Engineered expression of the invertebrate-specific scorpion toxin AaHIT reduces adult longevity and female fecundity in the diamondback moth Plutella xylostella.
RIDL
genetic biocontrol
genetic pest management
neurotoxin
non-cell-autonomous
tet-off
Journal
Pest management science
ISSN: 1526-4998
Titre abrégé: Pest Manag Sci
Pays: England
ID NLM: 100898744
Informations de publication
Date de publication:
Jul 2021
Jul 2021
Historique:
revised:
12
02
2021
received:
14
09
2020
accepted:
04
03
2021
pubmed:
5
3
2021
medline:
16
6
2021
entrez:
4
3
2021
Statut:
ppublish
Résumé
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.
Sections du résumé
BACKGROUND
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
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
CONCLUSIONS
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.
Substances chimiques
Scorpion Venoms
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
3154-3164Subventions
Organisme : UK Biotechnology and Biological Sciences Research Council (BBSRC)
ID : BBS/E/I/00007038
Organisme : European Union H2020 Grant nEUROSTRESSPEP
ID : 634361
Organisme : Biotechnology and Biological Sciences Research Council
ID : BBS/E/I/00007039
Pays : United Kingdom
Organisme : (BBSRC) Impact Acceleration Account grant
ID : BB/S506680/1
Organisme : UK Biotechnology and Biological Sciences Research Council (BBSRC)
ID : BBS/E/I/00007033
Organisme : Wellcome Trust Investigator Award
ID : 110117/Z/15/Z
Organisme : UK Biotechnology and Biological Sciences Research Council (BBSRC)
ID : BBS/E/I/00
Organisme : Biotechnology and Biological Sciences Research Council
ID : BBS/E/I/00007033
Pays : United Kingdom
Organisme : Biotechnology and Biological Sciences Research Council
ID : BBS/E/I/00007038
Pays : United Kingdom
Informations de copyright
© 2021 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.
Références
Furlong MJ, Wright DJ and Dosdall LM, Diamondback moth ecology and management: problems, progress, and prospects. Annu Rev Entomol 58:517-541 (2013).
Zalucki MP, Shabbir A, Silva R, Adamson D, Liu S-S and Furlong MJ, Estimating the economic cost of one of the world's major insect pests, Plutella xylostella (Lepidoptera: Plutellidae): just how Long is a piece of string? J Econ Entomol 105:1115-1129 (2012).
Talekar NS and Shelton AM, Biology, ecology, and management of the diamondback moth. Annu Rev Entomol 38:275-301 (1993).
Jin L, Walker AS, Fu G, Harvey-Samuel T, Dafa'alla T, Miles A et al., Engineered female-specific lethality for control of pest Lepidoptera. ACS Synth Biol 2:160-166 (2013).
Alphey L, Re-engineering the sterile insect technique. Insect Biochem Mol Biol 32:1243-1247 (2002).
Black WC, Alphey L and James AA, Why RIDL is not SIT. Trends Parasitol 27:362-370 (2011).
Harvey-Samuel T, Ant T, Gong H, Morrison NI and Alphey L, Population-level effects of fitness costs associated with repressible female-lethal transgene insertions in two pest insects. Evol Appl 7:597-606 (2014).
Tan A, Fu G, Jin L, Guo Q, Li Z, Niu B et al., Transgene-based, female-specific lethality system for genetic sexing of the silkworm, Bombyx mori. Proc Natl Acad Sci U S A 110:6766-6770 (2013).
Morrison NI, Simmons GS, Fu G, O'Connell S, Walker AS, Dafa'alla T et al., Engineered repressible lethality for controlling the pink bollworm, a lepidopteran pest of cotton. PLoS One 7:e50922 (2012).
Zhang ZJ, Niu BL, Ji DF, Li MW, Li K, James AA et al., Silkworm genetic sexing through W chromosome-linked, targeted gene integration. Proc Natl Acad Sci U S A 115:8752-8756 (2018).
Harvey-Samuel T, Morrison NI, Walker AS, Marubbi T, Yao J, Collins HL et al., Pest control and resistance management through release of insects carrying a male-selecting transgene. BMC Biol 13:49 (2015).
Zhou LQ, Alphey N, Walker AS, Travers LM, Morrison NI, Bonsall MB et al., The application of self-limiting transgenic insects in managing resistance in experimental metapopulations. J Appl Ecol 56:688-698 (2019).
Alphey N, Bonsall MB and Alphey L, Combining pest control and resistance management: synergy of engineered insects with Bt crops. J Econ Entomol 102:717-732 (2009).
Alphey N, Coleman PG, Donnelly CA and Alphey L, Managing insecticide resistance by mass release of engineered insects. J Econ Entomol 100:1642-1649 (2007).
