Dedicated acetic acid preference coded by broad spectrum ionotropic receptors in a moth species

Abstract

Acetic acid as one of the food related odorant cues attracts many insect species. In the moth Mythimna separata, the olfaction of acid was coded via multiple pathways including 3 sensilla types on the antennae and 3 glomeruli in the antennal lobes. Among, suitable dosages of acetic acid exclusively activated DC3 glomerulus that receives integrated projections across sensilla types, which drives attractiveness and feeding attempts of the moth. This circuit encodes broad spectrum ionotropic receptors 8a, 75q1 and 75q2 which were sufficient to confer acid responsiveness in Xenopus oocytes. Ir75q2 was expressed in vivo with Ir75q1 and it enhanced sensitivity of the receptor functional group toward acids. Furthermore, Ir75q1 and Ir75q2 are both necessary for the moth to conduct acetic acid induced reactions of sensilla, DC3 glomerulus as well as attractiveness. Together, it reveals that an indispensable tetramer IR-based unit is employed to fulfill acetic acid specialized preference under suitable dosages through balancing of transcription and peripheral coding. Understanding of the Ir75q1/2 olfactory pathway provides insights into investigations on acid sensory process in insects.\n\nAuthor SummaryThe preference to acids are common in various organisms, and it may involve both olfactory and gustatory reception. In particular, airborne acidity volatiles can be sensed through antennae of insects and later assessed to help locating foraging, mating, and egg laying sites. However, these stimulatory processes can only be delivered by suitable dosages of acids, as we all know that, high acidity could be fatal in most circumstances. To date, avoidance to acids has been well explained in insects, but attractiveness and its basis remain uncharted. In the brain of oriental armyworm Mythimna separata, we have located 3 olfactory pathways which may play roles in acetic acid reception. Fortunately, when acetic acid was applied at attractive dosages, it only activated 1 dedicated pathway among the three. Later we found that this attractiveness pathway employed two ionotropic receptor genes namely Ir75q1 and Ir75q2, to successfully deliver this trait. Both genes were necessary for the moth to conduct acetic acid preference, but their roles are different. Ir75q1 recognized the acetic acid ligand and Ir75q2 later amplify the sensitivity. By comparing with evidences from electrophysiology and brain imaging tests, we found that the expression bias of either of the two genes has caused the separation of the pathways. It has been revealed in this moth that a smart decision system for olfactory reception exists, and this system may extrapolate to other insect species, as Ir75q1 and Ir75q2 are commonly expressed in many insect families.