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Characterization of odorant receptors from a non-ditrysian moth, Eriocrania semipurpurella sheds light on the origin of the sex pheromone receptors in Lepidoptera

Yuvaraj, Jothi Kumar LU ; Corcoran, Jacob LU ; Andersson, Martin N LU ; Newcomb, Richard D.; Anderbrant, Olle LU and Löfstedt, Christer LU (2017) In Molecular Biology and Evolution 34(11). p.2733-2746
Abstract
Pheromone receptors (PRs) are essential in moths to detect sex pheromones for mate finding. However, it remains
unknown from which ancestral proteins these specialized receptors arose. The oldest lineages of moths, so-called
non-ditrysian moths, use short-chain pheromone components, secondary alcohols, or ketones, so called Type 0 pheromones
that are similar to many common plant volatiles. It is, therefore, possible that receptors for these ancestral
pheromones evolved from receptors detecting plant volatiles. Hence, we identified the odorant receptors (ORs) from a
non-ditrysian moth, Eriocrania semipurpurella (Eriocraniidae, Lepidoptera), and performed functional characterization
of ORs using HEK293 cells.... (More)
Pheromone receptors (PRs) are essential in moths to detect sex pheromones for mate finding. However, it remains
unknown from which ancestral proteins these specialized receptors arose. The oldest lineages of moths, so-called
non-ditrysian moths, use short-chain pheromone components, secondary alcohols, or ketones, so called Type 0 pheromones
that are similar to many common plant volatiles. It is, therefore, possible that receptors for these ancestral
pheromones evolved from receptors detecting plant volatiles. Hence, we identified the odorant receptors (ORs) from a
non-ditrysian moth, Eriocrania semipurpurella (Eriocraniidae, Lepidoptera), and performed functional characterization
of ORs using HEK293 cells. We report the first receptors that respond to Type 0 pheromone compounds; EsemOR3
displayed highest sensitivity toward (2S, 6Z)-6-nonen-2-ol, whereas EsemOR5 was most sensitive to the behavioral
antagonist (Z)-6-nonen-2-one. These receptors also respond to plant volatiles of similar chemical structures, but with
lower sensitivity. Phylogenetically, EsemOR3 and EsemOR5 group with a plant volatile-responding receptor from the
tortricid moth Epiphyas postvittana (EposOR3), which together reside outside the previously defined lepidopteran PR
clade that contains the PRs from more derived lepidopteran families. In addition, one receptor (EsemOR1) that falls at
the base of the lepidopteran PR clade, responded specifically to b-caryophyllene and not to any other additional plant or
pheromone compounds. Our results suggest that PRs for Type 0 pheromones have evolved from ORs that detect
structurally-related plant volatiles. They are unrelated to PRs detecting pheromones inmore derived Lepidoptera, which,
in turn, also independently may have evolved a novel function from ORs detecting plant volatiles. (Less)
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author
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
odorant receptor, sex pheromone, HEK293 cells, deorphanization
in
Molecular Biology and Evolution
volume
34
issue
11
pages
14 pages
publisher
Oxford University Press
external identifiers
  • scopus:85044114150
ISSN
0737-4038
DOI
10.1093/molbev/msx215http://dx.doi.org/https://doi.org/10.1093/molbev/msx244
language
English
LU publication?
yes
id
7bd1c64a-6986-4f10-ae3d-cb79257cf4c8
date added to LUP
2017-08-30 11:36:39
date last changed
2018-05-13 04:34:45
@article{7bd1c64a-6986-4f10-ae3d-cb79257cf4c8,
  abstract     = {Pheromone receptors (PRs) are essential in moths to detect sex pheromones for mate finding. However, it remains<br/>unknown from which ancestral proteins these specialized receptors arose. The oldest lineages of moths, so-called<br/>non-ditrysian moths, use short-chain pheromone components, secondary alcohols, or ketones, so called Type 0 pheromones<br/>that are similar to many common plant volatiles. It is, therefore, possible that receptors for these ancestral<br/>pheromones evolved from receptors detecting plant volatiles. Hence, we identified the odorant receptors (ORs) from a<br/>non-ditrysian moth, <i>Eriocrania semipurpurella</i> (Eriocraniidae, Lepidoptera), and performed functional characterization<br/>of ORs using HEK293 cells. We report the first receptors that respond to Type 0 pheromone compounds; EsemOR3<br/>displayed highest sensitivity toward (2S, 6Z)-6-nonen-2-ol, whereas EsemOR5 was most sensitive to the behavioral<br/>antagonist (Z)-6-nonen-2-one. These receptors also respond to plant volatiles of similar chemical structures, but with<br/>lower sensitivity. Phylogenetically, EsemOR3 and EsemOR5 group with a plant volatile-responding receptor from the<br/>tortricid moth <i>Epiphyas postvittana</i> (EposOR3), which together reside outside the previously defined lepidopteran PR<br/>clade that contains the PRs from more derived lepidopteran families. In addition, one receptor (EsemOR1) that falls at<br/>the base of the lepidopteran PR clade, responded specifically to b-caryophyllene and not to any other additional plant or<br/>pheromone compounds. Our results suggest that PRs for Type 0 pheromones have evolved from ORs that detect<br/>structurally-related plant volatiles. They are unrelated to PRs detecting pheromones inmore derived Lepidoptera, which,<br/>in turn, also independently may have evolved a novel function from ORs detecting plant volatiles.},
  author       = {Yuvaraj, Jothi Kumar and Corcoran, Jacob and Andersson, Martin N and Newcomb, Richard D. and Anderbrant, Olle and Löfstedt, Christer},
  issn         = {0737-4038},
  keyword      = {odorant receptor,sex pheromone,HEK293 cells,deorphanization},
  language     = {eng},
  number       = {11},
  pages        = {2733--2746},
  publisher    = {Oxford University Press},
  series       = {Molecular Biology and Evolution},
  title        = {Characterization of odorant receptors from a non-ditrysian moth, <i>Eriocrania semipurpurella</i> sheds light on the origin of the sex pheromone receptors in Lepidoptera},
  url          = {http://dx.doi.org/10.1093/molbev/msx215http://dx.doi.org/https://doi.org/10.1093/molbev/msx244},
  volume       = {34},
  year         = {2017},
}