How insects overcome two‐component plant chemical defence: plant β‐glucosidases as the main target for herbivore adaptation

Abstract

Insect herbivory is often restricted by glucosylated plant chemical defence compounds that are activated by plant β-glucosidases to release toxic aglucones upon plant tissue damage. Such two-component plant defences are widespread in the plant kingdom and examples of these classes of compounds are alkaloid, benzoxazinoid, cyanogenic and iridoid glucosides as well as glucosinolates and salicinoids. Conversely, many insects have evolved a diversity of counteradaptations to overcome this type of constitutive chemical defence. Here we discuss that such counter-adaptations occur at different time points, before and during feeding as well as during digestion, and at several levels such as the insects’ feeding behaviour, physiology and metabolism. Insect adaptations frequently circumvent or counteract the activity of the plant β-glucosidases, bioactivating enzymes that are a key element in the plant’s two-component chemical defence. These adaptations include host plant choice, non-disruptive feeding guilds and various physiological adaptations as well as metabolic enzymatic strategies of the insect’s digestive system. Furthermore, insect adaptations often act in combination, may exist in both generalists and specialists, and can act on different classes of defence compounds. We discuss how generalist and specialist insects appear to differ in their ability to use these different types of adaptations: in generalists, adaptations are often inducible, whereas in specialists they are often constitutive. Future studies are suggested to investigate in detail how insect adaptations act in combination to overcome plant chemical defences and to allow ecologically relevant conclusions.

Acylated Quinic Acids Are the Main Salicortin Metabolites in the Lepidopteran Specialist Herbivore Cerura vinula

“…It is widely accepted that the digestive activation of salicinoids leads to toxic products warding off non-adapted herbivores. For salicortin, it has been proposed that activation proceeds through deglucosylation by β-glucosidases (Clausen et al 1990;Lindroth 1988;Pentzold et al 2014). The aglycon is either hydrolyzed spontaneously in the alkaline gut environment or degraded enzymatically by insect esterases Lindroth 1989) to saligenin and a 1-hydroxy-6-oxocyclohex-2-en-1-oyl (HCH) fragment (Haruta et al 2001;Julkunen-Tiitto and Meier 1992).…”

“…Generally, the salicinoid breakdown follows reported routes like deglucosylation, ester cleavage and conjugation (Clausen et al 1990;Lindroth 1988;Pentzold et al 2014). The structural diversity of the compounds -namely, the differential substitution of quinic acid with salicylate or benzoate -can be rationalized by acyl migration under basic conditions as present in the insect gut (Appel and Martin 1990).…”

Struggle to survive: aphid—plant relationships under low-light stress. A case of Acyrthosiphon pisum (Harris) and Pisum sativum L.

“…Therefore, the activity of this enzyme is often used as a biochemical indicator in research on plant metabolic status under different experimental situations. Pentzold et al (2013) reported that insect herbivory is often restricted by glucosylated plant chemical defense compounds that are activated by plant b-glucosidases to release toxic aglycones upon plant tissue damage.…”

“…Pea (Pisum sativum L.) (Fabaceae), originally a plant of the Near East and one of the most ancient crops dating back to the end of the last Ice Age in Europe, is currently grown all over the world in temperate regions, at low and high elevations or during cool seasons in warm regions (Ljuština and Mikić 2010;Pavek 2012). Pea is cultivated basically in pure stands as a commercial crop but it is also used as a forage, rotational, and cover crop or green manure.…”

Deciphering the route to cyclic monoterpenes in Chrysomelina leaf beetles: source of new biocatalysts for industrial application?

“…Enzymes that catalyze such reactions often belong to the glycosyl hydrolase family 1 (GH1) according to CAZy [96,97]. Whereas in plants, GH1s play an important role in the activation of glucosides for defense purpose [98][99][100][101], insects use those enzymes mainly for digestion, either in the gut or in the salivary glands [24,102,103]. In addition to this, GH1s may also be involved in the production of chemical defenses widely distributed in insects [104].…”