The Multiple Strategies of an Insect Herbivore to Overcome Plant Cyanogenic Glucoside Defence

Abstract

Cyanogenic glucosides (CNglcs) are widespread plant defence compounds that release toxic hydrogen cyanide by plant β-glucosidase activity after tissue damage. Specialised insect herbivores have evolved counter strategies and some sequester CNglcs, but the underlying mechanisms to keep CNglcs intact during feeding and digestion are unknown. We show that CNglc-sequestering Zygaena filipendulae larvae combine behavioural, morphological, physiological and biochemical strategies at different time points during feeding and digestion to avoid toxic hydrolysis of the CNglcs present in their Lotus food plant, i.e. cyanogenesis. We found that a high feeding rate limits the time for plant β-glucosidases to hydrolyse CNglcs. Larvae performed leaf-snipping, a minimal disruptive feeding mode that prevents mixing of plant β-glucosidases and CNglcs. Saliva extracts did not inhibit plant cyanogenesis. However, a highly alkaline midgut lumen inhibited the activity of ingested plant β-glucosidases significantly. Moreover, insect β-glucosidases from the saliva and gut tissue did not hydrolyse the CNglcs present in Lotus. The strategies disclosed may also be used by other insect species to overcome CNglc-based plant defence and to sequester these compounds intact.

Comparative venomics of Psyttalia lounsburyi and P. concolor, two olive fruit fly parasitoids: a hypothetical role for a GH1 β-glucosidase

“…The neo-formed glycosides can then possibly be stored, similarly to the ingested plant glycosides that are indeed sequestered by several insect species. By doing so, these insects prevent the production of toxic compounds363738, and some even use them for their own defense39.…”

Plant defense and herbivore counter-defense: benzoxazinoids and insect herbivores

“…For example, the act of snipping the leaf into larger pieces during feeding minimizes plant tissue disruption and, together with an alkaline gut, can inhibit the activation of plant chemical defenses such as BXDs. These mechanisms allow Zygaena filipendulae to limit hydrolysis of cyanogenic glucosides in its host plant and to sequester these compounds for use against predators (Pentzold et al 2014a). …”

Taste discriminating capability to different bitter compounds by the larval styloconic sensilla in the insect herbivore Papilio hospiton (Géné)

“…This result suggests that a spatial coding mechanism (two GRNs activated by salicin and quercitrin and three by nicotine and caffeine) is used by P. hospiton larvae to distinguish between different bitter compounds. Since it is known that alkaloids are toxic compounds, while salicin and quercitrin are unpalatable but non-toxic (Després et al, 2007;Detzel and Wink, 1993;Pentzold et al, 2014;Schuler, 1996;Steppuhn et al, 2004), we speculate that the activation of lat-M2 and med-M2 GRNs may signal the presence of non-noxious bitter compounds, and that lat-L GRN (activated only by nicotine and caffeine) may act as a ''labeled-line'', which indicates the presence of toxic compounds.…”