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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.