'A Theoretical and Experimental Study of Cell Specification in The

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'A Theoretical and Experimental Study of Cell Specification in The Zurich Open Repository and Archive University of Zurich Main Library Strickhofstrasse 39 CH-8057 Zurich www.zora.uzh.ch Year: 2013 A theoretical and experimental study of cell specification in the female gametophyte Lituiev, D S Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-89950 Dissertation Originally published at: Lituiev, D S. A theoretical and experimental study of cell specification in the female gametophyte. 2013, University of Zurich, Faculty of Science. ATHEORETICAL AND EXPERIMENTAL STUDY OF CELL SPECIFICATION IN THE FEMALE GAMETOPHYTE Dissertation zur Erlangung der naturwissenschaftlichen Doktorwürde (Dr. sc. nat.) vorgelegt der Mathematisch-naturwissenschaftlichen Fakultät der Universität Zürich von Dmytro Sergiiovycˇ Lituiev aus der Ukraine Promotionskomitee Prof. Dr. Ueli Grossniklaus (Leitung der Dissertation) Prof. Dr. Enrico Martinoia Prof. Dr. Barbara Hellriegel Dr. Bruno Müller Zürich 2013 Typeset with LATEX Copyright c 2013 by Dmytro S. Lituiev, University of Zürich Contents Curriculum Vitæ .........................................VII Zusammenfassung .........................................IX Abstract ............................................... XI Preface ................................................XIII Introduction ............................................. 1 0.1 Morphology of the female gametophyte in flowering plants . 1 0.2 Patterning in the female gametophyte of flowering plants through the prisms of theoretical paradigms (mini-review) .................... 3 0.2.1 Introduction ............................... 3 0.2.2 Classical paradigms of patterning ................... 5 0.2.3 Sorting out ............................... 5 0.2.4 In pursuit of factors deterimining positional information in develop- ing female gametophyte ........................ 5 0.2.5 Combinatorial and dynamic nature of positional information . 7 0.2.6 Robustness as a measure of (theoretical) success .......... 9 0.2.7 What first: Positioning or Specification . 10 0.2.8 Conclusion and Outlook ........................ 11 0.3 Auxin and its role in plant morphogenesis . 13 0.3.1 Morphogensis in plants and phytohormones: A historical overview . 13 0.3.2 Role of auxin and its polar transport in plant morphogensis . 14 1 Theoretical and experimental evidence indicates that there is no detectable auxin gradient in the angiosperm female gametophyte (Development paper) .................................. 19 1.1 Introduction ................................... 21 1.2 Results ...................................... 22 1.2.1 Mathematical modelling shows that only shallow auxin gradients can be maintained in FGs ....................... 22 1.2.2 PGP19 and AUX1 auxin carriers are expressed in the Arabidopsis FG. 22 1.2.3 Measures of gradient steepness .................... 24 1.2.4 Simulation of the model in one dimension . 24 III Contents 1.2.5 The theoretically achievable gradient of auxin cannot provide a suffi- ciently robust readout of positional information for cell specification ...................................... 28 1.2.6 Microscopy analyses of auxin activity in Arabidopsis and maize ovules reveal no auxin activity inside the FG . 33 1.2.7 Sporophytic non-cell-autonomous effects may explain cell fate changes in the FG ................................ 35 1.3 Discussion ................................... 36 1.4 Materials and Methods ............................. 40 Appendix to the Development paper ........................ 46 2 The role of auxin in the female gametophyte of Arabidopsis thaliana – a modelling approach ................................. 73 2.1 Introduction ................................... 75 2.2 Model formulation ............................... 76 2.2.1 General assumptions .......................... 76 2.2.2 Regime 1: External auxin source (influx) . 77 2.2.3 Regime 2: Localized synthesis of auxin . 77 2.2.4 Regime 3: Localized degradation of auxin . 78 2.2.5 Regime 4: Efflux of auxin ....................... 78 2.2.6 Regime 5: Auxin re-distribution by transmembrane fluxes . 78 2.2.7 Approximation of female gametophyte geometry in two dimensions 78 2.2.8 Measure of the gradient steepness ................... 79 2.3 Analytical and numerical results ........................ 79 2.3.1 Parameter values ............................ 79 2.3.2 Analytical solution in one dimension . 81 2.3.3 Numerical simulation of two-dimensional model . 82 2.3.4 Error contributed by the quasi steady-state assumption . 83 2.3.5 Sensitivity analysis ........................... 84 2.4 Discussion .................................... 86 Conclusion and Outlook .................................... 99 .1 Conclusion .................................... 