The Octopamine Receptor Octβ2R Regulates Ovulation in Drosophila melanogaster

Oviposition is induced upon mating in most insects. Ovulation is a primary step in oviposition, representing an important target to control insect pests and vectors, but limited information is available on the underlying mechanism. Here we report that the beta adrenergic-like octopamine receptor Oct beta 2R serves as a key signaling molecule for ovulation and recruits protein kinase A and Ca2+/calmodulin-sensitive kinase II as downstream effectors for this activity. We found that the oct beta 2r homozygous mutant females are sterile. They displayed normal courtship, copulation, sperm storage and post-mating rejection behavior but were unable to lay eggs. We have previously shown that octopamine neurons in the abdominal ganglion innervate the oviduct epithelium. Consistently, restored expression of Oct beta 2R in oviduct epithelial cells was sufficient to reinstate ovulation and full fecundity in the oct beta 2r mutant females, demonstrating that the oviduct epithelium is a major site of Oct beta 2R's function in oviposition. We also found that overexpression of the protein kinase A catalytic subunit or Ca2+/calmodulin-sensitive protein kinase U led to partial rescue of oct beta 2r's sterility. This suggests that Oct beta 2R activates cAMP as well as additional effectors including Ca2+ /calmodulin-sensitive protein kinase II for oviposition. All three known beta adrenergic-like octopamine receptors stimulate cAMP production in vitro. Oct beta 1R, when ectopically expressed in the oct beta 2r's oviduct epithelium, fully reinstated ovulation and fecundity. Ectopically expressed Oct beta 3R, on the other hand, partly restored ovulation and fecundity while OAMB-K3 and OAMB-AS that increase Ca2+ levels yielded partial rescue of ovulation but not fecundity deficit. These observations suggest that Oct beta 2R have distinct signaling capacities in vivo and activate multiple signaling pathways to induce egg laying. The findings reported here narrow the knowledge gap and offer insight into novel strategies for insect control.