Bolton M, Collins HL, Chapman T, Morrison NI, Long SJ, Linn CE et al., Response to a synthetic pheromone source by OX4319L, a self-limiting diamondback moth (Lepidoptera: Plutellidae) strain, and field dispersal characteristics of its progenitor strain. J Econ Entomol 112:1546-1551 (2019).
Shelton AM, Long SJ, Walker AS, Bolton M, Collins HL, Revuelta L et al., First field release of a genetically engineered, self-limiting agricultural pest insect: evaluating its potential for future crop protection. Front Bioeng Biotechnol 7 (2020). https://doi.org/10.3389/fbioe.2019.00482.
Phuc HK, Andreasen MH, Burton RS, Vass C, Epton MJ, Pape G et al., Late-acting dominant lethal genetic systems and mosquito control. BMC Biol 5:11 (2007).
Gossen M and Bujard H, Tight control of gene-expression in mammalian-cells by tetracycline-responsive promoters. Proc Natl Acad Sci U S A 89:5547-5551 (1992).
Bryk J, Reeves RG, Reed FA and Denton JA, Transcriptional effects of a positive feedback circuit in Drosophila melanogaster. BMC Genomics 18:990 (2017).
Fu GL, Lees RS, Nimmo D, Aw D, Jin L, Gray P et al., Female-specific flightless phenotype for mosquito control. Proc Natl Acad Sci U S A 107:4550-4554 (2010).
Labbe GMC, Scaife S, Morgan SA, Curtis ZH and Alphey L, Female-specific flightless (fsRIDL) phenotype for control of Aedes albopictus. PLoS Negl Trop Dis 6:e1724 (2012).
Marinotti O, Jasinskiene N, Fazekas A, Scaife S, Fu G, Mattingly ST et al., Development of a population suppression strain of the human malaria vector mosquito, Anopheles stephensi. Malar J 12:142 (2013).
Haghighat-Khah RE, Harvey-Samuel T, Basu S, StJohn O, Scaife S, Verkuijl S et al., Engineered action at a distance: blood-meal-inducible paralysis in Aedes aegypti. PLoS Negl Trop Dis 13:e0007579 (2019).
Deng SQ, Chen JT, Li WW, Chen M and Peng HJ, Application of the scorpion neurotoxin AaIT against insect pests. Int J Mol Sci 20 (2019). https://doi.org/10.3390/ijms20143467.
Martins S, Naish N, Walker AS, Morrison NI, Scaife S, Fu G et al., Germline transformation of the diamondback moth, Plutella xylostella L., using the piggyBac transposable element. Insect Mol Biol 21:414-421 (2012).
Fu W, Xie W, Zhang Z, Wang SL, Wu QJ, Liu Y et al., Exploring valid reference genes for quantitative real-time PCR analysis in Plutella xylostella (Lepidoptera: Plutellidae). Int J Biol Sci 9:792-802 (2013).
Perkins JR, Dawes JM, McMahon SB, Bennett DLH, Orengo C and Kohl M, ReadqPCR and NormqPCR: R packages for the reading, quality checking and normalisation of RT-qPCR quantification cycle (Cq) data. BMC Genomics 13:296 (2012).
Hellemans J, Mortier G, de Paepe A, Speleman F and Vandesompele J, qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol 8:R19 (2007).
Therneau MT and Grambsch PM, Modeling Survival Data: Extending the Cox Model. Springer, New York, NY (2000).
Wickham H, Averick M, Bryan J, Chang W, D'agostino McGowan L, Francois R et al., Welcome to the tidyverse. J Open Source Software 4:43 (2019).
Kokoza V, Ahmed A, Cho WL, Jasinskiene N, James AA and Raikhel A, Engineering blood meal-activated systemic immunity in the yellow fever mosquito, Aedes aegypti. Proc Natl Acad Sci U S A 97:9144-9149 (2000).
Romans P, Tu ZJ, Ke ZX and Hagedorn HH, Analysis of a vitellogenin gene of the mosquito, Aedes aegypti and comparisons to vitellogenins from other organisms. Insect Biochem Mol Biol 25:939-958 (1995).
Kokoza VA and Raikhel AS, Targeted gene expression in the transgenic Aedes aegypti using the binary Gal4-UAS system. Insect Biochem Mol Biol 41:637-644 (2011).
Vella MR, Gould F and Lloyd AL, Mathematical modeling of genetic pest management through female lethality with independently segregating alleles. bioRxiv (2020). https://doi.org/10.1101/2020.04.06.028738.
Furlong MJ, Pell JK, Pek Choo O and Abdul Rahman S, Field and laboratory evaluation of a sex pheromone trap for the autodissemination of the fungal entomopathogen Zoophthora radicans (Entomophthorales) by the diamondback moth, Plutella xylostella (Lepidoptera: Yponomeutidae). Bull Entomol Res 85:331-337 (1995).