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A sex pheromone receptor in the Hessian fly Mayetiola destructor (Diptera, Cecidomyiidae)

Andersson, Martin N LU ; Corcoran, Jacob LU ; Zhang, Dandan LU ; Hillbur, Ylva; Newcomb, Richard D. and Löfstedt, Christer LU (2016) In Frontiers in Cellular Neuroscience 10(SEP2016).
Abstract
The Hessian fly, Mayetiola destructor Say (Diptera,
Cecidomyiidae), is a pest of wheat and belongs to a group of
gall-inducing herbivores. This species has a unique life history and
several ecological features that differentiate it from other Diptera
such as Drosophila melanogaster and blood-feeding mosquitoes.
These features include a short, non-feeding adult life stage (1–2 days)
and the use of a long-range sex pheromone produced and released by adult
females. Sex pheromones are detected by members of the odorant receptor
(OR) family within the Lepidoptera, but no receptors for similar
long-range sex pheromones have been characterized from the Diptera.
Previously, 122 OR... (More)
The Hessian fly, Mayetiola destructor Say (Diptera,
Cecidomyiidae), is a pest of wheat and belongs to a group of
gall-inducing herbivores. This species has a unique life history and
several ecological features that differentiate it from other Diptera
such as Drosophila melanogaster and blood-feeding mosquitoes.
These features include a short, non-feeding adult life stage (1–2 days)
and the use of a long-range sex pheromone produced and released by adult
females. Sex pheromones are detected by members of the odorant receptor
(OR) family within the Lepidoptera, but no receptors for similar
long-range sex pheromones have been characterized from the Diptera.
Previously, 122 OR genes have been annotated from the Hessian fly
genome, with many of them showing sex-biased expression in the antennae.
Here we have expressed, in HEK293 cells, five MdesORs that display
male-biased expression in antennae, and we have identified MdesOR115 as a
Hessian fly sex pheromone receptor. MdesOR115 responds primarily to the
sex pheromone component (2S,8E,10E)-8,10-tridecadien-2-yl acetate, and secondarily to the corresponding Z,E-isomer.
Certain sensory neuron membrane proteins (i.e., SNMP1) are important
for responses of pheromone receptors in flies and moths. The Hessian fly
genome is unusual in that it encodes six SNMP1 paralogs, of which five
are expressed in antennae. We co-expressed each of the five antennal
SNMP1 paralogs together with each of the five candidate sex pheromone
receptors from the Hessian fly and found that they do not influence the
response of MdesOR115, nor do they confer responsiveness in any of the
non-responsive ORs to any of the sex pheromone components identified to
date in the Hessian fly. Using Western blots, we detected protein
expression of MdesOrco, all MdesSNMPs, and all MdesORs except for
MdesOR113, potentially explaining the lack of response from this OR. In
conclusion, we report the first functional characterization of an OR
from the Cecidomyiidae, extending the role of ORs as long-range sex
pheromone detectors from the Lepidoptera into the Diptera.

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keywords
deorphanization, functional characterization, heterologous expression, HEK293 cells, odorant receptor, pheromone receptor, sensory neuron membrane protein
in
Frontiers in Cellular Neuroscience
volume
10
issue
SEP2016
pages
12 pages
publisher
Frontiers
external identifiers
  • scopus:84988643173
  • scopus:84988643173
ISSN
1662-5102
DOI
10.3389/fncel.2016.00212
language
English
LU publication?
yes
id
8a87bf00-2ba7-4dab-8d5b-a768e8290ed5
date added to LUP
2016-09-21 14:44:17
date last changed
2019-08-14 03:28:59
@article{8a87bf00-2ba7-4dab-8d5b-a768e8290ed5,
  abstract     = {The Hessian fly, <i>Mayetiola destructor</i> Say (Diptera, <br>
Cecidomyiidae), is a pest of wheat and belongs to a group of <br>
gall-inducing herbivores. This species has a unique life history and <br>
several ecological features that differentiate it from other Diptera <br>
such as <i>Drosophila melanogaster</i> and blood-feeding mosquitoes. <br>
These features include a short, non-feeding adult life stage (1–2 days) <br>
and the use of a long-range sex pheromone produced and released by adult<br>
 females. Sex pheromones are detected by members of the odorant receptor<br>
 (OR) family within the Lepidoptera, but no receptors for similar <br>
long-range sex pheromones have been characterized from the Diptera. <br>
Previously, 122 OR genes have been annotated from the Hessian fly <br>
genome, with many of them showing sex-biased expression in the antennae.<br>
 Here we have expressed, in HEK293 cells, five MdesORs that display <br>
male-biased expression in antennae, and we have identified MdesOR115 as a<br>
 Hessian fly sex pheromone receptor. MdesOR115 responds primarily to the<br>
 sex pheromone component (2<i>S</i>,8<i>E</i>,10<i>E</i>)-8,10-tridecadien-2-yl acetate, and secondarily to the corresponding <i>Z</i>,<i>E</i>-isomer.<br>
 Certain sensory neuron membrane proteins (i.e., SNMP1) are important <br>
for responses of pheromone receptors in flies and moths. The Hessian fly<br>
 genome is unusual in that it encodes six SNMP1 paralogs, of which five <br>
are expressed in antennae. We co-expressed each of the five antennal <br>
SNMP1 paralogs together with each of the five candidate sex pheromone <br>
receptors from the Hessian fly and found that they do not influence the <br>
response of MdesOR115, nor do they confer responsiveness in any of the <br>
non-responsive ORs to any of the sex pheromone components identified to <br>
date in the Hessian fly. Using Western blots, we detected protein <br>
expression of MdesOrco, all MdesSNMPs, and all MdesORs except for <br>
MdesOR113, potentially explaining the lack of response from this OR. In <br>
conclusion, we report the first functional characterization of an OR <br>
from the Cecidomyiidae, extending the role of ORs as long-range sex <br>
pheromone detectors from the Lepidoptera into the Diptera.<br/><br/>},
  articleno    = {212},
  author       = {Andersson, Martin N and Corcoran, Jacob and Zhang, Dandan and Hillbur, Ylva and Newcomb, Richard D. and Löfstedt, Christer},
  issn         = {1662-5102},
  keyword      = {deorphanization,functional characterization,heterologous expression,HEK293 cells,odorant receptor,pheromone receptor,sensory neuron membrane protein},
  language     = {eng},
  month        = {09},
  number       = {SEP2016},
  pages        = {12},
  publisher    = {Frontiers},
  series       = {Frontiers in Cellular Neuroscience},
  title        = {A sex pheromone receptor in the Hessian fly <i>Mayetiola destructor</i> (Diptera, Cecidomyiidae)},
  url          = {http://dx.doi.org/10.3389/fncel.2016.00212},
  volume       = {10},
  year         = {2016},
}