title: Detoxification of hostplant's chemical defence rather than its anti-predator co-option drives β-glucosidase-mediated lepidopteran counteradaptation.
abstract: The evolutionary plant-herbivore arms race sometimes gives rise to remarkably unique adaptation strategies. Here we report one such strategy in the lepidopteran herbivore Manduca sexta against its hostplant Nicotiana attenuata's major phytotoxins, 17-hydroxygeranyllinalool diterpene glycoside, lyciumoside IV and its malonylated forms. We show that alkalinity of larval regurgitant non-enzymatically demalonylates the malonylated forms to lyciumoside IV. Lyciumoside IV is then detoxified in the midgut by β-glucosidase 1-catalysed deglycosylation, which is unusual, as typically the deglycosylation of glycosylated phytochemicals by insects results in the opposite: toxin activation. Suppression of deglucosylation by silencing larval β-glucosidase 1 by plant-mediated RNAi causes moulting impairments and mortality. In the native habitat of N. attenuata, β-glucosidase 1 silencing also increases larval unpalatability to native predatory spiders, suggesting that the defensive co-option of lyciumoside IV may be ecologically advantageous. We infer that M. sexta detoxifies this allelochemical to avoid its deleterious effects, rather than co-opting it against predators.
authors.affiliation: Department of Molecular Ecology, Max-Planck-Institute for Chemical Ecology, 07745 Jena, Germany.
authors.forename: Spoorthi
authors.initials: S
authors.lastname: Poreddy
authors.affiliation: Department of Molecular Ecology, Max-Planck-Institute for Chemical Ecology, 07745 Jena, Germany.
authors.forename: Sirsha
authors.initials: S
authors.lastname: Mitra
authors.affiliation: Department of Molecular Ecology, Max-Planck-Institute for Chemical Ecology, 07745 Jena, Germany.
authors.forename: Matthias
authors.initials: M
authors.lastname: Schöttner
authors.affiliation: Department of Biosynthesis/NMR Research Group, Max-Planck-Institute for Chemical Ecology, 07745 Jena, Germany.
authors.forename: Jima
authors.initials: J
authors.lastname: Chandran
authors.affiliation: Department of Biosynthesis/NMR Research Group, Max-Planck-Institute for Chemical Ecology, 07745 Jena, Germany.
authors.forename: Bernd
authors.initials: B
authors.lastname: Schneider
authors.affiliation: Department of Molecular Ecology, Max-Planck-Institute for Chemical Ecology, 07745 Jena, Germany.
authors.forename: Ian T
authors.initials: IT
authors.lastname: Baldwin
authors.affiliation: Department of Molecular Ecology, Max-Planck-Institute for Chemical Ecology, 07745 Jena, Germany.
authors.forename: Pavan
authors.initials: P
authors.lastname: Kumar
authors.affiliation: Department of Molecular Ecology, Max-Planck-Institute for Chemical Ecology, 07745 Jena, Germany.
authors.forename: Sagar S
authors.initials: SS
authors.lastname: Pandit
mesh_terms: D000222:Adaptation, Physiological / Q000235:genetics*; D000818:Animals; D041981:Gastrointestinal Tract / Q000378:metabolism; D020868:Gene Silencing; D008658:Inactivation, Metabolic / Q000235:genetics; D007814:Larva / Q000378:metabolism; D007915:Lepidoptera; D018402:Manduca / Q000502:physiology*; D014026:Nicotiana / Q000378:metabolism*; D014118:Toxins, Biological / Q000378:metabolism*; D001617:beta-Glucosidase / Q000235:genetics*
chemical_list: D014118:Toxins, Biological; D001617:beta-Glucosidase