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Equipped with His Five Senses, Man Explores the Universe Around Him and Calls the Adventure Science.” - Edwin Powell Hubble

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Equipped with His Five Senses, Man Explores the Universe Around Him and Calls the Adventure Science.” - Edwin Powell Hubble “Equipped with his five senses, man explores the universe around him and calls the adventure Science.” - Edwin Powell Hubble Promoters: Prof. dr. ir. Tina Kyndt Laboratory of Epigenetics and Defence Department of Biotechnology Faculty of Bioscience Engineering Ghent University Prof. dr. ir. Tim De Meyer BIOBIX Laboratory Department of Data Analysis and Mathematical Modelling Faculty of Bioscience Engineering Ghent University Dean: Prof. dr. ir. Marc Van Meirvenne Rector: Prof. dr. ir. Rik Van de Walle INSIGHTS INTO THE INTERACTION BETWEEN RICE AND ROOT-KNOT NEMATODES FROM AN EPIGENETIC PERSPECTIVE Ir. Bruno Verstraeten Promoters: Prof. dr. ir. Tina Kyndt Prof. dr. ir. Tim De Meyer Academic year: 2020 - 2021 Dissertation submitted to Ghent University in fulfilment of the requirements for the degree of Doctor of Bioscience Engineering: Biotechnology Dutch translation of the title Inzichten in de interactie tussen rijst en wortelknobbelaaltjes vanuit een epigenetisch oogpunt. Please refer to this work as follows Verstraeten, B. (2021), Insights into the interactions between rice and root-knot nematodes from an epigenetic perspective, PhD Thesis, Department of Biotechnology, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium. ISBN: 978-94-6357-393-1 Financing institutions Fonds Wetenschappelijk onderzoek-Vlaanderen (G007417N) Bijzonder Onderzoeksfonds UGent (BOF-starting grant) The author and the promoters give the authorization to consult and to copy parts of this work for personal use only. Any other use is limited by copyright law. Permission to reproduce any material contained in this work should be obtained from the author. Promoters Author Prof. dr. ir. Tina Kyndt Ir. Bruno Verstraeten Prof. dr. ir. Tim De Meyer The cover art is a photograph made by Gunilla Elam/science Photo Library, titled ‘Cellular Dna And Epigenetics’. iv Promoters Prof. dr. ir. Tina Kyndt Epigenetics and Defence Research Group Department of Biotechnology Faculty of Bioscience Engineering Ghent University, Belgium Prof. dr. ir. Tim De Meyer BIOBIX laboratory Department of Data analysis and mathematical modelling Faculty of Bioscience Engineering Ghent University, Belgium Examination committee Prof. dr. ir. Thomas Van Leeuwen (Chair) Department of Plants and Crops Faculty of Bioscience Engineering Ghent University, Belgium Prof. dr. ir. Gerben Menschaert (Secretary) BIOBIX Laboratory Department of Data analysis and mathematical modelling Faculty of Bioscience Engineering Ghent University, Belgium Prof. dr. Jurriaan Ton Ton Laboratory Department of Animal and Plant Sciences University of Sheffield, United Kingdom Prof. dr. Klaas Vandepoele a. Department of Plant Biotechnology and Bioinformatics (WE09), Ghent University b. VIB Center for Plant Systems Biology Dr. ir. Annelies Haegeman Plant Sciences Unit Flanders Research Institute for Agriculture, Fisheries and Food, Belgium v Table of contents Table of contents ................................................................................................................... vi List of abbreviations ............................................................................................................... x Problem statement ............................................................................................................... xv Thesis outline ...................................................................................................................... xvi 1. General introduction ....................................................................................................... 1 1.1. Rice ......................................................................................................................... 2 1.1.1. Importance as a food crop ................................................................................ 2 1.1.2. Importance as a model system ......................................................................... 3 1.2. Nematodes .............................................................................................................. 3 1.2.1. Introduction ...................................................................................................... 3 1.2.2. Plant-parasitic nematodes ................................................................................ 4 1.2.3. Plant response to nematode infection .............................................................. 6 1.2.4. Nematode control strategies ............................................................................. 8 1.3. Epigenetics ............................................................................................................11 1.3.1. Introduction .....................................................................................................11 1.3.2. DNA methylation .............................................................................................14 1.3.3. Histone modifications ......................................................................................18 1.3.4. Non-coding RNAs ...........................................................................................22 1.3.5. Interaction between epigenetic marks .............................................................30 1.3.6. Sequencing techniques used in epigenetic research .......................................31 1.4. Research questions ................................................................................................33 2. Genome-wide DNA hypomethylation shapes nematode pattern-triggered immunity in plants ...................................................................................................................................35 2.1. Abstract ..................................................................................................................36 2.2. Introduction ............................................................................................................36 2.3. Materials and Methods ...........................................................................................38 2.3.1. Plant growth and treatments ............................................................................38 2.3.2. ELISA-based global DNA methylation assay and H2O2 quantification .............38 2.3.3. Infection assays on RdDM mutants and 5-Azacytidine treated plants ..............38 2.3.4. DNA extraction, library preparation and whole genome bisulfite sequencing (WGBS) 39 2.3.5. WGBS data analysis .......................................................................................39 2.3.6. RNA-sequencing data analysis .......................................................................40 2.3.7. Association between DMRs and genomic regions ...........................................40 2.3.8. RT-qPCR and Chop-qPCR ..............................................................................40 2.3.9. Data availability ...............................................................................................41 vi 2.3.10. Further statistical analyses ..........................................................................41 2.4. Results ...................................................................................................................41 2.4.1. DNA hypomethylation is part of a PTI response upon root-knot nematode infection 41 2.4.2. WGBS supports a central role for CHH hypomethylation .................................43 2.4.3. DNA hypomethylation correlates with a delayed transcription response in gall tissue 46 2.4.4. RdDM and DDM1 mutants confirm that DNA methylome changes are involved in plant defence against nematodes ..............................................................................48 2.5. Discussion ..............................................................................................................49 2.6. Supplementary information .....................................................................................52 3. Histone modification changes at early stage of rice infection with Meloidogyne graminicola ...........................................................................................................................65 3.1. Abstract ..................................................................................................................66 3.2. Introduction ............................................................................................................66 3.3. Materials and methods ...........................................................................................68 3.3.1. Plant growth conditions ...................................................................................68 3.3.2. Nematode culture and inoculation ...................................................................68 3.3.3. Application of chemical inhibitors and evaluation of plant susceptibility ...........69 3.3.4. Western blot analysis ......................................................................................69 3.3.5. Data analysis...................................................................................................69 3.3.6. Synchronization of infection and chromatin immunoprecipitation (ChIP)..........69 3.3.7. Library preparation and sequencing ................................................................70 3.3.8. Data analysis of ChIP-sequencing data ...........................................................70 3.3.9. Association between gene sets .......................................................................71 3.3.10. Gene
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