Odorant receptors from the light brown apple moth (Epiphyas postvittana) recognize important volatile compounds produced by plants.

Moths recognize a wide range of volatile compounds, which they use to locate mates, food sources, and oviposition sites. These compounds are recognized by odorant receptors (OR) located within the dendritic membrane of sensory neurons that extend into the lymph of sensilla, covering the surface of insect antennae. We have identified 3 genes encoding ORs from the tortricid moth, Epiphyas postvittana, a pest of horticulture. Like Drosophila melanogaster ORs, they contain 7 transmembrane helices with an intracellular N-terminus, an orientation in the plasma membrane opposite to that of classical GPCRs. EpOR2 is orthologous to the coreceptor Or83b from D. melanogaster. EpOR1 and EpOR3 both recognize a range of terpenoids and benzoates produced by plants. Of the compounds tested, EpOR1 shows the best sensitivity to methyl salicylate [EC(50) = 1.8 x 10(-12) M], a common constituent of floral scents and an important signaling compound produced by plants when under attack from insects and pathogens. EpOR3 best recognizes the monoterpene citral to low concentrations [EC(50) = 1.1 x 10(-13) M]. Citral produces the largest amplitude electrophysiological responses in E. postvittana antennae and elicits repellent activity against ovipositing female moths. Orthologues of EpOR3 were found across 6 families within the Lepidoptera, suggesting that the ability to recognize citral may underpin an important behavior.

[1]  Ilya Raskin,et al.  Airborne signalling by methyl salicylate in plant pathogen resistance , 1997, Nature.

[2]  T. Yasuda,et al.  Identification of receptors of main sex‐pheromone components of three Lepidopteran species , 2008, The European journal of neuroscience.

[3]  R. Crowhurst,et al.  Expressed sequence tags from the midgut of Epiphyas postvittana (Walker) (Lepidoptera: Tortricidae) , 2007, Insect molecular biology.

[4]  Yoshiaki Nagamura,et al.  The genome sequence of silkworm, Bombyx mori. , 2004, DNA research : an international journal for rapid publication of reports on genes and genomes.

[5]  Christine Woodcock,et al.  Insect host location: a volatile situation. , 2005, Trends in plant science.

[6]  W. Danthanarayana The Bionomics, Distribution and Host Range of the Light Brown Apple Moth, Epiphyas Postvittana (Walk.) (Tortricidae). , 1975 .

[7]  Dawei Li,et al.  A Draft Sequence for the Genome of the Domesticated Silkworm ( Bombyx mori ) , 2004 .

[8]  C. Merlin,et al.  Molecular identification and characterization of two new Lepidoptera chemoreceptors belonging to the Drosophila melanogaster OR83b family , 2008, Insect molecular biology.

[9]  Silke Sachse,et al.  Atypical Membrane Topology and Heteromeric Function of Drosophila Odorant Receptors In Vivo , 2006, PLoS biology.

[10]  D. Cavener,et al.  Comparison of the consensus sequence flanking translational start sites in Drosophila and vertebrates. , 1987, Nucleic acids research.

[11]  M. Pfaffl,et al.  A new mathematical model for relative quantification in real-time RT-PCR. , 2001, Nucleic acids research.

[12]  M. Zalucki,et al.  Role of chemical cues from cotton in mediating host selection and oviposition behaviour in Helicoverpa armigera (Hubner) (Lepidoptera : Noctuidae) , 1999 .

[13]  E. Csiro,et al.  Differences between single cell responses to different components of the sex pheromone in males of the lightbrown apple moth (Epiphyas postvittana) , 1983 .

[14]  J. Gershenzon,et al.  Biochemistry of Plant Volatiles1 , 2004, Plant Physiology.

[15]  A. Krogh,et al.  Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. , 2001, Journal of molecular biology.

[16]  F. Speleman,et al.  Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes , 2002, Genome Biology.

[17]  John R Carlson,et al.  The Molecular Basis of Odor Coding in the Drosophila Antenna , 2004, Cell.

[18]  Richard Axel,et al.  An Olfactory Sensory Map in the Fly Brain , 2000, Cell.

[19]  Leslie B. Vosshall,et al.  Or83b Encodes a Broadly Expressed Odorant Receptor Essential for Drosophila Olfaction , 2004, Neuron.

[20]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[21]  John R. Carlson,et al.  A Novel Family of Divergent Seven-Transmembrane Proteins Candidate Odorant Receptors in Drosophila , 1999, Neuron.

[22]  A. Sen,et al.  Electroantennogram responses of the potato tuber moth, Phthorimaea operculella (Lepidoptera; Gelichiidae) to plant volatiles , 2007, Journal of Biosciences.

[23]  Erik L. L. Sonnhammer,et al.  A Hidden Markov Model for Predicting Transmembrane Helices in Protein Sequences , 1998, ISMB.

[24]  Aidan Kiely,et al.  Functional and structural analyses of an olfactory receptor from Drosophila melanogaster. , 2008 .

[25]  Kazushige Touhara,et al.  Insect Sex-Pheromone Signals Mediated by Specific Combinations of Olfactory Receptors , 2005, Science.

