title: Complex Evolutionary Dynamics of Massively Expanded Chemosensory Receptor Families in an Extreme Generalist Chelicerate Herbivore.
abstract: While mechanisms to detoxify plant produced, anti-herbivore compounds have been associated with plant host use by herbivores, less is known about the role of chemosensory perception in their life histories. This is especially true for generalists, including chelicerate herbivores that evolved herbivory independently from the more studied insect lineages. To shed light on chemosensory perception in a generalist herbivore, we characterized the chemosensory receptors (CRs) of the chelicerate two-spotted spider mite, Tetranychus urticae, an extreme generalist. Strikingly, T. urticae has more CRs than reported in any other arthropod to date. Including pseudogenes, 689 gustatory receptors were identified, as were 136 degenerin/Epithelial Na+ Channels (ENaCs) that have also been implicated as CRs in insects. The genomic distribution of T. urticae gustatory receptors indicates recurring bursts of lineage-specific proliferations, with the extent of receptor clusters reminiscent of those observed in the CR-rich genomes of vertebrates or C. elegans Although pseudogenization of many gustatory receptors within clusters suggests relaxed selection, a subset of receptors is expressed. Consistent with functions as CRs, the genomic distribution and expression of ENaCs in lineage-specific T. urticae expansions mirrors that observed for gustatory receptors. The expansion of ENaCs in T. urticae to > 3-fold that reported in other animals was unexpected, raising the possibility that ENaCs in T. urticae have been co-opted to fulfill a major role performed by unrelated CRs in other animals. More broadly, our findings suggest an elaborate role for chemosensory perception in generalist herbivores that are of key ecological and agricultural importance.
authors: Department of Plant Systems Biology, VIB, Ghent, Belgium.|Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, Belgium.
authors: Phuong Cao Thi
authors: PC
authors: Ngoc
authors: Department of Biology, University of Utah, Salt Lake City, Utah.
authors: Robert
authors: R
authors: Greenhalgh
authors: Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium.
authors: Wannes
authors: W
authors: Dermauw
authors: Department of Plant Systems Biology, VIB, Ghent, Belgium.|Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, Belgium.
authors: Stephane
authors: S
authors: Rombauts
authors: Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium.|Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, The Netherlands.
authors: Sabina
authors: S
authors: Bajda
authors: Department of Biology, The University of Western Ontario, London, ON, Canada.
authors: Vladimir
authors: V
authors: Zhurov
authors: Department of Biology, The University of Western Ontario, London, ON, Canada.|University of La Rioja, Logroño, Spain.
authors: Miodrag
authors: M
authors: Grbić
authors: Department of Plant Systems Biology, VIB, Ghent, Belgium.|Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, Belgium.|Bioinformatics Institute Ghent, Ghent, Belgium.|Department of Genetics, Genomics Research Institute, University of Pretoria, Pretoria, South Africa.
authors: Yves
authors: Y
authors: Van de Peer
authors: Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium.|Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, The Netherlands.
authors: Thomas
authors: T
authors: Van Leeuwen
authors: Department of Plant Systems Biology, VIB, Ghent, Belgium clark@biology.utah.edu pierre.rouze@psb.vib-ugent.be.
authors: Pierre
authors: P
authors: Rouzé
authors: Department of Biology, University of Utah, Salt Lake City, Utah clark@biology.utah.edu pierre.rouze@psb.vib-ugent.be.|Center for Cell and Genome Science, University of Utah, Salt Lake City, Utah.
authors: Richard M
authors: RM
authors: Clark
mesh_terms: D000053:Acari / Q000235:genetics* / Q000378:metabolism / Q000502:physiology; D000818:Animals; D053503:Epithelial Sodium Channels / Q000235:genetics* / Q000378:metabolism; D019143:Evolution, Molecular; D060434:Herbivory / Q000235:genetics; D019476:Insect Proteins / Q000235:genetics* / Q000378:metabolism; D005810:Multigene Family; D011956:Receptors, Cell Surface / Q000235:genetics* / Q000378:metabolism; D013649:Taste
chemical_list: D053503:Epithelial Sodium Channels; D019476:Insect Proteins; D011956:Receptors, Cell Surface
keywords: Tetranychus urticae; channels; chemosensory receptor; degenerin/epithelial Na+; gustatory receptor; herbivore