et al. 2004), frog ( Xenopus tropicalis ) (Joint Genome Institute, http://genome.jgi-psf.org/Xentr4/Xentr4.home.html), zebrafish ( Danio rerio ) and two pufferfish species ( Takifugu rubripes (Aparicio et al. 2002) , and Tetradodon nigroviridis (Jaillon et al. 2004)). Obviously, this list is far from complete, and there are, for example, many more mammalian taxa in progress. The first
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