Assessment of insecticidal effects and selectivity of CAPA-PK peptide analogues against the peach-potato aphid and four beneficial insects following topical exposure.

CAPA aphicide biosafety pest control topical application

Journal

Pest management science
ISSN: 1526-4998
Titre abrégé: Pest Manag Sci
Pays: England
ID NLM: 100898744

Informations de publication

Date de publication:
Oct 2020
Historique:
received: 28 09 2019
revised: 12 06 2020
accepted: 25 06 2020
pubmed: 26 6 2020
medline: 21 10 2020
entrez: 26 6 2020
Statut: ppublish

Résumé

Insect Capability neuropeptides (CAP2b/CAPA-PKs) play a critical role in modulating different physiologies and behavior in insects. In a previous proof-of-concept study, the CAP2b analogues 1895 (2Abf-Suc-FGPRLamide) and 2129 (2Abf-Suc-ATPRIamide) were reported to reduce aphid fitness when administered by injection. In the current study, the insecticidal efficacy of 1895 and 2129 on the peach potato aphid Myzus persicae was analyzed by topical application, simulating a spray application scenario in the field. Additionally, the selectivity of the tested analogues was evaluated against a selection of beneficial insects, namely three natural enemies (Adalia bipunctata, Chrysoperla carnea and Nasonia vitripennis) and a pollinator (Bombus terrestris). Within 3-5 days post topical exposure of aphids to 1895, higher mortality (33%) was observed, as was the case for the treatment with 2129 (17%) and the mixture of 1895 + 2129 (47%) compared to the control (3%). 1895 and the mix 1895 + 2129 showed the strongest and comparable insecticidal effects. Additionally, surviving aphids treated with 1895 showed a reduction in total lifetime reproduction (GRR) of 30%, 19% with 2129 and 39% with the mix 1895 + 2129. Of interest from a biosafety perspective is that by using the same delivery method and dose, no significant effects on survival, weight increase and food intake was observed for the representative natural enemies and the pollinator. This study highlights the potential of exploiting CAP2b analogues such as 1895 (core structure FGPRL) as aphicides. Additionally, the CAP2b analogues used in this study were selective as they showed no effects when applied on four representative beneficial insects.

Sections du résumé

BACKGROUND BACKGROUND
Insect Capability neuropeptides (CAP2b/CAPA-PKs) play a critical role in modulating different physiologies and behavior in insects. In a previous proof-of-concept study, the CAP2b analogues 1895 (2Abf-Suc-FGPRLamide) and 2129 (2Abf-Suc-ATPRIamide) were reported to reduce aphid fitness when administered by injection. In the current study, the insecticidal efficacy of 1895 and 2129 on the peach potato aphid Myzus persicae was analyzed by topical application, simulating a spray application scenario in the field. Additionally, the selectivity of the tested analogues was evaluated against a selection of beneficial insects, namely three natural enemies (Adalia bipunctata, Chrysoperla carnea and Nasonia vitripennis) and a pollinator (Bombus terrestris).
RESULTS RESULTS
Within 3-5 days post topical exposure of aphids to 1895, higher mortality (33%) was observed, as was the case for the treatment with 2129 (17%) and the mixture of 1895 + 2129 (47%) compared to the control (3%). 1895 and the mix 1895 + 2129 showed the strongest and comparable insecticidal effects. Additionally, surviving aphids treated with 1895 showed a reduction in total lifetime reproduction (GRR) of 30%, 19% with 2129 and 39% with the mix 1895 + 2129. Of interest from a biosafety perspective is that by using the same delivery method and dose, no significant effects on survival, weight increase and food intake was observed for the representative natural enemies and the pollinator.
CONCLUSION CONCLUSIONS
This study highlights the potential of exploiting CAP2b analogues such as 1895 (core structure FGPRL) as aphicides. Additionally, the CAP2b analogues used in this study were selective as they showed no effects when applied on four representative beneficial insects.

Identifiants

pubmed: 32583901
doi: 10.1002/ps.5971
doi:

Substances chimiques

Insecticides 0
Peptides 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

3451-3458

Subventions

Organisme : Research Foundation
Organisme : Ghent University
Organisme : Special Research Fund
Organisme : Horizon 2020
Organisme : European Union

Informations de copyright

© 2020 Society of Chemical Industry.

