The Adipokinetic Peptides of Hemiptera: Structure, Function, and Evolutionary Trends

Abstract

The Hemiptera comprise the most species-rich order of the hemimetabolous insects. Members of a number of superfamilies, most notably especially the more basal ones such as white flies, psyllids and aphids, belong to the most destructive agricultural insects known worldwide. At the other end of the phylogenetic tree are hemipterans that are notorious medical pests (e.g. kissing bugs). Most of the hemipteran species are good flyers, and lipid oxidation plays a pivotal role to power the contraction of flight muscles and, in aquatic water bugs, also deliver the ATP for the extensive swimming action of the leg muscles. Mobilization of stored lipids (mostly triacylglycerols in the fat body) to circulating diacylglycerols in the hemolymph is regulated by a set of small neuropeptides, the adipokinetic hormones (AKHs). We searched the literature and publicly available databases of transcriptomes and genomes to present here AKH sequences from 191 hemipteran species. Only few of these peptides were sequenced via Edman degradation or mass spectrometry, and even fewer were characterized with molecular biology methods; thus, the majority of the AKHs we have identified by bioinformatics are merely predicted sequences at this stage. Nonetheless, a total of 42 AKH primary sequences are assigned to Hemiptera. About 50% of these structures occur also in other insect orders, while the remaining 50% are currently unique for Hemiptera. We find 9 novel AKHs not shown to be synthesized before in any insect. Most of the hemipteran AKHs are octapeptides (28) but there is an impressive number of decapeptides (12) compared to other speciose orders such as Diptera and Lepidoptera. We attempt to construct a hypothetical molecular peptide evolution of hemipteran AKHs and find quite a bit of overlapping with current phylogenetic ideas of the Hemiptera. Lastly, we discuss the possibility to use the sequence of the aphid AKH as lead peptide for the research into a peptide mimetic fulfilling criteria of a green insecticide.

Keywords: AKH primary structure; Hemiptera; insect flight; lipid metabolism; molecular evolution of hemipteran AKHs; phylogeny of Hemiptera; regulation by adipokinetic hormone (AKH); true bugs.

Figure 1

Evolutionary tree of Hemiptera. Adapted from Johnson et al., 2018 (3), this condensed tree reflects only the superfamilies dealt with in the current study. Orders are indicated in purple CAPITAL LETTERS (left); Suborders are in bold letters (left); Infraorders are shown with a black dot and by name on the tree, while superfamilies are indicated on the right of the tree.

Figure 2

Hypothetical molecular evolution of adipokinetic peptides in Hemiptera. Galyu-AKH is assumed as ancestral peptide for this order: 5 AKHs can be directly derived from Galyu-AKH and via point mutations and elongation, the remaining 36 hemipteran AKHs can be derived. Due to space constraints, the figure is split into two panels (A, B). The amino acid substitution or elongation in each peptide is indicated in a larger font than in the peptide from which it is hypothetically derived.