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.
Highlights
The evolutionary plant–herbivore arms race sometimes gives rise to remarkably unique adaptation strategies
The susceptibility of Manduca sexta (Ms). sexta larvae to hydroxygeranyllinalool d diterpene glycosides (HGL-DTG) was demonstrated using different Nicotiana species such as N. attenuata, N. bigelovii and N. clevelandii, which differ in their HGL-DTG contents and composition, and, more convincingly, with different transgenic isogenic lines of N. attenuata with varying levels of HGL-DTGs16–18
M. sexta larvae grew three times larger than controls when they were fed transgenic N. attenuata plants depleted in their HGL-DTG content by silencing geranylgeranyl pyrophosphate synthase (GGPPS), the gene responsible for the synthesis of the HGL-DTG precursor, geranylgeranyl pyrophosphate[19,20]
Summary
The evolutionary plant–herbivore arms race sometimes gives rise to remarkably unique adaptation strategies. 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. Released aglycones cause cellular damage in herbivores and severely affect their physiology and fitness[6,7] On ingestion, these glycosides are deglycosylated in the midgut by insect glycosidases[3,8]. Deglycosylation or glycoside hydrolysis in insects is commonly thought to result in toxin activation and glycosylation is regarded as a form of detoxification[11,12,13,14]. We investigated M. sexta’s counteradaptation strategy against HGL-DTGs, using Lyc[4] and its malonylated forms as model HGL-DTGs. We discovered unusual mechanisms evolved by M. sexta to demalonylate and detoxify these allelochemicals. We discuss why M. sexta could have chosen the detoxification of Lyc[4] in spite of it being ecologically disadvantageous
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