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Patterns in Teleost Photoreceptor Organization: A PATTERNS IN TELEOST PHOTORECEPTOR ORGANIZATION: A CHARACTERIZATION OF BASAL BODY POSITIONING IN ZEBRAFISH PHOTORECEPTORS AND VARIATIONS IN SWORDTAIL PHOTORECEPTOR MOSAICS A Dissertation by MICHELLE BRITTANY RAMSEY Submitted to the Office of Graduate and Professional Studies of Texas A&M University in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY Chair of Committee, Gil G. Rosenthal Committee Members, Brian D. Perkins Hubert O. Amrein Michael S. Smotherman Head of Department, Thomas D. McKnight May 2014 Major Subject: Biology Copyright 2014 Michelle Brittany Ramsey ABSTRACT Vertebrate vision is enabled by light-sensitive photoreceptors arranged in a plane in the retina. This study investigates two aspects of this arrangement: 1) positioning of basal bodies within photoreceptors, and 2) positioning of photoreceptors themselves. First, the planar cell polarity of basal bodies, and therefore cilia, is often critical for proper cilia function and is controlled by the planar cell polarity (PCP) pathway. Cilia planar positioning in vertebrate photoreceptors, however, has not been characterized. Because zebrafish photoreceptors form an organized, well-characterized mosaic, they are an ideal system to address photoreceptor basal body positioning. Second, swordtail fish are frequently studied to investigate visually-mediated social behaviors such as mate choice and how these influence evolution. However, less is known about the morphology of their photoreceptor mosaic and how this mosaic influences behavior. Therefore, characterization of the swordtail photoreceptor mosaic is an important step in understanding this relationship between physiology and behavior. In this study, immunohistology is used to characterize cryosectioned flatmounted retinas from zebrafish and swordtails with various genetic, behavioral, and environmental backgrounds. The results of this study reveal that in adult zebrafish retinas, the basal bodies of red-, green-, and blue-sensitive cone photoreceptors localize asymmetrically on the cell edge nearest the optic nerve. In contrast, no patterning is in the basal bodies of ultraviolet-sensitive cones, of rod photoreceptors, or of larval cones. Both rod loss and ii UV-light addition do not affect cone basal body patterning. Darkness during development leads to bimodality of basal bodies. These results suggest that, after the transition to the adult mosaic, a cellular mechanism involving cell-cell contact, consistent with the PCP pathway, regulates photoreceptor basal body positioning. The results of this study also reveal that the swordtails Xiphophorus malinche, Xiphophorus birchmanni, and their hybrids exhibit an organized square mosaic, although some variations in this pattern exist, including between males and females. As square mosaics have been correlated with sensitivity to changes in light polarization, this warrants future studies in swordtail polarization vision, which may play an important role in visually-mediated behavior. Also, changes in the photoreceptor mosaic might have explanatory power for changes in visually-mediated behavior. iii ACKNOWLEDGEMENTS I am very grateful for the generous support I have received from Gil Rosenthal and from Brian Perkins during my time at Texas A&M. They have each played an important role in my intellectual development. I am thankful for all the opportunities they have given me and everything I have learned from them. I am also thankful for all the other faculty members at A&M, especially for Hubert Amrein, Mike Smotherman, Bruce Riley, Deb Bell-Pedersen, and Arne Lekven, who have guided me at various stages of my dissertation research. I sincerely appreciate all the assistance I have received from lab members, other graduate students, undergraduate students, and staff at Texas A&M. I am thankful for all I have learned from my peers and from my students. For Chapter II, I thank Brian Perkins for his valuable contributions to study design, to data analysis, and to drafting and revising the manuscript. I thank my committee and anonymous reviewers for their helpful comments. I am very grateful to James Fadool and his group for assistance with observing the photoreceptor mosaic. I also thank James Fadool, Sue Brockerhoff, David Hyde, Ann Morris, and Brian Link for the gifts of animals and reagents. This research was supported by NIH Grant EY017037 to Brian Perkins. For Chapter III, I thank Gil Rosenthal and Brian Perkins for their valuable contributions to study design and analysis, and I thank them and the rest of my committee for their helpful comments for this chapter. I am grateful to Carmen Montaña, Kirk Winemiller, and Kevin Conway for their assistance catching and iv identifying red shiners. This research was supported by NSF Grant