Références

Wilson C and Tisdell C, Why farmers continue to use pesticides despite environmental, health and sustainability costs. Ecol Econ 39:449-462 (2001).
Altstein M and Nassel DR, Neuropeptide signaling in insects, Geary TG, Maule AG, in Neuropeptide Systems as Targets for Parasite and Pest Control. Springer, Boston, MA, pp. 155-165 (2010).
Schoofs L, De Loof A and Van Hiel MB, Neuropeptides as regulators of behavior in insects. Annu Rev Entomol 62:35-52 (2017).
Altstein M, Insect neuropeptide antagonists. Biopolymers 60:460-473 (2001).
Audsley N and Down RE, G protein coupled receptors as targets for next generation pesticides. Insect Biochem Molec 67:27-37 (2015).
Smagghe G, Mandian K, Zubrzak P and Nachman RJ, Antifeedant activity and high mortality in the pea aphid Acyrthosiphon pisum (Hemiptera: Aphidae) induced by biostable insect kinin analogs. Peptides 31:498-505 (2010).
Zhang CL, Qu YY, Wu XQ, Song DL, Ling Y and Yang XL, Design, synthesis and aphicidal activity of N-terminal modified insect kinin analogs. Peptides 68:233-238 (2015).
Nachman RJ, Mahdian K, Nassel DR, Isaac RE, Pryor N and Smagghe G, Biostable multi-Aib analogs of tachykinin-related peptides demonstrate potent oral aphicidal activity in the pea aphid Acyrthosiphon pisum (Hemiptera: Aphidae). Peptides 32:587-594 (2011).
Zhang QR, Nachman RJ, Kaczmarek K, Zabrocki J and Denlinger DL, Disruption of insect diapause using agonists and an antagonist of diapause hormone. Proc Natl Acad Sci U S A 108:16922-16926 (2011).
Zhang QR, Nachman RJ, Kaczmarek K, Kierus K, Zabrocki J and Denlinger DL, Development of neuropeptide analogs capable of traversing the integument: a case study using diapause hormone analogs in Helicoverpa zea. Insect Biochem Mol Biol 67:87-93 (2015).
Yu N, Benzi V, Zotti MJ, Staljanssens D, Kaczmarek K, Zabrocki J et al., Analogs of sulfakinin-related peptides demonstrate reduction in food intake in the red flour beetle, Tribolium castaneum, while putative antagonists increase consumption. Peptides 41:107-112 (2013).
Nassel DR and Winther AME, Drosophila neuropeptides in regulation of physiology and behavior. Prog Neurobiol 92:42-104 (2010).
Davies SA, Cabrero P, Povsic M, Johnston NR, Terhzaz S and Dow JAT, Signaling by Drosophila capa neuropeptides. Gen Comp Endocr 188:60-66 (2013).
Terhzaz S, Alford L, Yeoh JG, Marley R, Dornan AJ, Dow JA et al., Renal neuroendocrine control of desiccation and cold tolerance by Drosophila suzukii. Pest Manag Sci 74:800-810 (2018).
Terhzaz S, Teets NM, Cabrero P, Henderson L, Ritchie MG, Nachman RJ et al., Insect Capa neuropeptides impact desiccation and cold tolerance. Proc Natl Acad Sci U S A 112:2882-2887 (2015).
Nachman RJ, Wang XDJ, Etzkorn FA, Kaczmarek K, Zabrocki J, Lopez J et al., Evaluation of insect CAP2b analogs with either an (E)-alkene, trans- or a (Z)-alkene, cis-Pro isostere identifies the Pro orientation for antidiuretic activity in the stink bug. Peptides 41:101-106 (2013).
Alford L, Marley R, Dornan A, Pierre JS, Dow JAT, Nachman RJ et al., Assessment of neuropeptide binding sites and the impact of biostable kinin and CAP2b analogue treatment on aphid (Myzus persicae and Macrosiphum rosae) stress tolerance. Pest Manag Sci 75:1750-1759 (2019).
Nault LR, Arthropod transmission of plant viruses: a new synthesis. Ann Entomol Soc Am 90:521-541 (1997).
Van Emden HF and Harrington R, Aphids as Crop Pests. CABI, Wallingford, p. 717 (2007).
Andrewartha HG and Birch C, The Distribution and Abundance of Animals. University of Chicago Press, Chicago, IL, p. 782 (1954).
Yeoh JGC, Pandit AA, Zandawala M, Nassel DR, Davies SA and Dow JAT, DINeR: database for insect neuropeptide research. Insect Biochem Mol Biol 86:9-19 (2017).
Pandit AA, Davies SA, Smagghe G and Dow JA, Evolutionary trends of neuropeptide signaling in beetles-a comparative analysis of coleopteran transcriptomic and genomic data. Insect Biochem Mol Biol 114:103227 (2019).
Tamura K, Peterson D, Peterson N, Stecher G, Nei M and Kumar S, MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731-2739 (2011).
Niu J, Yang WJ, Tian Y, Fan JY, Ye C, Shang F et al., Topical dsRNA delivery induces gene silencing and mortality in the pea aphid. Pest Manag Sci 75:2873-2881 (2019).
Shakesby AJ, Wallace IS, Isaacs HV, Pritchard J, Roberts DM and Douglas AE, A water-specific aquaporin involved in aphid osmoregulation. Insect Biochem Mol Biol 39:1-10 (2009).
Douglas AE, Phloem-sap feeding by animals: problems and solutions. J Exp Bot 57:747-754 (2006).
Davies SA, Huesmann GR, Maddrell SHP, ODonnell MJ, Skaer NJV, Dow JAT et al., CAP2b, a cardioacceleratory peptide, is present in Drosophila and stimulates tubule fluid secretion via cGMP. Am J Physiol Reg I 269:R1321-R1326 (1995).
Jing XF, White TA, Yang XW and Douglas AE, The molecular correlates of organ loss: the case of insect Malpighian tubules. Biol Lett 11:2150514 (2015).
Jiang HB, Wei ZJ, Nachman RJ, Kaczmarek K, Zabrocki J and Park YS, Functional characterization of five different PRXamide receptors of the red flour beetle Tribolium castaneum with peptidomimetics and identification of agonists and antagonists. Peptides 68:246-252 (2015).
Alford L, Marley R, Dornan A, Dow JAT, Nachman RJ and Davies SA, Desiccation, thermal stress and associated mortality in Drosophila fruit flies induced by neuropeptide analogue treatment. J Pest Sci 9:1123-1137 (2019).
Hauser F, Neupert S, Williamson M, Predel R, Tanaka Y and Grimmelikhuijzen CJP, Genomics and peptidomics of neuropeptides and protein hormones present in the parasitic wasp Nasonia vitripennis. J Proteome Res 9:5296-5310 (2010).

