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Manoj Kumar Valluru.Pdf ARGONAUTE10 inhibits INDEHISCENT to regulate shoot apical meristem and replum development in Arabidopsis thaliana A thesis submitted for the degree of Doctor of Philosophy Manoj Kumar Valluru December 2017 Department of Molecular Biology and Biotechnology University of Sheffield i Acknowledgments गु셁 ब्र륍हा गु셁 विष्णू Guru Brahmaa Guru Vishnu गु셁ԃ देिो महेश्िरा Gurur Devo Maheshwarah गु셁 शाक्षात परब्र륍हा Guru Saakshaata Parabrahma तस्मै श्री गु셁िे नमԃ Tasmai Shri Guruve Namah This verse from Skanda Purana translates as: The true teacher is Brahma (God as Creator), The true teacher is Vishnu (God as Sustenance), The true teacher is Shiva (God as the destroyer of the ego or ignorance), My Salutation to such a teacher, who is verily united with God. I would like to thank my supervisor Dr Karim Sorefan for all of his help, advice and understanding throughout my PhD. A great deal of help has also come from lab members both past and present, for which I am deeply grateful. This includes Peter Venn, Matthew Parker, James Thackery, Giulia Arsuffi, Colette L Baxter, Dr Nicholas Zoulias and colleagues from Dr Stuart Casson’s lab. I am grateful to the researchers who have contributed seeds and transgenic material to this study. The pIND::IND-YFP was kindly provided by Professor Lars Østergaard at John Innes Centre, United Kingdom. The 35S:LhGR>>PHB was kindly provided by Professor Miltos Tsiantis at Max Planck Institute for Plant Breeding Research, Germany. The pMDC32-GR plasmid was kindly provided by Dr Stuart Casson at Department of Molecular Biology and Biotechnology, The University of Sheffield, United Kingdom. Many thanks to Marion Bauch for advice on histological work, Dr Svetlana Sedelnikova for protein work, Dr Paul Heath for microarray work and Dr Chris Hill for Electron Microscopy work. I gratefully acknowledge the funding provided by the University of Sheffield studentship. I would also like to thank my parents and my family. Finally, I would like to dedicate this thesis to my loving wife, Judith Valluru. ii Abstract ARGONAUTE10 (AGO10) regulates shoot apical meristem (SAM) and gynoecium development by controlling Class III HOMEODOMAIN-LEUCINE ZIPPER (HD-ZIP III) transcription factor expression. The ago10zwl-3 mutant failed to establish SAM, leaf adaxial identity, and carpel margin meristems (CMMs). However, the factors that act downstream of AGO10 and HD-ZIP III genes to regulate development are not known. This work has identified that the INDEHISCENT (IND) bHLH transcription factor functions downstream of AGO10 and HD-ZIP III genes to ensure proper SAM and replum development. IND overexpression causes SAM defects similar to ago10zwl-3 mutants, and the ind mutation partially rescues ago10 mutant phenotypes. IND overexpression negatively regulates tissue bilateral symmetry by repressing polar auxin transport (PAT), AGO10 and probably CUC1 expression. However, HD-ZIP III transcription factors PHB and REV indirectly repress IND and promote CUC1 expression. AGO10 and IND regulate each other antagonistically. AGO10 repression of IND is essential for SAM and replum development because overexpression of IND impairs tissue bilateral symmetry. This is the first study to demonstrate a role for IND in SAM development and that the main function of AGO10 is to maintain proper IND expression. iii Table of Contents Acknowledgments--------------------------------------------------------------------------------------- ii Abstract ---------------------------------------------------------------------------------------------------- iii List of tables and figures ------------------------------------------------------------------------------ xii List of abbreviations --------------------------------------------------------------------------------- xvii CHAPTER 1. General Introduction ------------------------------------------------------------------- 2 1.1 Shoot apical meristem and leaf primordia ------------------------------------------------- 2 1.1.1 Hormonal regulation ----------------------------------------------------------------------- 3 1.1.1.1 Auxins regulate SAM and leaf development ------------------------------------ 5 1.1.1.2 Cytokinins regulate SAM and leaf development ------------------------------- 8 1.1.2 CLAVATA/WUSCHEL loop ---------------------------------------------------------------- 10 1.1.3 Adaxial, abaxial and boundary genes ------------------------------------------------- 13 1.2 ARGONAUTE proteins -------------------------------------------------------------------------- 15 1.2.1 ARGONAUTE proteins control SAM and leaf development ---------------------- 16 1.3 Similar genes regulate SAM and floral to fruit transition ------------------------------ 19 1.4 Hypothesis and Objectives -------------------------------------------------------------------- 24 CHAPTER 2. Materials and Methods --------------------------------------------------------------- 27 2.1 Materials ------------------------------------------------------------------------------------------ 27 2.1.1 General laboratory materials ----------------------------------------------------------- 27 2.1.2 Plant materials ----------------------------------------------------------------------------- 27 iv 2.2 Plant methods ----------------------------------------------------------------------------------- 28 2.2.1 Plant growth conditions ------------------------------------------------------------------ 28 2.2.2 Hormone and chemical treatments --------------------------------------------------- 29 2.2.3 Shoot apical meristem phenotype analysis ------------------------------------------ 29 2.3 Nucleic acid techniques ----------------------------------------------------------------------- 30 2.3.1 Plant genomic DNA extraction --------------------------------------------------------- 30 2.3.2 Plant total RNA extraction --------------------------------------------------------------- 30 2.3.3 cDNA synthesis ----------------------------------------------------------------------------- 31 2.3.4 Primer design ------------------------------------------------------------------------------- 32 2.3.5 Polymerase chain reaction (PCR) ------------------------------------------------------ 33 2.3.6 Quantitative reverse transcriptase PCR (qRT-PCR) -------------------------------- 34 2.3.7 Agarose gel electrophoresis ------------------------------------------------------------- 35 2.3.8 DNA gel extraction ------------------------------------------------------------------------ 35 2.4 Chromatin immunoprecipitation (ChIP) methods --------------------------------------- 36 2.4.1 Chromatin immunoprecipitation ------------------------------------------------------ 36 2.4.2 ChIP qPCR and ChIP-Seq analysis ------------------------------------------------------ 37 2.5 Microarray methods --------------------------------------------------------------------------- 38 2.5.1 Microarray ---------------------------------------------------------------------------------- 38 2.5.2 Microarray analysis ----------------------------------------------------------------------- 38 2.6 Bioinformatics ----------------------------------------------------------------------------------- 39 2.6.1 Sequence alignments --------------------------------------------------------------------- 39 v 2.6.2 GSEA analysis ------------------------------------------------------------------------------- 39 2.6.3 Library files for GSEA ---------------------------------------------------------------------- 40 2.6.4 MOTIF and DAP-Seq analysis ------------------------------------------------------------ 40 2.6.5 Protein structure modelling ------------------------------------------------------------- 41 2.7 Imaging techniques ----------------------------------------------------------------------------- 42 2.7.1 β-Glucuronidase (GUS) assay ----------------------------------------------------------- 42 2.7.2 Sample fixation, clearing, and preparation ------------------------------------------ 42 2.7.3 Embryo dissection and light microscopy --------------------------------------------- 43 2.7.4 Confocal Microscopy ---------------------------------------------------------------------- 44 2.7.5 Scanning Electron Microscopy (SEM) ------------------------------------------------- 45 2.8 Statistical analysis ------------------------------------------------------------------------------- 45 CHAPTER 3. AGO10 and HD-ZIP III transcription factors regulate IND -------------------- 47 3.1 Introduction -------------------------------------------------------------------------------------- 47 3.2 Results --------------------------------------------------------------------------------------------- 49 3.2.1 Characterisation of AGO family gene expression in SAM and other tissues - 50 3.2.2 Characterisation of AGO10 -------------------------------------------------------------- 53 3.2.2.1 AGO10 expression -------------------------------------------------------------------- 53 3.2.2.2 Genotyping ago10 mutant zwl-3 ------------------------------------------------- 53 3.2.2.3 zwl-3 developmental phenotypes ------------------------------------------------ 54 3.2.2.4 Summary ------------------------------------------------------------------------------- 55 3.2.3 Characterisation of IND ------------------------------------------------------------------- 59 vi 3.2.3.1 IND expression ------------------------------------------------------------------------ 59 3.2.3.2 Loss of ind developmental phenotypes ----------------------------------------- 59 3.2.3.3 Overexpression
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