[26]  John R. Carlson,et al.  The Molecular Basis of Odor Coding in the Drosophila Larva , 2005, Neuron.

[27]  E. R. Rumbo,et al.  Spatial discrimination between sources of pheromone and an inhibitor by the light-brown apple mothEpiphyas postvittana (Walker) (Lepidoptera: Tortricidae) , 1993, Journal of Chemical Ecology.

[28]  Lukas Käll,et al.  Membrane topology of the Drosophila OR83b odorant receptor , 2007, FEBS letters.

[29]  K. Honda Chemical basis of differential oviposition by lepidopterous insects , 1995 .

[30]  H. Mustaparta,et al.  Chapter Ten – Olfaction and Learning in Moths and Weevils Living on Angiosperm and Gymnosperm Hosts , 2005 .

[31]  H Breer,et al.  Genes encoding candidate pheromone receptors in a moth (Heliothis virescens). , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[32]  A. Hill,et al.  Identification of two components of the sex pheromone of the moth,Epiphyas postvittana (Lepidoptera, Tortricidae) , 1983, Journal of Chemical Ecology.

[33]  B. Sauphanor,et al.  Plant volatiles affect oviposition by codling moths , 2005, CHEMOECOLOGY.

[34]  L. Vosshall,et al.  Functional conservation of an insect odorant receptor gene across 250 million years of evolution , 2005, Current Biology.

[35]  H. Breer,et al.  A candidate olfactory receptor subtype highly conserved across different insect orders , 2003, Journal of Comparative Physiology A.

[36]  D. Suckling,et al.  Electroantennogram and oviposition responses of Epiphyas postvittana (Lepidoptera: Tortricidae) to plant volatiles , 1996 .

[37]  Dhirendra Kumar,et al.  Methyl Salicylate Is a Critical Mobile Signal for Plant Systemic Acquired Resistance , 2007, Science.

[38]  J. Hildebrand,et al.  Electroantennographic and Behavioral Responses of the Sphinx Moth Manduca sexta to Host Plant Headspace Volatiles , 2003, Journal of Chemical Ecology.

[39]  J. Thompson,et al.  The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. , 1997, Nucleic acids research.

[40]  R. Crowhurst,et al.  Expressed sequence tags and proteomics of antennae from the tortricid moth, Epiphyas postvittana , 2008, Insect molecular biology.

[41]  Regine Heller,et al.  Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels , 2008, Nature.

[42]  A. Moorman,et al.  Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data , 2003, Neuroscience Letters.

[43]  Kazushige Touhara,et al.  Identification and functional characterization of a sex pheromone receptor in the silkmoth Bombyx mori. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[44]  E. Grosse-Wilde,et al.  Candidate pheromone receptors of the silkmoth Bombyx mori , 2005, The European journal of neuroscience.

[45]  Pritam Singh A General Purpose Laboratory Diet Mixture for Rearing Insects Une Nourriture , 1983 .

[46]  R. Newcomb,et al.  Female‐biased expression of odourant receptor genes in the adult antennae of the silkworm, Bombyx mori , 2007, Insect molecular biology.

[47]  H. Breer,et al.  A divergent gene family encoding candidate olfactory receptors of the moth Heliothis virescens , 2002, The European journal of neuroscience.

[48]  P Argos,et al.  Prediction of transmembrane segments in proteins utilising multiple sequence alignments. , 1994, Journal of molecular biology.

[49]  Andrey Rzhetsky,et al.  A Spatial Map of Olfactory Receptor Expression in the Drosophila Antenna , 1999, Cell.

[50]  J. Bain,et al.  A Review of biological control of invertebrate pests and weeds in New Zealand 1874 to 1987 , 1991 .

[51]  Kay Hofmann,et al.  Tmbase-A database of membrane spanning protein segments , 1993 .

[52]  D. Cavener,et al.  Eukaryotic start and stop translation sites. , 1991, Nucleic acids research.

[53]  A. Borg-Karlson,et al.  Methyl salicylate, identified as primary odorant of a specific receptor neuron type, inhibits oviposition by the moth Mamestra brassicae L. (Lepidoptera, noctuidae). , 2008, Chemical senses.

[54]  Richard D. Newcomb,et al.  Functional analysis of a Drosophila melanogaster olfactory receptor expressed in Sf9 cells , 2007, Journal of Neuroscience Methods.

[55]  Leslie B. Vosshall,et al.  Insect olfactory receptors are heteromeric ligand-gated ion channels , 2008, Nature.

[56]  C Giovanni Galizia,et al.  The molecular receptive range of an olfactory receptor in vivo (Drosophila melanogaster Or22a). , 2006, Journal of neurobiology.

[57]  Aidan Kiely,et al.  Drosophila odorant receptors are novel seven transmembrane domain proteins that can signal independently of heterotrimeric G proteins. , 2008, Insect biochemistry and molecular biology.

[58]  E. Grosse-Wilde,et al.  Candidate pheromone receptors provide the basis for the response of distinct antennal neurons to pheromonal compounds , 2007, The European journal of neuroscience.