99 .2 Outlook .....................................101 References ..............................................103 Appendices .............................................115 IV Contents Appendix 1. Diffusion, Transport, and Reactions: Physical Basis, Ana- lytical and Numerical Techniques . 115 A1.1 Simulation of diffusion, transport, and reactions in developmental biology . 115 A1.1.1 Methods of spatio-temporal simulation for physico-chemical biology 115 A1.2 Physical Basis of Diffusion and Transmembrane Transport . 116 A1.3 Analytical solution of partial differential equations . 117 A1.3.1 Method of Green’s functions . 117 A1.3.2 Method of Fourier series . 120 Appendix 2: Supplementary material to the chapter 2 (modelling paper) 123 A2.1 Formulation of the model in natural dimensions and rescaling . 123 A2.1.1 Equations for variables in natural units . 123 A2.1.2 Regime 4 ................................124 A2.1.3 Rescaling scheme ............................124 A2.1.4 Parameter interdependence . 124 A2.2 A model for carrier-independent transmembrane fluxes due to auxin disso- ciation ......................................126 A2.3 A general inter-compartmental flux model for estimation of flux parameters 128 A2.4 Estimation of auxin degradation rate . 136 Appendix 3. Inference Algorithm for Mutation Mapping with High- Throughput Sequencing ................................139 A3.1 Introduction ...................................140 A3.1.1 Background ...............................140 A3.1.2 Aim ...................................140 A3.1.3 Experimental Procedure: Crosses and Selection . 140 A3.2 Results ......................................141 A3.2.1 Graph Model ..............................141 A3.2.2 Probability Assignment . 141 A3.2.3 Simulator ................................142 A3.2.4 Data and Preliminary Results . 142 A3.3 Open Questions and Outlook . 143 A3.4 Acknowledgements ...............................143 A3.5 References for Appendix 3 . 144 Appendix 4. A tool for user-assisted tracking of the pollen tube tip . 145 A4.1 Background ...................................145 A4.2 Algorithm ....................................145 A4.3 Outlook .....................................151 V Contents A4.4 References for Appendix 4 . 151 Appendix 5: ANXUR Receptor-Like Kinases Coordinate Cell Wall In- tegrity with Growth at the Pollen Tube Tip via NADPH Oxidases 153 Appendix 6: A Robust and Sensitive Synthetic Sensor to Monitor the Transcriptional Output of the Cytokinin Signaling Network in Planta ..................................................171 VI Curriculum Vitæ Personal Data Surname Lituiev Given name Dmytro Patronymic Segiiovyč Date of birth September 9, 1986 Place of Birth Donetsk, Ukraine Education 2001 — 2003 High school Lyceum of the Donetsk National University, Ukraine 2003 — 2007 Undergraduate Taras Shevchenko National University of Kyiv, studies Ukraine 2007 — 2009 Master studies National University of ‘Kyiv-Mohyla Academy’, Ukraine 2009 Master thesis Development and characterization of monoclonal (Hons) antibodies against human sodium-phosphate cotransporter NaPi2b. (wth Prof. Dr. Valery Filonenko and Dr. Ramziya Kiyamova) 2009 — 2013 Doctoral University of Zürich, Switzerland studies (wth Prof. Dr. Ueli Grossniklaus) Zusammenfassung In Blütenpflanzen ist der weibliche Gametophyt ein Teil der Samenanlage. Nach der Bestäubung und Befruchtung der weiblichen Gameten im Gametophyten entwickelt sich ein Same. In den meisten Pflanzen entwickelt sich der siebenkernige weibliche Gametophyt aus einer einkernigen Zelle. Obwohl viele Einzelheiten über die Entwicklung des weiblichen Gametophyten bekannt sind, kann man sie kaum so zusammenfassen, daßsie ein klares Bild ergeben. Versuche an der Modellpflanze Ackerschmalwand (Arabidopsis thaliana) führten vor Kurzem zu einer Behauptung, die das Problem umfassend erklären sollte. Angeblich soll das Pflanzenhormon Auxin das Schicksal der Zellen des weiblichen Game- tophyten bestimmen. Im vorliegenden Werk gehe ich dieser Hypothese nach. Zuerst ging ich an diese Hypothese durch Zusammenstellung eines mathematischen Modells heran, welches die früher vorgeschlagenen Faktoren zur Unterhaltung des Auxingradienten aufn- immt. Dieses Model samt Hilfsexperimenten machte deutlich, daß früher unberücksichtigte Faktoren, wie die Hemmung der Diffusion durch die grosse Vakuole des weiblichen Game- tophyten und der Transport von Auxin durch Membranen zur Entstehung des Gradienten beitragen und ihn steiler machen können. Dahingegen führen die effektiven Raten des Auxin-Abbaus und der Auxin-Diffusion zu einem Gradienten mit einer Konzentrationsdif- ferenz von nur 3.21 % zwischen den Polen. Weiterhin zeigte ich, daß bei einer Schwankung der Auxinzufuhr von mehr als 3.31% die Differenzierung der Zelltypen, die durch einen solchen
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