Abstract
Gut enzymes can metabolize plant defense compounds and thereby affect the growth and fitness of insect herbivores. Whether these enzymes also influence feeding preference is largely unknown. We studied the metabolization of taraxinic acid β-D-glucopyranosyl ester (TA-G), a sesquiterpene lactone of the common dandelion (Taraxacum officinale) that deters its major root herbivore, the common cockchafer larva (Melolontha melolontha). We have demonstrated that TA-G is rapidly deglucosylated and conjugated to glutathione in the insect gut. A broad-spectrum M. melolontha β-glucosidase, Mm_bGlc17, is sufficient and necessary for TA-G deglucosylation. Using cross-species RNA interference, we have shown that Mm_bGlc17 reduces TA-G toxicity. Furthermore, Mm_bGlc17 is required for the preference of M. melolontha larvae for TA-G-deficient plants. Thus, herbivore metabolism modulates both the toxicity and deterrence of a plant defense compound. Our work illustrates the multifaceted roles of insect digestive enzymes as mediators of plant-herbivore interactions.
Highlights
Plants produce an arsenal of toxic secondary metabolites, many of which protect them against phytophagous insects by acting as toxins, digestibility reducers, repellents, and deterrents (Mithöfer and Boland, 2012)
To test if taraxinic acid (TA)-G is hydrolyzed during M. melolontha feeding, we analyzed larvae that had ingested defined amounts of TA-G-c ontaining T. officinale latex
TA-glutathione (TA-G SH) and TA-cysteine (TA-C ys) were identified in latex-fed larvae based on mass spectral and nuclear magnetic resonance (NMR) data, with the Cys sulfhydryl moiety being conjugated to TA at the exocyclic methylene group of the α-methylene-γ-lactone moiety (Figure 1B–C, Figure 1—figure supplements 1–6)
Summary
Plants produce an arsenal of toxic secondary metabolites, many of which protect them against phytophagous insects by acting as toxins, digestibility reducers, repellents, and deterrents (Mithöfer and Boland, 2012). Enzymes involved in carbohydrate digestion may play a particular role in processing plant defense glycosides Such compounds are typically considered protoxins, non-toxic, glycosylated precursors that are brought into contact with compartmentalized plant glycosidases upon tissue damage to yield toxic aglycones (Wittstock and Gershenzon, 2002). Sesquiterpene lactones form a large group of over 2000 plant defense compounds found principally in the Asteraceae family, with glycosides especially common in the latex-producing tribe Cichorieae, which enters the human diet through lettuce, endive, and chicory (Chadwick et al, 2013) These substances have a long appreciated role in defense against insect herbivores (Picman, 1986), but it is not clear if glycosylated sesquiterpene lactones should be considered as protoxins that are activated by plant damage. Our results reveal that β-glucosidases modify the effects of plant defense metabolites on both herbivore performance and host plant choice, with potentially important consequences for the ecology and evolution of plant-h erbivore interactions
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