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Investigation and Characterisation of Diamide Insecticide Resistance Conferred by Target-Site Mutations in the Ryanodine Receptor of Lepidopteran Pests

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Investigation and Characterisation of Diamide Insecticide Resistance Conferred by Target-Site Mutations in the Ryanodine Receptor of Lepidopteran Pests Investigation and characterisation of diamide insecticide resistance conferred by target-site mutations in the Ryanodine Receptor of lepidopteran pests Thesis submitted in accordance with the requirements of Cardiff University for the degree of Doctor in Philosophy (Medicine) Ewan Patrick Blockey Richardson December 2019 Word Count: 45,848 Pages: 195 Summary Lepidopteran crop pests such as Tuta absoluta, Chilo suppressalis, Spodoptera frugiperda and Plutella xylostella are becoming increasingly problematic, as populations colonise new regions of the globe. The diamide insecticides are a relatively new class that is especially effective, and important, for controlling lepidopteran pests. However, over the past 10 years, resistance to diamides has emerged amongst various lepidopteran species, and is a major threat to crop protection in some cases. Resistance is thought to be caused by alterations to the Ryanodine Receptor, which is the target-site of Diamide insecticides, and previous studies have identified a variety of alterations, in field-populations of multiple lepidopteran species, which may be implicated in diamide resistance. This thesis aims to characterise RyR alterations in terms of their impact on the control-efficacy of diamide insecticides. A previously cloned RyR sequence from the moth, Plutella xylostella, was altered to reflect resistance-alterations present in the field. Alteration of positions 4946 and 4790 was found to reduce activation by diamides when expressed in cell lines. These same altered moth RyR sequences were inserted into Drosophila, by way of in-vivo confirmation. Flies expressing the resistant RyR genotypes survived diamide challenge more readily than those expressing the wild-type genotype of moth RyR. However, the resistant genotypes also climbed and crawled more slowly, suggesting a potential drawback of resistance. The alterations to residues 4946 and 4790 suggested a location of diamide interaction within the voltage-sensor-like domain of the RyR. In order to further define the interaction site, further alterations were made within the same region. Preliminary investigations indicated that these alterations strongly reduce diamide efficacy, when in combination, but exhibit somewhat minor reductions of efficacy as individual changes. It was concluded that the diamide interaction lies proximal to the Voltage-Sensor-like-Domain of the RyR. b c Table of Contents Table of Figures i Acknowledgements vi Abbreviations vii Chapter 1: Introduction 1.1 Modern Agriculture: Feeding a growing population 1.1.1 A strain on the planet ............................................................... 1 1.2 Insect control in the era of ‘Sustainable Intensification’…………… 2 1.2.1 Non-synthetic modes of insect control .................................... 3 1.2.2 Insecticidal Spray: There’s no better way ................................ 6 1.2.3 Strain on the Insecticide industry ............................................. 6 1.3 Diamide insecticides 8 1.3.1 A New Hope .............................................................................. 9 1.3.2 Flubendiamide: An exceptionally selective insecticide ............ 9 1.3.3 Chlorantraniliprole and Cyantraniliprole: A wider range of control .............................................................................................. 10 1.3.4 New diamide actives under development ............................. 12 1.4 The rise of resistance to diamide insecticides 14 1.4.1 Spodoptera frugiperda and other Noctuidae ........................ 14 1.4.2 Tuta absoluta .......................................................................... 17 1.4.3 Diamide Resistance in other Lepidopteran Species............... 21 d 1.4.4 Plutella xylostella .................................................................... 23 1.4.5 The Root of Resistance: Alterations to the Diamide target .. 24 1.5 Diamide Mode of Action 25 1.5.1 The Ryanodine Receptor......................................................... 26 1.5.2 Calcium Homeostasis ............................................................. 27 1.5.3 RyR2 ........................................................................................ 27 1.5.4 Excitation Contraction Coupling ............................................ 28 1.5.5 Modulation of RyRs ................................................................ 29 1.6 RyR Sequence, Structure and Function 33 Box 1.3: Highlights of imaging studies ............................................ 34 1.6.1 General Structural overview ................................................... 