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(–)-Germacrene D receptor neurones in three species of heliothine moths: structure-activity relationships

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Abstract

Specificity of olfactory receptor neurones plays an important role in food and host preferences of a species, and may have become conserved or changed in the evolution of polyphagy and oligophagy. We have identified a major type of plant odour receptor neurones responding to the sesquiterpene germacrene D in three species of heliothine moths, the polyphagous Heliothis virescens and Helicoverpa armigera and the oligophagous Helicoverpa assulta. The neurones respond with high sensitivity and selectivity to (–)-germacrene D, as demonstrated by screening via gas chromatography with numerous mixtures of plant volatiles. Germacrene D was present in both host and non-host plants, but only in half of the tested species. The specificity of the neurones was similar in the three species, as shown by the "secondary" responses to a few other sesquiterpenes. The effect of (–)-germacrene D was about ten times stronger than that of the (+)-enantiomer, which again was about ten times stronger than that of (–)-α-ylangene. Weaker effects were obtained for (+)-β-ylangene, (+)-α-copaene, β-copaene and two unidentified sesquiterpenes. The structure-activity relationship shows that the important properties of (–)-germacrene D in activating the neurones are the ten-membered ring system and the three double bonds acting as electron-rich centres, in addition to the direction of the isopropyl-group responsible for the different effects of the germacrene D enantiomers.

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Fig. 6A, B.

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Abbreviations

α-copaene:

(tricyclo[4.4.0.0.]dec-3-ene, 1,3-dimethyl-8-(1-methylethyl)-)

β-copaene:

(tricyclo[4.4.0.0.]decane, 1-methyl-3-methylene-8-(1-methylethyl)-)

GC:

gas chromatograph

GC-MS:

linked gas chromatography mass spectrometry

GC-SCR:

linked gas chromatography single cell recording

GD:

germacrene D (1,6-cyclodecadiene, 1-methyl-5-methylene-8-(1-methylethyl-, E,E))

α-ylangene:

(tricyclo[4.4.0.0]dec-3-ene, 1,3-dimethyl-8-(1-methylethyl)-)

β-ylangene:

(tricyclo[4.4.0.0.]decane, 1-methyl-3-methylene-8-(1-methylethyl)-)

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Acknowledgements

This paper is dedicated to Prof. em. Bertil Kullenberg on the occasion of his 90th birthday. The Norwegian Research Council (project no. 133958/420) provided the principal financial support for the project. We also acknowledge the support from The Nordic Academy of Advanced Studies via the visiting professorship for Dr. Anna-Karin Borg-Karlson (project no. 010434) and the support from the Swedish Institute (project in ecological biochemistry, the New Visby Program). The Insect Rearing Team at Syngenta, Basel, Switzerland, Prof. Ezra Dunkelblum at the Agricultural Research Organisation, the Volcani Centre, Bet Dagan, Israel, Prof. Kyung Saeng Boo at Seoul National University, South Korea, and Prof. Chen-Zhu Wang at the Chinese Academy of Sciences, Institute of Zoology, Beijing, People's Republic of China, are all acknowledged for providing insects. Dr. Sandrine Gouinguené and Dr. Ted C. J. Turlings, Laboratory of Animal Ecology and Entomology, University of Neuchâtel, Switzerland kindly provided the induced plant odours, Dr. Franz-Josef Hammerschmidt, Dragoco Gerberding & Co. AG, Holzminden, Germany provided the ylang-ylang oil for fractioning, Sina Escher, Firmenich, Switzerland the ylang-ylang fractions and Felisberto Pagula, University of Maputo, Mozambique, the essential oil of Eastern red cedar. We thank Prof. Linda White, Department of Neuroscience, NTNU for improving the language of the manuscript.

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Authors and Affiliations

  1. Neuroscience Unit, Department of Biology, Norwegian University of Science and Technology, 7489, NO-Trondheim, Norway

    M. Stranden, T. J. Almaas, A.-K. Borg-Karlson & H. Mustaparta

  2. Ecological Chemistry, Organic Chemistry, Department of Chemistry, Royal Institute of Technology, SE-100 44, Stockholm, Sweden

    I. Liblikas & A.-K. Borg-Karlson

  3. Laboratory of Ecochemistry, Estonian Agricultural University, Tartu EE-51005, Estonia

    I. Liblikas

  4. Institute of Organic Chemistry, University of Hamburg, DE-20146, Hamburg, Germany

    W. A. König

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  1. M. Stranden
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  2. I. Liblikas
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  3. W. A. König
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  4. T. J. Almaas
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  5. A.-K. Borg-Karlson
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Correspondence to M. Stranden.

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Stranden, M., Liblikas, I., König, W.A. et al. (–)-Germacrene D receptor neurones in three species of heliothine moths: structure-activity relationships. J Comp Physiol A 189, 563–577 (2003). https://doi.org/10.1007/s00359-003-0434-y

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  • DOI: https://doi.org/10.1007/s00359-003-0434-y

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