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Clasp: a Microtubule-Based Integrator of the Hormone-Mediated Transitions from Cell Division to Elongation in Arabidopsis Thaliana

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Clasp: a Microtubule-Based Integrator of the Hormone-Mediated Transitions from Cell Division to Elongation in Arabidopsis Thaliana CLASP: A MICROTUBULE-BASED INTEGRATOR OF THE HORMONE-MEDIATED TRANSITIONS FROM CELL DIVISION TO ELONGATION IN ARABIDOPSIS THALIANA by YUAN RUAN B.Sc., Shandong Normal University, 2005 M.Sc., Shandong Normal University, 2008 A THESIS SUBMITTED IN PARTIAL FULFILMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY in The Faculty of Graduate and Postdoctoral Studies (Botany) THE UNIVERSITY OF BRITISH COLUMBIA (Vancouver) October 2015 © Yuan Ruan, 2015 ABSTRACT Microtubules have long been known to play a vital role in plant growth and development, which is a complex process and needs to be regulated by both environmental and endogenous hormonal signals. CLASP, an important microtubule- associated protein, has been shown to be involved in both cell division and expansion. The major goal of my thesis was to explore the function of CLASP in new pathways as well as to identify novel factors that are responsible for its function and distribution. Yeast 2-hybird analysis done independently by two of our collaborators indicated that CLASP interacts strongly with the endocytic membrane-associated protein SNX1. SNX1 had been implicated in the intracellular trafficking of the auxin efflux carrier PIN2. We proved the direct interaction between CLASP and SNX1 by colocalization and BiFC using live cell imaging and we found that clasp-1 mutants have an altered distribution pattern of SNX1, reduced abundance of PIN2 and a series of auxin-related phenotypes such as dwarfism, enhanced lateral branching and aberrant auxin distribution. Drug- induced microtubule disruption caused clasp-1-like defects on PIN2 stability. This study illustrated the role of CLASP and microtubules in polar auxin transport and auxin signalling pathway. Previous studies revealed a cross-talk between auxin and brassinosteroids. I found that the two major transcription factors in the brassinosteroid signalling pathway directly target the CLASP promoter to repress its transcription. Reduced CLASP expression is correlated with a transverse orientation of cortical microtubules in root meristematic cells, switching them from division to differentiation. Also CLASP and microtubules stabilize the BR receptor BRI1 by preventing its degradation, a similar mechanism as for PIN2. This research highlights the importance of CLASP in BR-modulated meristem cell identity and the potential role of CLASP as a node between auxin and BR pathways. I carried out an immunoprecipitation experiment to identify putative CLASP interactors and obtained TRM19. Further analysis failed to confirm a direct interaction but suggested that TRM19 is a microtubule-associated protein. Its high expression in dividing cells is consistent with prior report that it functions in PPB formation during the cell cycle. ii PREFACE Chapter 1 has been published as: Ruan, Y., and Wasteneys, G.O. (2014) CLASP: a microtubule-based integrator of the hormone-mediated transitions from cell division to elongation. Curr Opin Plant Biol. 22: 149-158 © Copyright Elsevier Ltd., 2014 (http://www.journals.elsevier.com/current-opinion-in-plant-biology/). Prof. Geoffrey Wasteneys and Yuan Ruan conceived the idea. Yuan Ruan prepared the figures and wrote the manuscript. Chapter 2 has been published as: Ambrose, C., Ruan, Y., Gardiner, J., Tamblyn L.M., Catching, A., Kirik, V., Marc, J., Overall, R., and Wasteneys, G.O. (2013) CLASP interacts with soring nexin 1 to link microtubules and auxin transport via PIN2 recycling in Arabidopsis thaliana. Dev Cell. 24: 649-659 © Copyright Elsevier Inc., 2013 (http://www.journals.elsevier.com/developmental-cell/). Yeast 2-hybrid screens were conducted separately by our collaborators Dr. John Gardiner at the University of Sydney and Dr. Viktor Kirik at Illinois State University and both identified SNX1. Dr. John Gardiner also predicted and created the 3D structure of the interacting site on SNX1. DR5:GUS analysis was performed by Dr. Viktor Kirik. An undergraduate student, Laura Tamblyn, prepared the RNA samples for RT-PCR. Yuan Ruan carried out BiFC, GFP- SNX1134-219 reporter experiments, analyzed SNX1-GFP in WT and clasp-1, and tracked SNX1-RFP vesicle trajectories. Yuan Ruan also wrote the corresponding materials and methods section. Dr. Chris Ambrose did most of the remaining experiments and processed the data. This work was done under the supervision of Prof. Geoffrey Wasteneys. Chapter 3 has been prepared as a manuscript: Ruan, Y., Ambrose, C., and Wasteneys, G.O. (2015) CLASP modulates its own transcription via brassinosteroid signalling to drive stem cell differentiation in plants. Yuan Ruan and Prof. Geoffrey Wasteneys designed the