Differences in Nicotine Metabolism of Two Nicotiana attenuata Herbivores Render Them Differentially Susceptible to a Common Native Predator

Kumar, Pavan; Rathi, Preeti; Schöttner, Matthias; Baldwin, Ian Thomas; Pandit, Sagar Subhash

doi:10.1371/journal.pone.0095982

Cited by 23 publications

(17 citation statements)

References 54 publications

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“…Hence, that such carcasses were not found on EV or irGGPPS plants, clearly suggested that the BG1-silenced larvae experienced some distinctive predator behaviour. During the night, M. sexta larvae are mainly preyed on by the wolf spiders ( Camptocosa parallela ; Lycosidae), which are abundant in this habitat 32 37 ( Fig. 5d ).…”

Section: Resultsmentioning

confidence: 99%

“…to evaluate if HGL-DTG co-option has evolved in them; such comparisons between the nicotine metabolism of Manduca spp. and generalist herbivores were highly useful in evaluating the costs and benefits of detoxification and co-option of nicotine 37 . The observation that spiders that ingest BG1-silenced larvae show signs of locomotor distress suggests that Lyc4 affects spider's nervous system.…”

Section: Discussionmentioning

confidence: 99%

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Detoxification of hostplant’s chemical defence rather than its anti-predator co-option drives β-glucosidase-mediated lepidopteran counteradaptation

et al. 2015

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The evolutionary plant–herbivore arms race sometimes gives rise to remarkably unique adaptation strategies. Here we report one such strategy in the lepidopteran herbivore Manduca sexta against its hostplant Nicotiana attenuata's major phytotoxins, 17-hydroxygeranyllinalool diterpene glycoside, lyciumoside IV and its malonylated forms. We show that alkalinity of larval regurgitant non-enzymatically demalonylates the malonylated forms to lyciumoside IV. Lyciumoside IV is then detoxified in the midgut by β-glucosidase 1-catalysed deglycosylation, which is unusual, as typically the deglycosylation of glycosylated phytochemicals by insects results in the opposite: toxin activation. Suppression of deglucosylation by silencing larval β-glucosidase 1 by plant-mediated RNAi causes moulting impairments and mortality. In the native habitat of N. attenuata, β-glucosidase 1 silencing also increases larval unpalatability to native predatory spiders, suggesting that the defensive co-option of lyciumoside IV may be ecologically advantageous. We infer that M. sexta detoxifies this allelochemical to avoid its deleterious effects, rather than co-opting it against predators.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Detoxification of hostplant’s chemical defence rather than its anti-predator co-option drives β-glucosidase-mediated lepidopteran counteradaptation

et al. 2015

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“…There are however also insects that perform well on cultivated tobacco, e.g. Helicoverpa zea (Gog et al 2014) and the Hawmoth caterpillar Manduca sexta, that not only tolerates nicotine but even uses the metabolite to deter its natural enemy (Kumar et al 2014).…”

Section: Alkaloidsmentioning

confidence: 99%

Endogenous plant metabolites against insects

2018

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Herbivorous insects are responsible for large losses to agriculture through feeding damage itself but also by vectoring pathogens such as viruses. Plants have evolved various mechanisms to defend themselves against insects, including the production of specialised metabolites that act as natural insecticides. Throughout history, plants and plant extracts harbouring specialised metabolites have been exploited by man for their antiinsect properties. Also, commercial insecticides are often based on plant-specialised metabolites and adapted further e.g. to give them the physicochemical properties that render them systemic. The development and application of these synthetic pesticides has made it possible to scale up the production and to increase the yield of food crops worldwide. However, their adversary effects on the environment and on non-target organisms, first discussed in Rachel Carson's Silent Spring, continue to cause debate and recently resulted in a ban on the use of certain pesticides in the European Union. The trait of insect defence has been largely overlooked during crop domestication and resulted in basically unarmed crop plants. Endogenous production of specialised metabolites could be reintroduced in modern crop varieties to retrieve self-defences. However, despite the fact that a plethora of specialised metabolites from plants has been described, studies that validate their deterrent or insecticidal effect in planta (crop), let alone in field situations, are sparse. To answer the question whether it is feasible to reintroduce endogenous insecticides to bring about insect resistance, the defence metabolites of plants, their synthesis and regulatory mechanisms underlying their production are examined.

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“…prot.) [28]; threonine deaminase 2 (TD2) degrades the essential amino acid threonine; the toxic alkaloid nicotine is subject to detoxification by a cytochrome P450 enzyme (CYP6B46) [34]; the maize cysteine protease (Mir1) affects the integrity of the peritrophic matrix, which may be compensated for by the insect by new synthesis of the structure (refill) [18]; insects use multiple strategies to neutralize toxic glucosinolates, including metabolism by sulfatase [74]. being inhibited by Ile.…”

Section: Summary and Perspectivesmentioning

confidence: 99%

Interaction of plant defense compounds with the insect gut: new insights from genomic and molecular analyses

Howe

Herde

2015

Current Opinion in Insect Science

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SummaryThe co-evolutionary conflict between insect herbivores and their host plants is profoundly influenced by biochemical reactions associated with passage of toxin-laden plant material through the herbivore digestive canal. Insect herbivores provide excellent models in which to understand the mechanistic interplay between nutrition and detoxification, how plant defense compounds hijack these processes, and how insects adapt to host defense chemistry. Expanding genome sequence information and genetic approaches to manipulate gene function in both interacting partners are providing new insights into the genetic underpinnings of host preference and plasticity in gut physiology. Fundamental knowledge gained from these studies has practical application in understanding how insects evolve resistance to pesticides, and may also inform efforts to better understand how plant chemicals impact human health.3

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Differences in Nicotine Metabolism of Two Nicotiana attenuata Herbivores Render Them Differentially Susceptible to a Common Native Predator

Cited by 23 publications

References 54 publications

Detoxification of hostplant’s chemical defence rather than its anti-predator co-option drives β-glucosidase-mediated lepidopteran counteradaptation

Detoxification of hostplant’s chemical defence rather than its anti-predator co-option drives β-glucosidase-mediated lepidopteran counteradaptation

Endogenous plant metabolites against insects

Interaction of plant defense compounds with the insect gut: new insights from genomic and molecular analyses

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