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Juan Sebastian Chahda ANALYSIS OF SCALING PROPERTIES OF EMBRYONIC MORPHOGEN GRADIENTS DURING DROSOPHILA EVOLUTION by JUAN SEBASTIAN CHAHDA Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy Biology Department CASE WESTERN RESERVE UNIVERSTIY August, 2015 CASE WESTERN RESERVE UNIVERSITY SCHOOL OF GRADUATE STUDIES We hereby approve the thesis/dissertation of JUAN SEBASTIAN CHAHDA candidate for the degree of Doctor of Philosophy *. Committee Chair Michael Bernard Committee Member Claudia Mieko Mizutani Committee Member Peter Harte Committee Member Jocelyn McDonald Committee Member Brian McDermott Date of Defense July 2nd 2015 *We also certify that written approval has been obtained for any proprietary material contained therein. 2 TABLE OF CONTENTS Table of Contents ………...…………………………………………………...… 1 List of Tables ...…… ……………………………………………..…………...… 4 List of Figures ….… .……………………………………………..…………...… 5 Acknowledgements …… ...……………………..………………..…………...… 6 List of Abbreviations … .…………………..………………..………...……...… 7 Abstract ………………… …..………………..…………………...…...……...… 8 Chapter I: Background and Significance …………………………………….. 10 1.1 Morphogenetic gradients specify cell fate in a concentration-dependent manner ……………………………………………………………………….. 10 1.2 The Dorsal/NF-κB gradient initially subdivides the Drosophila dorsal-ventral axis into mesoderm, neuroectoderm and ectoderm …………………….……. 16 1.3 The Dorsal/NF-κB and Dpp/BMP-4 morphogen gradients work together to pattern the neuroectoderm …………………………………………..….…… 21 1.4 The neuroblast map is heavily conserved across arthropods despite great differences in embryo size …………………………………………… ……. 24 1.5 Investigating the scaling of morphogenetic gradients ………… ..............… 27 1.6 Dorso-ventral scaling of germ layers in related Drosophila species ………..31 1.7 Mathematical modeling as a tool to test predictions of Dl gradient scaling during evolution …………………...… ................................................…….. 34 1.8 Research aims……………………………………………………….… …… 36 Chapter 2: Variation in the Dorsal Gradient Distribution is a Source for Modified Scaling of Germ Layers in Drosophila ……………………… ……. 37 Published in Chahda JS, Sousa-Neves R, Mizutani CM. Curr Biol. 2013 Apr 22;23(8):710-6. doi: 10.1016/j.cub.2013.03.031 2.1 Abstract ………………………………………………… ………………….. 38 2.2 Results and Discussion ……………………………..…… ………………… 38 2.2.1 Cross-species comparison of nuclear Dl protein levels reveals gradients of different shapes …………………………...………… …………………. 40 2.2.2 Mesodermal expansion does not rely on altered sna or twi sensitivity to Dl levels in sibling species ……………………………… ……………….... 41 2.2.3 Different gradients in the same scale of threshold levels reveal unique properties of scaling ………………………………… …………………. 42 1 2.2.4 The Dl gradient shape in D. melanogaster is sensitive to changes in nuclear size and packing …………………………… …………..……… 43 2.2.5 Fast evolution of the Dl gradient and maintenance of the neuroectoderm …………………………………………………………………………... 46 2.3 Materials and Methods ………………………………… …………………... 48 2.3.1 Fly stocks and genetic crosses ……………………… ……………….… 48 2.3.2 Measurements of egg size, nuclear number, size, and packing densities ………………………………………………………………………...… 49 2.3.3 Immunohistochemistry …………………………… ………………….... 50 2.3.4 Quantification of the Dl gradient ………………… ……………………. 52 2.4 Supplemental Information …………………………… .........................…… 52 2.4.1 Normalization of Dl gradient allows cross-species comparison …… ..… 52 2.4.2 Scoring of hybrid crosses and embryos with altered ploidy ………… … 53 2.4.3 Measurements of egg size, nuclear numbers, size, and packing densities …………………………………………………………………………... 54 2.4.4 Method for Dl gradient graph transformation based on data from hybrids ………………………………………………………………...………… 55 2.5 Tables and Figures ………………………………………………… .……… 57 2.6 Conclusions and future directions ………………………………… ……….. 71 2.6.1 Changes to the Dl Gradient Directly Alter Mesoderm Specification … .. 71 2.6.2 Conservation of the Neuroectoderm is Unaffected by Changes to the Dl Gradient ……………………………………………………………….... 72 Chapter 3: Modeling of the Dorsal Gradient across Species Reveals Interaction between Embryo Morphology and Toll Signaling Pathway during Evolution ………………………………………………………… ….... 74 Published in Ambrosi P*, Chahda JS*, Koslen HR, Chiel HJ, Mizutani CM. PLoS Comput Biol. 2014 Aug 28;10(8):e1003807. doi: 0.1371/journal.pcbi.1003807. * First co-authors 3.1 Abstract ……………………………………………………………… …….. 75 3.2 Introduction ………………………………………………………… ……… 76 3.3 Results ……………………………………………………………… …….... 80 3.3.1 Reconstruction of the Kanodia model reproduces the Dl gradient shape in some mutant conditions ………………………………………… ...