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

By Vincent Croset, R. Rytz, S. Cummins, Aidan Budd, D. Brawand, Henrik Kaessmann, Toby J. Gibson, Richard Benton. PLoS Genetics, 2010

706 citations recorded by the source corpus.

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.

Subfields: Cellular and Molecular Neuroscience, Ecology, Evolution, Behavior and Systematics, Genetics

View Paper: https://www.semanticscholar.org/paper/36ab43f6faaec81491fbf351ccedf952d87e75aa

How researchers see this paper

The researchers whose trusted networks rank it highest, strongest advocate first. Every researcher gets a different order.

In Cellular and Molecular Neuroscience

In Ecology, Evolution, Behavior and Systematics

Owain Edwards

In Genetics

Citations in the corpus

Insect olfaction and the evolution of receptor tuning (2015, methodology): “…(2012b) showed that differences between stimuli in their release rates from commonly used Pasteur pipette odor cartridges can significantly confound conclusions about OR specificities, and used the D. melanogaster ab3A neuron, co-expressing Or22a and Or22b (Dobritsa et al., 2003), as an example.”
Complementary Function and Integrated Wiring of the Evolutionarily Distinct Drosophila Olfactory Subsystems (2011, methodology): “Peripheral and central spatial maps of IR olfactory sensory neurons To characterize the anatomy and function of individual populations of IR neurons and compare these properties with the organization of the OR sensory pathways, we generated and verified the fidelity of a panel of IR promoter–GAL4 dr”
Uncovering the novel characteristics of Asian honey bee, Apis cerana, by whole genome sequencing (2015, background): “The number of identified Irs in insects is increasing [63,90,91], and a large complement of Irs has been described in the complete genomes of four hymenopteran species: A.”