Final published version
Licence: CC BY: Creative Commons Attribution 4.0 International License
Research output: Contribution to Journal/Magazine › Journal article › peer-review
Research output: Contribution to Journal/Magazine › Journal article › peer-review
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TY - JOUR
T1 - Engineered expression of the invertebrate-specific scorpion toxin AaHIT reduces adult longevity and female fecundity in the diamondback moth Plutella xylostella
AU - Harvey-Samuel, T.
AU - Xu, X.
AU - Lovett, E.
AU - Dafa'alla, T.
AU - Walker, A.
AU - Norman, V.C.
AU - Carter, R.
AU - Teal, J.
AU - Akilan, L.
AU - Leftwich, P.T.
AU - Reitmayer, C.M.
AU - Siddiqui, H.A.
AU - Alphey, L.
PY - 2021/7/31
Y1 - 2021/7/31
N2 - BACKGROUND: 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. RESULTS: 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. CONCLUSION: 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.
AB - BACKGROUND: 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. RESULTS: 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. CONCLUSION: 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.
KW - genetic biocontrol
KW - genetic pest management
KW - neurotoxin
KW - non-cell-autonomous
KW - RIDL
KW - tet-off
U2 - 10.1002/ps.6353
DO - 10.1002/ps.6353
M3 - Journal article
VL - 77
SP - 3154
EP - 3164
JO - Pest Management Science
JF - Pest Management Science
SN - 1526-498X
IS - 7
ER -