research. Yuan Ruan performed the experiments, processed the data, prepared figures and wrote the manuscript. For Chapter 4, Prof. Geoffrey Wasteneys and Yuan Ruan designed the research. Yuan Ruan performed the experiments and analyzed the data. iii TABLE OF CONTENTS ABSTRACT ....................................................................................................................... ii PREFACE ......................................................................................................................... iii TABLE OF CONTENTS ................................................................................................. iv LIST OF TABLES ........................................................................................................... vii LIST OF FIGURES ....................................................................................................... viii LIST OF ABBREVIATIONS .......................................................................................... ix ACKNOWLEDGEMENTS ........................................................................................... xii CHAPTER 1: INTRODUCTION .................................................................................... 1 1.1 Meristem maintenance and plant development .................................................... 1 1.2 Hormones, auxin transport and meristem maintenance ..................................... 1 1.3 Auxin-driven microtubule entrainment ................................................................. 4 1.4 Cytoskeleton control of auxin levels through PIN endocytosis ........................... 6 1.5 Microtubule control of cell division and its link to cellular geometry ................ 8 1.6 The transition to cell division ............................................................................... 10 1.7 Conclusions and future directions ........................................................................ 13 1.8 Thesis objectives .................................................................................................... 15 CHAPTER 2: CLASP INTERACTS WITH SORTING NEXIN 1 TO LINK MICROTUBULES AND AUXIN TRANSPORT VIA PIN2 RECYCLING IN ARABIDOPSIS THALIANA ........................................................................................... 16 2.1 Introduction ........................................................................................................... 16 2.2 Results ..................................................................................................................... 17 2.2.1 SNX1 interacts with CLASP ............................................................................ 17 2.2.2 Central region between PHOX and BAR domains of SNX1 confers interaction with CLASP ............................................................................................................... 18 2.2.3 CLASP686-779 interacts with SNX1 .................................................................... 20 2.2.4 CLASP stabilizes SNX1 endosomes ................................................................. 21 2.2.5 SNX1 endosomes associate with CLASP and MTs .......................................... 24 iv 2.2.6 SNX1 vesicles form dynamic clusters that associate with GFP-CLASP ......... 27 2.2.7 clasp-1 mutants exhibit enhanced PIN2 degradation but retain PIN2 polar distribution ................................................................................................................. 29 2.2.8 MTs inhibit degradation of PIN2 to facilitate recycling ................................... 32 2.2.9 clasp-1 mutants exhibit auxin-related phenotypes ............................................ 33 2.3 Discussion ............................................................................................................... 37 2.4 Methods .................................................................................................................. 39 2.4.1 Plant materials and growth conditions .............................................................. 39 2.4.2 Microscopy and image analysis ........................................................................ 39 2.4.3 Drug treatments ................................................................................................. 40 2.4.4 Yeast Two-hybrid analysis ................................................................................ 40 2.4.5 RNA extraction following hormone treatments ................................................ 41 2.4.6 BiFC analysis .................................................................................................... 42 2.4.7 Immunofluorescence of PINs in roots .............................................................. 43 CHAPTER 3: A MICROTUBULE-ASSOCIATED CLASP-BRI1-BZR1/2 FEEDBACK LOOP MODULATES BRASSINOSTEROID-DEPENDENT ROOT DEVELOPMENT IN ARABIDOPSIS THALIANA ....................................................
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