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The Plasma Membrane Attachment of Remorin Microdomain Marker Proteins Is Stabilized by S-Acylation

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The Plasma Membrane Attachment of Remorin Microdomain Marker Proteins Is Stabilized by S-Acylation The plasma membrane attachment of Remorin microdomain marker proteins is stabilized by S-acylation Dissertation An der Fakultät für Biologie der Ludwig-Maximilians-Universität München Institut für Genetik vorgelegt von SEBASTIAN STEFAN ALOIS KONRAD aus München 2015 Die vorliegende Arbeit wurde im Bereich Genetik der Arbeitsgruppe von Herrn Prof. Dr. Thomas Ott angefertigt. Erstgutachter: Herr Prof. Dr. Thomas Ott Zweitgutachter: Herr Prof. Dr. Marc Bramkamp Tag der Abgabe: 23.06.2015 Tag der mündlichen Prüfung: 20.10.2015 Für meine Eltern Sometimes feeling small is necessary. It helps you grow. -Chris Burkard Eidesstattliche Versicherung Hiermit erkläre ich an Eides statt, dass ich die vorliegende Arbeit selbstständig, und ohne unerlaubte Hilfe von Dritten angefertigt habe. München, den ______________________________ (Sebastian Stefan Alois. Konrad) Erklärung Ich habe weder anderweitig versucht, eine Dissertation einzureichen oder mich einer Doktorprüfung zu unterziehen, noch habe ich diese Dissertation oder Teile derselben einer anderen Prüfungskommission vorgelegt. München, den ______________________________ (Sebastian Stefan Alois Konrad) Table of contents 1 Summary ............................................................................................................................................. 11 1.1 Summary .................................................................................................................................... 11 1.2 Zusammenfassung ................................................................................................................... 13 2 Introduction ....................................................................................................................................... 15 2.1 The plasma membrane is an interface for cell signalling .................................................... 15 2.1.1 Physical interactions and behaviour of plasma membrane components ..................... 16 2.2 Membrane compartmentalization .......................................................................................... 28 2.2.1 Lipid raft hypothesis............................................................................................................ 28 2.2.2 Extrinsic factors alter membrane compartmentalization ............................................... 30 2.2.3 Diversity of membrane domains ....................................................................................... 34 2.3 Remorins as a model to label membrane domains .............................................................. 39 3 Results ................................................................................................................................................. 43 3.1 Overview of Publications ........................................................................................................ 43 3.2 Publication I: Plasma Membranes are Sub-compartmentalized into a Plethora of Coexisting and Diverse Microdomains in Arabidopsis and Nicotiana benthamiana .......................... 45 3.3 Publication II: S-Acylation anchors remorin proteins to the plasma membrane but does not primarily determine their localization in membrane microdomains ....................................... 73 3.4 Publication III: Knockin’ on pollen’s Door: Live cell imaging of early polarization events in germinating Arabidopsis pollen ......................................................................................................... 99 3.5 Manuscript: Dissecting the multi-component assembly of a meso-scale membrane domain that controls host cell infection in Medicago truncatula ....................................................... 127 3.6 Current projects ...................................................................................................................... 171 3.6.1 Results ................................................................................................................................. 171 3.6.2 Material and Methods ....................................................................................................... 177 4 Discussion ........................................................................................................................................ 183 4.1 Membrane domains represent a new layer of compartmentalization ............................. 183 4.1.1 The role of Remorin lipidation ........................................................................................ 183 4.1.2 The diversity of Remorin labelled membrane domains opens new possibilities to investigate PM sub-compartmentalization .................................................................................. 186 4.1.3 The influence of the cytoskeleton and cell-wall on membrane dynamics ................. 187 4.1.4 Investigating the biological function of punctate membrane domains by active mislocalization of the immune receptor FLS2 within the PM ................................................. 189 5 Abbreviations ................................................................................................................................... 193 6 Danksagung ...................................................................................................................................... 195 7 References ........................................................................................................................................ 197 8 Curriculum Vitae ............................................................................................................................. 217 Additionally to the indicated publications, parts of the introduction and discussion of this work have been published in: Konrad, S. and Ott, T.(2015). Molecular principles of membrane microdomain targeting in plants. Trends in Plant Science. 20: 351–361. The manuscript underlying this publication was written by Sebastian S. A. Konrad I hereby confirm the above mentioned statements: ……………………… ………………………… Prof. Dr. Thomas Ott Sebastian S. A. Konrad Summary 1 Summary 1.1 Summary Prokaryotic as well as eukaryotic cells are always surrounded by a lipid bilayer, the plasma membrane. This membrane enables the cell to sustain a defined reaction volume and prevent the loss of metabolic products. Plasma membranes are special as they are areas of information exchange between the cell and its environment. They are complex multi-component systems composed of lipids and proteins. Non-random segregation of lipids as well as proteins into distinct areas, so-called membrane domains, was shown in various cell-biological model organisms. Up-to- now, the basic principles of membrane domain formation and the physiological relevance of these areas in plants have been unanswered. Using modern microscopy techniques, the occurrence of different classes of membrane domains has been demonstrated. Mesoscale microdomains are the most commonly observed pattern of membrane domains. Sizes, close to the resolution limit of advanced light microscopy are specific for this type of membrane domain. In this work, Remorin proteins of the model organism Arabidopsis thaliana, are established as marker proteins for different plant plasma membrane microdomains. Quantitative image analysis revealed that microdomains labelled by Remorin proteins differed in size, fluorescence intensity, circularity, domain density as well as in lateral diffusion behaviour. Comprehensive co-localization analysis demonstrated that phylogenetically closely related Remorins also labelled more similar types of membrane domains compared to those targeted by distantly related ones. This set of marker proteins provides a useful tool for further characterization of plant microdomains. Furthermore, the membrane binding mechanism of Remorin proteins was investigated during this work. The covalent binding of lipid anchors was shown to be a key feature of membrane attachment for Remorin proteins. Contrasting to other proteins, this so-called S-acylation reaction happens at the carboxy-terminal end of Remorins. Even though S-acylation often correlates with protein localization to membrane domains, it was shown that this post-translational modification does not enhance localization of Remorin proteins to microdomains. Thereby this work contributed important information on the constitution of membrane domain resident proteins in plants. In summary, this work has provided the basis for future studies to investigate the influence of protein sub-organization during signal transduction of extracellular stimuli. 11 Zusammenfassung 1.2 Zusammenfassung Pro- und eukaryotische Zellen sind grundsätzlich von einer Lipiddoppelschicht umgeben. Diese Biomembranen ermöglichen es einer Zelle, ein definiertes Reaktionsvolumen aufrecht zu erhalten und verhindern den Verlust von Syntheseprodukten zellulärer Stoffwechselreaktionen. Die eine Zelle umschließende Plasmamembran ist ferner ein Ort des regen Informationsaustausches zwischen der Zelle und ihrer Umgebung. Speziell diese Plasmamembran ist ein komplexes Mehrkomponentensystem aus Lipiden und Proteinen. Die Unterteilung von Plasmamembranen in voneinander abgegrenzte Bereiche, den sogenannten Membrandomänen, konnte in verschiedensten zellbiologischen Modellorganismen gezeigt werden. jedoch sind bis zum heutigen Tag die grundlegenden Mechanismen, welche zur Bildung dieser Bereiche beitragen, sowie deren physiologische Relevanz nicht abschließend geklärt. Anhand mehrzelliger Organismen, wie beispielswiese Pflanzen,
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