Functional expression and characterization of CAPA receptor in the digestive tract and life stages of Drosophila suzukii, and differential activities with insect PRXamide peptides

Abstract

AbstractSpotted‐wing drosophila, Drosophila suzukii (Matsumura), is an invasive vinegar fly that is a major threat to the small fruits industries globally. Insect capa genes encode multiple neuropeptides, including CAPA‐periviscerokinin (CAPA‐PVK) peptides, that are specifically known to cause diuresis or anti‐diuresis in various organisms. Here we identified and characterized a corresponding G protein‐coupled receptor (GPCR) of the D. suzukii CAPA‐PVK peptides: CAPA receptor (CAPA‐R). To better characterize the behavior of D. suzukii CAPA‐R, we used insect cell‐based functional expression assays to evaluate responses of CAPA‐R against D. suzukii CAPA‐PVKs, CAPA‐PVKs from five species in Insecta, one species from Mollusca, modified CAPA‐PVK peptides, and some PRXamide family peptides: pyrokinin (PK), diapause hormone (DH), and ecdysis‐triggering hormone (ETH). Functional studies revealed that the D. suzukii CAPA‐R is strongly activated by both of its own natural D. suzukii CAPA‐PVKs, and interestingly, it was strongly activated by other CAPA‐PVK peptides from Frankliniella occidentallis (Thysanoptera), Solenopsis invicta (Hymenoptera), Helicoverpa zea (Lepidoptera) and Plutella xylostella (Lepidoptera). However, D. suzukii CAPA‐R was not activated by Mollusca CAPA‐PVK or the other PRXamide peptides. Gene expression analyses showed that the CAPA‐R was highly expressed in the Malpighian tubules and moderately in hindgut compared to other digestive organs or the rest of body, supporting diuretic/antidiuretic functionality. When compared across life stages of D. suzukii, expression of CAPA‐R was approximately 1.5x greater in the third instar than the other stages and minimally detected in the eggs, 4‐day old pupae and 3‐day old adults. Our results functionally characterized the D. suzukii CAPA‐R and a few short peptides were identified as potential biological targets to exploit the CAPA‐R for D. suzukii management.