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Isolation of Eye Selector Genes in Two Bivalvian Molluscs, Arca Noae and Pecten Maximus

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Isolation of Eye Selector Genes in Two Bivalvian Molluscs, Arca Noae and Pecten Maximus Molecular insights into the eye evolution of bivalvian molluscs Inauguraldissertation Zur Erlangung der Würde eines Doktors der Philosophie vorgelegt der Philosophisch-Naturwissenschaftlichen Fakultät der Universität Basel von Lukas Emanuel Keller Sarmenstorf (AG) Ausgeführt unter der Leitung von: Prof. Dr. Walter J. Gehring Abteilung Zellbiologie Biozentrum der Universität Basel CH-4056 Basel 2006 Genehmigt von der Philosophisch-Naturwissenschaftlichen Fakultät auf Antrag der Herren Prof. W.J. Gehring Prof. H. Reichert Prof. M. Affolter Referent Koreferent Vorsitz ……………………. ……………………. ……………………. Basel, den ………………………. ………………………….. Prof. Dr. Hans-Peter Hauri Dekan Philosophisch-Naturwissenschaftlichen Fakultät Universität Basel 2 Summary The intention of my PhD project was to gain more insights into eye evolution and to provide further evidence for the recently proposed idea that all eye-types found in eumetazoans derive from a common Pax6-dependent proto-type eye (Gehring and Ikeo, 1999). To do so, we de- cided to focus on eyes found in bivalves. Two main reasons prompted us to investigate the molecular basis of bivalvian eye formation. In the first place, all major eye-types, the com- pound eye, consisting of numerous ommatidia, the camera eye with a single lens and the mir- ror eye with a reflecting mirror in the back of the eye, are found in bivalves. Hence, the occur- rence of different eye-types within the same phylogenetic class makes it very unlikely that these eyes arose as independent formations during evolution. A more elegant alternative is to assume that the compound-, camera-, and mirror eyes of clams evolved monophyletically from a common ancestral precursor. The second reason why we decided to investigate bival- vian eyes is their unusual anatomical position, the edge of the mantle. So far, molecular data and most prominently Pax6 expression were exclusively gathered from “cerebral eyes” of bi- laterians, with the only exception of the non-cerebral Hesse eyecups of the lancelet, which by the way do not show any Pax6 expression (Glardon et al., 1998). In this study we focused on two bivalvian species, Arca noae and Pecten maximus, representing the compound eye-type and the mirror eye-type, respectively. We isolated two genes, Pax6 and Six1/2, known to be high up in the genetic regulatory cascade of eye development, from Arca and Pecten. Our expression studies of Pax6 and Six1/2 support the idea that these two genes are necessary for the formation of the olfactory system throughout the animal kingdom. In contrast, we could not assign Pax6 and Six1/2 expression to the visual system with absolute certainty. In a second project, we isolated three opsin genes, one from Arca and two opsin genes from Pecten. A Go-coupled opsin was isolated from Pecten which was shown to be exclusively expressed in the rhabdomeric photoreceptor cells of the proximal retina. The second opsin gene isolated from Pecten and the opsin gene from Arca were shown to be expressed in various tissues, suggesting a putative role in the photic regulation of peripheral circadian clocks. Moreover, phylogenetic analysis indicate that each of these two opsin genes may constitute a novel opsin subfamily. 3 Acknowledgements I am deeply grateful to Professor Walter J. Gehring for giving me the opportunity to perform my Ph.D. thesis in his laboratory. I would like to thank him for his interest in my project and for his enthusiasm to work on such exotic animals like Arca noae and Pecten maximus. I would like to thank him especially for the many times he helped me to organize fresh Arca from Banyuls. Thanks a lot Walter. Special thanks to my supervisor committee Prof. W.J. Gehring, Prof. M. Affolter and Prof. H. Reichert. I am indebted to Makiko, Hiroshi and Robin who read and corrected this manuscript. Many thanks also to Hiroshi Suga who was a great help in many technical aspects. He not only taught me a lot about phylogenetic analysis but also invested many hours to generate alignments and phylogenetic trees. Special thanks goes to Makiko Seimiya who helped me to inject the flies and provided the basis to successfully induce ectopic eyes in Drosophila. I would also like to thank Paul Baumgartner who introduced me into molecular biology and always had an answer for tricky clonal problems. During my time as a diploma and PhD student I met a lot of people who contributed in one way or the other to my education. Especially I would like to thank Christopher Brink, Robin Vuilleumier, Veronique Charpignon, Frederic Prince, Paul Baumgartner, Raphael Fünfschilling, Greta Backhaus, Urs Kloter, Lydia Michaut, Nicole Grieder, Jorge Blanko, and Ursula Sauder for their help and friendship during these years. Many thanks also to all people that contributed to the nice atmosphere in the lab: Tobias Pauli, Tomoko Nagao, Sacha Glardon, Claudio Punzo, Serge Plaza, Daria Graziussi, Marina Beaufils, Yoshi Adachi, Georg Gentsch, Sina Henrichs, Bernadette Bruno, Karin Mauro, Gina Evora, Roland Kirchhofer, Patrick Tschopp, Stefan Wenmalm, Erica Oesch, Liliane Devaja, Ilias Charlafti, Polychronis 4 Dimitrakis, Daniel Felix, Christina Gonzales, Suzanne Flister and all the people I might have forgotten and all the members of the second floor. I’m deeply grateful for the love and support of Claudia and for her endless patience during these years. I would like to thank my whole family for their enormous support during my Ph.D. and for all the hours we spent together in Eriswil. The work presented in this thesis was supported by the Kantons of Basel and the Swiss National Science Foundation. 5 Table of contents Summary………………………………………………………………………..3 Acknowledgments………………………………………………………………4 Table of contents………………………………………………………………..6 I. Introduction..................................................................................................... 9 1. Pecten maximus................................................................................................................. 9 1.1 General description of Pecten maximus....................................................................... 9 1.2 Embryogenesis ........................................................................................................... 10 1.3 The scallop mirror eye................................................................................................ 13 1.4 Gills ............................................................................................................................ 16 2. Arca noae......................................................................................................................... 17 2.1 General description of Arca noae............................................................................... 17 2.2 Compound eyes in ark clams ..................................................................................... 19 3. Different eye-types in the animal kingdom .................................................................... 19 3.1 General comments...................................................................................................... 19 3.2 Pigment cup eyes........................................................................................................ 20 3.3 Pinhole eyes................................................................................................................ 21 3.4 Compound eyes.......................................................................................................... 21 3.5 The camera type eye................................................................................................... 22 4. Eye evolution ................................................................................................................... 24 5. Photoreception................................................................................................................. 27 5.1 Two different types of photoreceptor cells ................................................................ 27 5.2 Usage of distinct phototransduction pathways in rhabdomeric versus ciliary photoreceptors .................................................................................................................. 30 6. Genes involved in the genetic cascade of eye development ........................................... 31 6.1 The Pax Gene family.................................................................................................. 31 6.2 Pax6............................................................................................................................ 34 6.3 The Six family genes.................................................................................................. 42 7. The opsin gene family ..................................................................................................... 44 II. Material and Methods.................................................................................. 48 1. Molecular methods.......................................................................................................... 48 2. Collection of the animals ................................................................................................ 48 3. Preparation of genomic DNA ......................................................................................... 48 4. Isolation of mRNA and cDNA synthesis ........................................................................ 49 5. Cryosections....................................................................................................................
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