Reductive Conversion Leads to Detoxification of Salicortin-like Chemical Defenses (Salicortinoids) in Lepidopteran Specialist Herbivores (Notodontidae)

Abstract

Lepidopteran specialist herbivores of the Notodontidae family have adapted to thrive on poplar and willow species (Salicaceae). Previous research showed that Cerura vinula, a member of the Notodontidae family occurring throughout Europe and Asia, uses a unique mechanism to transform salicortinoids, the host plant’s defense compounds, into quinic acid-salicylate conjugates. However, how the production of this conjugates relates to the detoxification of salicortinoids and how this transformation proceeds mechanistically have remained unknown. To find the mechanisms, we conducted gut homogenate incubation experiments with C. vinula and re-examined its metabolism by analyzing the constituents of its frass. To estimate the contribution of spontaneous degradation, we examined the chemical stability of salicortinoids and found that salicortinoids were degraded very quickly by midgut homogenates and that spontaneous degradation plays only a marginal role in the metabolism. We learned how salicortinoids are transformed into salicylate after we discovered reductively transformed derivatives, which were revealed to play key roles in the metabolism. Unless they have undergone the process of reduction, salicortinoids produce toxic catechol. We also studied constituents in the frass of the Notodontidae species Cerura erminea, Clostera anachoreta, Furcula furcula, Notodonta ziczac, and Pheosia tremula, and found the same metabolites as those described for C. vinula. We conclude that the process whereby salicortinoids are reductively transformed represents an important adaption of the Notodontidae to their Salicaceae host species.

Different fates of metabolites and small variation in chemical composition characterise frass chemistry in a specialist caterpillar

“…If larger structural modifications to salicinoids occurred, they thus probably led to decomposition of the salicinoid‐like structure by the cleavage of ester bonds (Boeckler et al, 2016). This is in line with other studies that showed that salicinoids are largely metabolised when ingested by insect herbivores (Boeckler et al, 2011, Ruuhola et al, 2001; Schnurrer & Paetz, 2023).…”

“…to negatively affect polyphagous caterpillars (Boeckler et al, 2016), it would be interesting to test whether L. populi has some mechanisms that allow to circumvent these effects as reported for other host-plant specialists associated with Salicaceae (Schnurrer & Paetz, 2023).…”

“…However, a large fraction of flavonoids ingested by caterpillars is usually excreted almost unchanged (Burghardt et al, 1997; Salminen, Lahtinen, et al, 2004; Wiesen et al, 1994). Salicinoids, by contrast, are metabolised and detoxified to a much larger extent in lepidopteran larvae, irrespective from the degree of dietary specialisation (e.g., Boeckler et al, 2016; Feistel et al, 2018; Ruuhola et al, 2001; Schnurrer & Paetz, 2023). Polyphagous gypsy moth caterpillars ( Lymantria dispar L.), for instance, were found to detoxify salicinoids by converting them into water‐soluble sugar, phosphate and amino acid conjugates (Boeckler et al, 2016).…”

Anti-Inflammatory Salicin Derivatives from the Barks of Salix tetrasperma

“…This information coupled with the comparable ECD curve with those of 1 – 3 determined the absolute configuration of 6 as 1′ S , 2′ R , 3′ S , 4′ S , 5′ R , 1″ S , which was corroborated further by TDDFT-ECD analysis (Figure ). The absolute configurations of compounds 4 and 5 were assigned as the same as that of 6 , as deduced from their consistent 1D NMR data of fragment B and similar tendencies of the ECD curves, and supported by TDDFT-ECD analysis of 4 (Figure ), as well as their shared biosynthesis from salicin derivatives. , …”

“…The absolute configurations of compounds 4 and 5 were assigned as the same as that of 6, as deduced from their consistent 1D NMR data of fragment B and similar tendencies of the ECD curves, and supported by TDDFT-ECD analysis of 4 (Figure 3), as well as their shared biosynthesis from salicin derivatives. 49,50 Compounds 7 (salixteroside G) and 8 (salixteroside H) were initially obtained as pale-yellow gum. Their molecular formulas were determined as C 23 H 30 O 12 based on the HRESIMS and 13 C NMR data, implying nine IHDs.…”