Larvae of the fall webworm, <i>Hyphantria cunea</i>, inhibit cyanogenesis in <i>Prunus serotina</i>

Fitzgerald, Terrence D.

doi:10.1242/jeb.013664

Cited by 16 publications

(14 citation statements)

References 26 publications

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“…A similar inhibition of plant cyanogenesis by a highly alkaline midgut pH has only been reported in a few cases such as the ugly nest caterpillar or the fall webworm larva feeding on cherry [36], [37]. Highly alkaline conditions in the insect midgut may also inhibit plant β-glucosidases known from other two-component plant defence systems.…”

Section: Discussionmentioning

confidence: 67%

“…This percentage is lower than found in other insect herbivore species feeding on cyanogenic plant material. For example, feeding of the lepidopteran ugly nest caterpillar ( Archips cerasivoranus ) and the fall webworm ( Hyphantria cunea ) on cherry ( Prunus ) species, results in emission of more than 2.5% and 10% of the total leaf HCN potential, respectively [36], [37]. Feeding of the orthopteran desert locust ( Schistocerca gregaria ) on lima beans ( Phaseolus lunatus ) results in emission between ∼ 2.5% and 15% of the HCN present in consumed leaf material, depending of the cyanogenic capacity and potential of the plant cultivar [38].…”

Section: Discussionmentioning

confidence: 99%

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

et al. 2014

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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.

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Section: Discussionmentioning

confidence: 67%

Section: Discussionmentioning

confidence: 99%

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

et al. 2014

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“…Differences in pH may affect enzymatic reactions by changing the charge of certain amino acids, affecting protein conformation and their catalysis (Johnson & Felton, ; Harrison, ). Whereas the haemolymph of insects is mostly neutral with pH ranging from 6.4 to 7.5, the pH of the midgut lumen varies from a strongly acidic pH 3.1 to extremely alkaline pH 12.4 among different insect orders (Berenbaum, ; Dow, ; Schultz & Lechowicz, ; Johnson & Felton, ; Appel & Joern, ; Harrison, ; Cristofoletti et al , ; Fitzgerald, ; Terra & Ferreira, ). Regulation of midgut pH mainly involves H + V‐ATPases that are located in the apical membrane of goblet cells in the midgut (Wieczorek et al , ).…”

Section: From Feeding To Digestion: Targets For Insect Herbivore Adapmentioning

confidence: 99%

“…Although caterpillars of the generalist fall webworm Hyphantria cunea (Lepidoptera, Arctiidae) are vulnerable to hydrogen cyanide, they can feed on leaves of black cherry ( Prunus serotina , Rosaceae) containing cyanogenic glucosides without any adverse effects (Fitzgerald, ). A high alkaline midgut lumen at pH 11 was shown to prevent the hydrolysis of cyanogenic glucosides into toxic hydrogen cyanide during passage of the plant parts through the gut (Fitzgerald, ), most likely due to inhibition of plant β‐glucosidases. A direct link between an alkaline midgut and reduced plant β‐glucosidase activity towards benzoxazinoid glucosides was shown in the generalist fall armyworm feeding on maize containing DIMBOA‐glucosides (Dutartre et al , ).…”

Section: From Feeding To Digestion: Targets For Insect Herbivore Adapmentioning

confidence: 99%

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

et al. 2013

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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.

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“…Any residual β -glucosidase activity left on the leaf edges or in the leaf pieces will be inhibited by the alkaline midgut pH. Larvae of the fall webworm (Hyphantria cunea) also has an alkaline midgut environment which allow them to feed on black cherries without trigging their cyanogenic potential (Fitzgerald, 2008). Amelot et al, (2006) demonstrated that larvae of Heliconius erato released less hydrogen cyanide than Spodoptera furgiperda when feeding on Passiflora capsularis (5.8 fold difference).…”

Section: Heliconius Larvae Avoid Degradation Of Cnglcs During Feedingmentioning

confidence: 99%

Sequestration and functional diversification of cyanogenic glucosides in the life cycle of Heliconius melpomene

Castro

Demirtas

Orteu

et al. 2019

Preprint

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Heliconius butterflies are highly specialized in Passiflora, laying eggs and feeding as larvae only on these plants. Interestingly, Heliconius butterflies and Passiflora plants both contain cyanogenic glucosides (CNglcs). While feeding on specific Passiflora species, Heliconius melpomene larvae are able to sequester simple cyclopentenyl CNglcs, the most common CNglcs in this plant genus. Yet, aromatic, aliphatic, and modified CNglcs have been reported in Passiflora species and they were never tested for sequestration by heliconiine larvae. As other cyanogenic lepidopterans, H. melpomene also biosynthesize the aliphatic CNglcs linamarin and lotaustralin, and their toxicity does not rely exclusively on sequestration. Although the genes encoding the enzymes in the CNglc biosynthesis have not yet been fully biochemically characterized in butterflies, the cytochromes P450 CYP405A4, CYP405A5, CYP405A6 and CYP332A1 are hypothesized to be involved in this pathway in H. melpomene. In this study, we determine how the CNglc composition and expression of the putative P450s involved in the biosynthesis of these compounds vary at different development stages of Heliconius butterflies. We also established which kind of CNglcs H. melpomene larvae can sequestered from Passiflora. By analysing the chemical composition of the haemolymph from larvae fed with different Passiflora diets, we observed that H. melpomene is able to sequestered prunasin, an aromatic CNglcs, from P. platyloba. They were also able to sequester amygdalin, gynocardin, [C 13 /C 14 ]linamarin and [C 13 /C 14 ]lotaustralin painted on the plant leaves. The CNglc tetraphyllin B-sulphate from P. caerulea was not detected in the larval haemolymph, suggesting that such modified CNglcs cannot be sequestered by Heliconius. Although pupae and virgin adults contain dihydrogynocardin resulting from larval sequestration, this compound was metabolized during adulthood, and not used as nuptial gift or transferred to the offspring. Thus, we speculate that dihydrogynocardin was catabolized to recycle nitrogen and glucose, and/or to produce fitness signals during courtship and calling. Mature adults had a higher concentration of CNglcs than any other developmental stages due to intense de novo biosynthesis of linamarin and lotaustralin. All CYP405As were expressed in adults, whereas larvae mostly expressed CYP405A4. Our results shed light on the importance of CNglcs in Heliconius biology and for their coevolution with Passiflora.

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Larvae of the fall webworm, Hyphantria cunea, inhibit cyanogenesis in Prunus serotina

Cited by 16 publications

References 26 publications

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

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

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

Sequestration and functional diversification of cyanogenic glucosides in the life cycle of Heliconius melpomene

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