[en] Olfaction is crucial for short distance host location and pheromone detection by insects. Complexes of
olfactory receptors (ORs) are composed of odor-specific ORs and OR co-receptors (Orco). Orcos are widely
co-expressed with odor-specific ORs and are conserved across insect taxa. A number of Orco orthologs
have been studied to date, although none has been identified in cereal aphids. In this study, an Orco gene
ortholog was cloned from the grain aphid, Sitobion avenae, and named “SaveOrco”; RNA interference
(RNAi) reduced the expression of SaveOrco to 34.11% in aphids, resulting in weaker EAG (electroantennogram)
responses to plant volatiles (Z-3-hexene-1-ol; methyl salicylate, MeSA) and aphid alarm
pheromone (E-b-farnesene, EBF). Aphid wing differentiation induced by EBF was investigated in both
RNAi treated and untreated aphids. EBF induced production of winged aphids in both pre-natal and postnatal
periods in untreated aphids, but no such induction was observed in the RNAi-treated aphids. We
conclude that SaveOrco is crucial for the aphid's response to pheromones and other volatiles, and is
involved in wing differentiation triggered by EBF
Disciplines :
Entomology & pest control
Author, co-author :
Fan, Jia; Chinese Academy of Agricultural Sciences > Institute of Plant Protection > State Key Laboratory of Plant Diseases and Insect Pests
Zhang, Yong ; Chinese Academy of Agricultural Sciences > Institute of Plant Protection > State Key Laboratory of Plant Diseases and Insect Pests
Francis, Frédéric ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Entomologie fonctionnelle et évolutive
Cheng, Dengfa; Chinese Academy of Agricultural Sciences > Institute of Plant Protection > State Key Laboratory of Plant Diseases and Insect Pests
Sun, Jingrun; Chinese Academy of Agricultural Sciences > Institute of Plant Protection > State Key Laboratory of Plant Diseases and Insect Pests
Chen, Julian; Chinese Academy of Agricultural Sciences > Institute of Plant Protection > State Key Laboratory of Plant Diseases and Insect Pests > chenjulian@caas.cn
Language :
English
Title :
Orco mediates olfactory behaviors and winged morph differentiation induced by alarm pheromone in the grain aphid, Sitobion avenae
Publication date :
27 May 2015
Journal title :
Insect Biochemistry and Molecular Biology
ISSN :
0965-1748
eISSN :
1879-0240
Publisher :
Pergamon Press (part of Elsevier Science), Oxford, United Kingdom
Ankersmit G.W., Dijkman H. Alatae production in the cereal aphid Sitobion avenae. Neth. J. Plant Pathol. 1983, 89:105-112.
Araujo R.N., Santos A., Pinto F.S., Gontijo N.F., Lehane M.J., et al. RNA interference of the salivary gland nitrophorin 2 in the triatomine bug Rhodnius prolixus (Hemiptera: Reduviidae) by dsRNA ingestion or injection. Insect Biochem. Mol. Biol. 2006, 36:683-693.
Beale M.H., Birkett M.A., Bruce T.J.A., Chamberlain K., Field L.M., et al. Aphid alarm pheromone produced by transgenic plants affects aphid and parasitoid behavior. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:10509-10513.
Benton R., Sachse S., Michnick S.W., Vosshall L.B. Atypical membrane topology and heteromeric function of Drosophila odorant receptors invivo. PLoS Biol. 2006, 4:e20.
Benton R., Vannice K.S., Gomez-Diaz C., Vosshall L.B. Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell 2009, 136:149-162.
Bruce T.J.A., Birkett M.A., Blande J., Hooper A.M., Martin J.L., et al. Response of economically important aphids to components of Hemizygia petiolata essential oil. Pest Manag. Sci. 2005, 61:1115-1121.
Carey A.F., Wang G., Su C.Y., Zwiebel L.J., Carlson J.R. Odorant reception in the malaria mosquito Anopheles gambiae. Nature 2010, 464:66-71.
