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Proc Natl Acad Sci U S A


Title:"An unbiased approach elucidates variation in (S)-(+)-linalool, a context-specific mediator of a tri-trophic interaction in wild tobacco"
Author(s):He J; Fandino RA; Halitschke R; Luck K; Kollner TG; Murdock MH; Ray R; Gase K; Knaden M; Baldwin IT; Schuman MC;
Address:"Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, 07745 Jena, Germany. Department of Evolutionary Neuroethology, Max Planck Institute for Chemical Ecology, 07745 Jena, Germany. Department of Biochemistry, Max Planck Institute for Chemical Ecology, 07745 Jena, Germany. College of Life Sciences, Brigham Young University, Provo, UT 84606. Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, 07745 Jena, Germany; Baldwin@ice.mpg.de meredith.schuman@geo.uzh.ch. Department of Geography, University of Zurich, 8057 Zurich, Switzerland"
Journal Title:Proc Natl Acad Sci U S A
Year:2019
Volume:20190701
Issue:29
Page Number:14651 - 14660
DOI: 10.1073/pnas.1818585116
ISSN/ISBN:1091-6490 (Electronic) 0027-8424 (Print) 0027-8424 (Linking)
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 ovipositing moths in increasingly complex environments. The enantiomers had opposite effects on oviposition preference, but the magnitude 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"
Keywords:Acyclic Monoterpenes/metabolism/*toxicity Animals Arizona Female Genotype Geography Host-Parasite Interactions/genetics Hydro-Lyases/*genetics/metabolism Larva/drug effects/growth & development Male Manduca/*drug effects/physiology Oviposition/drug effect;
Notes:"MedlineHe, Jun Fandino, Richard A Halitschke, Rayko Luck, Katrin Kollner, Tobias G Murdock, Mark H Ray, Rishav Gase, Klaus Knaden, Markus Baldwin, Ian T Schuman, Meredith C eng Research Support, Non-U.S. Gov't 2019/07/03 Proc Natl Acad Sci U S A. 2019 Jul 16; 116(29):14651-14660. doi: 10.1073/pnas.1818585116. Epub 2019 Jul 1"

 
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