Adaptation of tobacco hornworms to the ingestion of nicotine

Self, L. S.; Guthrie, F. E.; Hodgson, Ernest

doi:10.1016/0022-1910(64)90081-2

Cited by 123 publications

(37 citation statements)

References 11 publications

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“…on the polar metabolites of nicotine, such as cotinine and the N-oxides of both nicotine and cotinine, which are commonly found in the urine and blood of human smokers (8,11,12); cytochrome P450s (CYPs) are thought to mediate nicotine's oxidation to these metabolites (8,11,(13)(14)(15), but other researchers have been unable to find the oxides in M. sexta's excretions and propose that nicotine is rapidly excreted without modification (16)(17)(18). Although this theory is widely accepted, most studies have not been able to recover all of the ingested nicotine in the frass and nicotine can be found in the hemolymph of larvae feeding on nicotine-containing diets.…”

Section: Significancementioning

confidence: 99%

Natural history-driven, plant-mediated RNAi-based study reveals CYP6B46 ’s role in a nicotine-mediated antipredator herbivore defense

Kumar

Pandit

Steppuhn

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

118

119

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Significance When hornworm ( Manduca sexta ) larvae feed on Nicotiana attenuata plants in native habitats, more disappear at night when they feed on transgenic, nicotine-free N. attenuata plants because wolf spiders ( Camptocosa parallela ) selectively prey on nicotine-free larvae. When larvae consume nicotine-replete plants, their midgut-expressed cytochrome P450 6B46 ( CYP6B46 ) is upregulated. The larvae in which CYP6B46 is silenced by plant-mediated RNAi excrete more of their ingested nicotine. Silencing CYP6B46 impairs the mechanisms of passing ingested nicotine from the midgut to the hemolymph to be exhaled from the spiracles during spider attack. Spiders are deterred by this nicotine-rich halitosis. Thus, the CYP6B46 -silenced larvae exhale less nicotine and become ready spider prey, demonstrating that CYP6B46 functions to repurpose the normally excreted nicotine for defense.

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Section: Significancementioning

confidence: 99%

Natural history-driven, plant-mediated RNAi-based study reveals CYP6B46 ’s role in a nicotine-mediated antipredator herbivore defense

Kumar

Pandit

Steppuhn

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

118

119

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“…The ethylene burst is a result of "stealthy" feeding which benefits the herbivore. M. sexta larvae are negatively affected by dietary nicotine intake in a dosedependent fashion (Baldwin 1988;Krischik et al 1991) and nicotine metabolism requires large metabolic expenditures to maintain Manduca's nicotine resistance physiology (Self et al 1964;Maddrell and Gardiner 1976;Appel and Martin 1992;Snyder et al 1993;Murray et al 1994). 2.…”

Section: Discussionmentioning

confidence: 98%

Herbivore-induced ethylene burst reduces fitness costs of jasmonate- and oral secretion-induced defenses in Nicotiana attenuata

2001

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Specialist herbivores are known to alter their host's wound-induced responses but the beneficiaries of these alterations are unknown. Nicotiana attenuata plants release a burst of ethylene specifically in response to feeding by Manduca sexta larvae, which is known to suppress wound- and methyl jasmonate (MeJA)-inducible nicotine accumulation. The ethylene burst may be a mechanism by which M. sexta larvae feed "stealthily" on their host plants or, alternatively, it may allow the plant to optimize its defense response against this specialist herbivore by reducing costs of induction. We examined the impact of the ethylene burst on defense-related fitness costs that are readily observed when plants are treated with MeJA and grown in competition with untreated plants. We elicited nicotine induction (with MeJA), the ethylene burst (with the ethylene releasing compound, ethephon) and inhibited the plant's ability to perceive ethylene (with applications of an antagonist of ethylene receptors, 1-methylcyclopropene, 1-MCP). By simultaneously applying MeJA and ethephon we mimicked the plant's hormonal response to larval attack. We hypothesized that if the ethylene burst benefited the plant, the fitness costs of MeJA induction should be reduced by ethephon and restored if the plants were additionally treated with 1-MCP. In a second experiment, we applied larval oral secretion (OS) to elicit endogenous hormone production and predicted that the 1-MCP treatment should reduce the fitness of OS-treated plants. Our measures of plant fitness, namely the rate of stalk elongation and lifetime capsule production, supported these predictions. We conclude that the ethylene burst elicited by this specialist herbivore can reduce MeJA-induced fitness costs and increase the competitive strength of OS-treated plants. Suppressed nicotine production is likely to contribute to, but is not sufficient to explain, the observed fitness outcomes. The intensity of intra-specific competition and herbivore attack will likely determine the adaptive value of the M. sexta-elicited ethylene response.

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“…avoids nicotine by selectively feeding in the phloem (Guthrie et al 1962). Manduca sexta L. (Lepidoptera: Sphingidae), which commonly feeds on tobacco and other solanaceous plants, rapidly excretes most of the nicotine it ingests (Self et al 1964b). Ingestion of dietary nicotine (0.75% wet weight) also induces midgut cytochrome P-450 activities in M. sexta and may represent an additional adaptation to tobacco feeding in this species (Snyder et al 1993) and other lepidopterans (Rose et al 1991).…”

Section: Introductionmentioning

confidence: 99%

The roles of nicotine and natural enemies in determining larval feeding site distributions of Manduca sexta L. and Manduca quinquemaculata (Haworth) on tobacco

et al. 2002

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Field observations indicated that hornworms select feeding sites non-randomly on tobacco. We tested the hypotheses that differences in feeding site locations of larvae of Manduca sexta L. and Manduca quinquemaculata (Haworth) (Lepidoptera: Sphingidae) on tobacco could be explained by differential nicotine concentrations within plants and leaves, species-specific responses to nicotine, or pressure exerted by natural enemies. Results showed that third-instar larvae of M. sexta fed more proximally and centrally on the leaf, whereas M. quinquemaculata fed more distally. Withinplant selection of leaves did not differ; both species selected leaves in the middle region of the plant. Nicotine concentrations in a high nicotine genotype, NC95, varied within each leaf, increasing 2 -3 fold from the basal to apical portion of the leaf, and within each plant, increasing 7 -10 fold from the first fully expanded leaf to the twelfth (lowest) leaf. In laboratory bioassays, both Manduca species responded to nicotine as a feeding deterrent. Electrophysiological studies demonstrated that gustatory organs of both species responded to nicotine at concentrations found in tobacco leaves and that M. quinquemaculata generally showed a less vigorous response to nicotine than M. sexta. Field mortality of M. sexta due to parasitism by Cotesia congregata (Say) and to parasitism and predation combined differed among feeding sites; predation alone did not. Results suggest that although nicotine concentration and species specific responses to nicotine play a role in determining feeding site locations, pressure exerted by natural enemies, especially parasitism by C. congregata, is more important.

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Adaptation of tobacco hornworms to the ingestion of nicotine

Cited by 123 publications

References 11 publications

Natural history-driven, plant-mediated RNAi-based study reveals CYP6B46 ’s role in a nicotine-mediated antipredator herbivore defense

Natural history-driven, plant-mediated RNAi-based study reveals CYP6B46 ’s role in a nicotine-mediated antipredator herbivore defense

Herbivore-induced ethylene burst reduces fitness costs of jasmonate- and oral secretion-induced defenses in Nicotiana attenuata

The roles of nicotine and natural enemies in determining larval feeding site distributions of Manduca sexta L. and Manduca quinquemaculata (Haworth) on tobacco

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