Clyne P.J., Warr C.G., Freeman M.R., Lessing D., Kim J., et al. Anovel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 1999, 22:327-338.
Cui L., Liu Y., Yuan H., Liu J., Dong J., Chen J., Francis F., Song X., Liu Y. The functional significance of E-β-Farnesene: does it influence the behavioural responses of aphid natural enemies in the fields. Biol. Control 2012, 60(2):108-112.
Francis F., Vandermoten S., Verheggen F., Lognay G., Haubruge E. Is the (E)-beta-farnesene only volatile terpenoid in aphids?. J.Appl. Entomol. 2005, 129:6-11.
Gao Q., Chess A. Identification of candidate Drosophila olfactory receptors from genomic DNA sequence. Genomics 1999, 60:31-39.
Hallem E.A., Nicole Fox A., Zwiebel L.J., Carlson J.R. Olfaction: mosquito receptor for human-sweat odorant. Nature 2004, 427:212-213.
Jones P.L., Pask G.M., Romaine I.M., Taylor R.W., Reid P.R., et al. Allosteric antagonism of insect odorant receptor ion channels. PLoS One 2012, 7:e30304.
Kain P., Chakraborty T.S., Sundaram S., Siddiqi O., Rodrigues V., et al. Reduced odor responses from antennal neurons of Gqα, phospholipase Cβ, and rdgA mutants in Drosophila support a role for a phospholipid intermediate in insect olfactory transduction. J.Neurosci. Off. J. Soc. Neurosci. 2008, 28:4745-4755.
Kiely A., Authier A., Kralicek A.V., Warr C.G., Newcomb R.D. Functional analysis of a Drosophila melanogaster olfactory receptor expressed in Sf9 cells. J.Neurosci. Methods 2007, 159:189-194.
Kunert G., Weisser W.W. The importance of antennae for pea aphid wing induction in the presence of natural enemies. Bull. Entomol. Res. 2005, 95:125-131.
Kunert G., Otto S., Rose U.S.R., Gershenzon J., Weisser W.W. Alarm pheromone mediates production of winged dispersal morphs in aphids. Ecol. Lett. 2005, 8:596-603.
Kunert G., Trautsch J., Weisser W.W. Density dependence of the alarm pheromone effect in pea aphids, Acyrthosiphon pisum (Sternorrhyncha: Aphididae). Eur. J. Entomol. 2007, 104:47-50.
Larsson M.C., Domingos A.I., Jones W.D., Chiappe M.E., Amrein H., et al. Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 2004, 43:703-714.
Li R., Li S. Influence of temperature on wheat aphid's development and productivity. J.Shanxi Agric. Univ. Nat. Sci. Ed. 2002, 22:319-321.
Liu Y., Chen J., Ni H. Electroantennogram responses of Sitobion avenae and Rhopalosiphum padi to wheat plant volatiles. Acta Entomol. Sin. 2003, 46:679-683.
Müller C.B., Williams I.S., Hardie J. The role of nutrition, crowding and interspecific interactions in the development of winged aphids. Ecol. Entomol. 2001, 26:330-340.
Mustaparta H. Chemical information processing in the olfactory system of insect. Physiol. Rev. 1990, 70:199-245.
Pickett J.A., Wadhams L.J., Woodcock C.M., Hardie J. The chemical ecology of aphids. Annu. Rev. Entomol. 1992, 67-90.
Read D.P., Feeny P.P., Root R.B. Habitat selection by the aphid parasite Diaeretiella rapae (Hymenoptera: Braconidae) and hyperparsite Charips brassicae (Hymenoptera: Cynipidae). Can. Entomol. 1970, 102:1567-1578.
Sato K., Pellegrino M., Nakagawa T., Nakagawa T., Vosshall L.B., et al. Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature 2008, 452:1002-1006.
