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

Thi Ngoc Phuong Cao, Robert Greenhalgh, Wannes Dermauw UGent, Stephane Rombauts UGent, Sabina Bajda, Vladimir Zhurov, Miodrag Grbić, Yves Van de Peer UGent, Thomas Van Leeuwen UGent, Pierre Rouzé, et al. (2016) GENOME BIOLOGY AND EVOLUTION. 8(11). p.3323-3339
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.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
Tetranychus urticae, gustatory receptor, degenerin/epithelial Na+, channels, chemosensory receptor, herbivore
journal title
GENOME BIOLOGY AND EVOLUTION
Genome Biol. Evol.
volume
8
issue
11
pages
3323 - 3339
Web of Science type
Article
Web of Science id
000393815300007
JCR category
GENETICS & HEREDITY
JCR impact factor
3.979 (2016)
JCR rank
42/166 (2016)
JCR quartile
2 (2016)
ISSN
1759-6653
DOI
10.1093/gbe/evw249
project
Bioinformatics: from nucleotids to networks (N2N)
language
English
UGent publication?
yes
classification
A1
additional info
the first three authors arre co-first authors
copyright statement
Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
id
8510559
handle
http://hdl.handle.net/1854/LU-8510559
date created
2017-02-21 10:43:18
date last changed
2017-04-20 07:50:27
@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},
}

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.