Abstract
Previous genetic pest management (GPM) systems in diamondback moth (DBM) have relied on expressing lethal proteins ('effectors') that are 'cell-autonomous', that is, they do not leave the cell in which they are expressed. To increase the flexibility of future GPM systems in DBM, we aimed to assess the use of a non-cell-autonomous, invertebrate-specific, neurotoxic effector - the scorpion toxin AaHIT. This AaHIT effector was designed to be secreted by expressing cells, potentially leading to effects on distant cells, specifically neuromuscular junctions. Expression of AaHIT caused a 'shaking/quivering' phenotype that could be repressed by provision of an antidote (tetracycline): a phenotype consistent with the AaHIT mode-of-action. This effect was more pronounced when AaHIT expression was driven by the Hr5/ie1 promoter (82.44% of males, 65.14% of females) rather than Op/ie2 (57.35% of males, 48.39% of females). Contrary to expectations, the shaking phenotype and observed fitness costs were limited to adults in which they caused severe reductions in mean longevity (-81%) and median female fecundity (-93%). Quantitative polymerase chain reactions of AaHIT expression patterns and analysis of piggyBac-mediated transgene insertion sites suggest that restriction of the observed effects to the adult stages may be due to the influence of the local genomic environment on the tetO-AaHIT transgene. We demonstrated the feasibility of using non-cell-autonomous effectors within a GPM context for the first time in Lepidoptera, one of the most economically damaging orders of insects. These findings provide a framework for extending this system to other pest Lepidoptera and to other secreted effectors. © 2021 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.
Highlights
The diamondback moth - DBM (Plutella xylostella) is a highly invasive and economically important pest of brassicas, costing upwards of $5 billion in damage and control measures each year.[1, 2] Contributing to the notoriety of this pest is its extreme insecticide resistance with populations having developed resistance to most classes of insecticides, including Bacillus thuringiensis (Bt) Cry toxins and DDT.[3]
We have demonstrated the feasibility of using non cellautonomous effectors within a Genetic Pest Management (GPM) context for the first time in the Lepidoptera, one of the most economically damaging orders of insects
In terms of the doublesex-based female-lethal system developed in DBM, glasshouse trials have shown that repeated releases of these homozygous males can result in eradication of caged wild-type populations and, delay evolution of Bt resistance[11, 12], a finding in agreement with previous modelling.[13, 14]
Summary
The diamondback moth - DBM (Plutella xylostella) is a highly invasive and economically important pest of brassicas, costing upwards of $5 billion in damage and control measures each year.[1, 2] Contributing to the notoriety of this pest is its extreme insecticide resistance with populations having developed resistance to most classes of insecticides, including Bacillus thuringiensis (Bt) Cry toxins and DDT.[3]. A related technology not utilising the doublesex cassette and which resulting in lethality of both males and females off tetracycline has been developed in pink bollworm.[9] An orthogonal system in B. mori to the female lethal system described above utilises a W-chromosome linked (female-linked) germline expressing Cas[9] insertion, and an autosomal sgRNA targeting the transformer 2 gene essential for embryonic viability Crosses between these two lines resulted in embryonic death of all female offspring.[10] In terms of the doublesex-based female-lethal system developed in DBM, glasshouse trials have shown that repeated releases of these homozygous males can result in eradication of caged wild-type populations and, delay evolution of Bt resistance[11, 12], a finding in agreement with previous modelling.[13, 14] Wind tunnel experiments have demonstrated that these males retain the ability to locate and respond to female pheromone plumes[15] and open-field trials have shown that these males are able to disperse within a realistic crop setting.[16]. This AaHIT effector was designed to be secreted by expressing cells, potentially leading to effects on distant cells, neuromuscular junctions
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