The taste of ribonucleosides: The molecular and cellular basis underlying chemosensory detection of previously unknown macronutrients

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Insects are the most abundant class of animals, next to vertebrates. For example, the biomass of termites alone equals that of humans, the most abundant mammal. There are about 1 million named insect species and approximately another 5 million yet to be classified, compared to about 66,000 species of vertebrates. While overall beneficial to our ecosystem, some insects have considerable negative impact on human health. Disease vectors, mostly flies and mosquitoes, are major transmitter of microbes that cause devasting human diseases, including yellow fever, dengue, malaria and zika. These insect vectors kill close to a million people each year, sicken hundreds of millions more and incur billions of dollars annually in costs for treatment and lost productivity. Other insect species are agricultural pests and consume crops and fruits of cultivated plants, leading to famine in many parts of the world. In light of these facts, a better understanding of insect biology and behavior, in particular chemosensory behavior, is paramount for developing specific and effective strategies for population control of harmful pests. Drosophila melanogaster, with its array of experimental tools, is uniquely suited to uncover the basic principles underlying these behaviors. Like mammals and other insects, Drosophila depend on chemosensory systems to navigate their external world appropriately. The sense of taste is particularly important to identify food sources and avoid harmful chemicals. To assure that all essential food chemicals are consumed, insects have evolved appetitive taste receptors for the three major macronutrients, proteins, carbohydrates and fats. Intriguingly, Drosophila larvae, in contrast to adult flies, can also sense ribonucleosides and RNA in their food. These chemicals represent an essential resource required to support rapid growth and survival during the fast-growing larval stages. Larvae employ a small number of closely related taste receptors, the Gustatory Receptors (Grs) 28 to detect these chemicals. The Gr28 genes are among the most conserved insect taste receptor genes, homologs of which are found in all insect genomes, from flour beetles to honeybees to mosquitoes. These observations suggest that the Gr28 genes have a conserved role, namely to detect RNA and ribonucleosides in insects. Remarkably, some of the Gr28 genes have been implicated in temperature and light sensing, expanding their role to sensory pathways beyond taste. Thus, an in-depth understanding of the function of receptors for RNA and ribonucleosides is of considerable interest, especially because they are broadly conserved in diverse insect species, from disease vectors (mosquitoes and flies), to agricultural pests (beetles, grasshoppers) and ecologically beneficial pollinators (honeybees). Exploiting the ability of insects to sense RNA and ribonucleosides via specific taste receptors may provide new opportunities to develop strategies for control of harmful insects.