Metabolism of poplar salicinoids by the generalist herbivore Lymantria dispar (Lepidoptera)

Abstract

The survival of insect herbivores on chemically defended plants may often depend on their ability to metabolize these defense compounds. However, only little knowledge is available on how insects actually process most plant defense compounds. We investigated the metabolism of salicinoids, a major group of phenolic glycosides in poplar and willow species, by a generalist herbivore, the gypsy moth (Lymantria dispar). Seven salicinoid metabolites identified in gypsy moth caterpillar feces were mostly conjugates with glucose, cysteine or glycine. Two of the glucosides were phosphorylated, a feature not previously reported for insect metabolites of plant defense compounds. The origins of these metabolites were traced to specific moieties of three major poplar salicinoids ingested, salicin, salicortin and tremulacin. Based on the observed metabolite patterns we were able to deduce the initial steps of salicinoid breakdown in L. dispar guts, which involves cleavage of ester bonds. The conjugated molecules were effectively eliminated within 24 h after ingestion. Some of the initial breakdown products (salicin and catechol) demonstrated negative effects on insect growth and survival in bioassays on artificial diets. Gypsy moth caterpillars with prior feeding experience on salicinoid-containing poplar foliage converted salicinoids to the identified metabolites more efficiently than caterpillars pre-fed an artificial diet. The majority of the metabolites we identified were also produced by other common poplar-feeding insects. The conversion of plant defenses like salicinoids to a variety of water-soluble sugar, phosphate and amino acid conjugates and their subsequent excretion fits the general detoxification strategy found in insect herbivores and other animals.

Identifying candidate detoxification genes in the ecdysteroid kinase-like (EcKL) and cytochrome P450 gene families inDrosophila melanogasterby integrating evolutionary and transcriptomic data

“…Other hydroxylated toxins that could be X-class EcKL substrates include withanolides, cardenolides, cucurbitacins and flavonoids (Agrawal et al, 2012; Dinan et al, 1997; Glotter, 2011; S. Wang et al, 2017). X-class EcKLs may also phosphorylate the products of phase I hydroxylation reactions or phase II glucosidation reactions, as is speculated to occur in locusts and moths (Boeckler et al, 2016; Olsen et al, 2015; 2014).…”

“…In perhaps a more ecologically relevant example, caterpillars of the gypsy moth, Lymantria dispar , phosphorylate the glycoside moiety of salicinoids found the leaves of a host plant, Populus tremula x tremuloides , a hybrid poplar tree. These phosphate conjugates—formed in the gut and perhaps also the Malpighian tubules— comprise a substantial proportion of excreted salicinoid-like compounds, especially when caterpillars are previously fed poplar leaves, suggesting this detoxification process is induced by the presence of poplar secondary metabolites (Boeckler et al, 2016). Likewise, the detoxicative kinase activity identified in Gromphadorhina portentosa , the Madagascar cockroach, is present in the midgut, fat body and Malpighian tubules of the insect and is inducible by in vivo exposure to phenobarbital (Gil et al, 1974; R. S. H. Yang and Wilkinson, 1973), a compound commonly used to induce detoxification gene expression (Misra et al, 2011; Willoughby et al, 2006).…”

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

“…o-Quinones have a high potential to bind to a variety of biomolecules, including amino acids and proteins (Haruta et al 2001;Smith 1985). Generalist lepidopteran species, such as the gypsy moth (L. dispar), have developed a strategy of detoxification (Boeckler et al 2016) where the major salicinoids in P. nigra, salicortin and tremulacin, are transformed into typical metabolic phase II conjugates (Grant 1991), with salicin as the major metabolite (Boeckler et al 2016).…”

“…The most representative salicinoid in Populus is salicortin (12), as so far it has been found in all investigated species (Boeckler et al 2011;Thieme 1964). Numerous studies have investigated the effect of salicinoids on lepidopteran herbivorous insects, such as Papilio glaucus (Lindroth 1991), Choristoneura conflictica (Clausen et al 1989), Malacosoma disstria and Lymantria dispar (Lindroth and Hemming 1990) or Operophtera brumata (Boeckler et al 2016;Ruuhola et al 2001). Coleopteran larvae belonging to the Chrysomelidae family can sequester salicinoids and use their host plant's chemical defense to ward off predators (Burse et al 2009).…”

“…Coleopteran larvae belonging to the Chrysomelidae family can sequester salicinoids and use their host plant's chemical defense to ward off predators (Burse et al 2009). Recently, a comprehensive study of the generalist herbivore L. dispar (Boeckler et al 2016) provided the first detailed description of how a lepidopteran detoxifies salicinoid compounds. The digestive degradation of salicinoids in the insect gut (Haruta et al 2001;Lindroth 1988;Ruuhola et al 2003) results in saligenin and an o-quinone (Clausen et al 1989;Julkunen-Tiitto and Meier 1992;Knuth et al 2011).…”