Journal article
Ancient Protostome Origin of Chemosensory Ionotropic Glutamate Receptors and the Evolution of Insect Taste and Olfaction
PLoS Genetics, Vol.6(8), e1001064
2010
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.
Details
- Title
- Ancient Protostome Origin of Chemosensory Ionotropic Glutamate Receptors and the Evolution of Insect Taste and Olfaction
- Authors
- V Croset (Author) - University of Lausanne, SwitzerlandR Rytz (Author) - University of Lausanne, SwitzerlandScott F Cummins (Author) - University of QueenslandA Budd (Author) - European Molecular Biology Laboratory, GermanyD Brawand (Author) - University of Lausanne, SwitzerlandH Kaessmann (Author) - University of Lausanne, SwitzerlandT J Gibson (Author) - European Molecular Biology Laboratory, GermanyR Benton (Author) - University of Lausanne, Switzerland
- Publication details
- PLoS Genetics, Vol.6(8), e1001064; 20
- Publisher
- Public Library of Science
- Date published
- 2010
- DOI
- 10.1371/journal.pgen.1001064
- ISSN
- 1553-7390
- Copyright note
- Copyright © 2010 Croset et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. This published version is reproduced in accordance with this policy.
- Organisation Unit
- School of Science and Engineering - Legacy; University of the Sunshine Coast, Queensland; School of Science, Technology and Engineering; Centre for Bioinnovation
- Language
- English
- Record Identifier
- 99449785202621
- Output Type
- Journal article
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