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The African froghopper Ptyelus flavescens (suborder: Cicadomorpha) contains two novel and one known peptides of the adipokinetic hormone (AKH) family: structure, function and comparison with aphid AKH (suborder: Sternorrhyncha)

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Abstract

The rationale of “green pesticides” in food security is to use information about endogenous hormones of pest insects to make peptide mimetics that will act against the pest insects to alter their behaviour or physiology, while taking care not to harm beneficial insects or other organisms in the food chain. Such “green” insecticides are designed thus, on the basis of neuropeptide ligand–receptor interaction and it is of paramount interest to have finally a mimetic at hand that is harmful only to pest insects. For this concept to work, one has to identify the ligands in pest and beneficial insects. In this study we investigate adipokinetic hormones (AKHs) from a hemipteran source. The most harmful hemipterans on an economic scale are aphids (Hemiptera: Sternorrhyncha: Aphidoidea) of which the AKH is known. Here we identify the AKH complement of a member of a related suborder, the raintree bug or froghopper Ptyelus flavescens (Hemiptera: Cicadomorpha: Cercopoidea). Identification and sequence elucidation of the adipokinetic peptides of this species was achieved by a heterospecific and conspecific trehalose-mobilizing bioassay, and by liquid chromatography coupled to positive electrospray mass spectrometry (LC–ESI–MS) including tandem MS2 spectra obtained by collision-induced dissociation. High resolution MS was employed to distinguish between Gln and Lys residues in the peptides. Three AKHs are discovered in the raintree bug: an octapeptide (Peram-CAH-I: pEVNFSPNW amide) previously known from cockroaches, and two novel decapeptides (Ptyfl-AKH-I: pEINFSTGWGQ amide and Ptyfl-AKH-II: pEINFSTAWGQ amide). The novel peptides were synthesized and the sequence assignments were unequivocally confirmed by co-elution of synthetic peptides and the natural equivalent and by identical MS data of the two forms. A conspecific bioassay in the froghopper describe the endogenous peptide Ptyfl-AKH-I as hypertrehalosemic. In heterologous bioassays the two novel AKHs induce an increase of circulating carbohydrates in cockroaches: Ptyfl-AKH-I is much more active than Ptyfl-AKH-II. Moreover, if the Ile2 in Ptyfl-AKH-II is replaced with a Leu2 residue, biological activity is further diminished. The current data show that the raintree AKH decapeptides differ by four amino acids from the aphid AKH (Acypi-AKH: pEVNFTPTWGQ amide). Therefore, it may be permissible to use the aphid AKH ligand–receptor pair to develop a “green” insecticide to target aphid metabolism.

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Acknowledgements

This work is based on the research supported in part by the National Research Foundation of South Africa (Grant No 85768 [IFR13020116790 to GG] and Grant No. 10924 to HGM). The authors also thank the following organisations for financial support: the Research Council of the University of Cape Town (staff awards to GG and HGM) and the Czech Science Foundation (Project No. 17-22276S to PS). We thank P. Krusberska and M. Moos for help with the MS experiments, and Vic Le Roux for his help with collecting the raintree bugs.

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Authors and Affiliations

  1. Department of Biological Sciences, University of Cape Town, Private Bag, Rondebosch, 7700, South Africa

    Gerd Gäde & Heather G. Marco

  2. Biology Centre, Czech Academy of Sciences, 37005, České Budějovice, Czech Republic

    Petr Šimek

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  1. Gerd Gäde
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  2. Petr Šimek
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  3. Heather G. Marco
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Correspondence to Gerd Gäde.

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All applicable international, national and/or institutional guidelines for the care and use of animals were followed. This article does not contain any studies with human participants performed by any of the authors.

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Handling Editor: M. S. Palma.

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Gäde, G., Šimek, P. & Marco, H.G. The African froghopper Ptyelus flavescens (suborder: Cicadomorpha) contains two novel and one known peptides of the adipokinetic hormone (AKH) family: structure, function and comparison with aphid AKH (suborder: Sternorrhyncha). Amino Acids 49, 1679–1690 (2017). https://doi.org/10.1007/s00726-017-2461-y

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