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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 genes have been annotated from the... (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. (Less)
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Contribution to journal
publication status
published
subject
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
2016-11-09 03:00:06
@misc{8a87bf00-2ba7-4dab-8d5b-a768e8290ed5,
  abstract     = {The Hessian fly, Mayetiola destructor Say (Diptera, Cecidomyiidae), is a pest of wheat<br/>and belongs to a group of gall-inducing herbivores. This species has a unique life<br/>history and several ecological features that differentiate it from other Diptera such<br/>as Drosophila melanogaster and blood-feeding mosquitoes. These features include a<br/>short, non-feeding adult life stage (1–2 days) and the use of a long-range sex pheromone<br/>produced and released by adult females. Sex pheromones are detected by members<br/>of the odorant receptor (OR) family within the Lepidoptera, but no receptors for similar<br/>long-range sex pheromones have been characterized from the Diptera. Previously, 122<br/>OR genes have been annotated from the Hessian fly genome, with many of them<br/>showing sex-biased expression in the antennae. Here we have expressed, in HEK293<br/>cells, five MdesORs that display male-biased expression in antennae, and we have<br/>identified MdesOR115 as a Hessian fly sex pheromone receptor. MdesOR115 responds<br/>primarily to the sex pheromone component (2S,8E,10E)-8,10-tridecadien-2-yl acetate,<br/>and secondarily to the corresponding Z,E-isomer. Certain sensory neuron membrane<br/>proteins (i.e., SNMP1) are important for responses of pheromone receptors in flies and<br/>moths. The Hessian fly genome is unusual in that it encodes six SNMP1 paralogs,<br/>of which five are expressed in antennae. We co-expressed each of the five antennal<br/>SNMP1 paralogs together with each of the five candidate sex pheromone receptors<br/>from the Hessian fly and found that they do not influence the response of MdesOR115,<br/>nor do they confer responsiveness in any of the non-responsive ORs to any of the sex<br/>pheromone components identified to date in the Hessian fly. Using Western blots, we<br/>detected protein expression of MdesOrco, all MdesSNMPs, and all MdesORs except for<br/>MdesOR113, potentially explaining the lack of response from this OR. In conclusion, we<br/>report the first functional characterization of an OR from the Cecidomyiidae, extending<br/>the role of ORs as long-range sex pheromone detectors from the Lepidoptera into the<br/>Diptera.},
  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    = {ARRAY(0x809eab8)},
  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},
}