Acetylcholinesterase genes within the Diptera: takeover and loss in true flies

Abstract

It has recently been reported that the synaptic acetylcholinesterase (AChE) in mosquitoes is encoded by the ace-1 gene, distinct and divergent from the ace-2 gene, which performs this function in Drosophila. This is an unprecedented situation within the Diptera order because both ace genes derive from an old duplication and are present in most insects and arthropods. Nevertheless, Drosophila possesses only the ace-2 gene. Thus, a secondary loss occurred during the evolution of Diptera, implying a vital function switch from one gene (ace-1) to the other (ace-2). We sampled 78 species, representing 50 families (27% of the Dipteran families) spread over all major subdivisions of the Diptera, and looked for ace-1 and ace-2 by systematic PCR screening to determine which taxonomic groups within the Diptera have this gene change. We show that this loss probably extends to all true flies (or Cyclorrhapha), a large monophyletic group of the Diptera. We also show that ace-2 plays a non-detectable role in the synaptic AChE in a lower Diptera species, suggesting that it has non-synaptic functions. A relative molecular evolution rate test showed that the intensity of purifying selection on ace-2 sequences is constant across the Diptera, irrespective of the presence or absence of ace-1, confirming the evolutionary importance of non-synaptic functions for this gene. We discuss the evolutionary scenarios for the takeover of ace-2 and the loss of ace-1, taking into account our limited knowledge of non-synaptic functions of ace genes and some specific adaptations of true flies.

Organophosphates' resistance in the B-biotype of Bemisia tabaci (Hemiptera: Aleyrodidae) is associated with a point mutation in an ace1-type acetylcholinesterase and overexpression of carboxylesterase

“…Part of the complexity can be attributed to the finding that more than one ace gene is encoding the synaptic AChE target (Huchard et al, 2006). Only one ace gene (now called ace2) exists in all true flies (or Cyclorrhapha), a large monophyletic group of the Diptera including the Drosophila melanogaster, M. domestica, L. cuprina, and Bactrocera oleae species (Huchard et al, 2006). In contrast, many other insects and ticks have at least two genes encoding AChE, termed ace1 and ace2: Anopheles gambiae and Culex pipiens (Weill et al, 2002), Culex tritaeniorhynchus (Nabeshima et al, 2004), Anopheles albimanus (Weill et al, 2004), Boophilus microplus (Baxter and Barker, 2002), Aphis gossypii (Benting and Nauen, 2004;Toda et al, 2004), Myzus persicae (Nabeshima et al, 2003), Schizaphis graminum (Gao et al, 2002), Plutella xylostella (Baek et al, 2005) and Helicoverpa assulta (Lee et al, 2006).…”

“…These altered forms have wide differing spectra of insensitivity between species, as well as a marked range of insensitivity to different compounds within species. Part of the complexity can be attributed to the finding that more than one ace gene is encoding the synaptic AChE target (Huchard et al, 2006). Only one ace gene (now called ace2) exists in all true flies (or Cyclorrhapha), a large monophyletic group of the Diptera including the Drosophila melanogaster, M. domestica, L. cuprina, and Bactrocera oleae species (Huchard et al, 2006).…”

Terpenes: Natural Products for Controlling Insects of Importance to Human Health—A Structure-Activity Relationship Study

“…Thus, the control of the activity of this enzyme is very important in determining the insecticidal capacity of natural or synthetic chemicals, with AChE consequently being the primary target of organophosphorus pesticides and carbamates [85,86] as well as of some essential oils and their components [38,49,87,88]. However, the AChE in resistant insects is able to change its active site or create new forms of the enzyme, in response to selective pressure after several years of the application of synthetic pesticides [86,[89][90][91][92][93][94][95][96][97][98].…”

Untitled

“…Revista Bio Ciencias 4(6), Article ID 04.06.01 December 2017 presentes en A. gambiae (Weill et al, 2002;Fournier, 2005), sin embargo, en D. melanogaster la AChE es codificada úni-camente por ace2 (Fournier et al, 1993;Weill et al, 2002;Huchard et al, 2006); estudios en otros insectos que poseen ambos genes, sugieren que ace1 es el gen responsable de una mayor actividad de la AChE (Revuelta et al, 2009;Revuelta et al, 2011).…”