A honey bee odorant receptor for the queen substance 9-oxo-2-decenoic acid

doi:10.1073/pnas.0705459104

A honey bee odorant receptor for the queen substance 9-oxo-2-decenoic acid

*Department of Entomology, University of Illinois at Urbana–Champaign, Urbana, IL 61801; and
^†Department of Molecular and Cellular Pharmacology, Miller School of Medicine, University of Miami, Miami, FL 33136

Edited by Gene E. Robinson, University of Illinois at Urbana–Champaign, Urbana, IL, and approved July 23, 2007 (received for review June 11, 2007)

Abstract

By using a functional genomics approach, we have identified a honey bee [Apis mellifera (Am)] odorant receptor (Or) for the queen substance 9-oxo-2-decenoic acid (9-ODA). Honey bees live in large eusocial colonies in which a single queen is responsible for reproduction, several thousand sterile female worker bees complete a myriad of tasks to maintain the colony, and several hundred male drones exist only to mate. The “queen substance” [also termed the queen retinue pheromone (QRP)] is an eight-component pheromone that maintains the queen's dominance in the colony. The main component, 9-ODA, acts as a releaser pheromone by attracting workers to the queen and as a primer pheromone by physiologically inhibiting worker ovary development; it also acts as a sex pheromone, attracting drones during mating flights. However, the extent to which social and sexual chemical messages are shared remains unresolved. By using a custom chemosensory-specific microarray and qPCR, we identified four candidate sex pheromone Ors (AmOr10, -11, -18, and -170) from the honey bee genome based on their biased expression in drone antennae. We assayed the pheromone responsiveness of these receptors by using Xenopus oocytes and electrophysiology. AmOr11 responded specifically to 9-ODA (EC₅₀ = 280 ± 31 nM) and not to any of the other seven QRP components, other social pheromones, or floral odors. We did not observe any responses of the other three Ors to any of the eight QRP pheromone components, suggesting 9-ODA is the only QRP component that also acts as a long-distance sex pheromone.

Footnotes

^‡To whom correspondence should be addressed. E-mail: hughrobe{at}life.uiuc.edu
Author contributions: K.W.W. and A.S.N. contributed equally to this work; K.W.W., A.S.N., K.K.O.W., C.W.L., and H.M.R. designed research; K.W.W. and A.S.N. performed research; A.B. contributed new reagents/analytic tools; K.W.W., A.S.N., K.K.O.W., A.B., C.W.L., and H.M.R. analyzed data; and K.W.W., A.S.N., K.K.O.W., C.W.L., and H.M.R. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: The data reported in this paper have been deposited in the Gene Expression Omnibus (GEO) database, www.ncbi.nlm.nih.gov/geo (accession no. GSE8519).
This article contains supporting information online at www.pnas.org/cgi/content/full/0705459104/DC1.
Abbreviations:

Am,

Apis mellifera;

Cr,

chemoreceptor;

9-HDA,

9-hydroxy-2-decenoic acid;

HOB,

methyl p-hydroxybenzoate;

HVA,

4-hydroxy-3-methyoxyphenylethanol;

9-ODA,

9-oxo-2-decenoic acid;

Or,

odorant receptor;

QMP,

queen mandibular pheromone;

QRP,

queen retinue pheromone;

MG2,

macroglomerulus 2;

UIUC,

University of Illinois at Urbana–Champaign;

OBP,

odorant-binding protein;

qPCR,

quantitative real-time PCR.