The multiple strategies of an insect herbivore to overcome plant cyanogenic glucoside defence.

Stefan Pentzold,Mika Zagrobelny,Søren Bak,Birger Lindberg Møller,Pernille Sølvhøj Roelsgaard,Daniel Ballhorn

doi:10.1371/journal.pone.0091337

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.

Highlights

Plants are often endowed with chemical defence compounds, of which some are permanently present in anticipation of an herbivore or pathogen attack
Sequestration, the specific accumulation, storage and concentration of plant chemicals in the insect body [4,5], is an efficient strategy, because glucosylated plant defence compounds become spatially separated from the plant b-glucosidases which are retained in the gut lumen [2]
We measured the feeding rate of Z. filipendulae and found that larvae consume 3.8 cm2 (60.2 SE) of L. corniculatus leaves per hour

Summary

Introduction

Plants are often endowed with chemical defence compounds, of which some are permanently present in anticipation of an herbivore or pathogen attack These constitutive plant defence compounds may be stored in a non-toxic glucosylated form and be spatially separated from their bioactivating b-glucosidases [1,2]. This is known as a two-component defence system. Two-component plant defence systems constitute a challenge to herbivores during feeding and digestion, but the innate conditional toxicity and permanent presence may be key factors for insect herbivores to evolve counter strategies, such as sequestration. Sequestration, the specific accumulation, storage and concentration of plant chemicals in the insect body [4,5], is an efficient strategy, because glucosylated plant defence compounds become spatially separated from the plant b-glucosidases which are retained in the gut lumen [2]

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Results

Discussion

Conclusion