Evolutionary origin and status of two insect acetylcholinesterases and their structural conservation and differentiation

Abstract

Acetylcholinesterase (AChE) plays a pivotal role in synaptic transmission in the cholinergic nervous system of most animals, including insects. Insects possess duplicated AChE gene loci (ace1 vs. ace2) encoding two distinct AChEs (AChE1 and AChE2). A phylogenetic analysis suggested that the last common ancestor of two aces shared its origin with Platyhelminthes. In addition, the ace duplication event likely occurred after the divergence of Protostomian but before the split of Ecdysozoa. The ace1 lineage exhibited a significantly lower evolutionary rate (d and dN/dS ratio) than the ace2 lineage, suggesting that the ace1 lineage has retained the essential function of synaptic transmission following its duplication. Therefore, the putative functional transition from ace1 to ace2 observed in some Hymenopteran insects appears to be a local and relatively recent event. The amino acid sequence comparison and three-dimensional modeling of insect AChEs identified a few consistent differences in the amino acid residues in functionally crucial domains between two AChEs, which are likely responsible for the functional differentiation between two AChEs. A unique amino acid substitution causing a dramatic reduction in the catalytic activity of AChE1 in some Hymenopteran insects was suggested to be responsible for the aforementioned functional transition of ace.

Two Bombyx mori acetylcholinesterase genes influence motor control and development in different ways

“…Since then, the presence of two ace s have been confirmed in many insect species, including the mosquitoes Culex pipiens 4 , Aedes aegypti 5 , Culex tritaeniorhynchus 6 , the aphids Myzus persicae 7 , Rhopalosiphum padi and Sitobion avenae 8 , the cockroach Blattella germanica 9 , the lepidopterans Helicoverpa assulta 10 , Plutella xylostella 11 , Chilo suppressalis 12 and Cnaphalocrocis medinalis 13 , the whitefly Bemisia tabaci 14 and the red flour beetle, Tribolium castaneum 15 , to name some of them. It was suggested that two ace genes may have originated from gene duplication before insect speciation 15, 16 . However, outside of mosquitoes, ace2 , but not ace 1, have been reported in the model insect Drosophila melanogaster and other Drosophila species.…”

Comparisons of morphology and esterase levels between Blattella germanica and Blattella nipponica (Blattodea: Blattellidae)

“…Signal peptides were predicted by the signalP program only in Bgace2 and Bnace2 . In ace1 ‐type and ace2‐ type AChEs, the ace2‐ specific region was clearly identified (Cha & Lee ) (Figure S1), and the genes were located on a phylogenetic tree (Figure S2). Based on this result, invertebrate AChE and vertebrate AChE, as well as butyrylcholinesterase (BChE), were divergent from the ancient common ancestral cholinesterase (ChE).…”

Natural genomic amplification of cholinesterase genes in animals

“…In insects, there are one or two AChE genes ( ace1, ace2 ), of which at least one plays a major role in the central cholinergic nervous system (Huchard et al . ; Kim and Lee ; Cha and Lee ). In Arachnida (e.g.…”

“…A more thorough study determined that duplicated AChE genes in insects are under purifying selection and that some new specialization or essentiality appeared in the most divergent copy. Even though there are differences in the evolutionary rates of the two genes, the smallest value is not always associated with the gene that retained the main neuronal function (Cha and Lee ). However, carboxylesterases and AChE are rather large proteins and the number of amino acid residues crucial for the catalytic activity is limited (Sussman et al .…”