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To a First Approximation, All Animals Are Insects. Robert To a first approximation, all animals are insects. Robert May RNAi efficiency in insects: dsRNA uptake mechanisms and viral suppressors of RNAi ir. Kaat Cappelle Thesis submitted in fulfillment of the requirements for the degree of Doctor (PhD) in Applied Biological Sciences: Cell and Gene Biotechnology Dutch translation of the title: RNAi efficiëntie in insecten: dsRNA opnamemechanismen en virale suppressoren van RNAi Cover illustration: The author’s own artwork depicting the main subjects of this thesis: the RNAi process, the bumblebee and the Colorado potato beetle. Refer to this thesis as follows: Cappelle, K. (2017). RNAi efficiency in insects: dsRNA uptake mechanisms and viral suppressors of RNAi. PhD dissertation, Faculty of Bioscience Engineering, Ghent University, Belgium ISBN: 978-90-5989-967-4 This study was supported by a PhD grant provided by the Bijzonder Onderzoeksfonds (Ghent University, BOF12/DOC/295). The author and the promoters give the authorization to consult and copy parts of this work for personal use only. Every other use is subject to copyright laws. Permission to reproduce any material contained in this work should be obtained from the author. The promotors, The author, Prof. dr. ir. Guy Smagghe Kaat Cappelle Dr. Ivan Meeus Promotors Prof. dr. ir. Guy Smagghe Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University, Belgium Dr. Ivan Meeus Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University, Belgium Dean of the Faculty of Bioscience Engineering, Ghent University Prof. dr. ir. Marc Van Meirvenne Rector of Ghent University Prof. dr. Anne de Paepe Chair of the examination committee Prof. dr. ir. Nico Boon Department of Biochemical and Microbial Technology Faculty of Bioscience Engineering, Ghent University, Belgium Members of the reading committee Prof. dr. ir. Peter Bossier Department of Animal Production Faculty of Bioscience Engineering, Ghent University, Belgium Prof. dr. Joachim de Miranda Department of Ecology Swedish University of Agricultural Sciences, Sweden Prof. dr. Godelieve Gheysen Department of Molecular Biotechnology Faculty of Bioscience Engineering, Ghent University, Belgium Prof. dr. Jozef Vanden Broeck Department of Biology Faculty of Science, KU Leuven, Belgium TABLE OF CONTENTS List of abbreviations ................................................................................................................................. v List of Figures .......................................................................................................................................... ix List of Tables ............................................................................................................................................ xi Scope ..................................................................................................................................................... xiii Chapter I: Introduction ............................................................................................................................1 1.1 RNA interference ................................................................................................................ 3 1.1.1 Classes of non-coding RNAs and RNA interference ................................................... 3 1.1.2 Biological role of RNAi in insects ................................................................................ 4 1.1.3 The siRNA pathway .................................................................................................... 5 1.1.4 Environmental / systemic RNAi .................................................................................. 6 1.1.5 Applications of RNAi in entomology .......................................................................... 7 1.1.6 Problematic RNAi efficiency ....................................................................................... 7 1.2 dsRNA uptake mechanisms ................................................................................................ 9 1.2.1 Sid-1-like transmembrane proteins ........................................................................... 9 1.2.2 Receptor-mediated clathrin-dependent endocytosis ................................................ 9 1.3 Viral suppressors of RNAi ................................................................................................. 11 1.3.1 VRSs in plant viruses ................................................................................................. 11 1.3.2 VSRs in insects .......................................................................................................... 12 1.4 Insects and viruses used in this work ............................................................................... 15 1.4.1 Insect morphology .................................................................................................... 15 1.4.2 The Colorado potato beetle ..................................................................................... 16 1.4.3 The buff-tailed bumblebee ....................................................................................... 18 1.4.4 The Dicistroviridae.................................................................................................... 19 Chapter II: Intermezzo: RNAi core gene annotation in the Colorado potato beetle and the bumblebee ............................................................................................................................................ 25 2.1 Introduction ..................................................................................................................... 27 2.2 Materials and methods .................................................................................................... 28 2.3 Results and discussion ...................................................................................................... 28 Chapter III: The involvement of clathrin-dependent endocytosis and two Sid-1-like transmembrane proteins in double-stranded RNA uptake in the Colorado potato beetle midgut ..... 31 3.1 Introduction ..................................................................................................................... 33 3.2 Materials and methods .................................................................................................... 36 3.2.1 Insects ....................................................................................................................... 36 3.2.2 Target and reporter gene selection ......................................................................... 36 3.2.3 dsRNA synthesis ....................................................................................................... 36 3.2.4 Feeding assays .......................................................................................................... 38 3.2.5 RNA extraction, cDNA synthesis and RT-qPCR ......................................................... 38 3.3 Results .............................................................................................................................. 39 3.3.1 Identification of target and reporter genes ............................................................. 39 TABLE OF CONTENTS I 3.3.2 Involvement of both sil genes in dsRNA uptake ....................................................... 40 3.3.3 Involvement of the endocytic pathway components in dsRNA uptake ................... 41 3.3.4 Chc as a target for RNAi-based pest control ............................................................ 42 3.4 Discussion ......................................................................................................................... 43 Chapter IV: The pathogenicity of Cricket paralysis virus in Bombus terrestris ..................................... 49 4.1 Introduction ...................................................................................................................... 51 4.2 Material and methods ...................................................................................................... 52 4.2.1 Bumblebee rearing and infection methods ............................................................. 52 4.2.2 Virus production ....................................................................................................... 53 4.2.3 RNA extraction, cDNA synthesis, RT-PCR, negative-strand-specific RT-PCR and RT- qPCR…………………………………………………………………………………………………………………………………….54 4.2.4 CrPV screening in bumblebees collected from nature ............................................. 55 4.3 Results .............................................................................................................................. 56 4.3.1 Injection with CrPV causes mortality at high doses ................................................. 56 4.3.1 Tag-based negative strand RT-PCR detection in a wide host range ......................... 56 4.3.2 Injection with lower doses of CrPV or feeding with faeces of infected bees results in chronic infections ..................................................................................................................... 58 4.3.3 Negative strand detection for CrPV and IAPV in different tissues ........................... 59 4.4 Discussion ......................................................................................................................... 61 Chapter V: The interaction between Israeli acute paralysis virus and the RNA interference response of its host Bombus
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