35 1.6.2 Opening Mechanism: An Overview ........................................ 36 1.6.3 Opening Mechanism: Detailed investigations ....................... 37 1.6.4 Calcium and Caffeine: In search of a binding site ................. 39 1.6.5 RyR amino acid alterations in disease states: clues to function 41 Chapter 2: Methods 2.1 General Methods 46 2.1.1 Genomic DNA extraction ........................................................ 46 2.1.2 RNA extraction ........................................................................ 46 2.1.3 cDNA synthesis ....................................................................... 47 e 2.2 Polymerase chain reaction (PCR) 47 2.2.1 Primer Design .......................................................................... 47 2.2.2 Standard PCR .......................................................................... 47 2.2.3 High-fidelity PCR ..................................................................... 48 2.2.4 Site-directed Mutagenesis by PCR ......................................... 48 2.2.5 PCR product purification ........................................................ 49 2.2.6 Agarose gel electrophoresis ................................................... 49 2.2.7 Extraction of PCR products from agarose gels ...................... 49 2.3 Molecular Cloning and Transformation 50 2.3.1 Plasmid assembly by endonuclease digestion and ligation .. 50 2.3.2 Concentration by Ethanol Precipitation................................. 50 2.3.3 Bacterial transformation ........................................................ 51 2.3.4 Transformation Validation and plasmid Propagation .......... 51 2.3.5 Plasmid purification ................................................................ 52 2.4 Final Product Validation and Sequencing 53 2.4.1 Restriction Fragment Length Validation ................................ 53 2.4.2 Sequencing .............................................................................. 53 2.5 Generating RyR mutant genotypes (with RFCLM as example) - specific cloning strategy for RyR mutagenesis and assembly 53 2.5.1 Mutagenesis on individual PxRyR fragments ........................ 56 2.5.2 fragment assembly into the plasmid and plasmid propagation ...................................................................................... 56 f 2.5.3 pcDNA3.1(-) / pIZ/V5-His modified plasmid creation, for fragment assembly .......................................................................... 58 2.5.4 Plasmid Assembly Validation ................................................. 58 2.5.5 Transfer of Recombinant RyR constructs between vectors .. 59 Chapter 3: Validation of the perfusion Calcium Imaging system for quantifying diamide response in Sf9 cells 3.1 Chapter Summary 64 3.2 The need for a novel method for rapid in-vitro investigation of insecticide resistance mechanisms 64 3.3 Chapter Specific Methods 67 3.3.1 Overview of the experimental system ................................... 67 3.3.2 Insect cell husbandry .............................................................. 68 3.4 Characterising PxRyR-expressing Sf9 cells response to caffeine and diamides using the Ratiometric Imaging Perfusion Rig 69 3.4.1 Identification of the caffeine ‘type-response’ and cellular selection ........................................................................................... 69 3.4.2 Protocol optimisation to maximize the cat A response in PxRyR transfected cells .................................................................... 73 3.4.3 Calcium Imaging ..................................................................... 80 3.4.4 Characterisation of the recombinant WT-PxRyR Caffeine- response in Sf9 cells ......................................................................... 82 3.4.5 Characterisation of the recombinant WT-PxRyR diamide- response in Sf9 cells ......................................................................... 87 3.4.5.1 Agonist Diluents and Background Fluorescence ................ 88 g 3.4.5.2 Absolute [Ca2+] was not measured ..................................... 89 3.5 Absolute Ca2+ Imaging: An alternative method of diamide response quantification 94 3.5.1 Drawbacks of the Absolute Imaging system ......................... 97 3.6 Conclusions 99 Chapter 4: Target-Site Resistance to Diamide Insecticides 4.1 Chapter Summary 100 4.2 Introduction 100 4.2.1 Target Site Resistance ......................................................... 100 4.2.2 I4790M– A novel cause of resistance in diverse lepidopteran pests .............................................................................................. 102 4.3 Methods 106 4.3.1 Concentration-response assays .......................................... 106 4.3.2 In-silico analysis methods .................................................... 106 4.4 Results 109 4.4.1 Generation of novel PxRyR constructs ................................ 109 4.4.2 Functional Expression
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