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Complex evolutionary dynamics of massively expanded chemosensory receptor families in an extreme generalist chelicerate herbivore

(2016) GENOME BIOLOGY AND EVOLUTION. 8(11). p.3323-3339
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Bioinformatics: from nucleotids to networks (N2N)
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.
Keywords
Tetranychus urticae, gustatory receptor, degenerin/epithelial Na+, channels, chemosensory receptor, herbivore

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Citation

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Chicago
Cao, Thi Ngoc Phuong, Robert Greenhalgh, Wannes Dermauw, Stephane Rombauts, Sabina Bajda, Vladimir Zhurov, Miodrag Grbić, et al. 2016. “Complex Evolutionary Dynamics of Massively Expanded Chemosensory Receptor Families in an Extreme Generalist Chelicerate Herbivore.” Genome Biology and Evolution 8 (11): 3323–3339.
APA
Cao, T. N. P., Greenhalgh, R., Dermauw, W., Rombauts, S., Bajda, S., Zhurov, V., Grbić, M., et al. (2016). Complex evolutionary dynamics of massively expanded chemosensory receptor families in an extreme generalist chelicerate herbivore. GENOME BIOLOGY AND EVOLUTION, 8(11), 3323–3339.
Vancouver
1.
Cao TNP, Greenhalgh R, Dermauw W, Rombauts S, Bajda S, Zhurov V, et al. Complex evolutionary dynamics of massively expanded chemosensory receptor families in an extreme generalist chelicerate herbivore. GENOME BIOLOGY AND EVOLUTION. 2016;8(11):3323–39.
MLA
Cao, Thi Ngoc Phuong, Robert Greenhalgh, Wannes Dermauw, et al. “Complex Evolutionary Dynamics of Massively Expanded Chemosensory Receptor Families in an Extreme Generalist Chelicerate Herbivore.” GENOME BIOLOGY AND EVOLUTION 8.11 (2016): 3323–3339. Print.
@article{8510559,
  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\,{\textrangle}\,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.},
  author       = {Cao, Thi Ngoc Phuong and Greenhalgh, Robert and Dermauw, Wannes and Rombauts, Stephane and Bajda, Sabina and Zhurov, Vladimir and Grbi\'{c}, Miodrag and Van de Peer, Yves and Van Leeuwen, Thomas and Rouz{\'e}, Pierre and Clark, Richard M},
  issn         = {1759-6653},
  journal      = {GENOME BIOLOGY AND EVOLUTION},
  keyword      = {Tetranychus urticae,gustatory receptor,degenerin/epithelial Na+,channels,chemosensory receptor,herbivore},
  language     = {eng},
  number       = {11},
  pages        = {3323--3339},
  title        = {Complex evolutionary dynamics of massively expanded chemosensory receptor families in an extreme generalist chelicerate herbivore},
  url          = {http://dx.doi.org/10.1093/gbe/evw249},
  volume       = {8},
  year         = {2016},
}

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