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  An unbiased approach elucidates variation in (S)-(+)-linalool, a context-specific mediator of a tri-trophic interaction in wild tobacco

He, J., Fandino, R. A., Halitschke, R., Luck, K., Köllner, T. G., Murdock, M. H., et al. (2019). An unbiased approach elucidates variation in (S)-(+)-linalool, a context-specific mediator of a tri-trophic interaction in wild tobacco. Proceedings of the National Academy of Sciences of the United States of America, 116(29), 14651-14660. doi:10.1073/pnas.1818585116.

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 Creators:
He, Jun1, Author              
Fandino, Richard A.2, Author              
Halitschke, Rayko1, Author              
Luck, Katrin3, Author              
Köllner, Tobias G.3, Author              
Murdock, Mark H.1, Author              
Ray, Rishav1, 4, Author              
Gase, Klaus1, Author              
Knaden, Markus5, Author              
Baldwin, Ian Thomas1, Author              
Schuman, Meredith C.1, Author              
Affiliations:
1Department of Molecular Ecology, Prof. I. T. Baldwin, MPI for Chemical Ecology, Max Planck Society, ou_24029              
2Research Group Dr. M. Knaden, Insect Behavior, Department of Evolutionary Neuroethology, Prof. B. S. Hansson, MPI for Chemical Ecology, Max Planck Society, ou_421913              
3Department of Biochemistry, Prof. J. Gershenzon, MPI for Chemical Ecology, Max Planck Society, ou_421893              
4IMPRS on Ecological Interactions, MPI for Chemical Ecology, Max Planck Society, Jena, DE, ou_421900              
5Research Group Dr. M. Knaden, Insect Behavior, Department of Neuroethology, Prof. B. S. Hansson, MPI for Chemical Ecology, Max Planck Society, ou_421913              

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 Abstract: Plant volatile organic compounds (VOCs) mediate many interactions, and the function of common VOCs is especially likely to depend on ecological context. We used a genetic mapping population of wild tobacco, Nicotiana attenuata, originating from a cross of 2 natural accessions from Arizona and Utah, separated by the Grand Canyon, to dissect genetic variation controlling VOCs. Herbivory-induced leaf terpenoid emissions varied substantially, while green leaf volatile emissions were similar. In a field experiment, only emissions of linalool, a common VOC, correlated significantly with predation of the herbivore Manduca sexta by native predators. Using quantitative trait locus mapping and genome mining,we identified an (S)-(+)-linalool synthase (NaLIS). Genome resequencing, gene cloning, and activity assays revealed that the presence/absence of a 766-bp sequence in NaLIS underlies the variation of linalool emissions in 26 natural accessions. We manipulated linalool emissions and composition by ectopically expressing linalool synthases for both enantiomers, (S)-(+)- and (R)-(−)-linalool, reported to oppositely affect M. sexta oviposition, in the Arizona and Utah accessions.We used these lines to test ovipositingmoths in increasingly complex environments. The enantiomers had opposite effects on oviposition preference, but themagnitude of the effect depended strongly both on plant genetic background, and complexity of the bioassay environment. Our study reveals that the emission of linalool, a common VOC, differs by orders-of-magnitude among geographically interspersed conspecific plants due to allelic variation in a linalool synthase, and that the response of a specialist herbivore to linalool depends on enantiomer, plant genotype, and environmental complexity.

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 Dates: 20192019-07-012019-07-16
 Publication Status: Published in print
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 Table of Contents: -
 Rev. Type: -
 Identifiers: Other: ITB609
DOI: 10.1073/pnas.1818585116
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Title: Proceedings of the National Academy of Sciences of the United States of America
  Other : Proc. Acad. Sci. USA
  Abbreviation : PNAS
Source Genre: Journal
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Publ. Info: Washington, D.C. : National Academy of Sciences
Pages: - Volume / Issue: 116 (29) Sequence Number: - Start / End Page: 14651 - 14660 Identifier: ISSN: 0027-8424
CoNE: https://pure.mpg.de/cone/journals/resource/954925427230