IOS-0923825 to Gil Rosenthal and NIH Grant EY017037 to Brian Perkins. For Chapter IV, I thank Gil Rosenthal for his valuable contributions to study design and analysis, and I thank him and the rest of my committee for their helpful comments for this chapter. I thank Rongfeng Cui and Michael Stanley for their work on the behavioral trials. I thank Pablo Declos for assistance with the statistical analysis. I am grateful to Pablo Delclos, Gastón Jofre, Dan Powell, Mattie Squire, and undergraduates from the Rosenthal lab for fish collection and fish care. I thank Brian Perkins for histology supplies and reagents, and I thank Bruce Riley for cryostat use. This research was supported by NSF Grant IOS-0923825 to Gil Rosenthal. My accomplishments at Texas A&M would have been impossible without the previous investments others have made in my life for which I will always be grateful. My past teachers and professors have all contributed in a variety of ways to my intellectual growth. Finally, and most importantly, the unwavering support I have received from my husband, parents, family, and friends has been an irreplaceable encouragement to me. “If I have seen further it is by standing on the shoulders of Giants." Sir Isaac Newton (1676) v NOMENCLATURE 4C12 antibody that labels zebrafish rod photoreceptors AOSLO Adaptive Optics Scanning Laser Ophthalmoscopy CFP cyan fluorescent protein DAPI nuclear stain 4,6-diamidino-2-phenlindole dihydrochloride dfp days post fertilization DMSO dimethyl sulfoxide ERG electroretinogram GFP green fluorescence protein MSP microspectrophotometry OMR optomotor response ON overnight or (in figures) optic nerve ONL outer nuclear layer PBS phosphate buffered solution PBSTD 0.1% TWEEN 20 and 0.1% DMSO in PBS PCP planar cell polarity PFA paraformaldehyde red shiner Cyprinella lutrensis RPE retinal pigment epithelium RT room temperature RT-PCR reverse transcription polymerase chain reaction vi s.d. standard deviation swordtail fish within the genus Xiphophorus TFM tissue freezing medium UV ultraviolet X. birchmanni Xiphophorus birchmanni X. malinche Xiphophorus malinche XOPS-GFP transgenic zebrafish line Tg(XlRho:EGFP)fl1 XOPS-mCFP transgenic zebrafish line Tg(XlRho:gap43-CFP)q13 zebrafish Danio rerio Zpr-1 antibody that labels zebrafish red-/green-sensitive double cones vii TABLE OF CONTENTS Page ABSTRACT .......................................................................................................................ii ACKNOWLEDGEMENTS .............................................................................................. iv NOMENCLATURE .......................................................................................................... vi TABLE OF CONTENTS ............................................................................................... viii LIST OF FIGURES ............................................................................................................ x LIST OF TABLES ......................................................................................................... xiii CHAPTER I INTRODUCTION ...................................................................................... 1 Photoreceptors ................................................................................................................ 1 Planar cell polarity ......................................................................................................... 5 Planar cell polarity defects and ciliopathies ................................................................... 8 Retinomotor movements .............................................................................................. 12 Zebrafish model system ............................................................................................... 14 Teleost photoreceptor mosaics ..................................................................................... 16 Swordtail model system ............................................................................................... 19 Vision in swordtails ...................................................................................................... 22 Hybridization and hybrid breakdown ........................................................................... 23 Sensory dysfunction ..................................................................................................... 24 Summary ...................................................................................................................... 27 CHAPTER II BASAL BODIES EXHIBIT POLARIZED POSITIONING IN ZEBRAFISH CONE PHOTORECEPTORS ................................................................... 28 Overview.....................................................................................................................
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