Ionotropic Chemosensory Receptors Mediate the Taste and Smell of Polyamines

Abstract

The ability to find and consume nutrient-rich diets for successful reproduction and survival is fundamental to animal life. Among the nutrients important for all animals are polyamines, a class of pungent smelling compounds required in numerous cellular and organismic processes. Polyamine deficiency or excess has detrimental effects on health, cognitive function, reproduction, and lifespan. Here, we show that a diet high in polyamine is beneficial and increases reproductive success of flies, and we unravel the sensory mechanisms that attract Drosophila to polyamine-rich food and egg-laying substrates. Using a combination of behavioral genetics and in vivo calcium imaging, we demonstrate that Drosophila uses multisensory detection to find and evaluate polyamines present in overripe and fermenting fruit, their favored feeding and egg-laying substrate. In the olfactory system, two coexpressed ionotropic receptors (IRs), IR76b and IR41a, mediate the long-range attraction to the odor. In the gustatory system, multimodal taste sensation by IR76b receptor and GR66a bitter receptor neurons is used to evaluate quality and valence of the polyamine providing a mechanism for the fly’s high attraction to polyamine-rich and sweet decaying fruit. Given their universal and highly conserved biological roles, we propose that the ability to evaluate food for polyamine content may impact health and reproductive success also of other animals including humans.

Variant Ionotropic Receptors in the Malaria Vector Mosquito Anopheles gambiae Tuned to Amines and Carboxylic Acids

“…Importantly, DmIr41a , the Drosophila homolog of AgIr41a , confers sensitivity to 1,4 diaminobutane (putrescine) in ac2 coeloconic sensilla13. Moreover, DmIr41a and DmIr76b are required for behavioral attraction of fruitflies to putrescine and cadaverine32.…”

Molecular and Cellular Organization of Taste Neurons in Adult Drosophila Pharynx

“…We also examined a number of Ir-GAL4 drivers, focusing on 8 members of the Ir20a clade along with Ir11a and Ir100a , whose expression was reported in the pharynx (Koh et al, 2014, Croset et al, 2010). We included drivers for two broadly expressed Ir co-receptors, Ir25a and Ir76b , which are expressed in GRNs of external organs (Hussain et al, 2016, Zhang et al, 2013, Croset et al, 2010), and ppk28-GAL4 , which marks water-sensing neurons in the labellum (Cameron et al, 2010). For most receptors, we tested two independent transgenic lines using UAS-mCD8-GFP .…”

A molecular and neuronal basis for amino acid sensing in the Drosophila larva

“…This receptor is broadly expressed in multiple populations of chemosensory neurons, and, in adults, has been implicated in sensory transduction of diverse odours in the olfactory system4049, and in polyamine and salt sensing in distinct subsets of neurons in the gustatory system4950. IR76b has been suggested to function independently as a salt sensor (potentially by acting as sodium leak channel)50, but in other contexts it appears to function as a co-receptor with other more selectively-expressed IRs that determine ligand specificity4049. We propose that IR76b must also act with one, or more, different tuning IRs to mediate responses to amino acids.…”