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The Genetics of Resistance to Lufenuron in Drosophila Melanogaster

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The Genetics of Resistance to Lufenuron in Drosophila Melanogaster The Genetics of Resistance to Lufenuron in Drosophila melanogaster Michael Bogwitz Submitted for total fulfilment of the requirements for the degree of Doctor of Philosophy February 2005 Centre for Environmental Stress & Adaptation Research (CESAR) Department of Genetics University of Melbourne Abstract The rise of large scale agriculture in the 20th century created the need for effective strategies to control insect pests. Treatment with chemical insecticides has been a weapon of choice, but the inevitable evolution of resistance has followed in many insect species. Resistance represents a major challenge, not only for agricultural production, but also for environmental preservation and human health. Two major options for resistance have been identified, and these are target-site based and metabolic-based resistance. Much insecticide resistance research focuses on identifying these mechanisms through genetic and molecular analysis. The insecticide lufenuron is the focus of this study. It belongs to a novel insecticidal group called the insect growth regulators, which were introduced in 1970s as highly selective insecticides with low vertebrate toxicity. Resistance to lufenuron in the non- pest species Drosophila melanogaster has been observed in field populations, despite the lack of field usage of lufenuron (Wilson & Cain, 1997; O'Keefe, 1997). This study has taken advantage of this phenomenon to investigate resistance mechanisms in natural populations. At least two detoxification mechanisms were identified. A resistant isofemale strain isolated in Victoria, Australia was used to identify the detoxification gene, Cyp12a4, that may be involved in resistance. Tissue-specific overexpression of this gene appears to confer resistance to lufenuron, as confirmed through the generation and screening of transgenic overexpressing strains. ii A second mechanism was identified from an isofemale strain isolated from field populations in Coloardo, USA. Another detoxification gene, Cyp6g1, was found to be overexpressed in this strain. Transgenic screening confirms its involvement in conferring resistance to lufenuron. A partial transposon insertion (Accord) was identified, and implicated as the overexpression conferring mutation. An alternate allele containing a partial P-element within Accord was identified in a strain collected from Australian (Queensland) natural populations. The frequency of these alleles is high. Mutagenesis was also used in an attempt to identify the lufenuron target. 17 mutants were isolated, and due to an experimental bias, all carried the Cyp6g1 mechanism and another as yet unidentified mechanism on another chromosome. This study highlights the importance of the need for better understanding of insecticide resistance, and particularly, the arsenal of metabolic detoxification mechanisms available to insect pests, as a method of prolonging the effectiveness of insecticides. iii Declaration This is to certify that: i. This Thesis comprises only my original work ii. Due Acknowledgement has been made in the text to other material used iii. The thesis is less than 100,000 words in length, exclusive of tables, figure legends, bibliographies, and appendices. Michael Bogwitz This Copy Printed on Acid-Free paper iv Acknowledgements There are so many people who have helped me through these last few years practically, intellectually, and emotionally. To my supervisor Phil Batterham, my greatest gratitude goes to you for giving me the opportunity to explore the world of insecticide resistance, for guiding me and having faith, and for creating such a great lab in which to work. To my collaborators and co-workers, thankyou for providing valuable assistance that has mad my task much easier. To Tom Wilson for supplying the WC2 fly strain that became such a large part of my project. To Rene Feyereisen for creating and generously providing results of P450 microarrays. To Phil Daborn for sharing fly strains, data, and ideas, and at one stage, his home. To David Heckel, Charlie Robin, and Adam Williams for intellectual inputs that have helped me immensly. To my fellow Ph.D. student, Trent Perry, for collaboration, discussion, and generous sharing of data on many occasions. To Chris Lumb for performing microinjections. And to John Damiano and Jayne Lydall for assistance with EMS screens. To my friends who have been so supportive in so many different ways over the years, thanks especially to – Ben, Tim, and Tom for being such great housmates, to Affrica, the best friend I could have, to Lisa for getting me through the last year sanely and helping so much with my thesis, to Mel for being great support for over four years, and to Bec, Cameron, Taryn, and many others. And to Mum and Peter for helping me de-stress at Inverloch. And to all the lab members who have made my time in CESAR such an unforgettable experience. Thanks. Thankyou all for being a part of this with me. v Table of Contents Title-----------------------------------------------------------------------------------------------------------i Abstract ----------------------------------------------------------------------------------------------------ii Declaration -----------------------------------------------------------------------------------------------iv Acknowledgements-------------------------------------------------------------------------------------v Table of Contents --------------------------------------------------------------------------------------vi List of Figures ------------------------------------------------------------------------------------------xv List of Tables -----------------------------------------------------------------------------------------xxiii List of Abbreviations ----------------------------------------------------------------------------------xx vi CHAPTER 1 INTRODUCTION..........................................................................................................1 1.1 THE IMPORTANCE OF INSECTICIDE RESISTANCE.........................................2 1.2 THE “EVOLUTION” OF INSECTICIDES ..............................................................2 1.3 THE EVOLUTION OF RESISTANCE....................................................................3 1.4 MECHANISMS OF RESISTANCE ........................................................................6 1.4.1 BEHAVIOURAL AVOIDANCE .................................................................................8 1.4.2 REDUCED PENETRATION ....................................................................................8 1.4.3 TARGET SITE RESISTANCE.................................................................................9 1.4.3.1 Nervous system targets ............................................................................9 1.4.3.2 Developmental targets............................................................................11 1.4.4 METABOLIC RESISTANCE .................................................................................12 1.4.4.1 Transferases...........................................................................................12 1.4.4.2 Hydrolases..............................................................................................14 1.5 CYROCHROME P450S.......................................................................................16 1.5.1 STRUCTURE AND ORGANISATION......................................................................17 1.5.2 DIVERSITY AND SUBSTRATE SPECIFICITY .........................................................19 1.5.3 P450S AND INSECTICIDE RESISTANCE..............................................................19 1.5.4 MECHANISMS OF P450-BASED RESISTANCE .....................................................20 1.5.4.1 LPR strain of M. domestica.....................................................................21 1.5.4.2 Rutgers strain of M. domestica ...............................................................22 1.5.4.3 91-R strain of D. melanogaster ...............................................................24 1.5.5 CHARACTERISATION OF P450-MEDIATED RESISTANCE ......................................25 1.5.5.1 Indicators of P450 involvement...............................................................26 1.5.5.2 Criteria for demonstrating P450 involvement..........................................26 1.5.5.3 Summary of P450s .................................................................................27 1.5.6 REGULATION OF P450S ...................................................................................28 1.6 MOLECULAR MECHANISMS OF RESISTANCE ..............................................31 1.6.1 POINT MUTATIONS ...........................................................................................32 1.6.2 GENE AMPLIFICATION.......................................................................................33 1.6.3 CHROMOSOMAL ABNORMALITIES......................................................................35 vii 1.6.3.1 Transposable elements...........................................................................35 1.6.3.1.1 Insertions into coding regions...........................................................37 1.6.3.1.2 Insertions into introns .......................................................................38 1.6.3.1.3 Insertions into regulatory regions .....................................................39 1.7 TYPES OF INSECTICIDES .................................................................................41 1.7.1 IGRS ..............................................................................................................44
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