…… 80 3.3.2 Simulation of nuclei numbers and size can reproduce ssm gradient, but not the gyn gradient ……………………………………… ………………… 82 3.3.3 Refinement of the parameter values reveals the embryo geometry plus Dl diffusion and export rates play major roles in the model reproduction of the gyn gradient ……………………………………… ………………… 85 2 3.3.4 Embryonic Morphology alone does not fully explain species-specific Dl gradient shapes ……………………………………… ………………..... 88 3.3.5 Modulating a small subset of parameters affecting the Toll signaling pathway can reproduce species-specific Dl gradients … ………………. 89 3.3.6 Analyses of another pair of closely related sibling species suggest evolutionarily shared mechanisms for Dl gradient formation … ….…… 91 3.3.7 Dl and Cact protein sequence comparisons of melanogaster subgroup species support predictions made by the model ……………… ……..…. 93 3.3.8 Model robustness and sensitivity analysis reveals non-linear interaction between species morphology modifications and other relevant parameters ………………………………………………………………………..…. 95 3.4 Discussion ………………………………………………………… …..…… 96 3.4.1 Dorsal scaling within and across species ……………………… ….…… 96 3.4.2 Model sensitivity analysis support evolution of Dl gradient by small additive changes in Tl regulation pathway …………………… ……….. 99 3.4.3 The Dl gradient model predicts changes in the Tl pathway in Drosophila species that are consistent to their phylogenetic relationships ……...….. 99 3.5 Material and Methods ……………………………………………………… 101 3.5.1 Fly stocks ……………………………………………………………..... 101 3.5.2 Gradient quantification and measurements of nuclear size …………..... 102 3.5.3 Reproduction and modification of the Kanodia model in Mathematica ..102 3.5.4 Dimensionalized model of the last nuclear cycle ……………………… 103 3.5.5 Model validation ………………………………………………………. 103 3.5.6 Fit calculation and confidence intervals …………………………..…… 104 3.5.7 Sequence comparison of the Dl and Cact in melanogaster subgroup species ………..………………………………………………………… 104 3.6 Acknowledgements ………………………………………………………… 105 3.7 Tables and Figures ………………………………………………………..... 106 3.8 Conclusions and future directions …………………………...……… ……. 118 3.8.1 The Dl import, export and diffusion rates are greater than previously thought ………………………………………………….……… …….. 118 3.8.2 Evolution within the Toll signaling pathway can account for species- specific Dl gradient distributions ……………………………… …..…. 119 Chapter 4: Discussion ………… .......................................………………...… 121 4.1 Dorsal gradient amplitude and distribution can explain species-specific tissue allocation along the dorsal-ventral axis ……………… ..…………….…… 121 4.2 Morphological traits and fast evolution in Toll signaling pathway reshape the Dorsal gradient ……………………...………………… ..………………… 124 Bibliography …………………………………………………… …………..... 129 3 LIST OF TABLES Table 1: Cross-Species Comparison of Embryo Size and DV Nuclei … …….… 57 Table 2: DV Nuclei in D. melanogaster WT, Haploid, and Triploid Mutants .....58 Table 3: Parameter values used in model simulations for D. melanogaster wild type and mutant conditions shown in Figures 10 and 11 ……………………... .106 Table 4: Selected parameter sets used in model simulations of Dl gradient for three different Drosophila species, D. busckii, D. simulans and D. sechellia ....107 Table 5: Selected parameter sets used in model simulations of Dl gradient for Drosophila yakuba and Drosophila santomea ……………………… ...............108 4 LIST OF FIGURES Figure 1: The French Flag Model for Positional Specification in the Embryo .....12 Figure 2: The morphogenetic Dl gradient activates target genes that cross regulate each other to specify the DV axis .........................................................................18 Figure 3: The Bicoid gradient scales along the AP axis and establishes a proportional segmentation pattern in embryos of different sizes ..........................30 Figure 4: Divergence in embryo size in related Drosophila species .....................33 Figure 5: The Distributions of Nuclei, Mesodermal Domains, and Dl Levels Changed across Species .........................................................................................59 Figure 6: Sensitivity of Mesodermal Gene Activation Is Identical among D. melanogaster Sibling Species ...........................................................................61 Figure 7: Drosophila Species Vary in Nuclei Size and Densities ..........................62 Figure 8: The Dl Gradient Is Modified by Nuclear Size and Packing Density .....64 Figure 9: Dl gradient model rationale ..................................................................104 Figure 10: The Dl gradient is modulated by changes in nuclear size and density110 Figure 11: Comparison between experimental data and model output................111 Figure 12: Changes in kDeg allow the reproduction of the Dl gradient
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