Ancient Protostome Origin of Chemosensory Ionotropic Glutamate Receptors and the Evolution of Insect Taste and Olfaction

Abstract

Ionotropic glutamate receptors (iGluRs) are a highly conserved family of ligand-gated ion channels present in animals, plants, and bacteria, which are best characterized for their roles in synaptic communication in vertebrate nervous systems. A variant subfamily of iGluRs, the Ionotropic Receptors (IRs), was recently identified as a new class of olfactory receptors in the fruit fly, Drosophila melanogaster, hinting at a broader function of this ion channel family in detection of environmental, as well as intercellular, chemical signals. Here, we investigate the origin and evolution of IRs by comprehensive evolutionary genomics and in situ expression analysis. In marked contrast to the insect-specific Odorant Receptor family, we show that IRs are expressed in olfactory organs across Protostomia—a major branch of the animal kingdom that encompasses arthropods, nematodes, and molluscs—indicating that they represent an ancestral protostome chemosensory receptor family. Two subfamilies of IRs are distinguished: conserved “antennal IRs,” which likely define the first olfactory receptor family of insects, and species-specific “divergent IRs,” which are expressed in peripheral and internal gustatory neurons, implicating this family in taste and food assessment. Comparative analysis of drosophilid IRs reveals the selective forces that have shaped the repertoires in flies with distinct chemosensory preferences. Examination of IR gene structure and genomic distribution suggests both non-allelic homologous recombination and retroposition contributed to the expansion of this multigene family. Together, these findings lay a foundation for functional analysis of these receptors in both neurobiological and evolutionary studies. Furthermore, this work identifies novel targets for manipulating chemosensory-driven behaviours of agricultural pests and disease vectors.

Differential expression of olfactory genes in the southern house mosquito and insights into unique odorant receptor gene isoforms

“…Strictly speaking, these transcripts are for ionotropic glutamate receptors (iGluRs), with IRs being a related family found initially in Drosophila melanogaster (26) and later in various insect species, including Cx. quinquefasciatus (27). They belong to five phylogenetic groups, namely, NMDA iGluRs, non-NMDA iGluRs, IR25a/IR8a, divergent IRs, and antennal IRs.…”

Dissecting ant recognition systems in the age of genomics

“…The IR gene family is an ancient one, as IR genes are distributed across the wide swath of animals in the Protostomia (including molluscs, nematodes and molluscs) [41]. Unlike Ors and Grs (and the canonical ionotropic glutamate receptors), IRs are ligand-gated ion channels that function as transmembrane chemoreceptors.…”

Comparing the Expression of Olfaction-Related Genes in Gypsy Moth (Lymantria dispar) Adult Females and Larvae from One Flightless and Two Flight-Capable Populations

“…In general, OSNs will express either ORs or IRs, with the latter mostly tuned to compounds of lower molecular weight (Hallem et al, 2004(Hallem et al, , 2006Benton et al, 2009;Silbering et al, 2011). All analyzed Lepidoptera species possess more OR than IR types (Croset et al, 2010;Koenig et al, 2015;van Schooten et al, 2016), and these play a role in the detection of plant volatiles as well as pheromones (Nakagawa et al, 2005;Grosse-Wilde et al, 2006, 2007Tanaka et al, 2009). In insects, OSNs associated with basiconic or trichoid sensilla express one OR gene, along with the co-receptor ORCO, which is highly conserved and broadly expressed (Krieger et al, 2003;Touhara and Vosshall, 2009).…”

“…Recent reports suggest there are multiple variant IRs with different ligand-binding domains that lack the characteristic glutamate-interacting residues (Benton et al, 2009). Unlike ORs, which are exclusively found in pterygote insects, IRs are present in all protostome species studied so far and may have evolved as long as 550-850 million years ago (Croset et al, 2010;Missbach et al, 2014). Similar iGluR-like genes are also present in plants, animals and prokaryotes, indicating that this is an important and ancient group of chemoreceptors (Benton et al, 2009;Rytz et al, 2013).…”