Auteurs

Shun-Hua Gui (SH)

Laboratory of Agrozoology, Department of Plants and Crops, Ghent University, Ghent, Belgium.

Clauvis Nt Taning (CN)

Laboratory of Agrozoology, Department of Plants and Crops, Ghent University, Ghent, Belgium.

Kristof De Schutter (K)

Laboratory of Agrozoology, Department of Plants and Crops, Ghent University, Ghent, Belgium.

Qun Yang (Q)

Laboratory of Agrozoology, Department of Plants and Crops, Ghent University, Ghent, Belgium.

Pengyu Chen (P)

Laboratory of Agrozoology, Department of Plants and Crops, Ghent University, Ghent, Belgium.

Mohamad Hamshou (M)

Laboratory of Agrozoology, Department of Plants and Crops, Ghent University, Ghent, Belgium.

Ronald J Nachman (RJ)

U.S. Department of Agriculture, College Station, Insect Control and Cotton Disease Research Unit, Southern Plains Agricultural Research Center, TX, USA.

Aniruddha A Pandit (AA)

Institute of Molecular, Cell and Systems Biology, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, UK.

Julian At Dow (JA)

Institute of Molecular, Cell and Systems Biology, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, UK.

Shireen Davies (S)

Institute of Molecular, Cell and Systems Biology, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, UK.

Guy Smagghe (G)

Laboratory of Agrozoology, Department of Plants and Crops, Ghent University, Ghent, Belgium.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH