Ancient protostome origin of chemosensory ionotropic glutamate receptors and the evolution of insect taste and olfaction.

Vincent Croset,David Brawand,Toby J Gibson,Henrik Kaessmann,Scott F Cummins,Aidan Budd,Raphael Rytz,Richard Benton,David L Stern

doi:10.1371/journal.pgen.1001064

Vincent Croset, David Brawand + Show 7 more

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https://doi.org/10.1371/journal.pgen.1001064

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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.

Highlights

Ionotropic glutamate receptors are a conserved family of ligand-gated ion channels present in both eukaryotes and prokaryotes
We recently discovered a variant class of Ionotropic glutamate receptors (iGluRs) in the fruit fly (Drosophila melanogaster), named Ionotropic Receptors (IRs), which function as olfactory receptors in its ‘‘nose,’’ prompting us to ask whether iGluR/IRs might have a more general function in detection of environmental chemicals
The shared, unusual ‘‘S1-ion channel-S2’’ domain organisation of prokaryotic GluR0 and eukaryotic iGluRs is suggestive of a common ancestor of this family by fusion of genes encoding the separate domains that were present in very early life forms (Figure 9) [11]

Summary

Introduction

Ionotropic glutamate receptors (iGluRs) are a conserved family of ligand-gated ion channels present in both eukaryotes and prokaryotes. By regulating cation flow across the plasma membrane in response to binding of extracellular glutamate and related ligands, iGluRs represent an important signalling mechanism by which cells modify their internal physiology in response to external chemical signals. An extracellular amino-terminal domain (ATD) is involved in assembly of iGluR subunits into heteromeric complexes [3]. This precedes the ligand-binding domain (LBD), whose two halfdomains (S1 and S2) form a ‘‘Venus flytrap’’ structure that closes around glutamate and related agonists [4]. Separating S1 and S2 in the primary structure is the ion channel pore, formed by two transmembrane segments and a re-entrant pore loop [5]. S2 is followed by a third transmembrane domain of unknown function and a cytosolic carboxy-terminal tail

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