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MUCILAGE-RELATED Genes Facilitate the Biosynthesis of Cell Wall Polysaccharides

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MUCILAGE-RELATED Genes Facilitate the Biosynthesis of Cell Wall Polysaccharides MUCILAGE-RELATED Genes Facilitate the Biosynthesis of Cell Wall Polysaccharides Von der Fakultät für Mathematik, Informatik und Naturwissenschaften der RWTH Aachen University zur Erlangung des akademischen Grades eines Doktors der Naturwissenschaften genehmigte Dissertation vorgelegt von Master of Science Cătălin Voiniciuc aus Botoșani, România Berichter: Universitätsprofessor Dr. Björn Usadel Universitätsprofessor Dr. Markus Pauly Tag der mündlichen Prüfung: 01.06.2016 Diese Dissertation ist auf den Internetseiten der Hochschulbibliothek online verfügbar. Contents Contents ........................................................................................................................... i List of Figures.................................................................................................................. iv List of Tables ................................................................................................................... vi Publications and Declaration .......................................................................................... vii Acknowledgements ....................................................................................................... viii Abstract ........................................................................................................................... 1 Zusammenfassung .......................................................................................................... 2 1 Introduction ............................................................................................................. 3 1.1 Key Components of Plant Cell Walls ................................................................... 3 1.1.1 Cellulose ...................................................................................................... 7 1.1.2 Xyloglucan (XyG) ......................................................................................... 7 1.1.3 Heteromannans (HM) ................................................................................... 8 1.1.4 Heteroxylans ................................................................................................ 9 1.1.5 Pectins ....................................................................................................... 10 1.2 Industrial Applications of Polysaccharides ......................................................... 11 1.3 Seed Mucilage as a Cell Wall Model ................................................................. 12 1.3.1 The Seed Coat Epidermis (SCE) ................................................................ 12 1.3.2 Mucilage Architecture ................................................................................. 13 1.4 Biogenesis of Mucilage from Start to Finish ....................................................... 14 1.4.1 RG I and HG in Mucilage ............................................................................ 14 1.4.2 Putative Hemicelluloses ............................................................................. 17 1.4.3 Cellulosic Rays ........................................................................................... 18 1.4.4 Putative Glycoproteins ............................................................................... 19 1.4.5 Polar Secretion of Mucilage ........................................................................ 19 1.4.6 Modification of Polysaccharides in the Wall ................................................ 20 1.4.7 Regulation of SCE Differentiation ............................................................... 20 1.5 Research Objective ........................................................................................... 23 2 Methods ................................................................................................................ 24 i 2.1 Tools for Reverse Genetics ............................................................................... 24 2.2 Plant Growth Conditions .................................................................................... 24 2.3 Genotyping of Insertion Mutants ........................................................................ 26 2.4 RNA Isolation and Transcript Analysis ............................................................... 27 2.5 Mucilage Staining and Measurements ............................................................... 28 2.6 Analysis of Monosaccharide Composition ......................................................... 29 2.7 Glycosyl Linkage Analysis of Mucilage Extracts ................................................ 30 2.8 Cellulose Observation and Quantification .......................................................... 31 2.9 ELISA Analysis and In Situ Immunolabeling ...................................................... 31 2.10 Subcellular Localization of MUCI Proteins ..................................................... 32 2.11 MUCI Protein Purification and Activity Assays ............................................... 34 3 Results .................................................................................................................. 36 3.1 The Screen for MUCILAGE-RELATED (MUCI) Genes ...................................... 36 3.2 CSLA2 and MUCI10 Synthesize GGM in Mucilage ........................................... 40 3.2.1 MUCI10, a GT34 Protein, Promotes Mucilage Synthesis ............................ 40 3.2.2 The muci10 Mutant Has Impaired GGM Branching .................................... 43 3.2.3 MUCI10 Facilitates GGM Galactosylation in the Golgi ................................ 45 3.2.4 CSLA2 and MUCI10 Might Not Suffice for GGM Synthesis ........................ 46 3.2.5 GGM Maintains Cellulose Structure in Mucilage ......................................... 50 3.2.6 Mucilage Attachment Requires Cellulose and GGM ................................... 51 3.2.7 muci10 Mucilage Compactness Is Not Calcium-Dependent ....................... 55 3.3 IRX14 and MUCI21 Produce a Highly Branched Xylan ...................................... 57 3.3.1 MUCI21 Facilitates the Synthesis of Xyl-Rich Polymers ............................. 57 3.3.2 IRX14 and MUCI21 Produce Mucilage Xylan ............................................. 59 3.3.3 SCE Cells Contain a Novel, Highly Branched Xylan ................................... 63 3.3.4 MUCI21 Decorates Xylan, Elongated by IRX14 .......................................... 66 3.3.5 Substituted Xylan Maintains Mucilage Adherence ...................................... 67 3.3.6 Xylan Branches Link Pectins to Cellulosic Rays ......................................... 69 3.4 Additional MUCI Genes Facilitate Cell Wall Synthesis ....................................... 72 ii 3.4.1 MUCI59, a TRM Protein, Influences Mucilage Compactness ..................... 72 3.4.2 MUCI70, a Non-Classified GT, Enables Pectin Biosynthesis ...................... 74 4 Discussion ............................................................................................................ 78 4.1 GGM Biosynthesis, Structure and Function in Mucilage .................................... 78 4.1.1 MUCI10 Facilitates Substitution of GGM in Mucilage ................................. 78 4.1.2 Branched GGM Maintains the Architecture of Mucilage ............................. 79 4.1.3 MUCI10 Is Essential, but Not Sufficient for GGM Synthesis ....................... 81 4.2 An Unusual Xylan Maintains Seed Mucilage Properties .................................... 83 4.2.1 Mucilage Contains Hemicelluloses Typical of Secondary Walls.................. 83 4.2.2 MUCI21, a GT61 Protein, Decorates Xylan with Unusual Side Chains ....... 83 4.2.3 Two Distinct Mucilage Defects Cause Seed Flotation ................................. 85 4.2.4 Mucilage Adherence Is Maintained by Multiple Polymers ........................... 85 4.2.5 Exploring Xylan Biosynthesis Using Arabidopsis Mucilage ......................... 86 4.3 Other Mucilage Polymers Also Require MUCI Genes ........................................ 87 4.4 Conclusion ........................................................................................................ 89 5 References ........................................................................................................... 90 6 Appendices ......................................................................................................... 103 Appendix A. Top candidates from the MUCI screen. ................................................ 103 Appendix B. Genotypes and mucilage phenotypes of muci mutants. ....................... 106 Appendix C. Frequently Used Abbreviations. ........................................................... 110 iii List of Figures Figure 1. Models of several plant cell wall polysaccharides. ............................................ 5 Figure 2. Schematic of SCE cell development and mucilage release. ........................... 12 Figure 3. Mucilage monosaccharide composition and predicted polymers. ................... 14 Figure 4. Simplified model of the SCE cell development. .............................................. 15 Figure 5. Mucilage staining defects of selected Arabidopsis mutants. ........................... 16 Figure 6. Image segmentation in Fiji for mucilage area quantification. ........................... 28 Figure 7. Graphical summary of MUCI co-expression strategies. .................................. 36 Figure 8. CAZy families represented by the top MUCI candidates. ................................ 38 Figure 9. Mutations in five MUCI
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