Shakesby A.J., Wallace I.S., Isaacs H.V., Pritchard J., Roberts D.M., et al. Awater-specific aquaporin involved in aphid osmoregulation. Insect Biochem. Mol. Biol. 2009, 39:1-10.
Sloggett J.J.W., Weisser W.W. Ageneral mechanism for predator- and parasitoid-induced dispersal in the pea aphid, Acyrthosiphon pisum (Harris). Aphids in a New Millennium Proceedings of the Sixth International Symposium on Aphids, September, 2001. Rennes, France 2004, 79-85. J.C. Simon, C.A. Dedryver, C. Rispe, M. Hullé (Eds.).
Smadja C., Shi P., Butlin R.K., Robertson H.M. Large gene family expansions and adaptive evolution for odorant and gustatory receptors in the pea aphid, Acyrthosiphon pisum. Mol. Biol. Evol. 2009, 26:2073-2086.
Soong R., Ladányi A. Improved indicators for assessing the reliability of detection and quantification by kinetic PCR. Clin. Chem. 2003, 49:973-976.
Talluri S., Bhatt A., Smith D.P. Identification of a Drosophila G protein alpha subunit (dGq alpha-3) expressed in chemosensory cells and central neurons. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:11475-11479.
Taylor R.W., Romaine I.M., Liu C., Murthi P., Jones P.L., et al. Structure-activity relationship of a broad-spectrum insect odorant receptor agonist. ACS Chem. Biol. 2012, 7:1647-1652.
Upadhyay S.K., Chandrashekar K., Thakur N., Verma P.C., Borgio J.F., et al. RNA interference for the control of whiteflies (Bemisia tabaci) by oral route. J.Biosci. 2011, 36:153-161.
Visser J.H., Fu-shun Y. Electroantennogram responses of the grain aphids Sitobion avenae (F.) and Metopolophium dirhodum (Walk.) (Homoptera, Aphididae) to plant odour components. J.Appl. Entomol. 1995, 119:539-542.
Vosshall L.B., Hansson B.S. Aunified nomenclature system for the insect olfactory coreceptor. Chem. Senses 2011, 36:497-498.
Vosshall L.B., Amrein H., Morozov P.S., Rzhetsky A., Axel R. Aspatial map of olfactory receptor expression in the Drosophila antenna. Cell 1999, 96:725-736.
Webster B.E.N. The role of olfaction in aphid host location. Physiol. Entomol. 2012, 37:10-18.
Webster B., Bruce T., Pickett J., Hardie J. Volatiles functioning as host cues in a blend become nonhost cues when presented alone to the black bean aphid. Anim. Behav. 2010, 79:451-457.
Wetzel C.H., Behrendt H.J., Gisselmann G., Stortkuhl K.F., Hovemann B., et al. Functional expression and characterization of a Drosophila odorant receptor in a heterologous cell system. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:9377-9380.
Whyard S., Singh A.D., Wong S. Ingested double-stranded RNAs can act as species-specific insecticides. Insect Biochem. Mol. Biol. 2009, 39:824-832.
Wicher D., Schafer R., Bauernfeind R., Stensmyr M.C., Heller R., et al. Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels. Nature 2008, 452:1007-1011.
Wistrand M., Käll L., Sonnhammer E.L.L. Ageneral model of G protein-coupled receptor sequences and its application to detect remote homologs. Protein Sci. 2006, 15:509-521.
Wohlers P., Tjallingh W. Electroantennogram responses of aphids to the alarm pheromone (E)-beta-farnesene. Entomol. Exp. Appl. 1983, 33:79-82.
Yu X.D., Pickett J., Ma Y.Z., Bruce T., Napier J., Jones H.D., Xia L.Q. Metabolic engineering of plant-derived (E)-β-farnesene synthase genes for a novel type of aphid-resistant genetically modified crop plants. J.Integr. Plant Biol. 2012, 54(5):282-299.
Zhou H.B. Use of Intercropping and Infochemical Releasers to Control Aphids in Wheat 2012, (PhD dissertation), Liege University, Gembloux.