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

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T1 - Characterization of odorant receptors from a non-ditrysian moth, Eriocrania semipurpurella sheds light on the origin of the sex pheromone receptors in Lepidoptera

AU - Yuvaraj, Jothi Kumar

AU - Corcoran, Jacob

AU - Andersson, Martin N

AU - Newcomb, Richard D.

AU - Anderbrant, Olle

AU - Löfstedt, Christer

PY - 2017

Y1 - 2017

N2 - Pheromone receptors (PRs) are essential in moths to detect sex pheromones for mate finding. However, it remainsunknown from which ancestral proteins these specialized receptors arose. The oldest lineages of moths, so-callednon-ditrysian moths, use short-chain pheromone components, secondary alcohols, or ketones, so called Type 0 pheromonesthat are similar to many common plant volatiles. It is, therefore, possible that receptors for these ancestralpheromones evolved from receptors detecting plant volatiles. Hence, we identified the odorant receptors (ORs) from anon-ditrysian moth, Eriocrania semipurpurella (Eriocraniidae, Lepidoptera), and performed functional characterizationof ORs using HEK293 cells. We report the first receptors that respond to Type 0 pheromone compounds; EsemOR3displayed highest sensitivity toward (2S, 6Z)-6-nonen-2-ol, whereas EsemOR5 was most sensitive to the behavioralantagonist (Z)-6-nonen-2-one. These receptors also respond to plant volatiles of similar chemical structures, but withlower sensitivity. Phylogenetically, EsemOR3 and EsemOR5 group with a plant volatile-responding receptor from thetortricid moth Epiphyas postvittana (EposOR3), which together reside outside the previously defined lepidopteran PRclade that contains the PRs from more derived lepidopteran families. In addition, one receptor (EsemOR1) that falls atthe base of the lepidopteran PR clade, responded specifically to b-caryophyllene and not to any other additional plant orpheromone compounds. Our results suggest that PRs for Type 0 pheromones have evolved from ORs that detectstructurally-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.

AB - Pheromone receptors (PRs) are essential in moths to detect sex pheromones for mate finding. However, it remainsunknown from which ancestral proteins these specialized receptors arose. The oldest lineages of moths, so-callednon-ditrysian moths, use short-chain pheromone components, secondary alcohols, or ketones, so called Type 0 pheromonesthat are similar to many common plant volatiles. It is, therefore, possible that receptors for these ancestralpheromones evolved from receptors detecting plant volatiles. Hence, we identified the odorant receptors (ORs) from anon-ditrysian moth, Eriocrania semipurpurella (Eriocraniidae, Lepidoptera), and performed functional characterizationof ORs using HEK293 cells. We report the first receptors that respond to Type 0 pheromone compounds; EsemOR3displayed highest sensitivity toward (2S, 6Z)-6-nonen-2-ol, whereas EsemOR5 was most sensitive to the behavioralantagonist (Z)-6-nonen-2-one. These receptors also respond to plant volatiles of similar chemical structures, but withlower sensitivity. Phylogenetically, EsemOR3 and EsemOR5 group with a plant volatile-responding receptor from thetortricid moth Epiphyas postvittana (EposOR3), which together reside outside the previously defined lepidopteran PRclade that contains the PRs from more derived lepidopteran families. In addition, one receptor (EsemOR1) that falls atthe base of the lepidopteran PR clade, responded specifically to b-caryophyllene and not to any other additional plant orpheromone compounds. Our results suggest that PRs for Type 0 pheromones have evolved from ORs that detectstructurally-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.

KW - odorant receptor

KW - sex pheromone

KW - HEK293 cells

KW - deorphanization

UR - https://academic.oup.com/mbe/article/34/11/2733/4060563#supplementary-data

U2 - 10.1093/molbev/msx215

DO - 10.1093/molbev/msx215

M3 - Article

C2 - 29126322

VL - 34

SP - 2733

EP - 2746

JO - Molecular biology and evolution

JF - Molecular biology and evolution

SN - 0737-4038

IS - 11

ER -