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How the Plant-Parasitic Nematode Hirschmanniella Oryzae Is Able to Subdue the Defense System of Rice; a Molecular Analysis

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How the Plant-Parasitic Nematode Hirschmanniella Oryzae Is Able to Subdue the Defense System of Rice; a Molecular Analysis Always remember that you are absolutely unique. Just like everyone else.’ Margaret Mead (1901-1978) Promotor: Prof. Dr. Godelieve Gheysen Ghent University Dpt. Molecular Biotechnology Laboratory for Applied Molecular Genetics Dean: Prof. Dr. ir. Guido van Huylenbroeck Rector: Prof. Dr. Ann De Paepe How the plant-parasitic nematode Hirschmanniella oryzae is able to subdue the defense system of rice; a molecular analysis Lander Bauters Thesis submitted in fulfillment of the requirements for the degree of Doctor (PhD) of Applied Biological Sciences Het onderdrukken van het afweersysteem in rijst door de plantparasitaire nematode Hirschmanniella oryzae; een moleculaire analyse Bauters, L. (2015). How the plant-parasitic nematode Hirschmanniella oryzae is able to subdue the defense system of rice; a molecular analysis. PhD thesis, Ghent University, Ghent, Belgium ISBN-nummer: 978-90-5989-815-8 The author and the promotor give the authorization to consult and to copy parts of this work for personal use only. Any other use is limited by the Laws of Copyright. Permission to reproduce any material contained in this work should be obtained from the author. Promotor Author Prof. Dr. Godelieve Gheysen Lander Bauters Members of the examination committee Prof. Dr. Godelieve Gheysen (promotor) Dept. of Molecular Biotechnology Faculty of Bioscience Engineering, Ghent University Belgium Prof. Dr. Guy Smagghe (chairman) Dept. of Crop Protection Faculty of Bioscience Engineering, Ghent University Belgium Prof. Dr. ir. Kris Audenaert (secretary) Dept. of Applied Biosciences Faculty of Bioscience Engineering, Ghent University Belgium Prof. Dr. ir. Bartel Vanholme VIB Dept. of Plant Systems Biology Ghent University Belgium Prof. Dr. ir. Geert Smant Lab. of Nematology Wageningen University The Netherlands Prof. Dr. John Jones Cell and Molecular Sciences The James Hutton Institute Scotland UK Table of Contents List of abbreviations .................................................................................................................... i Chapter 1. Introduction .......................................................................................................... 1 1.1. Rice: the host ............................................................................................................... 3 1.1.1. General facts about rice ....................................................................................... 3 1.1.2. Pests and diseases ................................................................................................ 3 1.1.3. Rice: an ideal crop model ..................................................................................... 5 1.2. Nematodes: the pathogens ......................................................................................... 6 1.2.1. General introduction ............................................................................................ 6 1.2.2. Plant-parasitic nematodes ................................................................................... 7 1.3. The general plant-pathogen interaction model adapted to nematodes .................. 11 1.4. A rigid cell wall and hormonal signaling: adequate defense systems? ..................... 13 1.4.1. The cell wall: protecting the frontiers ................................................................ 14 1.4.2. Active defense mechanisms at the vanguard .................................................... 15 1.4.3. Plant hormones: instructors of defense............................................................. 16 1.5. Nematode effectors: effective weaponry? ............................................................... 22 1.5.1. Cell wall modifying proteins: hydrolyzing the first barrier ................................ 22 1.5.2. Other effectors: a more sophisticated attack .................................................... 27 1.6. Scope and outline of the thesis ................................................................................. 31 Chapter 2. Analysis of the transcriptome of Hirschmanniella oryzae to explore potential survival and infection strategies .............................................................................................. 33 2.1. Summary .................................................................................................................... 35 2.2. Introduction ............................................................................................................... 35 2.3. Results ........................................................................................................................ 37 2.3.1. Dataset characteristics ....................................................................................... 37 2.3.2. Comparison with protein databases and annotation ........................................ 38 2.3.3. Most abundant transcripts ................................................................................. 41 2.3.4. Survival in dry conditions ................................................................................... 43 2.3.5. Mining the transcriptome for cell wall-modifying proteins ............................... 44 2.3.6. Chorismate mutase and isochorismatase .......................................................... 45 2.4. Discussion .................................................................................................................. 49 2.5. Experimental procedures .......................................................................................... 54 2.5.1. RNA extraction and sequencing ......................................................................... 54 2.5.2. Clean up and assembly ....................................................................................... 54 2.5.3. Blast searches and annotation ........................................................................... 54 2.5.4. Protein domain search and sequence analysis .................................................. 55 2.5.5. Dehydration treatment ...................................................................................... 55 2.5.6. RNA extraction and cDNA synthesis ................................................................... 56 2.5.7. Q-RT-PCR ............................................................................................................ 56 2.5.8. Construction of a phylogenetic tree .................................................................. 56 2.5.9. Whole-mount in situ hybridization .................................................................... 57 Chapter 3. Characterization of two putative effector proteins of Hirschmanniella oryzae; chorismate mutase and isochorismatase ................................................................................ 59 3.1. Summary .................................................................................................................... 61 3.2. Introduction ............................................................................................................... 61 3.3. Results ........................................................................................................................ 63 3.3.1. Genetic structure of HoCM and HoICM ............................................................. 63 3.3.2. Protein properties .............................................................................................. 65 3.3.3. Protein structure ................................................................................................ 66 3.3.4. Activity assay ...................................................................................................... 69 3.3.5. Defense suppression .......................................................................................... 71 3.3.6. Localization studies ............................................................................................ 73 3.4. Discussion .................................................................................................................. 75 3.5. Experimental procedures .......................................................................................... 80 3.5.1. DNA extraction and gene amplification ............................................................. 80 3.5.2. Bioinformatic tools ............................................................................................. 81 3.5.3. Complementation assay with HoCM .................................................................. 81 3.5.4. Complementation assay with HoICM ................................................................. 82 3.5.5. Defense suppression assay................................................................................. 82 3.5.6. Subcellular localization studies .......................................................................... 83 Chapter 4. Ectopic expression of nematode derived chorismate mutase and isochorismatase induces changes in secondary metabolism and susceptibility in rice .......... 85 4.1. Summary .................................................................................................................... 87 4.2. Introduction ............................................................................................................... 87 4.3. Results ........................................................................................................................ 89 4.3.1. Overexpression lines .......................................................................................... 89 4.3.2.
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